Progress in Oceanography 176 (2019) 102122

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Progress in Oceanography
journal homepage: www.elsevier.com/locate/pocean

Tracing external sources of nutrients in the East China Sea and evaluating
their contributions to primary production

T⁎

Jing Zhanga,b,c, Xinyu Guob,d, , Liang Zhaoca

Key Laboratory of Physical Oceanography, Ministry of Education China, Ocean University of China, Qingdao, China
Center for Marine Environmental Studies, Ehime University, Matsuyama, Japanc
College of Marine and Environmental Sciences, Tianjin University of Science and Technology, Tianjin, Chinad
Key Laboratory of Marine Environment and Ecology, Ocean University of China, Ministry of Education, Qingdao, Chinab

A R T I C LE I N FO

A B S T R A C T

Keywords:
Nutrients
Primary production eﬃciency
The East China Sea
Kuroshio
Nutrient source

Nutrients (dissolved inorganic nitrogen (DIN) and dissolved inorganic phosphorus (DIP)) in the East China Sea(ECS) have four external sources, namely the Kuroshio, Taiwan Strait, rivers, and the atmosphere. In order toevaluate the contribution of each source of nutrients to the nutrient inventory and primary production over the
ECS shelf, a tracking technique was applied to all the state variables in a low-trophic ecosystem model. Eachsource of nutrients has strong seasonal variations in the spatial distribution that depends closely on circulation,
mixing, and stratiﬁcation. The primary production supported by each source of nutrient is under the control of a
combination of nutrients, temperature, and light. As a mean state over the entire ECS shelf, the Kuroshio contributes 72% of DIN input and 84% of DIP input, 57% of DIN inventory and 78% of DIP inventory, 50% DINbased primary production and 61% DIP-based primary production and therefore is the dominant one among four
sources. However, the contributions of four external nutrients have strong spatial dependence: the riverine
nutrients and the atmospheric DIN dominate the inner shelf (0–50 m), the nutrients from the Taiwan Strait
dominate the southern part of the middle shelf (50–100 m), and the nutrients from the Kuroshio dominate theouter shelf (100–200 m). The production eﬃciencies of the nutrients from the Kuroshio are low, while thosefrom the atmosphere and Taiwan Strait are high. The riverine DIN is ineﬃcient but DIP is eﬃcient. The nutrient
limitation, light and water temperature at the location of the nutrients determine the production eﬃciency ofeach speciﬁc sources.

1. Introduction
The East China Sea (ECS) is a productive marginal sea in the
Northwest Paciﬁc Ocean with a broad continental shelf. Large quantities of nutrients load into the ECS from diﬀerent external sources, suchas the Kuroshio, Taiwan Strait, rivers, and the atmosphere. Local rivers
continuously discharge nutrients into the ECS. The Changjiang River,
especially, accounts for most of the riverine nutrient inputs and is responsible for the phytoplankton blooms in coastal areas (Gao and Song,
2005; Zhang et al., 2007; He et al., 2013). Nitrogen input from atmospheric deposition is comparable to that of terrestrial sources and wasreported to lead to eutrophication (Zhang et al., 2010). The Taiwan
Strait currents and the Kuroshio Surface Water are relatively poor in
nutrients (Zhang et al., 2007). The Kuroshio subsurface waters, especially the Kuroshio Intermediate Water, however, are rich in nutrients,
especially the phosphorus, and are the most important nutrient sources⁎

for the ECS shelf (Chen, 1996; Chen and Wang, 1999; Zhang et al.,2007; Zhao and Guo, 2011).
The nutrients from diﬀerent sources are potentially controlled by
diﬀerent factors, such as anthropogenic activity or climate change (Liuet al., 2014b). Evaluating the roles of multiple sources of nutrients inthe nutrient inventory and primary production over the continental
shelf of the ECS may deepen our understanding of the related physicaland biogeochemical processes and provide a scientiﬁc background forpredicting the response of the ECS ecosystem to changes in local or
remote factors.
To aid in our understanding of this issue, observations and numerical modeling have been undertaken. Regarding observations, isotopes
and other natural markers provide convincing evidence of the eﬀects ofnutrients from distinguishable sources. Based on stable isotopes of NO3,
Umezawa et al. (2014) conﬁrmed that the Kuroshio Subsurface Waterand Yellow Sea Mixed Water dominate the northern ECS in winter,

Corresponding author at: Center for Marine Environmental Studies, Ehime University, 2-5 Bunkyo-Cho, Matsuyama 790-8577, Japan.
E-mail address: guoxinyu@sci.ehime-u.ac.jp (X. Guo).

https://doi.org/10.1016/j.pocean.2019.102122
Received 8 April 2018; Received in revised form 7 April 2019; Accepted 11 June 2019
Available online 12 June 20190079-6611/ © 2019 Elsevier Ltd. All rights reserved.

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while Changjiang Diluted Water and the Yellow Sea Cold Water Mass
dominate in summer. Wang et al. (2016) focused on the southern ECS
and conﬁrmed the contribution of the Kuroshio onshore branch current
to primary production. Due to limitations of sampling frequency andcoverage area, a ﬁeld-based method is not suﬃcient for evaluating theentire ECS shelf over the timescale of one year.
Based on the available measurements of water and nutrient ﬂuxes, abox model can be established for the nutrient budget over the entire
ECS (e.g., Chen and Wang, 1999; Zhang et al., 2007). However, thenutrient input may not be a very appropriate index for evaluating thecontribution of speciﬁc nutrients to the nutrient inventory and primary
production. On one hand, not all of the nutrients transported into the
ECS are assimilated by phytoplankton due to low concentrations orother limitations such as light and temperature (Umezawa et al., 2014).
On the other hand, some of the nutrients can be very active in thebiogeochemical cycle and are probably utilized more than once before
leaving the ECS. Thus, an overestimation or underestimation of thecontribution of the nutrients to primary production cannot be avoided if
nutrient input quantity alone is used.
Conducting sensitivity experiments in a numerical model is anotherway to evaluate the roles of the multiple sources of nutrients. Zhao andGuo (2011) carried out several sensitivity experiments over the ECS in
which the nutrient concentration from the Kuroshio was artiﬁciallychanged. Zhou et al. (2017) conﬁrmed the contribution of nutrientsfrom the Changjiang and Kuroshio to the formation of hypoxia oﬀ theChangjiang Estuary. Although this method may be useful for management purposes, it is not capable of evaluating the actual contribution ofa speciﬁc nutrient because artiﬁcial increasing or decreasing of nutrient
concentration does not occur in reality. Furthermore, such sensitivity
experiments can provide neither timescales nor pathways of speciﬁc
nutrient transport.
A technique tracing nutrients from a speciﬁc source in a simulated
ecosystem is the most realistic way to address this issue (Kawamiya,
2001; Ménesguen et al., 2006). This method is capable of tracking
nutrients from one speciﬁc source and considering related physical aswell as biological processes and therefore can provide information on
the relative importance of several sources of nutrients to the primary
production in a given domain. It has been applied in the North Sea(Ruddick et al., 2009), Baltic Sea (Neumann, 2007, Timmermann et al.,2010; Radtke et al., 2012), and Japan Sea (Onitsuka et al., 2007). Its
demerit is that it requires much more calculation time than ordinary
simulation.
In this study, we applied this technique to the ECS to evaluate therole of nutrients with diﬀerent external origins in the nutrient inventory
and primary production over the continental shelf of the ECS. Section 2
gives a brief description of the model and the tracking technique.
Section 3 presents the distributions and seasonal variations of nutrientsand primary production with diﬀerent origins. Section 4 discusses therelations between the inventory of nutrients and primary productionand examines the eﬃciency of nutrients with diﬀerent origins in primary production. A summary of this study is provided in Section 5.

Fig. 1. Bathymetric map of the East China Sea. The study area of interest is
shaded in dark blue. Contour lines in black represent the 50-m, 100-m, and 200m isobaths. The blue dots denote the positions of inﬂow from rivers. The blueline shows the position of two sections. (For interpretation of the references tocolor in this ﬁgure legend, the reader is referred to the web version of thisarticle.)following Ménesguen et al. (2006). Description of the ﬁrst part can befound in Zhao and Guo (2011) and Wang et al. (submitted for publication), and only the second part is described here.
In the tracking module, state variables from diﬀerent sources arecalculated separately rather than as a whole as in the original physicalbiological coupled model. The main nutrients limiting the primary
production in the ECS are dissolved inorganic nitrogen (DIN) and dissolved inorganic phosphorus (DIP). Besides DIN and DIP, the othermain state variables are tagged as well, i.e., the diatom (DIA), the ﬂagellate (FLA), and the detritus (DET).
Four external sources of nutrients, namely from rivers (R), theTaiwan Strait (T), the Kuroshio (K), and atmospheric deposition (A),were tracked in this study. Here, R, T, K, A are used as subscript for
distinguishing them. For example, we use DINR, DINT, DINK, and DINA,
for DIN from these sources. The residual DIN is denoted as DINO while
the total DIN is as DINW. The other state variables (DIP, DIA, FLA, andDET) are denoted in a similar way.
Because any external source of nutrient has the same physical andbiogeochemical processes as the total nutrients, it has the same governing equations as those used in the original biological module (Zhaoand Guo, 2011). To keep it independent from the others, we used an
addition of a complete subset of equations to handle the state variables
for each nutrient source, that is, four subsets of equations for four external sources of nutrients. With inclusion of residual nutrients, wesolved ﬁve subsets of equations in total.
Since the physical processes for state variables are linear, the advection and diﬀusion terms are easily separated for each source ofnutrients. The terms for biological processes are separated following theratio of each source of nutrient concentration to the total nutrient
concentration. For example, primary production supported by total
nutrients (denoted by PPW) is the product of the growth rate (μ) and the

2. Methods
The model domain covers the Bohai Sea, the Yellow Sea and theEast China Sea (24–41°N, 117.5–131.5°E). The main area of interest in
this study is the continental shelf of the ECS indicated by dark blue in
Fig. 1. We divided it into three regions with diﬀerent water depths:
inner shelf (0–50 m), middle shelf (50–100 m) and outer shelf(100–200 m). We expect that nutrients from multiple sources havediﬀerent characteristics among these three regions.
The model consists of two parts. The ﬁrst part is a physical-biological coupled module, which is for calculating cycles of total nutrients.
This part is based on Zhao and Guo (2011) and is the same as the oneused in Wang et al. (submitted for publication). The second part is the
newly added tracking module for nutrients from diﬀerent origins
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total phytoplankton concentration (PHYW).

PPW = PHYW ·μ = PHYW ·μ T ·μ L ·min(fDIN, fDIP, fSIL)(1)

Growth rate (μ) is the product of a temperature coeﬃcient (μT), alight coeﬃcient (μL) and a minimum of the nutrient concentrationcoeﬃcients (fDIN, fDIP, fSIL,). The formula for calculating these coeﬃcients can be found in Skogen et al. (1995). The nutrient limitation
terms (fDIN, fDIP, fSIL)are calculated from total nutrient concentration
rather than the nutrient concentration from a single source. Therefore,
the growth rate (μ) is the same for the phytoplankton supported by
diﬀerent sources of nutrients. The ratio of DIN and DIP diﬀers greatly indiﬀerent nutrient sources. Consequently, the primary production in the
ECS is limited by either DIN or DIP, depending on places. For thisreason, the tracking module was established for DIN and DIP, respectively.
The total PPW given by Eq. (1) is divided to that supported by asingle source of nutrient (PPX) by Eq. (2).

PPX = PPW ·NUTX, X = R, K, T, A, O
NUT

(2)

The variable NUT indicates total nutrient concentration, while
NUTX indicates nutrient concentration from a single source. The NUT
represents DIN in the case of tracking DIN and DIP in the case of
tracking DIP. The other biogeochemical processes such as respirationand mortality are calculated in a similar way.
The initial conditions for the nutrients concentration, phytoplankton, and detritus corresponding to the four external sources ofnutrients are set to 0. For the residual nutrients, the initial conditions
for all the state variables are set to the results from a standard model
calculation with all sources of nutrients. The lateral boundary conditions of riverine nutrients were from published data (Zhang, 1996; Liuet al., 2009). The data source for climatology data of atmospheric wet
and dry depositions was Zhang et al. (2011). The lateral boundary
conditions for nutrients, phytoplankton, and detritus for the Taiwan
Strait are from Prof. Chen-Tung Arthur Chen (personal communication)
while that for the Kuroshio east of Taiwan is from the Japan Meteorological Agency (http://www.data.jma.go.jp/gmd/kaiyou/db/vessel_
obs/data-report/html/ship/eﬁle_NoS2.html). The bottom boundary
conditions were independent among the four external sources of nutrients, i.e., the sinking of particles and remineralization of sedimentare included within the cycle of each external nutrient source. The
boundary condition for the residual nutrients is set to 0 at river mouths,
air-sea interface, Taiwan Strait and east of Taiwan.
Fig. 2 shows annual mean input ﬂuxes of DIN and DIP from diﬀerent
sources and their seasonal variation. The total input ﬂux of DIN loadingfrom rivers (DINR) into the ECS is about 1.2 kmol s−1 with a higher
amount in summer. The input ﬂux of DINA also shows a slightly higher
value in summer but with a weak seasonal variation. The input ﬂux of
DINT has an apparent seasonal variation, which is quite high in summer
but almost zero in winter with an annual mean of 1.5 kmol s−1. The
DINK was tracked from east of Taiwan, but the input ﬂux of DINK isdeﬁned as the net transport of DINK across the 200-m isobath into theshelf. The input ﬂux of DINK (12.6 kmol s−1) into the ECS shelf is oneorder of magnitude larger than those from other sources and reaches apeak in autumn; it accounts for more than 70% of the total input ﬂux of
DIN (17.4 kmol s−1) into the ECS shelf.
The input ﬂux of DIP from the Kuroshio (DIPK, 1.119 kmol s−1) isalso larger than that from the other external sources, accounting foralmost 85% of the total input ﬂux of DIP (1.324 kmol s−1) (Fig. 2b).
The DIP ﬂux through the Taiwan Strait (DIPT, 0.182 kmol s−1) is oneorder less than that from the Kuroshio. The seasonal variations of input
ﬂuxes of DIPK and DIPT are similar to those of DINK and DINT, respectively. However, the input ﬂuxes of DIP from local sources, i.e.,rivers and atmosphere (DIPR and DIPA) are much less than those fromoceanic sources, i.e., Kuroshio and Taiwan Strait (DIPK and DIPT).
With such conditions, both cases of tracking DIN and tracking DIP

Fig. 2. Monthly input ﬂux of (a) DIN and (b) DIP from each external source(kmol s−1). The values in the legend are the mean values for each source over a
year.

were run for eight years when inventories of nutrients, phytoplankton
and detritus within the ECS shelf reached a seasonal stationary state.
The averaged concentration of chlorophyll a (CHL) over the study areaof interest in case of tracking DIN is shown in Fig. 3. The concentrationsof CHL of the four sources change a lot within a single year, but thepatterns among years are similar. The annual mean and amplitude of
CHL concentration changed little after ﬁfth year, which means the statevariables related to the low trophic ecosystem of the ECS reached astationary steady state. The results in case of tracking DIP show a similar pattern with diﬀerent annual-mean values (Figure not shownhere). We used the results of both cases in sixth year for further analysis
in this study.
Concerning to the physical-biological module, Zhao and Guo (2011)
and Wang et al. (submitted for publication) had made great eﬀorts toverify the results by comparing distributions of nutrients and phytoplankton as well as nutrient ﬂuxes with available observations andsatellite data. Here, we showed another comparison with the observations of Umezawa et al. (2014). They conducted the surveys at line D(31°45′N, see blue line in Fig. 1 for its location) in February 2009, July2009 and July 2011. We picked up the distributions of chlorophyll
ﬂuorescence and nitrate concentrations in February and July 2009 for acomparison (Fig. 2 in Umezawa et al., 2014, ﬁgure not shown here).
The model results were interpolated at their station site and the corresponding results are shown in Fig. 4. Note that the CHL in the model
results and chlorophyll ﬂuorescence in the observations are diﬀerent invalue, but both reﬂect the distribution pattern of phytoplankton.
The model results and observations are similar with each other. The
concentration of CHL in winter is higher in the upper layer of the outer3

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Fig. 3. Daily concentration of chlorophyll a (CHL, mg Chla m−3) in case of tracking DIN over the study area of interest shown in Fig. 1. The tickers in the x-axis
indicate the middle day of a year. Open triangles indicate the annual mean of each year.

shelf, showing by the contour of 1 mg Chla m−3 (Fig. 4a). The CHL
concentrations in the inner and middle shelves are relatively low inboth model (Fig. 4a) and observation results (Umezawa et al., 2014). In
July (Fig. 4b), the depth of maximum CHL descends gradually eastward, which can be also found in the observations (Umezawa et al.,2014). The DIN concentration in February is vertically homogeneouswith shoreward horizontal gradient west of Sta. 10 (Fig. 4c). In theupper 75-m layer east of Sta. 10, the concentration of DIN is lower than
4 mmol m−3 and the horizontal gradient decreases. Beneath 75-m
depth, the DIN concentration shows a large vertical gradient and increases to 12 mmol m−3 gradually (Fig. 4c). These features can be also
found in observations (Umezawa et al., 2014). Under the inﬂuence ofstratiﬁcation, the DIN concentration in July (Fig. 4d) varies verticallywith contours tilting shoreward. A low-concentration area (< 1 mmolm−3) exists in the upper 50-m layer east of Sta. 9. After this comparison
and those given by Wang et al. (submitted for publication), we conclude
that the values and patterns of the model results generally agree withthose from observations, considering the presence of interannual variations.

mean of 0.17 mg Chla m−3 and annually varies over the range of 0.2 mg
Chla m−3. The concentrations of phytoplankton supported by the otherthree external sources of DIN (river, Taiwan Strait, and atmosphere) are
all on the same order of magnitude and all below 0.17 mg Chla m−3.
The peak value for each source ﬁrst occurs for the DIN from the Kuroshio, followed by those from rivers, the atmosphere, and the Taiwan
Strait. For a full understanding on these changes, we need to examine
the spatial distribution of currents, nutrients and primary production in
the following subsections.
3.1. Surface current distribution over the ECSThe currents ﬂow generally along isobaths in the ECS, although theacross-isobath currents also exist and play an important role in theexchange of water and materials between the shallow sea and open
ocean (Zhang et al., 2017). Fig. 5 shows surface current distributions.
The strong along-isobath circulation out of the shelf is the northeastward Kuroshio. The Kuroshio splits two branches across the shelf
break northeast of Taiwan and southwest of Kyushu, respectively. The
Kuroshio onshore intrusion northeast of Taiwan is strong and extends
farther onshore in winter (Tang et al., 2000; Hsin et al., 2013), while
the Kuroshio mainstream is strong and moves oﬀshore in summer(Ichikawa et al., 2008). When the Kuroshio mainstream reaches thearea southwest of Kyushu, it turns clockwise to the east and leaves the

3. Results
As shown in Fig. 3, the highest average concentration of phytoplankton is supported by DIN from the Kuroshio, which has an annual

Fig. 4. Vertical distributions of (a, b) CHL and (c, d) DIN concentration in February and July.
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Fig. 5. Mean current distribution at 2-m depth in (a) winter (November to April) and (b) summer (May to October). The arrows denote the current direction and thecolor denotes the velocity magnitude (cm s−1).

distributes over the entire shelf (Fig. 6, third row) due to strong mixing
with bottom layer water where the onshore intrusion of the Kuroshio
water supplies DINK from the lateral boundary. Since DINK in winterand autumn has a high concentration in the inner shelf and a tongueshaped area with low concentration in the middle shelf, the high concentration of DINK close to the coastal area is not transported directlyfrom the shelf break through the surface layer. In spring and summer,
the northern inner shelf also has a high concentration of DINK. The
upwelling region northeast of Taiwan shows a higher concentration of
DINK than the surrounding areas at all times, suggesting a persistentcontribution from the Kuroshio (Liu et al., 2000).
The DINT at the surface layer has a relatively low concentrationcompared to the other three sources (Fig. 6, fourth row) and is mainly
restricted to within the 100-m isobath. As for the DINK, DINT also inﬂuences a greater area in winter, especially north of 30°N. It is worth
noticing that nutrient is utilized by phytoplankton and then changed todetritus with mortality of phytoplankton. The remineralization of detritus could regenerate nutrient. After the running of the tracking
module for several years, both newly added and regenerated DINK and
DINT exist in the ECS. With the low temperature in winter, the photosynthesis process weakens. The DINK and DINT produced by respiration
and remineralization processes exceeds the consumption of the DINK
and DINT. Therefore, the biological processes tend to increase theconcentration of DINK and DINT in winter. On the other hand, thestrong monsoon in winter induces mixing from the surface to bottom inthe shallow area. The high-concentration nutrients in the bottom layer
therefore easily reach the surface layer. The high concentration of DINK
and DINT in the northern inner shelf is caused by local physical andbiological processes rather than by newly transported from the corresponding boundaries. In the area south of 30°N, DINT concentrates
along the coastal area. In summer, DINT intensively rushes out of thestrait and reaches the vicinity of the Changjiang estuary at about 30°N
due to the strong Taiwan Warm currents. Apparently, seasonal variations in DINT north and south of 30°N are diﬀerent. The distributions of
DINT in spring and autumn are the transitions between those in summer
and winter.
To identify the dominant area for each nutrient source, we present
the concentration of the total DIN (DINW) at the surface layer as a reference (Fig. 6, last row, DINW). The concentration of DINW is often
high in the inner shelf. The primary production in the inner shelf isusually limited by DIP (Wang et al., 2003) and the DIN cannot be fully
assimilated by the phytoplankton. In addition, the nutrients in thebottom layer of the inner shelf are easy to reach the surface layer due tothe shallow water depth and tidal mixing.
We deﬁned the area where the concentration of DIN from one

ECS through the Tokara Strait. As result of the conservation of potential
vorticity, another Kuroshio Branch Current west of Kyushu (KBCWK)
forms and intrudes over the outer shelf across the shelf break (Hsueh
et al., 1996; Lie et al., 1998; Isobe, 2000).
The Taiwan Strait Current is stable and northeastward in summer
but weak and ﬂexible in winter (Chen et al., 2016). In the middle shelfof the ECS, the Taiwan Warm Current ﬂows northeastward along theisobaths. The Taiwan Warm Current bifurcates into two branches insummer when arriving at the 28°N: an onshore branch which ﬂows
northward and turns to the northeast oﬀ the mouth of the ChangjiangRiver, and an oﬀshore branch which ﬂows along 100-m isobath andthen joins the west side of the Kuroshio (Su and Pan, 1987). When it
comes to winter, the Taiwan Warm Current ﬂows in an upwind direction and reaches the south of Changjiang Estuary (Lian et al., 2016).
The Min-Zhe Coastal Current and the CDW locate in the inner shelf,
both of which show opposite direction in summer and winter. In
summer, the CDW extends farther oﬀshore over the western shelf ofnorthern East China Sea (Lie et al., 2003; Hu et al., 2016); in winter, itreaches the Taiwan Strait against the Taiwan Warm Current (Hu, 1994;
Chang and Isobe, 2003).

3.2. Horizontal distribution of DIN from each source at the surface andbottom layers
We show the distribution of DIN from each source and their sum atthe surface layer (5 m depth) in four seasons (February for winter, May
for spring, August for summer, and November for autumn) in Fig. 6.
The DINR is concentrated at the inner shelf year round (Fig. 6, ﬁrstrow). The maximum concentration occurs at the Changjiang River estuary each season. In winter and autumn, DINR extends southward
within a narrow band along the coast and reaches the Taiwan Strait(Chen, 2008). In summer, it turns eastward and northeastward and has
a high concentration within the Tsushima Strait. As a natural thing, thedistribution of DINR corresponds well to seasonal variation of the
Changjiang Diluted Water (CDW).
The distribution of the DINA (Fig. 6, second row) is similar to that of
DINR. It is concentrated mainly in the northern ECS but also distributes
along the coastal area south of the Changjiang estuary. The surface
circulation of the ECS is mostly northward, and the currents are weak inthe coastal area, resulting in accumulation of DINA there. In winter, the
DINA reaches a maximum (∼18 mmol m−3). This follows the same
seasonal pattern as DINR in the coastal area of the southern ECS. In thenorthern ECS, DINA usually has a high concentration within 100-m
isobath but extends further and reaches the Tsushima Strait in summer.
The surface DINK has the highest concentration in winter and5

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Fig. 6. Distribution of DIN (mmol m−3) from rivers (DINR), the atmosphere (DINA), the Kuroshio (DINK), the Taiwan Strait (DINT) and the sum of the above four
sources (DINW) in four seasons at 5-m depth. Cross hatching indicates the region where the DIN from a speciﬁc source accounts for more than 50% of the total DIN.
The black contours denote 50-m, 100-m, and 200-m isobaths.

the Taiwan Strait current.
Distributions of DIN with diﬀerent origins and their sum in thebottom layer (the last sigma layer, at the level of 97.5% of the water
depth) are shown in Fig. 7. DINR (Fig. 7, ﬁrst row) is concentrated inshallow areas, showing a similar distribution with the surface DINR
except for in summer when DINR concentration is lower in the bottom
water than in the surface. Bottom DINA is also similar to surface DINA
but shows a lower concentration in summer (Fig. 7, second row). Strong
stratiﬁcation in summer likely prevents the transfer of DINR and DINA
from the surface layer to the bottom layer.
DINK has a much higher concentration in the bottom layer (Fig. 7,
third row) than in the surface (Fig. 7, third row). The diﬀerence in DINK
between the surface and bottom layers has the largest diﬀerence insummer and the least diﬀerence in winter. The high concentration areasof the bottom DINK are located northeast of Taiwan and southwest of
Kyushu where the strong Kuroshio onshore intrusion takes place (Guoet al., 2006; Zhang et al., 2017). The concentration of the bottom DINK
west of Kyushu is high in summer, and most of the DINK is transported
from there to the Tsushima Strait. In spring and summer, the bottom
DINK northeast of Taiwan bifurcates into two branches following theKuroshio onshore intrusion; the onshore branch reaches the vicinity of

speciﬁc source is higher than half of the total DIN concentration as its
dominant area (see cross-hatched area in Fig. 6). In winter, DINK controls the outer shelf, most of the middle shelf, and the Tsushima Strait;
DINR dominates the inner shelf; DINT and DINA are less important andhave almost no dominant area. In spring, DINA plays a leading role in
the northern parts of the middle and outer shelf despite of an actually
low concentration there; DINK dominates northeast of Taiwan; DINT
takes up the southern middle shelf; DINR dominates the coastal areas. In
summer, since DINR extends its dominant area northeastward, DINT
becomes the dominant one in the southern coast of China; the dominant
areas of the DINK and DINA change little. In autumn, the dominant areaof the DINR retreats to that of winter; DINA takes up only a small part of
the northern middle shelf and DINT also weakens; DINK regains controlof the outer shelf and the region northeast of Taiwan.
The dominant area in Fig. 6 indicates a competition between DINT
and DINK in the southern ECS. In winter and autumn, DINT concentrates
to the area around the Taiwan Strait while DINK takes up most of the
middle and outer shelf areas. In spring and summer, DINT controls atongue-shaped area in the middle shelf, while DINK occupies only the
upwelling region northeast of Taiwan. This competition probably corresponds to the interaction between the Kuroshio onshore intrusion and6

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Fig. 7. As in Fig. 6 but for the DIN in the bottom layer. The bottom layer is deﬁned as the deepest layer in the model that is 97.5% of the total water depth.

smaller in summer. DINA has no dominant role in the bottom layer.
Control of DINT in the bottom layer is weaker but shares similar seasonal distribution with those in the surface. DINK occupies the entire
outer shelf and the southern middle shelf year round and therefore
dominates the bottom layer.

the Changjiang estuary (Yang et al., 2011, 2012). In autumn andwinter, the onshore branch disappears while the oﬀshore branch isapparent and mainly distributes along the 100-m isobath (Liu et al.,2014a). The low concentration tongue-shaped pattern holds at thebottom layer in autumn and winter, implying that high concentration
DINK along the coast is not transported directly from the shelf break. A
possible explanation is that DINK in the northern part of the inner shelfis transported southward by southward coastal currents, being the same
as for DINR.
The concentration of bottom DINT (Fig. 7, fourth row) increases alittle compared to that in the surface layer (Fig. 6, fourth row). Patternsof DINT in winter and spring are also similar in the surface and bottom
layers. In summer and autumn, bifurcation of DINT is distinct at about
30°N. The northeastward DINT separates into two branches corresponding to the Taiwan Warm Current. The onshore current goes
northward along the 50-m isobath while the oﬀshore one makes ananti-clockwise rotation towards the Yellow Sea along the 100-m isobath(Su and Pan, 1987).
The distribution of DINW at the bottom layer shows little seasonalvariation (Fig. 7, last row). The concentration of DINW in the inner andouter shelf is higher than that in the middle shelf. The situations ofdominant nutrients are simple in the bottom layer. The dominant areaof the bottom DINR is almost the same as that of surface DINR but is3.3. Horizontal distribution of DIP from each source at the surface andbottom layers
The DIPR concentrates in the coastal area as well (Fig. 8, ﬁrst row),
but the high-concentration area is smaller than that of DINR (Fig. 5, ﬁrstrow). Because of high ratio of DIN/DIP in river water, the primary
production in the oﬀshore area of the Changjiang Estuary is usuallylimited by DIP, which is apparent in summer. Consequently, DIPR is
utilized locally rather than transported to the Tsushima Strait like DINR.
The concentration of DIPA is very low (Fig. 8, second row) with a relatively high value appearing only in the northern ECS in winter. On thecontrary, DIPK has a high concentration, especially in the outer shelf in
winter and autumn (Fig. 8, third row). In summer, the high-concentration area of DIPK locates at the northeast of Taiwan and out of theestuary. The pattern of DIPT in autumn and winter is similar to those of
DINT (Fig. 8, fourth row). In spring and summer, DIPT has a highconcentration in southern ECS and extends northeastward to the7Progress in Oceanography 176 (2019) 102122

J. Zhang, et al.

Fig. 8. As in Fig. 6 but for the DIP at 5-m depth.

Tsushima Strait.
The distribution of DIPW is shown in the last row of Fig. 8. The
concentration of DIPW is the highest in winter. Due to the low temperature in winter, the primary production is weak. The combined effects of the biological processes tend to add the amount of DIPW. In
spring and summer, the concentration of DIPW decreases with the increasing of primary production. The dominant area of DIPR is similar tothat of DINR, but two diﬀerences lie in the southern inner shelf in autumn and winter, and the oﬀshore area of the estuary in summer, respectively. There is no dominant area in the surface layer for DIPA due
to its low concentration. The dominant area of DIPK is larger in theouter shelf in spring than that of DINK. The dominant area of DIPT is
also consistent with DINT but expands wider in summer toward theTsushima Strait.
The DIP from each source in the bottom layer also shows weakseasonal variation (Fig. 9). Although DINR and DINA have higher concentration in the surface layer rather than in the bottom layer (Fig. 8),
DIPR and DIPA have higher concentration in the bottom layer than in
the surface layer, indicating that they are utilized by the phytoplankton
in the surface layer (Fig. 9, the ﬁrst two rows). The concentration of
DIPK increases extremely in the bottom layer and keeps a high value all
the year round, especially in the outer shelf. The distribution of DIPT in
the bottom layer is similar to DINT. The branch pattern of DIPT

corresponding to the Taiwan Warm Current is more apparent.

3.4. Horizontal distribution of the water column-integrated primary
production supported by each source
After clarifying the distribution of nutrients from diﬀerent sources,
we examine their contributions to primary production. Distributions ofintegrated primary production over the water column supported byeach source of DIN are shown in Fig. 10.
High primary production supported by DINR (PPR) mainly occurs inspring and summer within the inner shelf. One of the high PPR regions
is located outside of the Changjiang estuary, and the other one has astripelike distribution and lies along the 50-m isobath in the northern
ECS. PPA shares this stripelike distribution and is also high to the northof Jeju in spring and summer. PPK is higher in the outer shelf in winter.
In summer, PPK is high only in the southern ECS but can extend in an
onshore direction to the 50-m isobath. PPT is high in summer and spring
within the southern middle shelf. Total integrated primary production(PPW) is shown in the last row of Fig. 10. In winter, primary production
is weak and is only high in the outer shelf. It increases greatly in springand summer. The dominant areas of integrated primary production(cross hatch in Fig. 10) are essentially determined by DINX according to
Eq. (2). The area controlled by PPR is similar to that controlled by DINR
8

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Fig. 9. As in Fig. 8 but for the DIP in the bottom layer.

of the euphotic layer where the light intensity is reduced to 1% of thatin the surface.
DINR concentration is high only in a narrow area of the coastal
region (Fig. 11). The coastal region is well mixed all year round, consistent with the vertically homogeneous temperature (Fig. 13). DINR
has a horizontal shoreward gradient. The concentration of DINR islowest in summer when coastal currents move northward rather thansouthward. DINA shares similar patterns with DINR in autumn andwinter, but extends oﬀshore and concentrates in the top 10 m in springand summer when the strong thermocline isolates DINA in the surface
layer. DINK has a striking vertical distribution in spring and summer
when the strong thermocline severely limits the upward transport of
DINK and results in a low surface DINK concentration (Fig. 11). A nutricline forms at a depth of about 35 m, which is shallower than theeuphotic depth. In winter and autumn, DINK is uniform at upper 50 m
layer due to strong vertical mixing. Below the nutricline in spring/summer and the well-mixed surface 50 m layer in autumn/winter, ahigh-concentration area (greater than3 mmol m−3) is present. This highconcentration of DINK in the bottom layer is strongest in summer andcan move up the slope and reach areas shallower than 30 m. DINT also
reveals a homogeneous vertical structure in autumn and winter with amaximum at about 122.5°E. The core of the DINT is located at thebottom of the euphotic zone around 123°E in spring, and ampliﬁed inin the bottom layer. The area controlled by PPA also corresponds well tothat controlled by bottom DINA. The dominant patterns of PPT and PPK
are similar to those of surface DINT and DINK, respectively. A little
diﬀerence is found in spring when PPK is high throughout the entire
outer shelf, but surface DINK dominates only northeast of Taiwan.
The primary production supported by each source of DIP has no
essential diﬀerence in the distribution with those by each source of DIN
but the contribution ratio of each source to the total primary productionchanges a little in two cases. The PPR and PPA are lower in case of
tracking DIP than in case of tracking DIN while the PPK and PPT arehigher in case of tracking DIP than in case of tracking DIN. Such difference is caused by the relative magnitudes of the DIP and DIN fromeach source of nutrients.

3.5. Vertical distribution of DIN, DIP and PP from each source at section
DH
Section DH (based on DH5 in Wang et al., 2016) is generally perpendicular to the isobaths of the continental shelf of the ECS. All four
sources of nutrients aﬀect this section, as shown by the horizontal
distributions (Figs. 6–9). Distributions of the multiple sources of DIN(Fig. 11), DIP (Fig. 12) and temperature (contours in Fig. 13) at section
DH are presented here. The dashed lines in Figs. 11–13 show the depth9Progress in Oceanography 176 (2019) 102122

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Fig. 10. Distributions of water column integrated primary production (mg C m−2 d−1) supported by DIN from rivers (PPR), the atmosphere (PPA), the Kuroshio (PPK)and the Taiwan Strait (PPT) and the sum of the above four sources (PPW) in four seasons. Cross hatching indicates the region where primary production supported bya speciﬁc nutrient accounts for more than 50% of the total primary production. The black contours denote 50-m, 100-m, and 200-m isobaths.

DIN is shown by color in Fig. 14. The regions of primary production
dominantly supported by one DIN source are represented by crosshatch. As shown in Eq. (1), besides the nutrients, primary production
also depends on water temperature and light intensity. For this reason,
we show the euphotic depth (dashed line) and the boundary of the DINlimiting and DIP-limiting areas (black lines) at section DH in Fig. 13.
The DIP-limiting area usually appears in the shore side (Fig. 13a, b, d)and surface layer (Fig. 13c) while the DIN-limiting area shares theothers. Silicate is not a limiting factor at this section.
PPR is high within the coastal area in winter, summer, and autumn
but extends seaward with a lower value in spring. In the coastal area,
photosynthesis is limited by DIP rather than by DIN year round. In
winter and autumn, PPA is very weak and only shows relatively highvalues near the coast and the upper 30-m layer in the outer shelf. In
spring, PPA is high in the upper 30-m layer of the section and presents
its maximum at the surface of the middle shelf. In summer, PPA is highin the upper 10-m layer and decreases from the coast to the shelf break.
PPK is high in the top 50-m layer outside the inner shelf in autumn andwinter when DINK and temperature are high in the sunlit upper layer.

summer.
We compared the distribution of DINW at section DH in May (Fig. 11
last row and second column) with the observations (Fig. 4e in Wanget al., 2016). Both show a vertically homogeneous distribution of DINW
near the coast but a vertically increased pattern at the 60-m isobath. We
then used cross hatching to identify areas where DIN is dominant in thevertical distribution (Fig. 11). DINR dominates in the coastal areas,
especially in winter and autumn; DINA occupies only a thin surface
layer in spring and summer; DINT has no high concentrations in winterbut occupies the upper 50-m layer within the middle shelf in spring andsummer; DINK dominates the largest area, covering the entire middle
and outer shelves in winter and autumn as well as the lower areas inspring and summer.
The DIP from each source at section DH (Fig. 12) shares a similar
pattern with DIN. The concentrations of DIP from two local sources(rivers and atmosphere) are relatively low while those from oceanic
sources are relatively high. The dominant area of DIP from each sourceis also similar with that of DIN.
The vertical distribution of primary production supported by each10

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Fig. 11. Distributions of DIN (mmol m−3) at section DH from rivers (DINR), the atmosphere (DINA), the Kuroshio (DINK), the Taiwan Strait (DINT) and the sum of thefour sources (DINW) in four seasons. Cross hatching indicates the region where the DIN from a speciﬁc source accounts for more than 50% of the total DIN. The whitebroken line denotes the euphotic layer where the light intensity is 1% of that at sea surface.

3.6. Seasonal variations of DIN and DIP inventory and primary production
integrated over the water column

Its maximum is at the surface and is larger in winter than in autumn. In
spring, PPK is still high in the outer shelf but presents a maximum at a
depth of about 40 m due to the interplay of DINK, light, and temperature. The pattern of PPK in summer is similar to that in spring, exceptthat the region of high PPK extends further to the inner shelf, corresponding well with the distribution of DINK. PPT is very low in autumn
and winter but becomes high in spring in the middle shelf with amaximum at about 15 m depth that reaches a peak in summer. The
pattern of PPT in summer follows the deepening of the euphotic layer
depth to the west of 124°E. Like the horizontal distribution, the vertical
distribution of primary production supported by each source DIP at
section DH shares similar patterns with that by DIN but in diﬀerent
magnitudes (ﬁgure not shown here).

To summarize a quantitative characterization of the above distributions, we present the total inventory of DIN (TN) and DIP (TP), andthe primary production integrated over the water column supported by
DIN (N-IPP) and DIP (P-IPP) in the study area of interest in Tables 1 and
2, and their seasonal variations in Figs. 15 and 16. In these tables andﬁgures, results in the three sub-regions (inner, middle and outer
shelves) and over the whole area are shown separately.
The inventory of nutrients is the potential source for primary production. In the inner shelf, annual mean TNR and N-IPPR account for
about 60% of TNW and N-IPPW, followed by TNA and N-IPPA and themuch weaker contributions from the Kuroshio and the Taiwan Strait(Table 1). In the middle shelf, the contributions of TNR and N-IPPR
11

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Fig. 12. As in Fig. 11 but for DIP.

Table 2, corresponding to DIN in Table 1. In the inner shelf, TPT is 40%
of TPW and is the largest one among the four sources of TP. TPK and TPR
are a little less than TPT, while TPA is only 1% of TPW. The largest P-IPP
in the inner shelf is supported by DIPT (37%), following by DIPR and
DIPK. The percentage of P-IPPA is as the same as that of TPA. In the
middle shelf, TPK increases to 61% of TPW. The ratio of P-IPPK raises to
49% as well. The TPT in the middle shelf is almost 4 times of that in the
inner shelf, while the P-IPPT increases to only 2.6 times. However, theratio of P-IPPT to P-IPPW grows from 37% to 46%. The percentages
related to the DIP from rivers and atmosphere are all less than 5% in the
middle shelf. The percentages of TPR and P-IPPR reduce to 3% and 4%,
and the percentages of TPA and P-IPPA is 0.4% and 1%. In the outer
shelf, TPK plays a leading role with a percentage of 94%. Meanwhile,
the P-IPPK takes up 86% of the P-IPPW. The values of TPT and P-IPPT in
the outer shelf are almost the same as those in the inner shelf, but thecorresponding proportions are much smaller. TPR and P-IPPR accountdecrease to 10% but those of TNK and N-IPPK increase to about 40%.
Compared to the inner shelf, the percentage of TNT is doubled and thatof N-IPPT is tripled in the middle shelf. In the outer shelf, TNK and NIPPK account for more than 90% of TNW and 80% of N-IPPW. The residual 20% of N-IPPW is nearly half from N-IPPT and half from N-IPPA.
By considering all three regions together, the entire ECS can be
examined (Table 1). TNW is about 205 × 106 kmol, which is comparable to the mean of the summer and winter inventories from Chen
(2008, 190 × 106 kmol). The proportion of TNK is about 57% and is thelargest. TNR comes in second and accounts for 17%, which is a little
larger than the proportion of TNA (15%). TNT is lowest with a percentage of 12%. The N-IPPW in the ECS is about 39.9 kmol N s−1(=414 mg C m−2 d−1), which is comparable to the result of Gong et al.
(2003, 397 mg C m−2 d−1). Half of N-IPPW is from N-IPPK and the otherhalf is almost equally from N-IPPA, N-IPPT, and N-IPPR.
The TP and P-IPP from each source in diﬀerent regions are shown in12

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Fig. 13. Distributions of the temperature (color contours) at section DH in four seasons. The dashed line indicates the euphotic depth. The solid black line separates
the DIN-limiting (seaside) and DIP-limiting (shore side) regions.

N-IPPK weakens and assimilates less DINK. However, the input ﬂux of
DINK increases. Consequently, TNK increases after April.
In the entire shelf (Fig. 15d), TNW reaches its maximum in February
and minimum in June. The seasonal variation of N-IPPW is regulated by
all the four sources of DIN. In winter, N-IPPW is not so low due to thepresence of high N-IPPK in the outer shelf. The maximum N-IPPW in
May results from the combination of N-IPP from the Taiwan Strait, therivers and atmosphere. The growing N-IPPT after spring makes N-IPPW
decrease slowly until August.
The seasonal trends of TPs are consistent with the corresponding
TNs (Fig. 16). They are under the control of the same physical processes
as the same biological processes by following the Redﬁeld ratio for DIN
and DIP. However, the relative magnitudes of TPs are diﬀerent fromthose of TNs. The N-IPPW and P-IPPW are actually the same. They are
assigned to each source of nutrients according to DIN ratio and DIP
ratio that are diﬀerent for the same source of nutrient. As the result of
low input of DIP from river and atmosphere, the contributions from therivers and the atmosphere to P-IPPW reduce and those from the Kuroshio and Taiwan Strait become more important in P-IPPW than in NIPPW.

for only 0.1% and 0.2% of TPW and P-IPPW. The contributions from theatmosphere are even lower and its percentages are less than 0.1%. The
TPK and P-IPPK are the most important when considering the entire ECS
shelf. The DIP from the Taiwan Strait is a secondary contributor. The
contributions from the rivers are smaller than 10% and those from theatmosphere are even less.
The proportions of IPPR, both N-IPPR and P-IPPR, decrease from theinner shelf to outer shelf. On the contrary, the percentages of IPPK increase from the inner shelf to outer shelf. It is corresponding to the
distribution of nutrient from the rivers and the Kuroshio. The largest
percentages of IPPT and IPPA locate in the middle shelf, rather than in
the inner shelf as IPPR or in the outer shelf as IPPK.
Seasonal variations in nutrient inventory are very complex. The
inventory is an accumulation of input ﬂux and aﬀected by the physicalprocesses such as transport and biological processes such as photosynthesis. Seasonal variations of TN and N-IPP show diﬀerent patterns
in diﬀerent regions (Fig. 15). In the inner shelf (Fig. 15a), TNR and TNA
show almost the same seasonal variation as known from their similar
horizontal distributions. Both decrease from spring to summer and increase from autumn to winter. N-IPPR and N-IPPA peak in May and thendecrease slowly in summer. They are weak in the cold autumn andwinter when TNR and TNA are high. When it comes to the warm spring,large amounts of DINR and DINA are consumed, and TNR and TNA are
reduced. In summer, TNR and TNA continue to decrease. In addition tophotosynthesis, DINR and DINA are likely transported out of the ECS
through the Tsushima Strait according to their distributions at thesurface layer (Fig. 6). TNK and TNT have much weaker seasonal variations than TNR and TNA do. N-IPPK and N-IPPT show similar patterns
and are high from May to August.
The situation in the middle shelf is the most complex (Fig. 15b). TNK
and TNA show opposite trends while TNT and TNR share similar variations. The two oceanic sources, N-IPPK and N-IPPT, peak in August
while the two local sources, N-IPPR and N-IPPA, peak in May. Only NIPPK is present in winter due to relatively high water temperature. The
seasonal variation of TNT is weak while that of N-IPPT is strong, andconstant TNT indicates a balance between input and output. The strong
input ﬂux of DINT and favorable ocean environments contribute to the
maximum N-IPPT in summer.
In the outer shelf (Fig. 15c), both TNK and N-IPPK show dominantseasonal variations. TNK increases from April and peaks in October. NIPPK is highest in March and increases from August to March due to the
upward transport of DINK. With the beginning of stratiﬁcation in spring,

4. Discussion
We evaluated the roles of multiple sources of DIN and DIP for primary production based on aspects of input ﬂux, inventory, primary
production and the relations between these parameters.
In terms of input ﬂux (Fig. 2), the Kuroshio is the most importantsource. The input ﬂux of DINK takes up 70% of the DINW while each of
the other three sources only gains about 10%. The input ﬂux of DIPK
even takes up almost 85% of the total input ﬂux. These ratios werealready reported by previous box models (e.g., Chen and Wang, 1999;
Zhang et al., 2007), but is improved upon here by determining theinventory of each source. The proportion of TNK is smaller than that of
the input ﬂux of DINK while the proportion of TNR doubles that of input
ﬂux of DINR. The proportions of TPK and TPR are in the same situation.
These diﬀerences lie in their diﬀerent ﬂushing time, τ, which indicates
how long nutrients from a single source remain in an area (Takeoka,
1997; Monsen et al., 2002). The above three variables are related asfollows:

inventory = inputflux·τ(3)

τ depends mainly on the physical ﬁeld, and the biological processes
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J. Zhang, et al.

Fig. 14. As in Fig. 11 but for primary production in the case of tracking DIN (mg C m−3 d−1).

straightforward way to reﬂect their role in the primary production. But
results show that IPP has no connection with τ. A long τ for nutrients
does not correlate with a high contribution to IPP, as demonstrated byriverine nutrients. IPP is also not proportional to the inventory of nutrients (Umezawa et al., 2014). The proportion of N-IPPK is smaller thanthat of TNK, while the proportion of N-IPPT is larger than TNT (Table 1,
the whole shelf). The eﬀect of DINK on primary production is overestimated, while that of DINT is underestimated if we judge their eﬀects
on primary production from the proportion of inventory or input ﬂux.
Therefore, evaluating the contributions of multiple sources of nutrientsto primary production from inventory or input ﬂux is not appropriate.
The inventory of nutrients is only a potential source rather than abioavailable source for primary production. Only bioavailable nutrientscan be utilized by phytoplankton and thus inﬂuences biogeochemical
cycles (Jørgensen et al., 2014). This raises a question as to the production eﬃciency for nutrients from speciﬁc sources.
Production eﬃciency of the nutrient source based on Takeoka

play a second role. As a local source, the riverine nutrients concentratein the inner shelf, and it is diﬃcult for them to reach and leave theboundary of the ECS. Consequently, turnovers of DINR and DIPR takeabout 11 months and 8.7 months, respectively. The shorter τ of DIPR is
attributed to the DIP-limiting primary production in the inner shelfwhere DIPR is utilized easily.
The τ of the oceanic DINK is only 3.5 months because most of the
DINK is present in the outer shelf where the water exchange is strong.
The DIPK is similar with a τ of 4 months. DINT and DIPT mainly concentrate in the middle shelf and have an intermediate τ (about
6 months) between that of nutrients from the rivers and the Kuroshio.
The nutrients from the atmosphere near the coast remain longer in the
ECS while those near the shelf break easily exit the ECS. Thus, DINA and
DIPA have a τ (5.5 months and 4.4 months) close to that of nutrientsfrom the Taiwan Strait.
Does a long τ result in a high contribution to primary production?
Primary production supported by nutrients from a speciﬁc source is a14

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Table 1Inventory (TN, 107 kmol), primary production (N-IPP, kmol s−1), and production eﬃciency (EPC) of DIN from rivers, the Kuroshio, the Taiwan Strait and theatmosphere. Production eﬃciency is deﬁned as the ratio of N-IPP to TN. The ‘Total’ column shows the situation of the total DIN, sum of the DIN with diﬀerent
sources. The numbers in parentheses are the corresponding percentages.

Inner shelf(0–50 m)Middle shelf(50–100 m)
Outer shelf(100–200 m)
The entire shelf(0–200 m)

TN(107 kmol)
N-IPP(kmol s−1)
EPC
(day−1)
TN
N-IPP
EPC
TN
N-IPP
EPC
TN
N-IPP
EPC

RiversKuroshio

Taiwan Strait

AtmosphereTotal

2.5 (58%)

0.4 (9%)0.4 (9%)1.0 (23%)

4.3

4.1 (56%)

0.8 (11%)0.8 (11%)

1.6 (22%)

7.3

1/71

1/58

1/58

1/72

1/68

0.9 (12%)1.7 (11%)1/61
0.1 (0.6%)
0.2 (1%)1/29
3.5 (17%)
6.0 (15%)1/67

3.1 (42%)5.8 (38%)1/62
8.1 (92%)
13.5 (78%)
1/69
11.6 (57%)
20.1 (50%)
1/67

1.6 (22%)4.4 (29%)1/42
0.4 (5%)
1.6 (9%)1/29
2.4 (12%)6.8 (17%)1/41

1.7 (23%)
3.5 (23%)1/56
0.3 (3%)
1.9 (11%)1/18
3.0 (15%)7.0 (18%)
1/50

7.3
15.4
1/55
8.9
17.2
1/60
20.5
39.9
1/59

due to low temperature (Fig. 13). Consequently, a large amount of DIN
cannot be used by phytoplankton, resulting in the low EPC of DIN in the
inner shelf. Besides the low primary production, the excess DINR and
DINA intensify their lower eﬃciency. As the primary production islimited by DIP, the EPC of DIP in the inner shelf are larger than those of
DIN (Table 2). The rivers discharge and atmospheric depositions arelack of DIP. The DIPR and DIPA load into the ECS through the surface in
the inner shelf, which are easy to be utilized by phytoplankton than
DIPT and DIPK.
The middle shelf is away from the turbid coastal area. The EPC ofeach source of DIN increases and is larger than those in the inner shelf.
The Taiwan Strait is the most eﬃcient DIN source with a 42-day cycling
period. The DINT dominates high primary production areas in the
middle shelf in spring and summer (Fig. 6) but has a very low concentration in autumn and winter. The N-IPPT and input ﬂux of the DINT
have similar seasonal variations. Both are largest in summer, suggestingthat DINT is fully utilized without waste and therefore DINT is a very
eﬃcient source even though its concentration is low. The EPC for eachsource of DIP is less in the middle shelf than in the inner shelf. The local
sources of DIP keep a higher eﬃciency level than the oceanic sources of
DIP in the middle shelf.
The primary production in the outer shelf is limited by DIN rather
than by DIP (Fig. 13). In addition, the water is clear with a favorable
water temperature to phytoplankton. The DIN from each source except
for the Kuroshio has a high EPC. This is particularly true for DINA, which
is loaded from the ocean surface. In summer, DINA stays at the surface
layer in the outer shelf where the temperature and light condition aregood for primary production, and therefore becomes an eﬃcient DIN(1997) was used to standardize the eﬀects of nutrients from diﬀerent
origins on primary production. Takeoka (1997) used production eﬃciency to compare the function of nutrients in the ecosystems of several
semi-closed seas. The production eﬃciency is deﬁned as the ratio of IPP
to the inventory of nutrients, which indicates the cycling rate of nitrogen, or the reciprocal of one cycling period.

EPC = IPP/inventory(4)

A larger cycling rate means a more eﬃcient function as well as afaster utilization of a speciﬁc source of nutrient. Eﬃcient nutrient
supports higher primary production with lower inventory. In otherwords, the eﬃcient nutrient is bioavailable and easily utilized byphytoplankton.
The controlling factors for production eﬃciency can be represented
by EPC in the three sub-regions (Tables 1 and 2). The EPC of DIN and DIP
from speciﬁc sources (except for DINK) changes greatly in three subregions, suggesting that EPC depends mainly on the location of thenutrients. In diﬀerent regions, the three factors aﬀecting primary production, temperature, light and nutrient limitation vary greatly.
As indicated in Table 1 over the inner shelf, EPC of DIN from different sources are less than 1/50 day−1, indicates a cycling period for
DIN of more than 50 days. That means DIN from any source is relatively
ineﬃcient in the inner shelf. DIN at the surface layer has a higher
concentration in the inner shelf (Fig. 6), which means it may not beutilized eﬀectively. The primary production, which should be higher inthe coastal area, is limited by the low concentration of DIP, and highturbidity (Chai et al., 2006) caused by river loading and strong tidal
mixing. The primary production in the inner shelf in winter is too weak
Table 2
As in Table 1 but for the DIP and related variables.

Inner shelf

Middle shelf

Outer shelf

The entire shelf

6

TP (10 kmol)
P-IPP(kmol s−1)
EPC
(day−1)
TP
P-IPP
EPC
TP
P-IPP
EPC
TP
P-IPP
EPC

RiversKuroshio

Taiwan Strait

AtmosphereTotal

0.31 (26%)
0.16 (34%)

0.38 (32%)
0.13 (28%)

0.47 (40%)
0.17 (37%)

0.01 (1%)
0.004 (1%)

1.17
0.46

1/23

1/34

1/32

1/29

1/29

0.13 (3%)
0.04 (4%)
1/38
0.01 (0.1%)
0.002 (0.2%)
1/58
0.45 (3%)
0.20 (8%)
1/26

3.05 (61%)
0.47 (49%)
1/75
7.99 (94%)
0.92 (86%)
1/101
11.42 (78%)
1.52 (61%)
1/87

1.82 (36%)
0.44 (46%)
1/48
0.49 (6%)
0.15 (14%)
1/38
2.78 (19%)
0.76 (30%)
1/43

0.02 (0.4%)
0.01 (1%)
1/39
0.004 (0.05%)
0.001 (0.1%)
1/46
0.03 (0.2%)
0.01 (0.4%)
1/36

5.02
0.96
1/61
8.49
1.07
1/92
14.68
2.49
1/68

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Fig. 15. Monthly variations in TN from each source (upper panels) and N-IPP supported by each source (lower panels) in (a) inner shelf (0–50 m), (b) middle shelf(50–100 m), (c) outer shelf (100–200 m), and (d) the entire shelf area (0–200 m). Yellow, blue, green, red and black lines with circles represent the sources fromrivers, the Kuroshio, the Taiwan Strait, the atmosphere, and the sum of the four sources, respectively. In the upper panel of (a), the line of Kuroshio source isoverlapped by that of the Taiwan Strait source. (For interpretation of the references to color in this ﬁgure legend, the reader is referred to the web version of thisarticle.)1/41 and 1/50 day−1, are similar and both of them have a better eﬃciency than the DIN from the Kuroshio and the rivers. This is because
DINA and DINT take advantage of the favorable environment in the
middle and outer shelves. The EPC of DIP sources in the entire shelf arequite diﬀerent from those of DIN. With EPC of 1/26 day−1 and 1/
36 day−1, DIPR and DIPA become more eﬃcient sources than DIPK and
DIPT. An apparent reason for this diﬀerence is that DIPR and DIPA
distribute in the sunlit upper layer while DIPK and DIPT in the subsurface layer and even bottom layer. Consequently, the cycle rate of DIPK
(1/87 day−1) is only one third of that of DIPR.
The EPC of DINW and DIPW over the entire shelf are similar to that of
the Kuroshio source. This is because the Kuroshio source of nutrients
shares most proportions of nutrient inventory and supports mostsource. The EPC of DIP sources in the outer shelf decrease comparing tothose in the middle shelf (except for the DIPT), and are lower than thoseof DIN in the outer shelf.
The DINK is not eﬃcient in all three sub-regions. The poor EPC of
DINK results from its location. Most DINK exists below the euphotic
layer and phytoplankton cannot use it. It is only in late autumn andwinter when DINK comes to surface layer. Being the same as DINK, DIPK
is also the least eﬃcient source although they provide more than half ofthe total inventory of nutrients and support half of the primary production in the ECS.
As shown in Table 1, the EPC of DINR over the entire shelf is as same
low that of DINK. The low production eﬃciency of DINR is caused by
DIP and light limitations in the inner shelf. The EPC of DINT and DINA,

Fig. 16. As in Fig. 15 but for the TP and P-IPP.
16

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J. Zhang, et al.

represent the contribution of nutrients from diﬀerent sources to primary production. The production eﬃciency of each source of DIN and
DIP is a way to understand the relation among these evaluation
methods. The Kuroshio shows a leading role in input ﬂux, nutrient inventory, and primary production, but both its DIN and DIP have low
production eﬃciency because a large amount of them distribute below
the euphotic layer. The DIN from rivers has a dominant role in coastal
area, but its production eﬃciency is also low due to local limitations of
DIP and high turbidity. In contrast, the DIP from rivers is eﬃcient because of its full utilization by phytoplankton. The DIN and DIP from
Taiwan Strait are eﬃcient but has no advantage in terms of input ﬂux,
inventory of nutrient, or primary production. The DIN and DIP fromatmosphere are also eﬃcient because they enter the sea from the surface.

primary production over the entire shelf. The DINW is the least eﬃcientin the inner shelf, while the DIPW is the most eﬃcient there. This can be
explained by the DIP limitation on the primary production in the innershelf. Both DINW and DIPW are not eﬃcient in the outer shelf, due totheir higher concentration in the lower layer.
5. Conclusions
Using the physical-biological coupled model and a tracking module,
we examined the distributions of DIN and DIP with diﬀerent origins andthe corresponding primary production in four seasons over the ECS, andevaluated the roles of DIN and DIP with diﬀerent origins in primary
production in the inner, middle, outer and entire shelves of the ECS.
Both physical and biological processes aﬀect the distributions of
nutrients with diﬀerent origins. Physical processes regulate the distribution of the nutrients, mainly through transport and mixing. For
example, the dominant areas of each source nutrient in the inventory ofnutrients generally follow distributions of the water masses. On theother hand, biological processes likely contribute to change the concentrations of nutrients locally, which rely closely on local temperatureand light intensity. This appears as diﬀerent distributions of DIN and
DIP from the same source, which are determined only by biologicalprocesses.
Regarding horizontal distribution, DINR is likely transported with
CDW and coastal currents. DINA is concentrated in coastal and northern
ECS regions following surface currents. The DIP from the rivers andatmosphere show relatively lower concentration. The Taiwan Warmcurrent strongly regulates DINT and DIPT, and the Kuroshio onshore
intrusion has a signiﬁcant inﬂuence on DINK and DIPK. In winter andautumn, nutrients are vertically homogeneous due to strong mixing; inspring and summer, the stratiﬁcation prevents nutrients in the surface
layer from falling and nutrients in the bottom layer from rising. The
primary production supported by diﬀerent sources of nutrients is under
the combined control of nutrients, temperature, and light intensity. The
dominant area of primary production from a speciﬁc nutrient is generally consistent with the distribution of corresponding nutrient source.
In the inner shelf, the DIN from rivers (mainly the Changjiang)shares more than half of DIN inventory and supports more than half ofprimary production. The DIN from atmosphere is the secondary source(> 20%) while those from the Kuroshio and Taiwan Strait both share
only ∼10% of DIN inventory and support ∼10% of primary productionin the inner shelf. The DIP from rivers, the Kuroshio and Taiwan Strait
has almost the same ratio in the DIP inventory and supports almost thesame primary production in the inner shelf. The atmosphere contribution to DIP inventory is negligible. In the middle shelf, the DIN from
Kuroshio shares ∼40% of DIN inventory and supports ∼40% of primary production. The DIN from Taiwan Strait and atmosphere have asimilar ratio (∼20%) in the DIN inventory and primary production andthe DIN from rivers share the residual 10% in both DIN inventory andprimary production in the middle shelf. The DIP from Kuroshio andTaiwan Strait share ∼60% and ∼40% of DIP inventory and supports∼50% of primary production, respectively. Apparently, the contribution of DIP from rivers and atmosphere is negligible. In the outer shelf,
the DIN from Kuroshio shares > 90% of DIN inventory and supports∼80% of primary production, while the DIP from Kuroshio shares >90% of DIP inventory and supports > 80% of primary production.
Therefore, the Kuroshio is a dominant source for the nutrients inventory
and primary production.
Considering the ECS as a whole, both DIN and DIP from theKuroshio are the largest contributor in the nutrient inventory and primary production. The DIN from the Taiwan Strait, rivers and atmosphere shares equal contributions in nutrient inventory and primary
production. The DIP from the Taiwan Strait plays the secondary role,
while the contribution of DIP from rivers and atmosphere are weak.
Primary production supported by each source is a direct criterion,
while neither input ﬂux nor inventory of nutrient is a good index to

Declaration of Competing Interest
On behalf of all coauthors, we declared that there are no conﬂicts ofinterest to this work.
Acknowledgments
This study was supported by a Grant-in-Aid for Scientiﬁc Research(MEXT KAKENHI grant numbers: JP15H05821/26287116) and the
National Natural Science Foundation of China (NSFC) (No. 41576010).
L. Zhao was partly supported by the National Key Research andDevelopment
Programof
China(2016YFA0601301
and
2016YFC1401602), the Strategic Priority Research Program of theChinese Academy of Sciences (XDA11020305), 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). J. Zhang thanks the China
Scholarship Council (CSC) for supporting her stay in Japan and theMinistry of Education, Culture, Sports, Science and Technology, Japan(MEXT) under a Joint Usage/Research Center, Leading Academia in
Marine and Environment Pollution Research (LaMer) Project for supporting her short stay in Japan.
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