Estuarine, Coastal and Shelf Science 151 (2014) 355e360

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Estuarine, Coastal and Shelf Science

journal homepage: www.elsevier.com/locate/ecss

Looming hypoxia on outer shelves caused by reduced ventilation in

the open oceans: Case study of the East China Sea
Hon-Kit Lui a, Chen-Tung Arthur Chen a, b, c, *, Jay Lee a, Yan Bai c, Xianqiang He c
a

Department of Oceanography, National Sun Yat-Sen University, Kaohsiung 80424, Taiwan

Institute of Marine Chemistry and Environment, Zhejiang University, Hangzhou, China
c
State Key Laboratory of Satellite Ocean Environment Dynamics, Second Institute of Oceanography, State Oceanic Administration, Hangzhou, China
b

a r t i c l e i n f o

a b s t r a c t

Article history:
Accepted 12 August 2014
Available online 21 August 2014

The discharge of nitrate and phosphate from Changjiang (Yangtze River) has increased in recent decades.
Eutrophication off the mouth of Changjiang has subsequently become a serious problem, as evidenced by
the hypoxia area reaching 12,000 km2. This study demonstrates that in the wide East China Sea (ECS) the
nitrate and phosphate concentrations in the Kuroshio Intermediate Water (KIW) have also increased, but
the dissolved oxygen (DO) concentration has decreased since as early as 1982, most likely owning to
reduced ventilation in the North Pacic Intermediate Water (NPIW). Conversely, the Kuroshio Tropical
Water (KTW) has decreased in the nitrate and phosphate concentrations yet increased in DO concentration. As KIW contributes substantially to the upwelling, the nitrate and phosphate concentrations in
the bottom water on the outer shelf of the ECS appear to have increased as well, but the DO has
decreased. Given that the nutrient inputs from both the land and the Kuroshio Current have increased,
yet the input of DO from the Kuroshio has decreased, more severe eutrophication and hypoxia may occur
in the entire ECS. Similar processes may also affect other shelves that come into contact with NPIW.
2014 Elsevier Ltd. All rights reserved.

Keywords:
ventilation
East China Sea
eutrophication
hypoxia
Kuroshio
nutrient

1. Introduction
As is widely recognized eutrophication and related hypoxia
(dissolved oxygen (DO) < 2 mg L!1 or <30%) adversely impact
marine ecosystems (Howarth, 2008; Rabalais et al., 2010; Lui and
Chen, 2012). As the most sensitive and rst to be affected, coastal
regions suffer from increasing terrestrial inputs of nutrients and
organic matter. Recent decades have witnessed a several folds increase in riverine nitrate and phosphate uxes over their original
values (Howarth, 2008; Conley et al., 2009). Such nutrients are
largely consumed by phytoplankton in the river plume from spring
to summer. Stratication of seawater during the summer reduces
bottom seawater ventilation. Consequently, in addition to
consuming DO at the bottom, decomposition of the settled organic
matters causes hypoxia when the oxygen at the bottom is insufciently replenished. In 1970, 60 coastal ecosystems were reportedly

* Corresponding author. Department of Oceanography, National Sun Yat-Sen

University, Kaohsiung 80424, Taiwan.
E-mail addresses: hklui@staff.nsysu.edu.tw (H.-K. Lui), ctchen@mail.nsysu.edu.
tw (C.-T.A. Chen).
http://dx.doi.org/10.1016/j.ecss.2014.08.010
0272-7714/ 2014 Elsevier Ltd. All rights reserved.

under hypoxia, subsequently increasing to over 400 in 2007, when

they covered more than 245,000 km2 of the sea bottom (Diaz and
Rosenberg, 2008). Strengthening stratication of seawater under
global warming and increased nutrient uxes from terrestrial
sources are expected to exacerbate the above situation (Diaz and
Rosenberg, 2008; Chen, 2008a; Rabalais et al., 2010).
In the case of coastal eutrophication, incoming offshore
seawater has rarely been addressed. Although surface seawater
offshore generally contains low nutrient concentrations, the upwelled subsurface offshore seawater is a major source of nutrients
and DO to coastal regions and marginal seas (Feely et al., 2008;
Bauer et al., 2013; Yang et al., 2013), such as in the East China Sea
(ECS), one of the world's most productive marginal seas (Chen,
1996, 2008b).
Changjiang (Yangtze River) contributes roughly 90% of all
freshwater discharge to the ECS, and possibly the same proportion of land-derived nutrients as well (Chen and Wang, 1999).
However, it has been reported that the dominating source of
nutrients to the ECS, even all the way to the coast, comes from
the upwelling of subsurface waters from the Kuroshio Current
(Chen, 1996; Yang et al., 2013). Consider phosphate (PO3!
4 ) as an
example, in which the upwelled subsurface seawater from the

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Kuroshio Current contributes ten times more than all rivers

entering the ECS combined (Chen, 1996; Chen and Wang, 1999).
Correspondingly, any change in the nutrient concentration in the
subsurface of the Kuroshio seawater could signicantly impact
the nutrient dynamics on the ECS continental shelf. According to
a previous study, the nitrate (NO!
3 ) concentration in the middle
layers across the Kuroshio Current in the Okinawa Trough in the
ECS is also increasing, yet with a decreasing DO (Guo et al., 2012).
This study attempts to quantify the temporal rates of changes in
3!
DO, apparent oxygen utilization (AOU), NO!
and
3 , PO4
chlorophyll-a (Chl-a) concentrations, potential temperature (q),
and salinity (S) along the PN-line section (Fig. 1) with the rstorder simple linear regression (SLR) method. The distinguishing
patterns of changes between Kuroshio Intermediate Water (KIW)
and Kuroshio Tropical Water (KTW) are also described. Implications for the changes in the coastal eutrophication and hypoxia
are discussed as well.
2. Study area, dataset and methods
As one of the largest marginal seas and one of the most productive shing grounds worldwide, ECS is supported by nutrients
largely from the upwelled KIW and the Yangtze River (Chen, 1996).
In the eastern region of ECS, oceanographic observations have been
made regularly along a section, i.e. the PN line, by the Nagasaki
Marine Observatory of the Japan Meteorological Agency (JMA). The
PN-line data are generally collected on a quarterly basis each year.
Generally, time-series of each parameter has similar sampling
density and distribution at each station and depth. The data is
available in the website: http://www.data.kishou.go.jp/kaiyou/db/
vessel_obs/data-report/html/index_e.html.
In order to reduce inuences of the seasonal variations on
determining rates of temporal changes for each parameter,
3!
anomalies in q, S, DO, AOU, NO!
3 , PO4 and Chl-a are calculated.
Using the same classication of seasons as Guo et al. (2014), seasonal means of each parameter at each station and depth are
calculated by averaging each parameter at each station and depth

from March to May for spring, from June to August for summer,
from September to November for autumn, and from December to
February for winter. The anomalies are dened as observed data
minus seasonal mean.
The widely-used SLR method is used to model the long term
temporal changes in the anomalies at each station and depth. The
SLR model is in a general form as y y# mt, where y# is the
intercept, m is the slope, and t is time in the y anomaly vs. t plot. The
m value refers to an average rate of temporal change in y.
In this study, vertical distributions as well as rates of temporal
3!
changes in anomalies of q, S, DO, AOU, NO!
3 , PO4 , and Chl-a concentrations are provided, based on data from the PN line (126# E,
29# Ne128.3# E, 27.5# N) between 1982 and 2010 (1988e2010 for
!
3!
PO3!
4 data). Owing to the lack of NO3 and PO4 data before 1988,
average values and rates of temporal changes in anomalies of NO!
3
(only at station 30 ) and PO3!
4 are determined with data between
1988 and 2010. Variation in the sampling location at each station is
less than 0.03# . Statistical results are shown in the Supplementary
Table 1.
3. Results and discussion
3.1. Spatial distributions and upwelling of KIW
Fig. 2 shows the plot of the annual average q vs. average S at each
depth between 1982 and 2010. Obviously, the qeS distribution of
seawater along the PN-line is between that of the West Philippine
Sea (WPS) and the South China Sea (SCS). Generally speaking, the
WPS seawater mixes with the SCS seawater off the Luzon Strait
(Chen and Wang, 1998; Chen, 2005). Those waters ow off the
eastern coast of Taiwan into the ECS as the Kuroshio Current. Mixed
with surface and subsurface seawaters of the WPS and SCS, the
seawater with a maximum S of 34.85 is the KTW (Fig. 3). Mixed
with the WPS Intermediate Water (WPSIW, originated from the
North Pacic Intermediate Water (NPIW)) and the SCS Intermediate
Water (SCSIW), the seawater with a S minimum of 34.32 is the KIW
(Fig. 3). Besides the stations on the shelf (Stns. 6e40 ) which show

Fig. 1. Map of study area and station locations.

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357

concentrations decrease and increase with depth, respectively,

and the lower DO but higher AOU subsurface waters upwell toward the shelf. Fig. 4e and f also shows the upwelling of NO!
3 and
!
PO3!
4 between 1982 and 2010, respectively. Obviously, NO3 and
PO3!
4 concentrations at a few hundred meters are more than a
factor of ten higher than those found at the surface. It follows
that any upwelling of these subsurface waters would contribute
signicantly to the nutrient budget in the surface euphotic zone.
Fig. 4g shows the annual average Chl-a concentration. Obviously,
the surface shelf water contains a relatively high Chl-a
concentration.
3.2. Distributions of rates of temporal changes in KIW and KTW

Fig. 2. Average q vs. average S at each sampling depth at the PN-line stations between
1982 and 2010. The red and blue lines represent typical West Philippine Sea (WPS) and
South China Sea (SCS) water masses. (For interpretation of the references to color in
this gure legend, the reader is referred to the web version of this article.)

large variabilities, seawater at the PN-line has stable and uniform

qeS properties (Fig. 2). Fig. 3 shows a conceptual image of the
currents mentioned.
Fig. 4a shows the distribution of the annual average q between
1982 and 2010. The q distribution is characterized by slanted
isotherms, which tilt upward toward the west, reecting upwelling of the subsurface waters. Fig. 4b shows the distribution of the
annual average S, also between 1982 and 2010. On the deep,
continental slope side is the Kuroshio Current which ows
northeastward. Centered at a depth of 150e200 m is the KTW
with a maximum S of 34.85 extending westward to the shelf
break. Below the KTW is the broad KIW with a minimum S of
34.32 centering at the depth between 600 and 800 m. The KTW
and KIW upwell along the continental slope. Upwelled subsurface
waters reach the shelf break, and enter the shelf by hugging the
bottom. The fresher surface water with a S below 34.32 is the
surface shelf water.
Fig. 4c and d shows the distributions of the annual average
DO and AOU between 1982 and 2010. The DO and AOU

Linear regression results indicate that rates of temporal changes

3!
in anomalies of DO, AOU, q, S, NO!
3 , as well as PO4 have distinguished patterns of distribution in KTW and KIW (Fig. 5aef). AOU
refers to the difference between the saturated DO concentration
and the observed DO concentration, revealing the amount of oxygen consumed since seawater is last under the air-sea equilibrium.
Obviously, KIW has been decreasing in DO and q, yet increasing in
3!
AOU, NO!
3 and PO4 . Additionally, similar to the S, these trends
extend from the deep water region to the slope and ultimately
reach the bottom of the continental shelf.
The core of the KIW (with S minimum) locates at about 800 m
depth at Stn. 1 and tilts upward toward the west to a depth of about
600 m at Stn. 30 (Fig. 4b). Notably, the maximum rate of DO anomaly
change of around !0.15 mmol kg!1 yr!1 (Fig. 5a) is located at a
depth of around 200 m above the core of KIW (Fig. 4b). Interestingly, at this depth, the maximum rates of changes in AOU, q, NO!
3
and PO3!
4 anomalies are also located. Such results may simply be
owing to enhanced vertical mixing between the lower DO yet
higher nutrients KIW and waters above. The isolines of these
changes extend upward toward, and enter, the continental shelf.
Clearly, these signals are inter related, and have affected the bottom
of the outer continental shelf. Next, KTW is examined before
returning to KIW.
The temporal variations for KTW and the waters above it
generally mirror those of KIW. Restated, when DO and q decrease
3!
and NO!
3 and PO4 increase in KIW these values change oppositely
for more near-surface waters. Notably, warming reduces DO by
reducing the solubility of oxygen. The rates of temporal change in q
anomaly between the surface seawater and 200 m are similar with
an average of 0.03 0.01 # C yr!1. Such a warming rate, i.e. two
times the global ocean warming rate of 0.013 # C yr!1, is lower than
the observation based on the U.K. Meteorological Ofce Hadley
Centre dataset (Belkin, 2009).
3.3. Increasing DO of KTW due to increased productivity

Fig. 3. Conceptual frameworks for physical and chemical changes in seawaters in the
East China Sea (ECS). The KIW is the Kuroshio Intermediate Water, KTW is the Kuroshio
Tropical Water, NPIW is the North Pacic Intermediate Water, SCSIW and the SCSSW
are the South China Sea Intermediate Water and Surface Water, respectively.

The line of zero rate of temporal change in q anomaly is located

between KTW and KIW (Fig. 5c). Unexpectedly, KTW and the waters above have increased in DO concentration under seawater
warming. Consider surface seawater as an example, in which a
warming rate of ca. 0.03 # C yr!1 (Fig. 5c) causes a decreasing (rather
than increasing) DO rate of !0.11 mmol kg!1 yr!1 based on the
solubility of oxygen. Freshening in S increases DO concentration by
increasing its solubility. Although three times higher than that
found in the northwest Pacic Ocean (Durack et al., 2012), the
freshening rate of !0.006 yr!1 in S at the surface (Fig. 5d) yields an
increasing rate in DO of only 0.001 mmol kg!1 yr!1. In other word, as
discussed below, other factors must have increased DO in the KTW
and the waters above.
Production and subsequent decomposition of organic matter
naturally change DO and AOU. Enhanced productivity may

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H.-K. Lui et al. / Estuarine, Coastal and Shelf Science 151 (2014) 355e360

3!
Fig. 4. Distributions of average (a) q, (b) S, (c) DO, (d) AOU, (e) NO!
3 , (f) PO4 , and (g) Chl-a concentrations.

explain the increasing DO yet decreasing AOU of the abovementioned near-surface waters. While moving westward from
the two easternmost stations (Stations 1, 2) which are likely the
least affected by the upwelled KIW, the rates of temporal changes

in NO-3 and PO3!

4 concentrations between the surface to 250 m
depth shifts from decreasing trends to increasing trends (Fig. 5e,
f). Correspondingly, Chl-a shows an increasing trend (Fig. 5g) in
that layer.

3!
Fig. 5. Distributions of rates of temporal changes in anomalies of (a) DO, (b) AOU, (c) q, (d) S, (e) NO!
3 , (f) PO4 , and (g) Chl-a concentrations.

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359

Typical biological uptake due to photosynthesis, or the organic

matter decomposition due to microbial respiration is as follows:

3.4. Increasing nutrients yet decreasing DO under reduced

ventilation and its implications

!
106CO2 122H2 O 17H 16NO!
3 H2 PO4

Recent studies based either on direct observations or modeling

have demonstrated that subsurface water in the open ocean has
decreased in DO content in recent decades, possibly owing to
reduced seawater ventilation under global warming (Ono et al.,
2001; Deutsch et al., 2006; Whitney et al., 2007; Pierce et al.,
2012; Takatani et al., 2012). Obviously, an input of offshore
seawater with a lower DO yet higher nutrients and AOU exacerbates coastal eutrophication and spreads the hypoxia. As
mentioned before, Fig. 3 shows conceptual frameworks for physical
and chemical changes in seawater in the ECS.
In the northeast Pacic Ocean, DO at the Ocean Station Papa
(OSP) has decreased by 0.39e0.70 mmol kg!1 yr!1 on density surfaces (sq 26.3e27.0) between 100 and 400 m in water depth
(Whitney et al., 2007). Having a similar study period and using data
also from the JMA, recent study has indicated that the DO concentration of the North Pacic Intermediate Water (NPIW) has a
maximum decreasing rate of !0.36 0.08 mmol kg!1 yr!1 on the
potential density level of s 27.3 between 1985 and 2010 (Takatani
et al., 2012). In this study, the average rate of temporal change in DO
for KIW (S ( 34.35, s 26.7e27.1, at depths ca. 500e800 m)
is !0.11 0.07 mmol kg!1 yr!1 between 1982 and 2010. The
maximum rate of change in DO (rate ) !0.15 mmol kg!1 yr!1)
is !0.19 0.02 mmol kg!1 yr!1 on the potential density level of
s 24.7e27.0 (average 26.3 0.7) (Fig. 7). These values are
signicantly lower than that of NPIW. However, as mentioned
above, the maximum rate of changes for measured parameters
(including DO) in the study area is located 200 m above KIW. Some
vertical mixing between KIW and waters above, which has a
smaller decreasing rate in DO, may partially explain why the
maximum
rate
of
temporal
change
in
DO
(!0.19 0.02 mmol kg!1 yr!1) in the Kuroshio Current is smaller
than that found in NPIW. Moreover, as is expected, data in the study
area reect only what were observed in NPIW a few years earlier
when the effect of reduced ventilation was smaller.
KTW and the KIW both originate from the North Pacic with
inuences from the SCS (Chen and Wang, 1998; Chen, 2008b). SCS

CH2 O106 NH3 16 H3 PO4 138O2

Because the biological uptake and organic matter decomposition are two of the major processes governing the changes in C, DO,
3!
AOU, NO!
in the oceans, these changes in the open
3 and PO4
oceans, as well as in the ECS, generally agree well with the stoi3!
chiometric relationship that DC:DO2:DNO!
is about
3 :DPO4
106:!138:16:1. Fig. 6 shows that rates of temporal changes in NO!
3
and PO3!
4 anomalies are consistent with the ratio of 16:1. This is to
3!
say, rates of changes in anomalies of NO!
3 and PO4 are mainly due
to organic matter decomposition and biological uptake, but
complicated with enhanced upwelling and vertical mixing. The
3!
outliers at Stn. 30 are due to the fact that NO!
3 and PO4 anomalies
have opposite trends of temporal changes between 600 and 900 m
depths, and the reason for the difference needs further
investigation.
By using the equation above, rates of temporal changes in DO
and AOU anomalies due to physical and biological changes in the
KTW are discussed as follows. An average observed temporal
decreasing rate of !0.0011 0.0004 mmol kg!1 yr!1 in PO3!
4
anomaly (Fig. 5f) is observed at the easternmost station between
the surface and 200 m depth. While assuming that the decrease is
owing to biological uptake alone, yields a temporal decreasing rate
in AOU anomaly of (!0.0011 ' 138) !0.15 mmol kg!1 yr!1. As
warming reduces DO at a rate of !0.11 mmol kg!1 yr!1, and freshening in S increases DO at a rate of 0.001 mmol kg!1 yr!1, DO is
expected
to
have
changed
by
(0.15 ! 0.11) 0.001 0.04 mmol kg!1 yr!1. These results indeed
closely correspond to the observed temporal changing rates in DO
and AOU anomalies of ca. 0.032 0.042 mmol kg!1 yr!1
and !0.125 0.040 mmol kg!1 yr!1, respectively (Fig. 5a, b). As the
oxygen solubility is related to q and S, it is worth noting that the
amount of changes in DO and AOU due to photosynthesis or microbial respiration would be minimized under the air-sea oxygen
exchange.
The above results suggest that increased biological productivity
3!
can account for the decreasing AOU, NO!
3 and PO4 , yet increasing
Chl-a and DO in the KTW and waters above. Correspondingly, the
organic matter produced settles and decomposes in deeper waters,
3!
leading to a lower DO yet higher AOU, NO!
3 and PO4 in KIW. But
another factor is also at play.

!
Fig. 6. Rates of temporal changes in NO!
3 anomaly vs. PO4 anomaly at the PN-line
stations. The black line shows the 16:1 ratio.

Fig. 7. Potential density vs. rate of temporal change in DO or DO anomaly. The red
symbols and line refer to the rates of temporal change in DO anomaly at the PN-line
stations between 1982 and 2010. The black symbols and line show the rates of temporal change in DO at the 137# E hydrographic line between 1985 and 2010, taken from
Takatani et al. (2012). The KIW is the Kuroshio Intermediate Water, KTW is the Kuroshio Tropical Water, NPSTMW is the North Pacic Subtropical Mode Water, NPIW is
the North Pacic Intermediate Water (NPIW), and the OML is the DO Minimum Layer.
(For interpretation of the references to color in this gure legend, the reader is referred
to the web version of this article.)

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H.-K. Lui et al. / Estuarine, Coastal and Shelf Science 151 (2014) 355e360

the Ministry of Science and Technology of Taiwan are acknowledged for nancially supporting this research under contracts NSC
101-2611-M-110-010-MY3 and 102-2611-M-110-003. D.K. Chen, J.L.
Zhou, X.H. Wang and two anonymous reviewers provided valuable
comments that strengthened the manuscript.
Appendix A. Supplementary data
Supplementary data related to this article can be found at http://
dx.doi.org/10.1016/j.ecss.2014.08.010.
References
Fig. 8. Secular trend of nitrate and phosphate concentrations at 400 m depth at Stn. 30 .
The solid lines are regression lines.

waters contain higher concentrations of nutrients yet lower DO at

the same depth than those of the Kuroshio waters (Chen, 2005).
Unfortunately, given the lack of reported data for changes in DO and
nutrients in SCS, whether the rates of these changes in the KTW and
KIW are due partly to mixing with the SCS waters remain unclear.
Importantly, while not appearing to be large, the rates of temporal
changes in nitrate (0.197 0.030 mmol kg!1 yr!1; p <0.0001) and
phosphate (0.0104 0.0034 mmol kg!1 yr!1; p 0.0002) anomalies
at 400 m at Stn 30 on the continental slope (Fig. 8) amount to 1.2%
and 1% change annually, respectively. Clearly, these changes are
substantial on the decadal scale.
4. Conclusions
3!
In summary, the NO!
3 and PO4 concentrations in the wide ECS
away from the Changjiang River mouth appear to be increasing,
along with a decreasing DO yet increasing AOU. This event is due to
the upwelling of KIW along the continental slope and onto the
bottom of the shelf. This process has undoubtedly increased
nutrient inventories, yet reduced the DO concentration of bottom
waters on the shelf. Hurricanes during the summer and fall, and
winter cooling mix the increased nutrients to the surface layer,
making them available for biological production during the spring
and summer. Subsequent settling down of the excess organic
matter decomposes and consumes DO of the bottom water that
contains lower and lower DO, owing to the lower DO in the upwelled KIW, ultimately leading to the development of hypoxia.
Importantly, further warming of the global oceans strengthens
the stratication of the surface ocean, resulting in weaker ventilation of seawater. As more organic material decomposes with a
longer residence time, DO in the subsurface water continues to
decline accompanied with increasing nutrients. Incursion of lower
DO yet higher nutrients seawater into shelves and coastal basins
may further increase coastal eutrophication and cause hypoxia to
spread. This study on ECS illustrates a situation in which coastal
eutrophication and hypoxia could be worse than expected when
the feasibility of reducing DO but yet increasing nutrients in the
open ocean interior is considered along with increasing the uxes
of terrestrial and atmospheric nutrients.

Acknowledgments
The authors would like to thank the Nagasaki Marine Observatory of the Japan Meteorological Agency for providing the invaluable data. The Aim for the Top University Plan (03C 0302 04) and

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