Chemosphere 254 (2020) 126846

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Water conservancy project on the Yellow River modiﬁes the seasonalvariation of Chlorophyll-a in the Bohai Sea
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 ofChina, Ocean University of China, 238 Songling Road, Qingdao, 266100, China
Center for Marine Environmental Studies, Ehime University, 2-5 Bunkyo-Cho, Matsuyama, 790-8577, Japanc
Laboratory for Marine Ecology and Environmental Sciences, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266071, Chinad
Key Laboratory of Marine Chemistry Theory and Technology, Ministry of Education of China, Ocean University of China, 238 Songling Road, Qingdao,
266100, Chinab

h i g h l i g h t s

g r a p h i c a l a b s t r a c t

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

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 11 March 2020
Received in revised form
17 April 2020
Accepted 18 April 2020
Available online 23 April 2020

The Water Sediment Regulation Scheme (WSRS) is a unique engineering measure that has been regularly
performed to reduce reservoir sedimentation and increase the ﬂood capacity of the Yellow River in China
since 2002. As a side effect, the WSRS greatly increases the monthly input ﬂux of nutrients to the Bohai
Sea (BHS) in summer, potentially exacerbating eutrophication levels therein and subsequently affecting
the growth of phytoplankton. However, its inﬂuence on the Chlorophyll-a (Chl-a) dynamics over the BHS
is still poorly understood. In this study, two approaches were adopted to investigate it: 1) long-term insitu 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 theimpact of WSRS on seasonal Chl-a. The results showed that the surface Chl-a exhibited two peaks inspring and autumn until 2002, but has exhibited only one peak in spring-summer since 2002. Satellitederived Chl-a concentrations in spring-summer since 2002 have increased by 56% compared to thoseuntil 2002. The simulated results showed that the change in Yellow River discharge induced by the WSRS
has resulted in the appearance of high concentrations of Chl-a in summer over the Central 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.

Handling Editor: Derek Muir
Keywords:
Chlorophyll-a
Seasonal variation
Water Sediment Regulation Scheme
Yellow River
Bohai Sea

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

Fig. 3. Seasonal variations of Chl-a from in-situ observations (see Table 1 for details ofdata sources).

synchronous variation with the Yellow River discharge during
1998e2017, and the monthly ﬂuxes of dissolved inorganic nitrogen(DIN) and particulate phosphorus (PP) were both two orders ofmagnitude higher than the DIP and dissolved organic phosphorus(DOP). For a spin-up, the model was integrated for 5 years as forced
by climatological surface forcing (1998e2017) and monthly nutrients input in 1998. Then, the model was integrated for 20 years
from 1998 to 2017 using the same surface forcing as in the spin-up
and monthly nutrients input for these 20 years.
3. Results
3.1. Seasonal trends of Chl-a in recent decades
From in-situ observations (Fig. 3) in the BHS, the concentrationsof Chl-a exhibited higher values in spring and autumn than insummer and winter until 2001 except in 1992e1993, when Chl-a
was at a low level with no obvious seasonal variation. Until 2001,
the multiyear mean concentrations of Chl-a in spring, summer,

autumn, and winter were 1.02, 0.71, 1.11, and 0.83 mg,m3 ,respectively. Since 2006, Chl-a has seen an obvious increase inspring and summer with multiyear mean values of 3.02 and 3.39
mg,m3 , respectively. Further, Chl-a in autumn and winter has
somewhat increased with multiyear mean values of 1.89 and 1.18
mg,m3 , respectively. The Chl-a concentration in the summer of2016 over the Central Bohai Sea was also at a high level with themean value of ~2.5 mg,m3 (Wang et al., 2018a). Additionally, thelimited observations in the BHS indicated that Chl-a in the summerof 2002 had also been at a high level (~2.1 mg,m3 ) and exhibited
higher concentrations than all seasonal values until 2001 (Fig. 3).
Moreover, coastal observations indicated that the mean concentration of Chl-a in the spring of 2002 was ~1.88 mg,m3 (Li et al.,2003, 2006; Cao et al., 2006), which was lower than that in summer over the entire BHS (~2.1 mg,m3 ). 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-ain offshore areas in the spring of 2002. Consequently, Chl-a over theentire 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 thetwo peaks in spring and autumn to one peak in spring-summer haspresumably occurred in the BHS since 2002.
Satellite-derived data with high temporal resolution were used
to further analyze interannual and seasonal variations in Chl-a from1998 to 2017. In this study, February, May, August, and November
are deﬁned loosely as winter, spring, summer, and autumn,
respectively. As shown in Fig. 4, Chl-a in four seasons exhibited no
obvious differences from 1998 to 2001, with all values around 2
mg,m3 . This was inconsistent with the two peaks in spring andautumn from in-situ observations. The relatively high concentration of satellite-derived Chl-a in summer during 1998e2001 may
be attributed to the higher Chl-a along the coastal areas comparedto that in spring (Fig. 5bec). Since 2002, Chl-a in spring and summer has increased to 2.91 and 3.71 mg,m3 (on average), whereas
those in the other two seasons exhibited a slight decrease
compared to those until 2002. The Chl-a concentrations in springsummer have obviously declined after 2013, although they haveremained higher compared to those in autumn and winter (Fig. 4).
In addition, the strength of seasonal ﬂuctuation in Chl-a changed
with the seasonal shift. Here, we deﬁne one variable, the seasonalrange 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-ain 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, thereader 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,m3 ).

SRC ¼ Chlmax  Chlmin(1)where Chlmax and Chlmin represent the maximum and minimum of
the seasonal mean Chl-a, respectively. As shown in Fig. 4, the SRC
has increased signiﬁcantly with a mean value of ~2.2 mg·m3 since
2002 compared to that until 2002 (~0.4 mg·m3 ). The increasing
trend of the SRC is similar to the trend of Chl-a during summer,
indicating that the high Chl-a during summer is directly responsible for the large SRC.

other areas during the four seasons (Fig. 5aed). Since 2002, peakChl-a in the four seasons has been identiﬁed in summer over mostareas, especially in Qinhuangdao Coast and Liaodong Bay, followedby spring (Fig. 5eeh). Comparisons of Chl-a during the two periods
exhibited a signiﬁcantly increased Chl-a in summer, followed byspring, and a slight decrease in autumn and winter over the entire
BHS (Fig. 5iel). This directly resulted in a shift in the seasonalpattern of Chl-a. Meanwhile, the SRC for the multiyear average waslower than 1 mg,m3 in the entire BHS until 2002, but has since
exhibited an obvious increase with values higher than 2 mg,m3(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
distributions of Chl-a in four seasons before and since 2002 wereanalyzed using the satellite-derived data. As shown in Fig. 5, thecoastal Chl-a exhibited higher concentrations compared to those incentral areas. Until 2002, there was a weak bloom during spring inthe southwest of the Central Bohai Sea, where Chl-a in other seasons were all at a low level (Fig. 5aed). In addition, Chl-a in the
coastal areas of the BHS exhibited relatively high values than the

There are more than 40 rivers ﬂowing into the BHS (Liu and Yin,
2010) that add large amounts of nutrients, thereby promoting the
growth of phytoplankton. We chose the three largest rivers (Yellow
River, Haihe River, and Liaohe River) to analyze the correlation
between the mean river discharge during summer (from June toAugust) and the mean Chl-a concentration in August over the BHS
from 1998 to 2017. As shown in Table 1, there was a good correlation
between Chl-a in the Central Bohai Sea and the Yellow River6

X. Ding et al. / Chemosphere 254 (2020) 126846

Table 1
Correlation coefﬁcients (r) between Chl-a (satellite-derived data) and riverdischarge during summer in the Bohai Sea from 1998 to 2017. Five subregions:
Central Bohai Sea (CBS), Bohai Bay (BHB), Laizhou Bay (LZB), Qinhuangdao Coast(QHD), and Liaodong Bay (LDB).

Yellow River
Haihe River
Liaohe River
Total

CBS

BHB

LZB

QHD

LDB

Bohai Sea

0.82*
0.11
0.58*
0.80*

0.54*
0.02
0.21
0.40

0.26
0.18
0.53*
0.39

0.71*
0.05
0.59*
0.69*

0.63*
0.21
0.71*
0.63*

0.76*
0.10
0.65*
0.75*

*p < 0.05.

discharge (r ¼ 0.82). In addition, a good correlation between Chl-ain the Liaodong Bay (Qinhuangdao Coast) and Liaohe River (Yellow
River) discharge was exhibited. However, Chl-a in Laizhou Bay
exhibited little correlation with the Yellow River discharge, which
was probably affected by the numerously small rivers nearby andnonpoint sources (Guo et al., 2017; Jiang et al., 2018). The signiﬁcantcorrelation of Chl-a in Laizhou Bay with the discharge of the LiaoheRiver, which was far from Laizhou Bay, might result from the similar
trends between the Liaohe River discharge and the terrestrial input
around Laizhou Bay in summer.
4. Discussion
Our results indicated that a sharp increase in Chl-a in summer
has been found since 2002, as well as a slight increase in spring,which directly led to the seasonal shift (Figs. 3 and 4). Here, wemainly discuss the reason for the signiﬁcant increase in the concentration of Chl-a during summer in recent decades.

agreement with the interannual trend of Yellow River dischargeduring summer (Fig. 2a), implying that WSRS shifted the seasonalpattern of Chl-a in the Central Bohai Sea by loading a large amountof nutrients in summer. The response of Chl-a and primary production in the Central Bohai Sea to the monthly river discharge
from June to August were quantitatively estimated using linear
regression (Fig. 6b-6c). As represented by the slope of linear
regression, the monthly concentrations of Chl-a and primary production can respectively increase by 0.04 mg Chl-a m3 and3.19 mg C m2 d1 per 108 m3 of freshwater into the BHS. Usingsuch regression relations, the contributions of Yellow River
discharge to Chl-a (Chl AEi ) and primary production (PP AEi ) in theCentral Bohai Sea were estimated as follows:

0:04  Ri
;
Chli

(2)

3:19  Ri
;
PPi

(3)

Chl AEi ¼

PP AEi ¼

where i represents the year from 1998 to 2017, Ri is the monthly
mean Yellow River discharge from June to August, and Chli and PPi
represent the simulated monthly mean Chl-a and primary production from June to August in the Central Bohai Sea, respectively.
The calculated results indicated that WSRS had increased thecontribution of Yellow River discharge to Chl-a (primary production) during summer in the Central Bohai Sea from 18±7% (14±6%)
until 2002 to 37±15% (23±12%) since 2002. Consequently, WSRS
plays an important role in the seasonal variation of Chl-a by directly
promoting the growth of phytoplankton during summer in theCentral Bohai Sea.

4.1. Direct inﬂuence of Yellow River discharge on Chl-a in summer
Since 2002, WSRS on the Yellow River has caused a highmonthly water discharge and sediment load at least two months
prior to the normal high-ﬂow season (Liu, 2015). As shown in
Fig. 2a, the annual maximum water discharge began to appear insummer instead of autumn since 2002. The low summer discharge
in 2003 occurred because WSRS was carried out in September ofthat year (Wu et al., 2015). The decreased discharge after 2013
might be attributed to the reduced days of WSRS, which was eveninterrupted in 2016e2017 owing to the signiﬁcant reduction of thetotal amount of sediment in the Yellow River (Wu et al., 2015; Chenet al., 2019). Many studies have shown that the Yellow River
freshwater ﬂows northeastward during summer owing to thesoutheasterly wind (e.g., Wang et al., 2008; Wang et al., 2011). The
nutrients carried by the river freshwater may promote the growthof phytoplankton in the Central Bohai Sea, thereby exhibiting agood correlation between Chl-a and Yellow River discharge during
summer (Table 1). Since the phytoplankton biomass in the Central
Bohai Sea accounts for nearly half that in the BHS (Fig. S7), WSRS
likely plays an important role in the seasonal shift of Chl-a bypromoting the growth of phytoplankton during summer over theCentral Bohai Sea.
A 1D physical-biological model was applied to examine the inﬂuence of Yellow River discharge on the seasonal variability of Chla in the Central Bohai Sea from 1998 to 2017. With the Yellow River
input as the only exogenous nutrients source, the model can successfully reproduce the seasonal variation of the water temperatureand biological variables (see Text S4 on model validation). As
shown in Fig. 6a, the simulated surface Chl-a exhibited two peaks inspring and autumn until 2002, but has since exhibited one peak inspring-summer, indicating a shift in the seasonal pattern of Chl-a.
The interannual variation of summer Chl-a was in good

4.2. Long-term effect of Yellow River discharge on seasonalvariation in Chl-a
On the interannual scale, Chl-a in spring and summer display asigniﬁcant increasing trend in the BHS with p < 0.05 (Fig. 4). The
percentage increases in spring and summer since 2002 havereached 42% and 69% (on average), respectively, leading to an
overall annual average of Chl-a increasing by 30%. As shown in
Fig. 7, the Yellow River discharge during summer has been signiﬁcantly affecting the surface Chl-a within three months after
entering the sea (lag  3 months, r > 0.44). The discharge insummer of one year may also signiﬁcantly affect Chl-a in the next
spring-summer period (lag ¼ 10e14 months, r > 0.44) and even thethird year (lag ¼ 20e26 months). The accumulation of nutrientsover time, which often exists as a common phenomenon in coastal
seas (Nielsen et al., 2004; Neumann et al., 2018), might beresponsible for the increasing trends of Chl-a. Since there is only
one outlet (the Bohai Strait) connected to another water body (theYellow Sea), the water exchange is very weak with a renewal timeof several years (1.1e5.2 years) in the BHS (Cai, 2013; Li et al., 2015;
Li, 2017). Moreover, many studies emphasized that a signiﬁcant
fraction of the organic matter entering the coastal systems ismineralized by the benthos, and only a small fraction is permanently buried (Nixon and Pilson, 1983; Fennel et al., 2006). Hence,
the large amounts of nutrients carried by the Yellow River
discharge in summer are difﬁcult to remove completely from the
BHS in a short time. They may be stored as dissolved nutrients orparticulate organic matter, thereby promoting the growth ofphytoplankton in a few weeks to several months and even longer.
The relatively high Chl-a in spring-summer compared to that inother seasons in 2016e2017, when WSRS was interrupted, also
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,m3 ); (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.)

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 ofthat year in the Bohai Sea during 1998e2017. All data points represent values withp < 0.05. Five subregions: the Central Bohai Sea (CBS), Bohai Bay (BHB), Laizhou Bay(LZB), Qinhuangdao Coast (QHD), and Liaodong Bay (LDB). (For interpretation of thereferences to color in this ﬁgure legend, the reader is referred to the Web version ofthis article.)

4.3. Impact of other relevant factors on Chl-a in summer
In recent years, harmful algal blooms (HABs) have become more
frequent over the Liaodong Bay and Qinhuangdao Coast in summer(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 fromcoastal runoffs, mariculture, shipping operations, and other humanactivities (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 nutrientsand 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 Qinhuangdao Coast and Liaodong Bay was found in comparison withother subregions (Li, 2014, 2017). There is an isolated cyclonic circulation around the cold pool in Liaodong Bay during summer(Fig. S5a) that can block the transport of nutrients and phytoplankton to central areas as a retention system (Wei et al., 2003;
Zhou et al., 2017b). In addition, the slowly ﬂowing southwestward
water along the Qinhuangdao Coast has little offshore transport (Li,2014). Therefore, the particularly high Chl-a during summer in
Liaodong Bay and Qinhuangdao Coast may have a weaker effect on
the other subregions than the Yellow River diluted water, which canbe transported to the Central Bohai Sea and even to the Qinhuangdao Coast by the northeastward ﬂow (Wu et al., 2017b; Zhou
et al., 2017b). In addition, many other factors such as light, temperature, atmospheric deposition, groundwater discharge, andmariculture may also affect the Chl-a concentrations as reported inliteratures (Thomas et al., 2012; Sempere et al., 2015; Andersen

8

X. Ding et al. / Chemosphere 254 (2020) 126846

et al., 2017; Liu et al., 2017; Shou et al., 2018; Wang et al., 2018b;
Wang et al., 2019). Nevertheless, our results showed that they had
little effect on the increased Chl-a during summer in the BHS (seeText S5 in detail).
4.4. Uncertainties in results
The greatest challenge in the analysis of interannual variability
using satellite data is the missing data owing to cloud coverage (Heet al., 2013). We calculated the daily rate of spatial coverage (Ratesc )during 1998e2017, which was expressed as

Ratesc ¼

Nvalid 100%;
Nsum(4)

where Nvalid is the number of pixels with valid data over the BHS
from the satellite data, and Nsum is the total number of pixels. As
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,especially in June and July. The missing data on the daily scale in the
BHS brings great difﬁculties in accurately assessing the effect of
WSRS on Chl-a over the BHS. This work proved that the Yellow
River discharge into the sea during summer has greatly promoted
the growth of phytoplankton in the BHS since 2002. However, someinconsistent changes were found in the Central Bohai Sea, such as
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
only depended on the river water discharge but also on the concentrations of nutrients, which were considered to be invariant
over time in this study owing to a lack of observation data. In
addition, the southeasterly winds played a crucial role in driving
the Yellow River plume to extend northeastward into the Central
Bohai Sea in summer (Wang et al., 2008). Decreasing wind speed
and changes in wind direction can also impede the movement of
diluted water toward the central area. For instance, the winds
prematurely turned from southerly to northeasterly in August 2004
and 2012 (Fig. S12), which probably accounted for the relatively low
concentration of Chl-a despite the high river discharge during those
years. The riverine organic nitrogen may also play an important rolein biogeochemical cycle in coastal waters (Lee et al., 2017; Huang
et al., 2018). Liu et al. (2020) provided a useful method to estimate riverine organic matters ﬂuxes for Chinese rivers. However,the nutrients limiting phytoplankton growth in the Bohai Sea havechanged to phosphorus owing to the excessive nitrogen input sincethe 1990s (Wang et al., 2009; Xu et al., 2011). The extra nitrogensource of riverine organic nitrogen does not promote the growth ofphytoplankton in our simulation. In addition, the proportion ofriverine organic nitrogen that can be mineralized into DIN is notwell determined. Therefore we did not include the riverine organic
nitrogen in this study. In addition, the ﬂuxes of nutrients transported from the Yellow River estuary to the Central Bohai Sea,
which were roughly estimated using the horizontal water ﬂux andthe indeclinable concentrations of nutrients, may lead to someuncertainties in this study. On the spatial scale, the ecological effects of the nutrients carried by the Yellow River during summer inthe entire BHS remain unclear. These need to be quantitatively
evaluated using a 3D physical-biological coupling model.
5. Summary
This work discussed the seasonal variability of Chl-a in recent
decades over the BHS. Since 2002, the seasonal pattern of Chl-a has
gradually shifted from two peaks in spring and autumn to one peakin spring-summer. Meanwhile, the range of seasonal ﬂuctuation in
Chl-a increased obviously. A large amount of nutrients loads insummer owing to WSRS played a key role in the seasonal shift andﬂuctuations of Chl-a, whereas other factors might have little
impact. The 1D physical-biological modeling results for the past 20
years generally reproduced the observations in the Central Bohai
Sea, where the phytoplankton biomass accounted for nearly halfthat in the BHS. The modeling results show that the larger Yellow
River discharge has resulted in the peak value of Chl-a in summer
since 2002. The contribution of the river input to summer Chl-aover the Central Bohai Sea increased by 19% (on average)
compared to that until 2002. The signiﬁcant correlations between
the Yellow River discharge during summer and the Chl-a concentrations in the following different months implied that the inﬂuences of WSRS on Chl-a may extend from a few weeks to several
months and even longer. Water conservancy projects on rivers,
which are widely used around the world, have exhibited considerable inﬂuence on the ecosystem in coastal seas and need toreceive more attention.
Declaration of competing interest
The authors declare that they have no known competing
ﬁnancial interests or personal relationships that could haveappeared to inﬂuence the work reported in this paper.
CRediT authorship contribution statement
Xiaokun Ding: Writing - original draft. Xinyu Guo: Writing review & editing. Chao Zhang: Data curation. Xiaohong Yao:
Methodology. Sumei Liu: Methodology, Resources. Jie Shi: Resources. Chongxin Luo: Software. Xiaojie Yu: Resources. Yang Yu:
Visualization. Huiwang Gao: Writing - review & editing.
Acknowledgements
This study is funded by the National Nature Science Foundationof China (41876125) and the NSFC-Shandong Joint Fund (U1806211,
U1606404). X. Ding thanks the China Scholarship Council (CSC) for
supporting his stay in Japan and the Ministry of Education, Culture,
Sports, Science and Technology, Japan (MEXT) to a project on Joint
Usage/Research Center, Leading Academia in Marine and Environmental Research (LaMer) for supporting his study in Japan.
Appendix A. Supplementary data
Supplementary data to this article can be found online athttps://doi.org/10.1016/j.chemosphere.2020.126846.
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