Earth System Changes in Marginal Seas/Oceanologia 65 (2023) 278—296

Available online at www.sciencedirect.com

ScienceDirectjournal homepage: www.journals.elsevier.com/oceanologia

ORIGINAL RESEARCH ARTICLE

Biogeochemistry-ecosystem-social interactions on
the Chinese continental margins
Su Mei Liu a,b,∗, Wen Liang a, Xinyu Guo c, Nian Wu a,b, Wuchang Zhang b,d,
Xiujuan Shan e, Hua-De Zhao f, Juying Wang f, Jin Huang aaFrontiers Science Center for Deep Ocean Multispheres and Earth System, and Key Laboratory of Marine Chemistry Theory andTechnology, Ministry of Education, Ocean University of China, Qingdao, Chinab
Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology,
Qingdao, ChinacCenter for Marine Environmental Studies, Ehime University, Matsuyama, Japand
Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao,
Chinae
Key Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Yellow Sea Fisheries
Research Institute, Chinese Academy of Fishery Sciences, Qingdao, ChinafNational Marine Environmental Monitoring Center, Dalian 116023, China
Received 9 December 2021; accepted 1 December 2022
Available online 15 December 2022

KEYWORDS
Drivers;
Pressures;
Environmental
change;Social response;
Bohai

Abstract Chinese continental margins are experiencing remarkable environmental changes
driven by anthropogenic activities and climate change. As an important habitat and sea-based
ﬁsh farming resource in China, the Bohai was selected as a case study to understand how
ecosystems and social interactions are inﬂuenced by multi-stressors. The Bohai ecosystem has
been considerably modiﬁed. The Bohai coastline has been signiﬁcantly changed (e.g., total
sea area decreased and morphology changed) by sea reclamation and riverine sediment transport related to agriculture and erosion. Therefore, the strict reclamation policy and “Grainfor-Green” program have been issued to protect the coastline. Nutrient concentrations and∗ Corresponding author at: Frontiers Science Center for Deep Ocean Multispheres and Earth System, and Key Laboratory of Marine Chemistry Theory and Technology, Ministry of Education, Ocean University of China, Qingdao 266100, China; Laboratory for Marine Ecology andEnvironmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China; Phone: +86-532-66782100.
E-mail address: sumeiliu@ouc.edu.cn (S.M. Liu).
Peer review under the responsibility of the Institute of Oceanology of the Polish Academy of Sciences.

https://doi.org/10.1016/j.oceano.2022.12.001
0078-3234/© 2022 Institute of Oceanology of the Polish Academy of Sciences. Production and hosting by Elsevier B.V. This is an open accessarticle under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Earth System Changes in Marginal Seas/Oceanologia 65 (2023) 278—296
composition have been changed by fertilizer application, wastewater discharge, and variations
in seasonal patterns of riverine nutrient ﬂuxes. Hence, pollution control and prevention arenecessary. More seriously, ﬁshing resources have been altered, as a result of environmental
changes and overﬁshing. Therefore, a summer ﬁshing ban and stock enhancement should bevital besides environmental improvement. This study can help to predict and mitigate impacts
on global continental margins that are experiencing similar environmental stress.
© 2022 Institute of Oceanology of the Polish Academy of Sciences. Production and hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license(http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction

encing greater ecosystem and societal responses to environmental variations.

The ocean plays a critical role in supporting human societal
essential goods and services, but ocean ecosystems havebeen considerably altered by traditional and emerging anthropogenic activities such as overﬁshing, pollution, and sea
reclamation (Borja et al., 2016; Halpern et al., 2008), resulting in 41% of marine ecosystems being deeply affectedby multi-stressors (Halpern et al., 2008, 2012). Coastal marine ecosystems, in particular the Chinese marginal seas,
have demonstrated phenomena such as eutrophication, hypoxic events, harmful algal blooms, reduction in biodiversity, and changes in coastal morphology (Davidson et al.,2012; Evan et al., 2011; Landrigan et al., 2020). Thesechanges are mainly caused by population increase, damconstruction, and pollution discharge (Liu et al., 2012a;
Ning et al., 2010; Wu et al., 2021).
The Bohai is a shallow, semi-enclosed continental marginof the northwestern Paciﬁc, with a surface area of 7.7 × 104
km2 and an average water depth of 18.7 m. The Bohai includes Liaodong Bay, Laizhou Bay, Bohai Bay, the central Bohai, and Bohai Strait which connects with the Yellow Sea(Figure 1). River water discharge into the Bohai has been
substantially affected by anthropogenic activities, of which
the Huanghe (Yellow River) discharge accounts for > 75%of the total (Lin et al., 2001; Liu, 2015; Ren et al., 2002;
Wang et al., 2017). The Bohai is well known as an important habitat and sea farm base for ﬁshery resources in the
Chinese coastal seas; the Bohai ecosystems, however, havebeen signiﬁcantly modiﬁed by anthropogenic activities, resulting in eutrophication, low oxygen events, and extensive coastline changes (Su and Tang, 2002; Wei et al., 2019;
Zhai et al., 2019).
As a continental margin, the Bohai has been studied extensively, resulting in abundant hydrology and biogeochemistry data. This paper reﬂects the themes anddiscussions of the Continental Margins Working Group
which was established jointly by Integrated Marine Biosphere Research (IMBeR at https://imber.info/science/
regional- programmes- working- groups/cmwg) and Future
Earth Coasts. The objective of this paper is to outline spatial and temporal variations of the hydrological and biogeochemical variables of the Bohai, their multi-drivers andpressures, and the ensuing feedback to ecosystems and tosociety. This study is vital to understand how ecosystems
and society interact in the Bohai so that the information
here can be extrapolated globally to predict and alleviate
the stresses on similar continental margins that are experi-

2. Drivers and pressures of hydrographic andbiogeochemical variations
Since the 1950s, reforms of the socio-economic system, therapid growth of the population, and industrialization haveaccelerated China’s environmental change, which includes
land and water degradation (Bryan et al., 2018). Along withnatural drivers (i.e. climate change), drivers closely related
to intensive human activities in the Bohai Rim region substantially altered Bohai ecosystems, including populationpressure, urbanization, economic development, associatedwaste water discharge, fertilizer use, and ﬁshing pressure.

2.1. Population growth and urbanization
Although the population growth rate has slowed down in recent decades due to the family planning policy, the population has increased by approximately 150% in the Bohai Rim
region since the 1950s (Figure 2). In 2019, the population
was ca. 260 million representing 18.6% of the total national
population. In addition, the urbanization rate has increasedby ca. 45% in the last 70 years; more recently the rate has
exceeded 64% (Figure 2). As the population continues togrow and migrates to the economically developed coastal
areas, more waste water is emptied into the Bohai. During
1985−2015, industrial waste water discharge was stable because of the improvement of industrial wastewater treatment capacity, while domestic sewage efﬂuent had been
gradually increasing (Figure 3), related to population growthand urbanization and representing 75% of the total waste
water discharge.

2.2. Industrial structure and societal needs
China, as the second largest and one of the fastest growing economies in the world, is experiencing a contradiction
between economic development and environmental protection. On the positive side, it is believed that people’s
pursuit of material and spiritual satisfaction is constantly
improving. In addition, sustainability and strategic environmental health priorities, particularly for the Bohai Rim region, were established during the 18th National Congress(Wang et al., 2021). In the Bohai Rim region, the GDP exceeded CNY 1.8 × 104 billion in 2019, representing 18%
279

Earth System Changes in Marginal Seas

Figure 1

Map of the study area.

Figure 2 Population and urbanization rate in the Bohai Rim
region since the 1950s (data source: https://data.stats.gov.
cn/).

Figure 3 Waste water discharge in the Bohai Rim region sincethe 1980s (Wang et al., 2019).

of the national total (Figure 4). Rapid economic development means intense drivers directly from human activities(Figures 3, 5, and 6), which likely drive the changes in the
Bohai marine environment.
Although all major industries are experiencing growth,
the industrial structure of the Bohai Rim region is constantly
changing to promote the coordinated development of various industries in the national economy (Figure 4). In thelast 70 years, the proportion of primary sector economic activities, mainly agriculture, forestry, animal husbandry, andﬁsheries, has continued to decline from about 50% in the
1950s to 6% in recent years; The proportion of the secondary
sector, which is mainly industry, including construction, ﬁrst
increased and then decreased with the highest proportion(approximately 60%) in the late 1970s and approximately

Figure 4 GDP and industrial structure in the Bohai Rim region
since the 1950s (data source: https://data.stats.gov.cn/).

280

Earth System Changes in Marginal Seas/Oceanologia 65 (2023) 278—296

2.3. Coastline changes
Since 1978, China began to reform and open up, leading
to rapid economic development and urbanization which,in turn, has led to large-scale exploitation of coastal resources. Coastline changes (expansion and retreat) are frequent in China, particularly in the Bohai, due to estuarine deposits, erosion, sea reclamation, and protection engineering (Hou et al., 2016; Meng et al., 2017; Suzuki, 2003).
In the Bohai Rim region, coastline expansion occurs mainlyin the southern Bohai Bay to the Huanghe Delta, and coastline retreat occurs mainly on the southern shores of Laizhou
Bay (Duan et al., 2016; Hou et al., 2016).
The Huanghe has a high suspended sediment load due
to extensive cultivation in the loess plateau in the middle reaches of the river (Wang et al., 2017). In the lower
reaches, the shallow channel and highly elevated riverbed
which is > 8−10 m higher than the surrounding area, thus
forming a unique “suspended river”, has created catastrophic disasters in the ﬂuvial plain (Chen et al., 2012;
Wang et al., 2017). Moreover, the main channel of the
Huanghe has shifted often and has formed 11 delta lobes
since 1855, affecting the coastline along Bohai Bay, theHuanghe Estuary, and Laizhou Bay (Yang et al., 2011).
The total area of the Bohai has decreased by 7.06% overthe last 70 years from 81.3 × 103 km2 to 75.6 × 103 km2
with a shrinkage rate of ∼82 km2 /yr from the 1940s to2014 (Hou et al., 2016). Over the past decades, the total length of the shoreline has increased by 1159.9 km,
which is derived from an 80% decrease in the natural shoreline but an increase of 1977.9 km in artiﬁcial shoreline(Wei et al., 2019). Moreover, the area reclaimed from thesea has increased by 1988.5 km2 , with the further additionof areas under aquaculture and salt pans. The net effectis that construction land has increased and the area under
agriculture has signiﬁcantly decreased (Figure 7; Jin, 2020;

Figure 5 Fertilizer application rate in the Bohai Rim region
since the 1980s (data source: https://data.stats.gov.cn/).

35% in 2019. The proportion of the tertiary sector, which isdominated by the circulation and service industries, ﬁrst decreased and then increased with the lowest proportion (approximately 18%) in the late 1970s and approximately 59%
in 2019 (Figure 4). In short, the industrial structure of theBohai Rim region has evolved from being dominated by the
primary sector in the 1950s, to the secondary sector in the
1970s, and is now dominated by the tertiary economic sector. This change in industrial structure means changes in human lifestyles, which is closely related to changes in stressors and the effects of human activities throughout each period. With the development and increase of the tertiary sector, people have been pursuing spiritual and cultural needs
for a better life. Thus, a portfolio of national and regional
management and policies has been established to improvethe environment in the Bohai.

Figure 6 Area of varying sea water quality and the proportion of inferior to grade 4 sea water quality in the Bohai (data source:
Bulletin of the Ministry of Ecology and Environment of China 2001−2020, http://www.mee.gov.cn/hjzl/sthjzk/jagb/).

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Earth System Changes in Marginal Seas

Figure 7 The total area (× 104 hm2 ) of sea reclamation
caused by the development of aquaculture, salt pans, agriculture, construction, and land to be used from the period
1980−2017 (Wei et al., 2019).

Figure 8 Annual freshwater discharge and suspended
sediment load at station Lijin from 1950−2019 (datasource: Huanghe Water Conservancy Commission, http://www.
yellowriver.gov.cn/nishagonggao).

Wei et al., 2019). In addition, artiﬁcial wetlands increased
by 162.6% from 1980 to 2017 while natural wetlands decreased by 66% (Wei, 2018).
Sea reclamation and coastline change have had a profound inﬂuence on the morphology and ecological environment of the Bohai; for example, the tidal regime haschanged with M2 amplitudes increasing up to 20 cm in
1976−2011 (Pelling et al., 2013). Based on time series
data at the tidal gauges (i.e. Yangjiaogou and Longkougang
gauges), the mean relative sea level rose approximately 2.1
mm/ yr in western Laizhou Bay and 1.7 mm/yr in eastern
Laizhou Bay over the last 50−60 years (Deng et al., 2016).
In addition, the intertidal wetlands diminished quickly andcontinuously (Duan et al., 2016), resulting in the loss and/or
fragments of essential ﬁsh habitats (Jin, 2020; Meng et al.,2017).

Generally, the WSREs have substantially alleviated the siltation in both the Xiaolangdi Reservoir and the lower reachesof the Huanghe to prolong the reservoir’s operational life
and increase the ﬂood-carrying capacity of the downstream
channel (Wang et al., 2017). Freshwater discharge and sediment load during the WSREs represented 18−56% and 8−63%
with averages of 28% and 30% of the annual amount, respectively (Table 1). However, the riverbed in the lower reachhas armored due to coarsening, and bed scouring via reservoir regulation is not sustainable (Wu et al., 2020). The WSREs have led to high monthly runoff and sediment load advancing up to two months earlier than was the case before
the regulation events (Liu et al., 2012a). In particular, theHuanghe water has a long residence time in the Bohai withan average of 1.2 years (Liu et al., 2012b). In comparison,
the WSREs and natural ﬂoods contributed 29% and 19% ofannual freshwater discharge emptying into the Bohai during 2002−2012, respectively (Wu et al., 2017a). In addition,
the Huanghe sediment load to the sea was mainly depositedin the delta in summer and resuspended and transported
offshore in winter (Yang et al., 2011). Thus, changes in seasonal patterns of the Huanghe freshwater discharge and sediment load transport will have a far-reaching inﬂuence on
the ecological environment of the Bohai.

2.4. Freshwater discharge and sediment load tothe sea
The freshwater discharge and sediment load of the Huanghe
have shown interannual oscillation since 1950 with a decreasing rate of 0.61 km3 /yr and 0.21 × 108 ton/yr, respectively (Figure 8). Of the reductions, human activities
contributed ca. 55% and, in the 2000s, climate change accounted for the remainder (Miao et al., 2011). Historically,
the days with no water ﬂow near the Huanghe mouth increased ten-fold (up to 200 days) in the late 1990s due tothe increasing demand for water and the decrease in precipitation (cf. Zhang et al., 2001). Water consumption by agricultural and industrial activities increased three times fromthe 1950s to the 2010s, of which the consumption of water
through agricultural activities has decreased from ca. 90%
to 70% of total water consumption (Chen et al., 2005; China
Water Resources Bulletin at http://www.yrcc.gov.cn/).
Since 2002, the Huanghe Water Conservancy Commission has implemented 19 water-sediment regulation events(WSRE), using the reservoir-regulated ﬂood water at the
beginning of every ﬂood season, except in 2016 and 2017.

2.5. Hydrographic variations in the Bohai
The drivers of hydrographic variations in the Bohai include
winds, air-sea heat ﬂux, and freshwater ﬂux (river discharge, precipitation, and evaporation). All of them haveapparent seasonal variations. The wind direction over theBohai is northwesterly in winter and southeasterly in summer, and the wind speed is higher in winter (∼5 m/s) than insummer (∼2 m/s; Ren et al., 2017). More than 70% of precipitation concentrates from June to September while 35−50%
of evaporation occurs from April to June (Fu et al., 1994).
Since the annual precipitation (500—1000 mm) is lower than282

Earth System Changes in Marginal Seas/Oceanologia 65 (2023) 278—296

Table 1 Annual freshwater discharge and sediment load, and the days and their proportion during the WSRS in annual freshwater discharge and sediment load as well, respectively in the lower reach of Huanghe during 2001—2019. The data without
the regulation events in 2001, 2016, and 2017 are also provided for comparison. Data are from http://www.yellowriver.gov.
cn/nishagonggao.
Year

2001
2002
2003
2004
2005
2006
2007
2008
2009
2010
2011
2012
2013
2014
2015
2016
2017
2018
2019

Annual Flux

Water and Sediment Regulation Events

Water
discharge(km3 /yr)

Sediment
load(107 t/yr)

4.65
4.19
19.21
19.82
20.68
19.17
20.40
14.54
13.29
19.30
18.51
28.20
23.69
11.43
13.36
8.19
8.96
33.37
31.22

4.22
6.02
40.36
26.51
18.07
15.66
15.06
8.43
6.02
16.70
9.26
18.30
17.30
3.01
3.14
1.06
0.77
29.70
28.26

Day

Water
discharge(km3 /yr)

Proportionin annual
discharge

Sediment
load(107 t/yr)

Proportionin annualsediment

15
24
30
23
21
30
17
17
44
22
26
20
22
24

2.34
4.22
5.20
4.13
4.96
6.66
3.97
3.76
8.99
3.86
5.26
5.28
2.75
3.08

0.56
0.22
0.26
0.20
0.26
0.33
0.27
0.28
0.47
0.21
0.19
0.22
0.24
0.23

5.07
15.06
7.87
6.17
7.48
9.84
5.78
4.07
13.91
4.26
7.24
5.58
2.21
1.86

0.34
0.63
0.26
0.27
0.36
0.33
0.34
0.24
0.32
0.19
0.28
0.28
0.10
0.08

26
54

6.10
11.11

0.18
0.36

13.54
16.33

0.52
0.30

the annual evaporation (1500—2200 mm), the freshwater
discharge from rivers is important for maintaining salinity
in the Bohai.
Over the period of one year, the change in these drivers isdue to two factors; interannual oscillation and linear trend.
The wind direction and speed during the period 1950−2011
showed interannual oscillations with periods from several
years to 15 years (Ren et al., 2017). The strong wind events(>10.8 m/s) usually appeared in spring and had an apparent
weakening trend during 1971−2008 (Wu et al., 2012). The
precipitation around the Bohai during the period 1965−2014
had a declining trend (Zhao et al., 2018). However, inall months, the slopes of these trends are less than 0.78mm/yr; that is a negligible value when compared to annual
precipitation (>500 mm/yr) and therefore it is not expected
to cause a signiﬁcant change in salinity in the Bohai. On theother hand, the increasing and decreasing range of precipitation in the same month during the period 1965−2014 wasclose to its monthly mean value, indicating a possible larger
impact from oscillation than from linear trend on the contribution of precipitation to salinity in the Bohai. The airtemperature observed in the Bohai Rim region during theperiod 1951−2011 had a positive trend of ∼0.03 degree/yr(Peng and Han, 2013).

phorus fertilizers ﬁrst increased and then slowed down in
the last 40 years; compound fertilizer has been increasing
and its use has exceeded nitrogen fertilizer in recent years(Figure 5). Total fertilizer application had been increasing
until 2013, but since then it has been stable with a recent
decline in use. During the early stages, fertilizer application increases food production, but intensive fertilizer application induces fertilizer loss. It has been reported thatthe loss of fertilizer nitrogen in Chinese farmland can reach
19.1% of total fertilizer usage (Zhu et al., 2006). Thus, about
50−80 × 104 tons of nitrogen fertilizer (excluding nitrogenin compound fertilizer) are lost every year in the Bohai Rim
region, which can be transported into the Bohai via riverine
input and SGD, and affects the nutrient composition of theBohai.

2.7. Nutrient inputs to the Bohai

2.6. Fertilizer application

External nutrient sources to the Bohai include river input,
precipitation, submarine ground discharge (SGD), aquaculture efﬂuents, and water exchange through the Bohai Strait.
Internal nutrient sources mainly derive from nutrient regeneration in sediments and exchange between sediment andoverlying seawater interface, which plays an important rolein supporting nutrients for phytoplankton growth (Liu et al.,2003, 2011).

With population growth and increasing human demand forfood, fertilizer application generally increases to satisfy
this demand. In the Bohai Rim region, nitrogen and phos-

2.7.1. Nutrient transport from the HuangheDuring 2001−2019, nutrient concentrations exhibited awide range of variations in the Huanghe with the concen283

Earth System Changes in Marginal Seas
trations of NO3 — , DIN, dissolved organic nitrogen (DON),
PO4 3— , dissolved organic phosphorus (DOP), and Si(OH)4 being 97−501, 105−524, 0.0−268, 0.03−0.95, 0.01−0.59, and
0.5−167 μM, respectively (Liu et al., 2012a; Wang et al.,2022; Wu et al., 2021). On average, DIN and PO4 3— accounted for 91% and ca. 50% of total dissolved nitrogen andphosphorus, respectively. Among the rivers emptying into
the ocean (Smith et al., 2003), NO3 — concentration in the
Huanghe is very high, PO4 3— concentration is at the pristine level (0.50 μM) due to adsorption onto abundant sediment particles in the Huanghe, and Si(OH)4 level is high due
to high mechanical denudation and higher evaporation overprecipitation in the Huanghe watershed (Cai et al., 2008;
Li and Zhang, 2003; Liu et al., 2009). Therefore, the nutrient composition is characterized by a high ratio of N/P anda low ratio of Si/N.
Nutrient concentrations in the Huanghe showed high values in spring and low values in summer for NO3 — , higher
values for DON in summer than in other seasons, slightly
low values for PO4 3— and DOP in summer when sediment loads were highest, and no obvious seasonal variations for Si(OH)4 . Nutrient concentrations in the lower
reach of Huanghe showed generally decreasing trends during 2001−2019 at rates of 0.34 μM/month for NO3 — ,0.001 μM/month for PO4 3— , and 0.26 μM/month for Si(OH)4 ,respectively (Figure 9). The seasonal peaks of Huanghe
freshwater discharge and nutrient transports have bothbeen shifted by the WSREs with high monthly values appearing two months earlier than was the case before the WSREs (Liu et al., 2012a; Liu, 2015). Phosphate limitation ofphytoplankton growth is aggravated during extremely highfreshwater discharge periods (Liu et al., 2012a; Liu, 2015;
Turner et al., 1990).
Nutrient transport ﬂuxes from the Huanghe into the sea
were 0.28−19.3 × 108 mol/month for DIN, 0.04−32.7 × 107
mol/month for DON, 0.07−26.9 × 105 mol/month forphosphate, 0.47−39.7 × 105 mol/month for DOP, and0.02−92.5 × 107 mol/month for Si(OH)4 , respectively. Considering the drivers that inﬂuence nutrient levels in the
Huanghe, the proportional contributions of different nutrient sources (Figure 10) to the Huanghe are estimated to
be excess fertilizer run-off (46±1%) and sewage efﬂuents(38±1%) for DIN, sewage efﬂuents (86±1%) and excess fertilizer run-off (11±0.5%) for PO4 3— , and runoff (48%±9%) andrecharge water (47%±10%) for Si(OH)4 , respectively.

the riverine input for NO3 — and DIN, 38% of the riverine input for PO4 3— , and 6% of the riverine input for Si(OH)4 .
2.7.3. Nutrient transport via SGD and other sources
The SGD in the Huanghe delta should be important, withthe previously reported SGD value of 1280−1480 m3 /s
in September 2006 and July 2007 using 224 Ra isotope(Peterson et al., 2008). Nutrient ﬂuxes from SGD to the Bohai were 510, 3.6, and 240 × 108 mol/yr for DIN, PO4 3— , andSi(OH)4 , respectively in November 2014 (Liu et al., 2017).
These values were 7%, 43%, and 98% of the reported ﬂuxesof DIN, PO4 3— , and Si(OH)4 delivered by the SGD of two bays
(Eastern Laizhou Bay and Western Bohai Bay) of the Bohai(Wang et al., 2019a; Zhang, 2018; Zhang et al., 2016) andwere used later for comparison, considering the substantial
uncertainties of nutrients delivered by SGD. Nutrient ﬂuxes
delivered by SGD accounted for 70−90% of the sum of atmospheric deposition, riverine input, and SGD.
In addition, nutrients derived from feeding and nonfeeding marine aquaculture efﬂuents contributed <5% of
dissolved nitrogen and phosphorus discharged from industrial wastewater and sewage efﬂuents (Cui et al., 2005).
Moreover, nutrient exchange through the Bohai Strait is limited (Liu et al., 2008).
2.7.4. Nutrient exchange at sediment and overlying
seawater interface
Nutrient regeneration and exchange at sediment and overlying seawater interface is an important source of nutrients(Cowan et al., 1996; Liu et al., 2011). Based on pore water nutrient proﬁles in the Bohai, using a two-layer diagenetic equation (Liu et al., 2003), the benthic ﬂuxes of nutrients during August 2008−2009 were calculated as follows:
162±174, −7.6±35.5, 1.0±0.8, and 145±103 × 108 mol/yr
for NH4 + , NO3 — , PO4 3— , and Si(OH)4, respectively (Liu et al.,2011). In August 2015, the benthic ﬂuxes of nutrients weresimilar at 133, −15.5, 1.4, and 240 × 108 mol/yr of NH4 + ,NO3 — , PO4 3— , and Si(OH)4 , respectively (Huang, 2016). Sediment was a source for DIN, PO4 3— , and Si(OH)4 in the Bohai. Compared to the sum of atmospheric deposition andriverine input, the benthic ﬂuxes of nutrients contributed
more PO4 3— and Si(OH)4 , and less DIN. Thus, benthic nutrient
ﬂuxes can alleviate phosphorus limitation in the Huanghe
Estuary.

2.8. Fishing pressure
2.7.2. Atmospheric nutrient depositions
Based on limited observations, concentrations and depositions of water-soluble nitrogen and phosphorus fromaerosols were reported to be higher in winter than in summer at Qinhuangdao, a coastal city in northeastern Bohai(Yu et al., 2020a). Atmospheric dry and wet depositions contributed 75.9, 70.6, 146.6, and 0. 1 × 108 mol/yr of NO3 — ,NH4 + , DIN, PO4 3— , respectively to the Bohai (China Council for International Cooperation on Environment and Development Annual Policy Report, 2020), and atmospheric DIN
depositions to the Bohai could be up to 67.2 × 109 mol/yr(Shou, 2017). Atmospheric Si(OH)4 deposition to the Bohai
was 0.2 × 109 mol/yr (Liu et al., 2008). Compared to theriverine input (including the other rivers; Liu et al., 2009),
atmospheric nutrient depositions ware 1−2 times that ofOverﬁshing has a signiﬁcantly negative inﬂuence on ﬁsheryresources in the Bohai Sea. Fishing effort is commonly used
as an indicator to reﬂect ﬁshing pressure, and ﬁshing effort
is represented by ﬁshing vessel power. While ﬁshing yield (orcatch) and ﬁshing efﬁciency can reﬂect the utilization status of ﬁshery resources, and ﬁshing efﬁciency is represented
by catch per unit effort (CPUE). Based on statistical ﬁsherydata of China from 1979 to 2017 (Fisheries Bureau of the
Ministry of Agriculture and Rural Affairs, 1979—2017), theﬁshing effort in the Bohai Sea continuously increased before
2002, which is reﬂected by the horsepower of marine ﬁshing vessels. The horsepower of marine ﬁshing vessels in the
Bohai Sea exceeded 100 million kW in 1986, 200 million kW
in 1996, and 300 million kW in 2002, then ﬂuctuated from284

Earth System Changes in Marginal Seas/Oceanologia 65 (2023) 278—296

Figure 9 Monthly average concentrations (color data points) and ﬂuxes (black lines) of nutrients in the lower reach of the
Huanghe; the linear relationship lines for dissolved inorganic nutrients are also shown. Data are from Liu et al. (2012a),
Wang et al. (2022), Wu et al. (2021), and the references therein.

285

Earth System Changes in Marginal Seas

Figure 10

The proportions (%) of different nutrient sources to the Huanghe.

239 million kW to 340 million kW with an average of 286 million kW in recent years. For catch, the trend is incompletely
consistent with the catch effort. It exceeded 1 million tons
in 1993 and reached its maximum of 1.63 million tons in
1999. In the 21st century, it has been declining continuously
and has stabilized at about 1 million tons since 2007. For
CPUE, it showed a continuous downward trend from 0.52
tons/kW to 0.39 tons/kW in the 1980s. With the continuous improvement of ﬁshing technology, the CPUE ﬂuctuatedfrom 0.39 tons/kW to 0.66 tons/kW in the 1990s. In the 21st
century, overﬁshing has deteriorated, and the CPUE showeda decreasing trend with ﬂuctuation, reaching a minimum of
0.29 tons/kW in 2017 (Hu et al., 2020). Since the 21st century, the ﬁshing pressure of the Bohai Sea has been maintained at a high level, but the high ﬁshing pressure showed
low catch, indicating the decline of ﬁshery resources in the
Bohai Sea. In recent years, the ﬁshing pressure in the Bohai Sea has decreased signiﬁcantly, but the ﬁshing efﬁciency(CPUE) has continued to decline, indicating that the reduction of ﬁshing pressure has not effectively alleviated thedeclining trend of ﬁshery resources and the ﬁshing pressure
should be continuously reduced to promote the sustainable
development of ﬁshery resources (Xu, 2011).

the annual mean of SST and SSS was 0.011 degrees/yr and0.074/yr, respectively. Increasing air temperature and reduction in river discharge are likely the main causes forthese positive trends (Lin et al., 2001). Using SST datameasured at 11 stations along the coast from 1960 to2012, the warming trend in the Bohai was reported to be
0.021 degree/yr with a high value in winter (0.03∼0.04 degree/yr) and a low value in summer (0.01∼0.02 degree/yr)(Li et al., 2018). Because a long time series of SST forthe period 1901−2004 indicates the presence of a variation period of 40−50 years in the annual mean of SST in
the Bohai (Zhang et al., 2005), it should be noted thatthe reported trend depends strongly on the length of SST
records. The increasing salinity in the Bohai (Lin et al.,2001) was conﬁrmed by other studies (Wu et al., 2004;
Yu et al., 2009). However, the Huanghe discharge increased
since 2003 (Figure 8). Although a numerical simulation suggested that its direct effect on reducing salinity was limited
to Laizhou Bay (Mao et al., 2008), the increased freshwater
should distribute over the entire Bohai after a year or more
(Liu et al., 2012b) and eventually stop the increasing trendof SSS in the Bohai. Recently, the detachment of low salinity water from the Huanghe plume in summer, which forms
an isolated patch of low salinity in the offshore area, wasreported (Yu et al., 2020b).
A strong stratiﬁcation in summer was reported in central Bohai where two cold bottom water masses were reported (Lin et al., 2006). Based on the collected data fromthe World Ocean Database for June, July, and August from1970 to 1999, the vertical gradient of water temperature
was estimated to be in the order of 0.4−0.6 degrees/m;
this stratiﬁcation intensity had a slightly decadal variationfrom 1970 to 1999 (Hu et al., 2014).

3. Status of environmental change in theBohai
3.1. Hydrological change
The rising trend of sea surface temperature (SST) and sea
surface salinity (SSS) has been recognized for twenty years(Lin et al., 2001). For the period 1960−1997, the trend of286

Earth System Changes in Marginal Seas/Oceanologia 65 (2023) 278—296
The schematic pattern for the circulation in the Bohai
can be understood from the inﬂow in the northern Bohai
Strait and the outﬂow in the southern Bohai Strait, which isthe same throughout the year (Guan, 1994). Combined withthe local currents in Bohai Bay, this exchange ﬂow forms ananti-clockwise circulation in the southern area of the Bohai,
which is also the same throughout the year. On the other
hand, the local currents in Liaodong Bay have an opposite
pattern in winter and summer. The inﬂow in the northern
Bohai Strait follows the local currents in Liaodong Bay and,
therefore, a large clockwise circulation forms from the central Bohai to Liaodong Bay in winter. However, the inﬂow in
the northern Bohai Strait cannot enter Liaodong Bay in summer and the anti-clockwise circulation is limited around thehead of Liaodong Bay.
Many studies have been undertaken to better understandthe circulation dynamics in the Bohai (Hainbucher et al.,
2004; Huang et al., 1996; Zhao and Cao, 1998; Zhou et al.,2017). The wind is the major driving force for winter circulation (Huang et al., 1996) while the horizontal density
gradients or baroclinic forcing is the major driving force forsummer circulation (Zhou et al., 2017). The tidal residual
current is also an important component of circulation, but
it exhibits a relatively large magnitude only in limited areas
close to the coast (Wei et al., 2004).
Because the variations in circulation due to climatechange are not as easily detected as water temperature andsalinity, most reports on the long-term change of circulation are limited to some local features. For example, thechange in the Huanghe summer river discharge strongly affects the circulation around the river mouth; a larger riverdischarge induces a more apparent northward or northwestward shift of diluted water and a stronger and faster currentof diluted water (Shou et al., 2016; Yu et al., 2021). Thechange in coastline and water depth can induce a magnitude of ∼0.05 m/s in the tidal residual currents close to thecoast (Dong et al., 2020).
As a climate-related phenomenon, the long-term changeof sea ice in the Bohai presents an interesting pattern. In
winter, sea ice is found in a large area of Liaodong Bay andin the coastal area of Bohai Bay and Laizhou Bay (Shi andWang, 2012). The sea ice annual maximum and averagearea presented a decreasing linear trend from 1958 to 2015
(Yu et al., 2020b), being a likely natural response to global
warming. However, there were actually three different periods with different trends during the study period: a slightly
increasing trend from 1958 to 1980, a strong decreasing
trend from 1980 to 1995, and a moderately increasing trend
from 1995 to 2015 (Yan et al., 2020). Such different trends
resulted from oscillation with a period of ∼30 years and ∼17years, associated with the Arctic Oscillation and North Atlantic Oscillation (Yan et al., 2020).

Figure 11 Annual average concentrations (μM) of nutrientsin the Bohai (Wang et al., 2019b).

occurred from mid-June to late August, driven largely bystratiﬁcation, remineralization of organic matter, and lateral water exchange (Song et al., 2020; Zhao et al., 2017)
in which pelagic respiration and sediment respiration contributed >60% and <40%, respectively (Song et al., 2020).
Although the lowest DO values in the bottom water of theBohai were still higher than the threshold for hypoxia (i.e.,<63 μmol O2 /L), there has been a summertime declining
trend since the early 1980s (Zhai et al., 2019; Zhao et al.,2017).

3.3. Nutrient characteristics and evolution trends
in the Bohai
Nutrient concentrations are generally higher in the shallow
coastal areas than in the central Bohai and Bohai Strait because of the effects of rapid population growth and economic development in the Bohai Rim region (Liu et al., 2011;
Zhang et al., 2004; Zheng et al., 2020). There are also signiﬁcant seasonal variations, with lower nutrient concentrations in summer than in winter. Nutrient concentrations arehigher in bottom layer waters than in surface waters in summer when seawater stratiﬁcation is obvious; in contrast,
nutrients are also vertically constant in well-mixed winter(Wang et al., 2019b).
The changes in concentrations and composition of nutrients observed in the Bohai are mainly related to the
Huanghe freshwater discharge together with other sources
such as fertilizer application and sewage efﬂuent (Liu et al.,2011; Ning et al., 2010; Wang et al., 2019b; Zhang et al.,2004). During 1978−2016, dissolved inorganic nitrogen (DIN)
concentrations had increased since 1990 with the rate of increase becoming even greater since 2002. During the same
period, the annual average PO4 3— concentration had generally decreased, with a declining trend in summer and a slightrise in ﬂuctuation trend in winter; the Si(OH)4 concentration
had ﬁrstly shown a slight decrease before increasing from1987 (Figure 11). Thus, the N/P ratio increased and Si/N ratio decreased, indicating that PO4 3— was a limiting nutrient
for phytoplankton growth, leading to the limiting of Si(OH)4(Wang et al., 2019b). The incubation experiments off the
Huanghe Estuary also demonstrated that photosynthesis waslimited by PO4 3— (Turner et al., 1990; Zhang et al., 2004).

3.2. Changes in dissolved oxygen
In the Bohai, the accelerated daily depletion of bottom
dissolved oxygen (DO; 2.0−2.8 μmol O2 /kg) was ﬁrst noticed in the northern coastal area between June and August 2011 (Zhai et al., 2012). In August 2014, the low DO(<92 μmol O2 /kg) was reported as covering an area of
756 km2 , with an average water depth of 10.3 m above
the seabed (Zhao et al., 2017). Oxygen depletion mainly
287

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3.4. Water quality status in the Bohai

3.4.2. Status of sea water quality
Based on national standards, sea water quality is classiﬁed into four types according to function and protection
objectives: Grade 1 applies to marine ﬁshing, nature reserves, and rare and endangered protected regions; Grade
2 applies to aquaculture, bathing beaches, marine sports
and/or recreation directly contacting water, and industrial
use of water for food; Grade 3 applies to the waters affected by general industrial use and to scenic seashore
areas; and Grade 4 applies to waters used for marine
ports and development. The seawater quality of the Bohai went through three stages, from good overall to deteriorated, followed by gradual improvement along withthe continued acceleration of coastal socio-economic development, an increase in the scale and intensity of resource utilization, and changes in ecosystem management
and protection (Figure 6). At the start of the political andsocio-economic reform since 1978, the ecological environment was good. From the 1990s to 2012, marine ecosystem quality deteriorated because of eutrophication, pollution, aquaculture development, land reclamation, and land
use change due to intensiﬁed and low resource use efﬁciency during ocean exploitation (Su and Tang, 2002). During that period, the seriously polluted sea area extended
to 1.3 × 104 km2 , representing 17% of the Bohai surface
area. Since then, the marine ecological environment has improved, related to intensiﬁed pollution control and ecological restoration with the seriously polluted sea area decreasing to 1000 km2 , representing only 1.3% of the Bohai in 2019
(Figure 6).

3.4.1. Status of environmental parameters
National sea water quality standards cover 35 sets of parameters, the principal ones being smell, taste, suspended
particulate matter, E. coli, fecal coliform, pathogens, water temperature, pH, dissolved oxygen, chemical oxygen
demand (COD), DIN, PO4 3— , cadmium, mercury, zinc, copper, lead, cyanide, sulﬁde, total petroleum hydrocarbon,
DDT, BaP, methyl parathion, and radionuclides (60 Co, 90 Sr,
106
Rn, 134 Cs, 137 CS; National Sea Water Quality Standardsof the P. R. China, 1997). As examples, and based on observation data, several sets of environmental parameters
are addressed for levels of organic matter, trace metals,
petroleum hydrocarbons, and microplastics.
The concentrations of dissolved organic carbon (DOC) inthe surface water of the Bohai were 130.2−407.7 μM withan average of 225.9±75.4 μM in April 2010 (Chen et al.,2013). The concentrations of particulate organic carbon(POC) were 315−588 mg m—3 with seasonal patterns being
highest in spring and lowest in winter in the Bohai surface
water during 2002−2016. The POC concentration showed adecreasing trend prior to 2012, with an increasing trend until 2015, affected mainly by primary production and terrestrial inputs (Fan et al., 2018).
Using trace metal clean sampling and analytical techniques, several dissolved trace metals during summer inthe Bohai were reported to be 15.1−30.4 nM, 10.9−23.1
nM, 0.72−1.37 nM, 0.091−1.00 nM, 0.6−3.3 pM, 2−26 pM,
and 51−189 pM for Cu, Ni, Cd, Co, Zn, Ag, and Pb, respectively (Li et al., 2015, 2017). Trace metal levels weremainly affected by atmospheric deposition and riverine discharge (Liang et al., 2018), with their inﬂuence decreasing
due to air pollution management and a decrease in freshwater discharge from major rivers emptying into the Bohai.
In general, the concentrations of trace metals are at a pristine level in the Bohai in contrast to the other coastal seas
(Li et al., 2015, 2017).
Total petroleum hydrocarbon concentrations were23.7−508 μg/L in Bohai Bay with the highest levels in winter and the lowest in summer (Li et al., 2010). Marine oiland gas exploration increased methane concentrations by
up to 4.7 times in surface water (Zhang et al., 2014). Thus,
the Bohai was a source of atmospheric methane with sea
surface CH4 concentration of 2.27−25.63 nmol kg—1 and asaturation ratio of 107−1193% (Zhang et al., 2014). In general, petroleum hydrocarbon levels steadily decreased during 1996—2005 due to the decline of many industrial activities and a pollution control program in the Bohai Rim region(Li et al., 2010). Especially, ships are prohibited from directly discharging oily sewage into the water body in the
Bohai, and the sewage discharge equipment is subject tolead-sealing management.
Microplastics are distributed widely in the Bohai withconcentrations of 0.01−1.23 particles/m3 (an average of
0.33 ± 0.34 particles/m3 ), which included 51% polyethylene, 29% polypropylene, 16% polystyrene, 3% polyethylene
terephthalate, and <1% polyvinyl chloride, polyurethane,
and acrylonitrile, respectively (Zhang et al., 2017). The microplastic content is at a medium-low level in the Bohai
compared to other continental margins (Zhang et al., 2017).

4. Ecosystem responses to environmental
change4.1. Changes in phytoplankton composition andharmful algal blooms
The Bohai is an important ﬁsh habitat and sea farm base.
However, the ecosystem of the Bohai has changed sincethe 1950s, threatening the sustainability of this ﬁshery.
Along with environmental change, phytoplankton composition has changed signiﬁcantly since 1959 (Luan et al.,2018; Sun et al., 2002). Phytoplankton cell abundanceswere 8.33−472 × 104 cells/m3 , with diatoms accounting for65.3−99.8% (average 92.5%) during 1959—2015, in which average phytoplankton abundances were 168, 216, 101, 28.0,
and 68.7 × 104 cells/m3 in the 1960s, 1980s, 1990s, 2000s,
and 2010s, respectively (Figure 12). The abundance andspecies diversity declined in the last century before recovering in the 2000s. Phytoplankton succeeded from diatomdominated communities with mainly centric diatoms suchas Coscinodiscus spp. and Chaetoceros spp. to communities
co-dominated by diatoms (Thalassionema spp., Paralia sulcata) and dinoﬂagellates (such as Tripos spp. and Noctiluca
scintillans). Accordingly, there is an increase in the ratio of
dinoﬂagellates to diatoms in this century compared with lastcentury, with average dinoﬂagellates to diatoms ratios of
0.34, 0.16, 0.97, 1.52, and 1.24 in the 1960s, 1980s, 1990s,
2000s, and 2010s, respectively (Figure 12). Moreover, phytoplankton biomass appeared in two peaks annually during

288

Earth System Changes in Marginal Seas/Oceanologia 65 (2023) 278—296

Figure 12Long-term phytoplankton abundance and the ratio of dinoﬂagellates to diatoms (Luan et al., 2018).

Figure 13 The occurrence frequency (times, black line) and spatial extent (km2 , orange bar) of harmful algal blooms in the Bohai
from 2000 to 2019 (data source: http://english.mee.gov.cn/Resources/Reports//bomeaesoc/202012/P020201225370164112761.
pdf).

4.2. Changes in zooplankton composition

1959—1999 (Fei et al., 1991). Since 2002, the second bloomof phytoplankton has been initiated earlier due to the effects of the Huanghe WSREs evidenced by only one peakof the surface Chl-α in spring-summer (Ding et al., 2020a;
Liu et al., 2012a).
Harmful algal blooms (HAB) in the Bohai occurred mainly
from June to August 1952—2014 when there were 142 times
in total, with nearly 13% of HAB events covering an areaof over 1000 km2 (Song et al., 2016). The frequency andspatial extent of HAB outbreaks had increased signiﬁcantly
since 2000 although these have decreased in recent years(Figure 13). The dominant HAB causative species include Aureococcus anophagefferens, Gyrodinium spirale, Noctiluca
scientillans, Prorocentrum dentatum, Skeletonema costatum, and Phaeocystis globosa (Song et al., 2016; Xu et al.,2017; Zhang et al., 2012). Moreover, a green tide caused
by Ulva prolifera occurred near Qinhuangdao, threatening
the ecosystems and the tourism of the western coast of theBohai (Han et al., 2019).

The study of zooplankton composition and distribution characteristics in the Bohai began with the National Comprehensive Marine Survey in 1958−1960 (Ofﬁce of Marine Comprehensive Survey, 1977). In the Bohai, dominant zooplankton species are copepods (such as Paracalanus parvus, Centropages mcmurrichi, Calanus sinicus, and Labidocera euchaeta) and chaetognatha (Sagitta crassa). Warm water
species such as copepods (Euchaeta rimana and Pontellaspinicauda), salps (Cyclosalpa pinnata and Brooksia rostrata), and chaetognatha (Sagitta enﬂata) were also observed mainly in winter (Bi et al., 2000) when the Yellow Sea Warm Current water is the strongest. Zooplankton abundance peaked in summer and two minor peaks inspring and autumn with dominant species of Paracalanus
parvus and Paracalanus crassirostris in summer, Acartia biﬁlosa in spring, and Oithona similis in autumn, respectively(Bi et al., 2001).
289

Earth System Changes in Marginal Seas
Limited data imply that zooplankton abundance washigher in spring-summer of the late 1990s than those during
the 1950s to the early years of the 1990s (Tang et al., 2003),
but the long-term changes of zooplankton biomass in the Bohai have not yet been unraveled, except for some regions of
the Bohai. In the Caofeidian coastal area in the northwest of
the Bohai, zooplankton biomass showed an increasing trend
according to observations in 1959, 1984, 1990, and 2004
(Wang et al., 2015a). Monthly observations in Laizhou Bay,an important spawning, nursery, aquaculture, and recruitment region, indicated that abundant zooplankton species
succeeded; i.e., the abundant copepod Calanus sinicus, including C1-CV copepodites and adults, reproduce all year
round, peaking in May and June (Zuo et al., 2017a), with
Paracalanus parvus peaking in August (Wang et al., 2015b).
Since 2000, Centrapages dorsispinatus has become the only
dominant species of Centrapages from June to November,with a peak in September, replacing the previously dominant species, Centrapages tenuiremis (Zuo et al., 2017b).
Since the 2000s, giant jellyﬁsh blooms caused by species
Nemopilema nomurai, Cyanea nozakii and Aurelia aurita
have been observed frequently in the Bohai (Dong et al.,2010; Wu et al., 2017b; Zheng et al., 2014). Increased giant jellyﬁsh abundance caused changes in jellyﬁsh composition; for example, the abundance of the edible jellyﬁsh Rhopilema esculenta decreased with the increase of
Nemopilema nomurai (Wu et al., 2017b; Zheng et al., 2014).
Even human health and routine activities are threatened;in the summer of 2013, a giant jellyﬁsh Nemopilema nomurai bloom occurred near Qinghuangdao causing approximately 1000 cases of human sting accidents and the deathof one child (Wu et al., 2017b). In the summers of 2013 and2020, the inﬂowing cooling water for the Hongyanhe Nuclear
Power Plant in Liaoning Province was blocked by the jellyﬁsh Aurelia aurita, temporarily disrupting the operation of
the nuclear reactor (Qiu et al., 2020).

average rate of 0.17/decade in the last three decades ofthe last century, which was higher than the global trend(Zhang et al., 2007). In the Bohai, the food web has simpliﬁed (Shan et al., 2016), and the maturity of the ecosystems has declined, according to the comparison of the initial (1982) and end states (2008) of the Ecosim model, incorporating 17 functional groups (Lin et al., 2016). Fishingand environmental changes were regarded as the main factors affecting the changes in ﬁshery resources of the Bohai(Lin et al., 2016).

5. Societal responses to changing
biogeochemistry and ecosystems
5.1. The water-sediment regulation scheme
Since 2002, the WSREs have been instituted to reduce sediment deposition in the Xiaolangdi Reservoir and the lower
reaches of the Huanghe. The WSREs have generally attained their aim, i.e., inducing bed erosion in the lower
reach of Huanghe and mitigating siltation in the reservoir(Wang et al., 2017). However, the regulation events have
led to unexpected disruptions, including high monthly water
discharge values, with sediment load, and nutrient transports occurring two months earlier than was the case before
the WSRE interventions; this has led to aggravated nutrient
imbalance in the Huanghe Estuary and the Bohai (Liu et al.,2012a; Liu, 2015). However, the WSREs are not sustainable
due to continuous sediment siltation in the reservoir andthe sediment coursing in the downstream riverbed, which
impedes sediment escape from the reservoir and impedes
sediment transport downstream (Wu et al., 2020). The WSREs will, therefore, require modiﬁcation.

5.2. Coastline protection and management

4.3. Changes in ﬁshery resources

Sea reclamation and coastline change have a profound
impact on the ecological environment of the Bohai,such as diminished intertidal wetlands and ﬁsh habitats
lost/fragmented (Duan et al., 2016; Hou et al., 2016). In
July 2018, the State Council of China issued a directive
to strictly control reclamation to protect the coastline andits ecosystems. Moreover, measures, including the "Grain—
for—Green" Program issued in 1999 to increase vegetation
coverage, reduce erosion, and restore degraded ecosystems(Feng et al., 2016; Wang et al., 2016), can also decrease thesediment load to the rivers and the adjacent Bohai, thus alleviating coastline change and area shrinkage of the Bohai.

Along with changes in the environment and with plankton composition in the Bohai, ﬁshery resources have also
experienced decreases in biomass and changes in species
composition (Jin, 2020; Ning et al., 2010). The serious decline of ﬁshery resources was ﬁrst noticed during the early
1990s when no egg of the Chinese shrimp Penaeus chinensis was collected in the Bohai, where there was an important spawning and nursery habitat for this species (Su andTang, 2002). Based on monthly investigations of horizontal
trawls during 1982 to 2019, the species number and abundance index of ﬁsh eggs and larvae showed a decline in
the 20th century with an increase in recent years (except
in winter; Bian et al., 2018). In the Bohai, the dominant ﬁsh
species had shifted from 1959 to 2010. Since then, largesized and economically dominant species (such as the largehead hairtail Trichiurus lepturus and small yellow croaker
Larimichthys polyactis) have been substituted by smallsized and low-trophic-level species (such as the hairﬁn anchovy Setipinna tenuiﬁlis and Japanese anchovy Engraulisjaponicus), driven by both top-down effect (increasing ﬁshing pressure) and bottom-up effect (substantial environmental variations; Bian et al., 2018; Jin, 2020; Shan et al.,2016). The mean trophic level in the Bohai reduced at an

5.3. Pollution control and prevention
To restore and sustain the ecosystems of the Bohai, integrated management of the Bohai is necessary, including controlling pollutants from land-based sources and preventing
marine pollution. For example, the main DIN and PO4 3— inputs to the Huanghe and adjacent Bohai were excess fertilizer run-off and sewage efﬂuent. In 2015, the Ministryof Agriculture of China (now called Ministry of Agriculture
and Rural Affairs of China) issued a directive calling for zero290

Earth System Changes in Marginal Seas/Oceanologia 65 (2023) 278—296

Figure 14

The interlinkage of the drivers and pressures on the environmental state variables and social responses as well.

to September 1 during 1995−2016 and then from May 1
to September 1 since 2017, combined with stock enhancement, has, to some extent, played a role in restoring ﬁsheryresources. The ﬁsh species composition in the Bohai was affected by both top-down and bottom-up effects (Shan et al.,2016); a closed ﬁshing season can be an effective way torestore ﬁshery resources besides controlling pollutant emissions and protecting the environment. Moreover, with thecurrent ﬁshery resources conﬂicts in the Bohai, the development of equitable quota allocation schemes is necessary
if long-term ecological health and sustainability are to beachieved (Ding et al., 2020b). A complete 10-year ﬁshingban was issued by the Ministry of Agriculture and Rural Affairs of China to protect the biodiversity of the Changjiang

growth of synthetic fertilizer application after 2020 and provided an upper limit for fertilizer application. Ameliorating
the methods of fertilizer application and improving sewage
treatment technology can reduce nutrient input into the
Huanghe and the Bohai.

5.4. Fishery resources management andgovernance
The health of ﬁshery resources reﬂects the status of broader
ecosystems. The ultimate aim of integrated marine management is to restore ﬁshery resources and biodiversity. A
summer ﬁshing ban, which was implemented in the Bohai
during the ﬁsh nursing and spawning periods from June 1291

Earth System Changes in Marginal Seas
(Yangtze River), starting on Jan 1 2020; this might provide
useful experience and insight for the development of strategies to restore ecosystem and ﬁshery resources in the Bohai.
The conservation of ﬁshery resources and the restorationof water ecosystems is a complex task. A ﬁshing ban only
goes so far, so further integrated and systematic measures
must be carried out, especially the prevention and control
of pollution. In addition, the wetlands and estuaries provide
crucial habitats for marine living organisms; protecting andrestoring these wetland and estuary ecosystems can be vital for the restoration of the ﬁshery resources of the Bohai.
Lastly, controlling sea reclamation is crucial to the protection of the wetlands and shoreline.

the ﬁshery resources, including pollution control and protecting and restoring coastal ﬁsh habitats.

7. Summary and knowledge gaps
The ecological environment of the Bohai has been alteredby human activities and climate change. Urgent tasks include natural coastline protection and restoration; management of sea-based activities such as aquaculture, recreation and sea reclamation; integrated land-ocean pollution management; biodiversity conservation to enhance theprotection and effective use of coastline ecosystems andresources; promoting the health and sustainable development of coastal areas; as well as encouraging public participation and bottom-up initiatives. A quantitative understanding of biogeochemistry-ecosystem-social interactions
is also vital, including projections of human activities andfuture resource use, the potential risks from increased human activities, and the effectiveness of governance andmanagement of sustainability strategies. Various models delineate changing biogeochemistry and its potential effects
on ecosystems; coupled biogeochemistry-ecosystem-social
models, in particular, are needed to help ensure the sustainability of the Bohai ecosystems. This study is vital to understand how to mediate future human- induced changes in the
Bohai and extrapolate globally to predict and prevent similar marginal seas from experiencing major environmental
changes.

6. Cause-and-effect relationships
As discussed above, the Bohai ecological environment has
been signiﬁcantly modiﬁed by multi-stressors. To better understand the impacts of the variety of stressors, the interlinkage of the drivers and pressures on the environmental
state variables and social responses as well has been visualized (Figure 14). Mainly driven by climate change (air temperature increased) and generally decline in riverine freshwater discharge, SST and SSS have increased. Therefrom,the wintertime sea ice area has decreased but the summertime stratiﬁcation has increased. With societal basic needsof seafood, economic demand, and urbanization, extensive
sea reclamation (i.e. increases in aquaculture, salt pans,and construction land) in the Bohai Rim region has led todecrease in the total sea area of the Bohai and morphology
change. Moreover, extensive cultivation in the loess plateauof the Huanghe has led to abundant sediment load transported into the Bohai. As a result, tidal regime has changed,
intertidal wetlands have diminished, and essential ﬁsh habitats have lost and/or fragmented. Fortunately, strictly control reclamation has been issued to protect the coastline
and its ecosystems, and the “Grain-for-Green” program has
been issued to increase vegetation coverage and reduce
erosion.
Nutrient concentrations and composition have changed
due to fertilizer application and wastewater discharge.
Moreover, seasonal patterns of riverine nutrient ﬂuxes into
the Bohai affect dynamics of nutrients and seasonal variations of Chl-α in the Bohai. Pollution control and prevention, e.g. calling for zero growth of synthetic fertilizer application could decrease nutrient levels and reshape nutrient composition in the Bohai. To know its effects, it isnecessary to keep a continuous and long monitor on theecosystems of the Bohai, which have changed along withenvironmental change, including phytoplankton and zooplankton composition and ﬁshing resources. Besides environmental change, overﬁshing has signiﬁcantly negative inﬂuence on ﬁshery resources, which have experienced decreases in biomass and changes in species composition withlarge-sized and economically dominant species substituted
by small-sized and low-trophic-level species (Bian et al.,2018; Jin, 2020; Shan et al., 2016). Ongoing summer ﬁshing bun and stock enhancement can be an effective way torestore ﬁshery resources to some extent. Further integrated
and systematic measures can be vital for the restoration of

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.

Acknowledgements
This work was funded by the National Natural Science Foundation of China (NSFC: U1806211, 41776087), the Aoshan
Talents Program supported by Qingdao National Laboratory
for Marine Science and Technology. X. GUO thanks Drs. Ding
Xiaokun and Yu Xiaojie for the assistance and the support by a Grant-in-Aid for Scientiﬁc Research (MEXT KAKENHI grants: 20KK0239). This study is a contribution to the
IMBeR/FEC-CMWG Program.

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