The Changjiang is the largest river in Asia and the main
terrestrial source of freshwater and nutrients to the East China Sea (ECS).
Nutrient concentrations have long been increasing in the Changjiang,
especially after 1960 with urbanization, the development of industrial
animal production, and fertilizer application in agriculture, resulting in
coastal eutrophication and recurring summer hypoxia. The supply of
anthropogenic nitrogen (N) exceeds that of phosphorus (P) relative to the
Redfield ratio. This results in seasonal P limitation in the Changjiang
plume. P limitation and its effects on primary production, respiration, and
hypoxia in the ECS have not been studied systematically, although such
knowledge is needed to understand bloom dynamics in the region, to assess
the consequences of altered nutrient loads, and to implement nutrient
reduction strategies that mitigate hypoxia. Using a coupled
physical–biogeochemical model of the ECS that was run with and without P
limitation, we quantify the distribution and effects of P limitation. The
model shows that P limitation develops eastward of the Changjiang Estuary
and on the Yangtze Bank but rarely southward along the Zhejiang coast. P
limitation modifies oxygen sinks over a large area of the shelf by partly
relocating primary production and respiration offshore, away from the
locations prone to hypoxia near the Changjiang Estuary. This relocation
drastically reduces sediment oxygen consumption nearshore and dilutes the
riverine-driven primary production and respiration over a large area
offshore. Our results suggest that the hypoxic zone would be 48 % larger
in its horizontal extent, on average, if P limitation was not occurring.
Results are summarized in a conceptual model of P limitation on the ECS
shelf that is also applicable to other systems. Then we carried out nutrient
reduction simulations which indicate that, despite the effect of P
limitation on hypoxia, reducing only P inputs as a nutrient reduction
strategy would not be effective. A dual N + P nutrient reduction strategy
would best mitigate hypoxia. The model results suggest that decreasing the
size of the hypoxic zone by 50 % and 80 % would require reductions in
N + P load of 28 % and 44 %, respectively.
Introduction
The expansion of eutrophication-driven hypoxic conditions, i.e., O2<2 mg L-1 or 62.5 mmol m-3, has been a growing issue for
the coastal ocean in the past decades (Diaz and
Rosenberg, 2008; Fennel and Testa, 2019). Coastal eutrophication occurs when
excess nitrogen (N) and phosphorus (P) nutrients, associated mainly with the
use of synthetic fertilizer in agriculture, wastewater discharge in urban
areas, and livestock farming
(Alexander et al., 2008; Chen
et al., 2020) reach the coastal ocean where they stimulate primary
production, the development of harmful algal blooms
(Glibert et al., 2014;
Heisler et al., 2008), and subsequently respiration and O2 depletion in
subsurface waters (Fennel and Testa, 2019). Low O2
can have detrimental effects on the benthos
(Levin et al., 2009) and the food web
(Kidwell et al., 2009) and ultimately have economic
consequences for fisheries (Rabalais
and Turner, 2001; Smith et al., 2017).
In large eutrophicated estuaries and river plumes (e.g., Mississippi River
plume, Changjiang Estuary, Chesapeake Bay), phytoplankton growth is typically
limited by light in winter, as well as in the highly turbid waters in the
vicinity of the river outflow, whereas maximum production often occurs
downstream where both light and nutrients are plentiful
(Cloern, 1987; Fennel et al., 2011;
Lohrenz et al., 1997, 1999). In downstream waters, productivity is
controlled by the availability of nutrients
(Fennel and Laurent, 2018; Malone et al.,
1996). There, the stoichiometry of dissolved inorganic N (DIN), P (DIP), and
possibly silicate (Si) in the river source will partly determine where, when,
and which nutrient is most limiting
(Dagg et al., 2004; Laurent et al.,
2012).
The stoichiometry of dissolved inorganic N (DIN) and P (DIP) inputs from
rivers has been modified by the onset of cultural eutrophication. Sources of
DIN are usually spatially diffuse, associated with the use of fertilizer for
agriculture (Seitzinger and Harrison,
2008). Although diffuse sources of DIP are also important in intensive
farming regions (Boesch, 2019; Wurtsbaugh et al.,
2019), sewage point sources can dominate DIP export (Harrison
et al., 2010). The construction of dams in a river basin may also alter the
delivery of particulate phosphorus to the coastal ocean
(Beusen et al., 2016; Hu et
al., 2020). Successful point source mitigation has modified nutrient
stoichiometry in rivers resulting in a growing excess of N and DIN : DIP
ratios significantly larger than the Redfield ratio of 16
(Westphal et al., 2020). This leads to P limitation of
phytoplankton growth in coastal waters and the modification of bloom
dynamics (Laurent et al., 2012) and consequently
hypoxia (Laurent and Fennel, 2014, 2017).
One of the world's largest eutrophication-induced hypoxic zones is in the
East China Sea (ECS), a large and highly productive marginal sea on the
western edge of the North Pacific surrounded by Taiwan, China, Korea, and
Japan. The main terrestrial source of freshwater and nutrients to the ECS is
the Changjiang (Tong et al.,
2015), the largest river in Asia (Liu et al.,
2003). Nutrient concentrations have long been increasing in the Changjiang,
especially after 1960 with the development of urbanization, industrial
animal production, and fertilizer application in agriculture
(Dai
et al., 2011; Jiang et al., 2014; Liu et al., 2009, 2018; Strokal et al.,
2016; Wang et al., 2020; Yan et al., 2003, 2010). Coastal eutrophication
within the Changjiang plume leads to recurrent algal blooms
(Chen et al., 2019a; Li
et al., 2014; Wang and Wu, 2009) and the development of subsurface hypoxic
conditions in summer (Li et al.,
2011; Ning et al., 2011; Wang et al., 2016). Although freshwater
(stratification) and wind (destratification) are important for the
establishment and sustainment of hypoxic conditions
(Zhang et al., 2020), the Changjiang's N load
has been shown to be the main contributor to hypoxia on the shelf
(Große et al., 2020).
Typically, primary production is limited by light in the Changjiang
estuarine and sediment plume waters, whereas nutrient limitation may occur
in the transition zone and further offshore
(Harrison et al., 1990; Li et al.,
2021; Zhu et al., 2009). As elsewhere, the unbalanced supply of DIN and DIP
from the Changjiang
(Liu
et al., 2003, 2018; Shi et al., 2022) led to the development of P limitation
on the shelf (Li et al., 2009; Wang et al., 2015).
Based on laboratory studies and local observations, there are indications
that high N : P and the onset of P limitation on the ECS shelf alter the
species composition of phytoplankton blooms
(Li et al., 2009; Ou et
al., 2020; Xing et al., 2016; Zhou et al., 2008). Despite this knowledge, P
limitation has not been studied systematically in the region, and its effects
on primary production, respiration, and hypoxia remain unknown. However,
understanding the effects of nutrient limitation on O2 biogeochemistry
is essential for assessing the consequences of altered nutrient loads on
hypoxia dynamics and therefore to implement nutrient reduction strategies to
mitigate hypoxia on the shelf. Preliminary N load reduction experiments in
the Changjiang show that significant N reduction is necessary to mitigate
hypoxia (Große et al., 2020;
Zhou et al., 2017). P was not included in these experiments but needs to be
considered to assess the efficiency of single versus dual nutrient
management strategies.
Here, through simulations with and without P limitation in the coupled
circulation–biogeochemical model of Zhang
et al. (2020), we investigate nutrient limitation in the ECS. The goal is to
quantify the effects of P limitation and provide insights for reducing
hypoxia in the region. First, we validate the model with observed nutrient
concentrations. We then describe the occurrence and spatial distribution of
P limitation on the shelf and its effect on O2 sources and sinks and
hypoxia. Using these results, we develop a conceptual model of P limitation
for the ECS. Finally, by conducting scenario simulations with reduced
nutrient loads from the Changjiang, we investigate the efficiency of
different nutrient reduction strategies to mitigate hypoxia on the shelf.
MethodsModel description
The circulation model is a regional implementation of the Regional Ocean
Modelling System (ROMS, version 3.7;
Haidvogel et al., 2008)
configured for the East China Sea and surrounding areas
(Bian et al., 2013; Fig. 1). The
grid has a 1/12∘ resolution and 30 vertical layers with increased
resolution near the surface and bottom. The circulation model uses the
recursive multidimensional positive definite advection transport algorithm
(MPDATA) for the horizontal advection of tracers and a third-order upwind
scheme for the advection of momentum. Vertical mixing is parameterized using
the generic length scale (GLS) turbulence closure scheme
(Umlauf and Burchard, 2003).
Model domain and bathymetry (a), subregions used for analysis
(zones 1–6, b), and schematic of the biological model (c). Details on O2 sources and sinks are provided in
Laurent et al. (2017). On the left panel, the Changjiang is
shown in red. The CE–Jeju Island transect is represented by a red line. The
black box is the limit of the region shown in (b).
The circulation model is coupled online with the biogeochemical model of
Fennel et al. (2006, 2011) that was extended to
include phosphate (Laurent et al., 2012),
O2 (Fennel et al., 2013), river dissolved organic matter
(DOM; Yu et al., 2015), and a light attenuation scheme that
simulates higher attenuation in shallow areas and in the river plume
(Zhang et al., 2020). The model has 10 state
variables: phytoplankton, chlorophyll, zooplankton, nitrate and ammonium
(DIN), phosphate (DIP), O2, and three detritus pools (small and large
detritus, river DOM). Silicate (Si) is not included in the model as it is
assumed to be non-limiting. During the simulation period, observed Si / N and
Si / P were close to and above Redfield, respectively
(Shi et al., 2022). The single
phytoplankton group includes all phytoplankton types and therefore does not
differentiate between diatoms and dinoflagellates.
Zhang et al. (2020) showed that these
choices are appropriate to represent the bulk surface chlorophyll in the
Changjiang plume, as well as spatial and temporal variations in subsurface
O2. At the sediment–water interface, sinking particulate organic N
(PON) and P (POP) are instantaneously remineralized into ammonium and
phosphate, respectively, accounting for a fraction of PON lost through
denitrification (Fennel et al., 2006). Sediment O2
consumption (SOC) is parameterized assuming a linear relationship with
denitrification (Fennel et al., 2013; Seitzinger and
Giblin, 1996).
The model includes seven rivers. Daily freshwater discharge observations
from Datong hydrological station (Fig. 1) and
monthly NO3 and PO4 loads from the Global NEWS model
(Wang et al., 2015) are used to represent Changjiang
conditions. Monthly or annual climatologies are used for the other rivers.
Boundary conditions for temperature, salinity, NO3, PO4, and
O2 are specified from the World Ocean Atlas
(Garcia
et al., 2013a, b; Locarnini et al., 2013; Zweng et al., 2013), whereas
horizontal velocities and sea surface elevation use the SODA dataset
(Carton and Giese, 2008). A
small positive value is used for all other biological variables. Surface
forcing is prescribed using the ECMWF ERA-Interim dataset
(Dee et
al., 2011).
A schematic of the biogeochemical model is provided in
Fig. 1. The model equations are available in the
supporting information of Laurent et al. (2017); setup and
validation are described in detail in
Zhang et al. (2020). Biogeochemical model
parameters are also available in Zhang et
al. (Table S1).
Nutrient limitation
Phytoplankton growth is limited by light (E), temperature (T), and the most
limiting nutrient (either DIN or DIP) such that the specific phytoplankton
growth rate (μ; d-1) is calculated as
follows:
μ=μmax(ET)⋅Ltot,
where μmax(ET) is the light- and temperature-dependent
maximum growth rate of phytoplankton, and Ltot
(0<Ltot<1) is the minimum of the nutrient limitation factor
for DIN (LN) and DIP (LP). Ltot is
calculated from nitrate (NO3), ammonium (NH4), and DIP
using Eqs. (2)–(5) below.
2LNO3=NO3kNO3+NO3⋅11+NH4/kNH4,3LNH4=NH4kNH4+NH4,4LN=LNO3+LNH4,5LP=DIPkDIP+DIP.
Following Laurent et al. (2012), we assume in
the following analysis that N is limiting when
Ltot<0.85 and LN<LP,
whereas P is limiting when Ltot<0.85 and
LP<LN. Although this threshold is somewhat
arbitrary, our assumption is only used to describe the regions where N and P
are most limiting, and therefore, the selected value does not influence the
simulation results, only their interpretation.
Simulations
All the simulations were run for 8 years with daily output. The first 2
years were considered spin-up, and the period 1 January 2008 to 31 December 2013 was used for analysis. The “baseline” simulation, as described above,
is identical to Zhang et al. (2020). To
assess the effect of P limitation, the baseline is compared to a simulation
without P limitation (“NoPlim”), which is implemented by disabling P in the
biological model but otherwise keeping everything identical to the
“baseline” simulation. Because this model did not include P, it simulated
the situation without any P limitation. In addition, 15 scenario simulations
were carried out where riverine N, riverine P, and riverine N and P
concentrations were decreased stepwise in 20 % increments. Otherwise,
these simulations were identical to the baseline simulation. Each reduction
level is applied to all nutrient subspecies (i.e., dissolved inorganic,
dissolved and particulate organic).
For analysis, the shelf region adjacent to the Changjiang Estuary (CE) is
divided into six zones. Zone 1 represents the Jiangsu coastal area (z<25 m; lat: 31.70∘–33.50∘). Zones 2 and 3 are the northern and
southern hypoxia cores, respectively, defined in
Zhang et al. (2020). Zone 4 represents
the Yangtze Bank area (z<50 m; lat: 30.75∘–33.50∘),
whereas Zones 5 (lat: 30.75∘–33.50∘) and 6 (lat: 28.52∘–30.75∘) represent the northern and southern deep shelf waters
(50<z<100 m), respectively.
ResultsRiverine input
DIN and DIP concentrations are high year-round in the Changjiang
(Fig. 2), although DIP concentration tends to peak
in the fall, whereas DIN concentrations can vary from year to year. DIN and
DIP loads are highly correlated with freshwater discharge (Pearson's
correlations of 0.95 and 0.98, respectively), and therefore, their annual
maxima occur at the time of highest discharge, usually from June to August.
The DIN : DIP ratio is 69 on average, well above the Redfield ratio of 16, and
ranges from 54 to 78. Hence, nutrient loads from the Changjiang are
conducive to P limitation on the continental shelf near the CE.
Changjiang river forcing data. (a) Freshwater discharge
from the Datong hydrological station (Fig. 1) and
nutrient loads. (b) Nutrient concentrations and ratio.
Surface nutrient concentration
In fall and winter, the Changjiang plume is restricted to the coast, and the
surface PO4 concentration is high (>2 mmol m-3) in the
CE and Hangzhou Bay (Fig. 3a, d). PO4
concentration in the plume is at an annual maximum at this time, and PO4
is transported southwestward with the plume along the Zhejiang coast. The
circulation reverses in spring when the plume transports Changjiang waters
offshore northeastward over the Yangtze Bank (Fig. 3b). Offshore transport is at its annual maximum in summer
(Fig. 3c). PO4 is ∼ 2 mmol m-3 in the CE, but plume concentrations decrease to very low values
offshore (Fig. 3e, g, h, k). NO3 follows
similar seasonal and spatial patterns, but plume concentrations remain
elevated offshore in summer (20–40 mmol m-3; Fig. S1), contrasting
with PO4 concentrations.
(a–d) Simulated seasonal means of surface PO4 (2008–2013). The
black contours indicate the 25 and 30 isohalines. (e–k) Comparison of
simulated surface PO4 (colored maps) with the observations of
Gao et al. (2015) for the dates indicated in each panel
(colored dots). Simulated PO4 corresponds to the average conditions
during the cruise.
Simulated surface nutrient concentrations are compared with the observations
of Gao et al. (2015) in Fig. 3e–k (PO4) and Ge et al. (2020) in the Supplement Fig. S1 (NO3). PO4 and NO3 concentrations compare reasonably well
with Pearson's correlation coefficients of 0.75 and 0.84, respectively. The
model simulates the observed CE offshore gradient, as well as the magnitude
of nutrient concentrations in the CE and the Changjiang plume. The model
also captures the locations of PO4 and NO3 depletion in offshore
waters in summer.
P limitation on the ECS shelf
The spatial distribution of nutrient limitation is shown in
Fig. 4. As mentioned earlier, we assume hereafter
that N or P limitation occurs when the limitation factor is <0.85,
and otherwise there is light limitation or no limitation. In
Fig. 4, the daily occurrence of such conditions
for N and P is presented as an annual average (days of N or P limitation per
year). Near the CE, nutrient concentrations are high (see
Figs. 3 and S1), and neither N (left panel) nor P
(right panel) is limiting. Nonetheless, light can limit phytoplankton
growth in this region (Zhang et al., 2020).
Offshore (z>5 m) and outside the freshwater plume and
along the northern Jiangsu coast, N is limiting for most of the year. P
limitation occurs for 2–3 months near and on the Yangtze Bank in zones 2
and 4. It also occurs occasionally further east and in zone 3 but never in
the coastal area north of the CE where N is limiting. N limitation is
prevalent offshore (zones 5 and 6).
Annual duration in days of N (a) and P (b) limitation in
surface waters. The grey contours indicate the limits of the six zones (see
Fig. 1).
Spatial variability in P limitation occurs mainly along a west–east axis
from the CE, in particular along the CE–Jeju Island (JI) line
(northeastward; Fig. 1). The variability along
this axis is presented through CE–JI transects in
Figs. 5, 6, and
S2. P limitation develops about 100 km offshore of the CE
between May and September (Fig. 5) and is found
sporadically all the way to Jeju Island in August–September. Outside of a
100–150 km wide area that forms the core of seasonal P limitation, mostly
within zone 4, the occurrence of P limitation is variable and depends on the
offshore expansion of the Changjiang plume, as represented by the 29
isohaline in Fig. 5. For example, in 2010 (high
discharge; Fig. 2) P limitation occurred over 68.0 × 103 km2 on average (May–August), extending all the way
to Jeju Island for >2 weeks in August. In comparison, P
limitation covered only 31.4 × 103 km2 on average in 2011
(low discharge). The maximum annual extent of P limitation usually occurs in
late July–early August (95.4 × 103 km2, 2008–2012 average;
Table 1). The annually integrated area of P limitation is highly correlated
with freshwater discharge from the Changjiang (r=0.79,
p=0.06). Higher discharge promotes a larger and more sustained
area of P-limited surface waters.
Time series of the nutrient limitation factor along the CE–JI
transect (see Fig. 1). The color represents the
most limiting nutrient at each time and location, either N (blue) or P (red).
The thin black line indicates the location of the 29 isohaline. The dots on
the right y axis indicate the limits of zones 2, 4, and 5.
Extent of P limitation on the shelf in 2008–2012 and timing of the
maximum area.
Mean areaMax areaIntegrated area(103 km2) (103 km2 yr)200834.071.9 (26 Jul)4800200953.494.6 (4 Jul)7454201068.0126.4 (4 Aug)9122201131.486.5 (2 Aug)4520201253.7100.0 (16 Jul)7580201345.593.0 (9 Aug)6224
In most years, the expansion of P limitation along the transect occurs over
two periods: one of limited spatial extent in the spring and the main one in
summer (Fig. 5). In spring and summer when the
plume does not reach Jeju Island, the shelf area surrounding the island is
strongly N-limited.
The vertical distribution along the transect line indicates that P
limitation is well developed in late July and occurs mainly in the upper 5 m
of zone 4, where the offshore edge of the plume is located
(Fig. 6a). Further offshore, outside of the plume,
strong N limitation occurs within the upper 10 m. P limitation is more
variable and starts to break down in late August
(Fig. 6d).
Mean vertical transects along the CE–JI line (see
Fig. 1) for 15–31 July (a–c) and 15–31 August
(d–f). Left panels (a, d): nutrient limitation factors. The color represents
the most limiting nutrient at each location and depth, either N (blue) or P
(red). Central and right panels: change in primary production (b, e) and
water column respiration (c, f) due to P limitation (baseline – NoPlim).
Thin grey lines represent the no limitation isoline in panels (a) and (d)
(limitation factor = 1) and are indicative of PP and WR contours in panels
(b) and (e) and panels (c) and (f), respectively. The x axis is in kilometers from the CE along
the CE–JI line.
Consequences of P limitation
The effects of P limitation are quantified from the difference between the
baseline and NoPlim simulations. Along the CE–JI transect, P limitation
reduces primary production by 20 and 45 mmol O2 m-2 d-1 on
average in July in zones 2 and 4, respectively
(Fig. 6b, Supplement Table S1). The reduction
occurs at the surface, whereas an increase is found just below (zone 4) and
offshore (+45.0 mmol O2 m-2 d-1 in zone 5). The decrease in
primary production translates into sediment O2 consumption (SOC) which
decreases significantly around zone 4 (-32.9 mmol O2 m-2 d-1;
Supplement Fig. S2) and into water column respiration (WR) that is also
reduced at the surface in zone 4 (Fig. 6c). This
WR reduction is compensated by a subsurface increase; thus, integrated over
the water column, the change in WR is negligible in zone 4 in July
(Supplement Table S1). The change in respiration can be explained by the
effect of particulate organic matter (POM) concentration on POM flux
(Supplement Fig. S2). As primary production decreases at the surface of
zone 4, less organic matter settles down to the bottom (-4.6 mmol N m-2 d-1). Concurrently, as POM aggregation is proportional to the square of
small POM concentration (phytoplankton + small detritus), the POM sinking rate
decreases, and proportionally more remineralization occurs in the water
column and less in the sediment. This explains the subsurface increase in
water column respiration in zone 4 despite the decrease in surface primary
production. Further offshore in zone 5, WR increases as well (+5.20 mmol O2 m-2 d-1).
When P limitation breaks down in late August (Fig. 6d–f), primary production is still reduced near the coast (-25.0 mmol O2 m-2 d-1 in zone 2) but increases in the upper 5 m in the
northeastern part of zone 4 and in zone 5 (+17.0 mmol O2 m-2 d-1). Concomitantly, a significant increase in water column respiration
occurs throughout the water column in the northeastern part of zone 4
(+4.90 mmol O2 m-2 d-1 overall) and in the surface waters
of zone 5 (+9.90 mmol O2 m-2 d-1).
Figure 7 provides the spatially integrated seasonal
evolution of the effect of P limitation on production and respiration. Note
that the zones have different sizes (Fig. 1), and
therefore, at the same magnitude, the effect shown in
Fig. 7 is spatially more concentrated in smaller
areas (zone 2) and more diffuse in larger areas (zones 4–5). Spatially
averaged values are also available for each zone in the Supplement Fig. S3. In
zone 2, P limitation has a negative effect on primary production that is
reduced from April to September (-546 × 108 mol O2 yr-1), whereas it supports primary production in zone 5 from May to
October, with a peak in July–August (+684 × 108 mol O2 yr-1; Fig. 7a). In the intermediate zone 4,
primary production decreases from April to July and then increases between
August and October (-197 × 108 mol O2 yr-1). This
temporal switch is also found when the effect of P limitation on primary
production is integrated over the shelf (zones 1–6, grey area). Overall, the
integrated change in primary production is negligible relative to total primary production (PP; -34.0 × 108 mol O2 yr-1; Supplement Table S2). The
spatial relocation also occurs in the O2 sinks, but simultaneously,
there is a shift in respiration from the sediment to the water column
(Fig. 7b–c). Water column respiration does not
change significantly in zone 2 (-21.0 × 108 mol O2 yr-1) but increases in zones 4 (August–October, +188 × 108 mol O2 yr-1) and 5 (June–October, +329 × 108 mol O2 yr-1; Fig. 7b). Sediment
respiration increases simultaneously in zone 5 (+202 × 108 mol O2 yr-1; Fig. 7c), somewhat
compensating for the decrease in zone 2 (-271 × 108 mol O2 yr-1). A large decrease in sediment respiration occurs in zone 4
between May and August (-553 × 108 mol O2 yr-1;
Fig. 7c). The shift in respiration is clear when
integrating over the shelf (shaded areas in Fig. 7b–c). The negative effect on sediment respiration is larger than the
positive effect on water column respiration, and therefore, the total change
in respiration over the shelf (zones 1–6) is -164 × 108 mol O2 yr-1 (Supplement Table S2).
Spatially integrated change due to P limitation for primary
production (a), water column respiration (b), and sediment O2
consumption (c) in zone 2 (blue), zone 4 (orange), zone 5 (red), and zones
1–6 combined (shaded area). Each dot represents a monthly mean for
2008–2013.
The effect of P limitation on respiration influences the duration and
spatial extent of hypoxia mainly north of 30∘ N (Fig. 8a). The
largest effect occurs in the region adjacent to the CE where hypoxia
duration decreases by up to 31 d yr-1 on average. Hypoxia extends
further north and northeast into zone 4 without P limitation; hypoxia is less
frequent in this area but can last up to 20 d yr-1 on average (Fig. 8a). The areal difference in the region exposed to hypoxia with and without
P limitation is 21 957 km2, which represents a 34 % decrease due to P
limitation (Fig. 8a). Integrating hypoxia in time and/or space is
informative for the effect of P limitation (Fig. 9). Typically, the
hypoxic area starts developing in June and extends throughout August to reach
its maximum size in early September (Fig. 9a). The effect of P
limitation on the hypoxic area is large in August and remains significant at
the peak extent in September. The decrease in hypoxia extent occurs mainly
in zones 2 and 4, with a small additional decrease in zone 3 in September
and October (Fig. 9b). In zone 2, the change is somewhat
proportional to the size of the hypoxic area, whereas in zone 4 most of the
effect is concentrated in August, hence the large decrease in hypoxic area
in August.
Change in hypoxia duration due to (a) P limitation (baseline –
NoPlim) and to (b–e) nutrient reduction in the Changjiang. The black contour
indicates the area where annual hypoxia duration is at least 1 d in the
baseline simulation (2008–2013 mean). The orange contour (a) and the
dashed red and blue contours (b–e) are the equivalents in the NoPlim
and nutrient load simulations, respectively.
Averaged hypoxic area in the baseline (blue) and NoPlim (red)
simulations (a) and difference in time-integrated hypoxic area for each
zone (baseline – NoPlim) (b). Both panels represent averaged values for
2008–2013.
Effects of altered nutrient loads
Reducing N and/or P concentration in the Changjiang river affects the
spatial distribution and the duration of hypoxia on the shelf
(Fig. 8b–e). Lowering nutrient concentrations
first reduces hypoxia duration in the northern hypoxia core next to the
Changjiang Estuary (Fig. 8b–c). The effect of
nutrient reduction extends to the southern hypoxia core at higher reduction
levels (Fig. 8c–d). The spatial differences for
each reduction type (N + P, N-only, or P-only) are small for a 20 %
reduction (corresponding to 80 % load; Fig. 8b)
but significant at a 40 % nutrient reduction or more
(Fig. 8c–e). N + P and N-only reductions have a
similar effect on hypoxia reduction in the southern area (zone 3), but N + P
reduction enhances hypoxia reduction in the northern area (zone 2). The
N + P and N-only reduction strategies reduce hypoxia to the two core zones at
a 60 % nutrient reduction level (Fig. 8d) and
lead to normoxic waters with an 80 % reduction
(Fig. 8e). On the contrary, hypoxia remains widely
distributed with a P-only strategy, especially in the southern hypoxia core
that does not respond to P reduction. Even at 80 % P reduction the effect
on hypoxia is limited in this area (Fig. 8e).
The general outcome of the three strategies is explored by integrating the
hypoxic area over time in zones 2–3 and over all areas at various nutrient
loadings (Fig. 10, Table 2,
and the Supplement Tables S3 and S4). The N + P strategy has the largest effect
on hypoxia over the ECS. At 80 % and 60 % of the original river N + P
load, hypoxia is reduced on average by 37 % and 69 %, respectively
(Table 2). The N-only strategy has a lesser effect,
whereas the effect of a P-only strategy is limited. The P limitation effect
on hypoxia is not spatially homogeneous and varies between zone 2 (north)
and zone 3 (south) (Fig. 10, Supplement Tables S3
and S4). N + P reduction is clearly the best strategy to reduce hypoxia in
zone 2, whereas N-only and P-only have a similar effect at low to
intermediate reductions, and P-only has less of an effect at high P reduction.
Although N + P reduction has the largest effect on hypoxia in zone 3, there
is little difference with the N-only strategy. In this region the P-only
strategy has a much smaller effect on hypoxia.
Effect of nutrient reduction on the size of the hypoxic area
(time integrated) for zones 1–6 combined (a), zone 2 (b), and zone 3 (c). The results presented are an average for 2008–2010. The equivalent
for 2011–2013 is presented in the Supplement Fig. S4.
Summary of time-integrated hypoxic area (km2 year) in the
baseline and nutrient reduction experiments. Experiments are indicated as
percent load relative to the baseline.
Overall, the efficiency of a N + P nutrient reduction strategy, i.e.,
percent reduction in hypoxia (Hbar) per percent reduction in nutrients
(Table 2), is 1.87, 1.73, and 1.52 for a 20 %,
40 %, and 60 % reduction, respectively. At these levels the average
efficiency of a N-only nutrient reduction strategy is 1.31, whereas the
average efficiency is only 0.84 for a P-only nutrient reduction strategy.
The efficiency is somewhat higher in zone 2 at 2.02, 1.86, and 1.58 for a
20 %, 40 %, and 60 % N + P reduction and an average of 1.31 for N-only
and 1.01 for P-only reductions (Supplement Table S3). The efficiency is
lower in zone 3 at 1.58, 1.55, and 1.44 for a 20 %, 40 %, and 60 %
N + P reduction and an average of 1.29 for N-only and 0.58 for P-only
reductions (Supplement Table S4).
DiscussionDistribution of P limitation on the shelf
Simulated nitrogen and phosphorus distributions off the CE
(Figs. 3, S1) were in good
agreement with observations
(Gao et al.,
2015; Tseng et al., 2014; Wang et al., 2014). P limitation did not occur in
the vicinity of the CE where both NO3 and PO4 are high, as well as
along the Jiangsu coast. This northwestern area is N-limited for most of the
year, indicating a general lack of influence by Changjiang nutrients. During
the productive season, PO4 was depleted rapidly in the plume and the
excess nitrogen transported northeastward with the Changjiang plume in late
spring and summer.
The resulting P limitation in offshore waters expanded to Jeju Island in the
northeast at the seasonal peak of the plume expansion
(Fig. 5). Observations were limited to the inner
shelf, and nutrient addition bioassays were not available to compare with the
simulated patterns. Nonetheless, early bioassay measurements confirm the
presence of P limitation in the region (Harrison et
al., 1990). Furthermore, the large-scale distribution of surface nutrients
and their limitation effect on primary production are consistent with the
main seasonal circulation (Bai et al.,
2014; Liu et al., 2021), with observations off the CE
(Li et al., 2009; Wang et al., 2015), as well as
with observations of Changjiang-related excess NO3 in the northeastern
ECS (Wong et al., 1998) and near Jeju
Island (Kodama et al., 2017; Moon et al., 2021). Yet,
additional bioassay data would be useful to validate the simulated patterns
of nutrient limitation.
Despite its large-scale distribution, P limitation was most prominent over
the southwestern part of the Yangtze Bank (Fig. 4)
from mid-July to early August (Fig. 6), i.e.,
around the peak of the discharge. The temporal evolution (appearance in late
spring, peak in mid-summer, disappearance in late summer and fall) and
spatial distribution of P limitation (development downstream in the plume,
peak at mid-shelf, switch to N limitation further offshore) were
characteristic of river-induced P limitation in open, dispersive systems
(Laurent and Fennel, 2017). For instance, in the somewhat
similar Mississippi River plume in the northern Gulf of Mexico, seasonal P
limitation is observed around mid-shelf at the peak of annual production,
between a light-limited area in the vicinity of the river and the N-limited
downstream and offshore waters
(Laurent et al., 2012;
Sylvan et al., 2006). Phytoplankton growth limitation in the ECS followed
these general patterns along the CE–JI transect but over a larger spatial
scale given the dispersive nature of the Changjiang plume
(Liu et al., 2021).
The particularity of the ECS was the lack of sustained P limitation in the
southern hypoxia core (zone 3). Several factors may be at play there: local
P regeneration, offshore P supply, or the plume orientation. N and P
regeneration have different dynamics in the model; regenerated N is partly
lost through denitrification in the sediment, whereas P is regenerated
following Redfield (1:16 N : P). “Excess” P (relative to Redfield) is
therefore produced during remineralization in the sediment. Yang et al. (2017) found the highest sediment P recycling and DIP sediment–water flux along
the Zhejiang coast (zone 3), which is consistent with the spatial
distribution of P limitation in the baseline simulation. P limitation
reduces SOC in zones 2 and 4 (Fig. 7c) and
therefore lowers the “excess” P associated with sediment recycling, which
represents a positive feedback on P limitation in the northeastern area.
This decrease is 14 % and 16 % in zones 2 and 4, respectively (-0.06 and
-0.05 mmol P m-2 d-1), but only 4 % in zone 3 (-0.01 mmol P m-2 d-1) on average. Nonetheless, this effect is somewhat small,
and therefore P regeneration is only partly responsible for the lack of P
limitation in zone 3. Große et al. (2020) recently showed that N supply from the Kuroshio and Taiwan Strait
contributes 38 % of oxygen consumption in the southern hypoxic region
(equivalent to zone 3). Assuming at least equal contributions of N and P,
then offshore supply should be an important factor mitigating P limitation
in zone 3. Evidence of P supply from the Kuroshio (Yang et
al., 2012) and from the Taiwan Strait (Huang et al., 2019) to
the southern ECS supports this mechanism. Those are also a source of O2
to the region (Zhang et al., 2020). Hypoxia
occurs later in the southern core region, when the circulation reverses in
late summer/early fall. This different timing and the dynamic of the plume
at that time (i.e., attached to the coast) may also prevent the development
of P limitation in the southern hypoxia core.
Effects on oxygen dynamics and hypoxiaSpatial shift and dilution
The hotspot of P limitation off the CE and on the Yangtze Bank had an
important controlling effect on primary production, respiration
(Figs. 6, 7,
S2, and S3), and consequently on the duration and extent of
the hypoxic area in summer (Fig. 8). In estuarine
and coastal systems, P limitation promotes N export to downstream waters,
thereby shifting primary production both in time and space
(Paerl et al., 2004). This shift is
concomitant with a dilution in dispersive systems and therefore limits the
deoxygenation of bottom waters (Laurent and Fennel, 2017). The
shift/dilution effect occurred in our simulations (Fig. 7a). Part of the
production was spatially relocated from zones 2 and 4 (spring–summer) to
zones 4 and 5 (summer). The total change in primary production in the study
area (zones 1–6) varied by less than 1 % between the baseline and the
NoPlim simulations, and therefore the induced variations remained within the
shelf. The downstream dilution effect can therefore be quantified by
calculating the area-specific change in primary production between the
baseline and the NoPlim simulations (Supplement Table S5). The annual change
in primary production due to P limitation was -3010 mmol O2 m-2
in zone 2 and +1310 mmol O2 m-2 in zone 5. The decrease in the
area-specific value from zone 2 to zone 5 reveals that primary production was
diluted during its relocation downstream. In comparison, the area-specific
change in primary production is small in the intermediate zone 4 (-328 mmol O2 m-2). The dilution of PP is an important characteristic of P
limitation because it modifies POM flux, respiration, and therefore the
formation of hypoxia (Laurent and Fennel, 2017). Similarly, we
can calculate that the annual change in total respiration (WR + SOC) is
-1610 mmol O2 m-2 in zone 2 and +1020 mmol O2 m-2 in
zone 5, which represents a 37 % decrease in the absolute change (+1230 mmol O2 m-2 and a 23.6 % decrease for zone 4).
Conceptual model of P limitation on the ECS shelf. Dashed lines
indicate the effects without P limitation (NoPlim simulation). (1)–(5)
Conceptual model of river-induced P limitation along the Changjiang–Jeju
Island transect adapted from Laurent and Fennel (2017). (1) dominant limitation factor; (2) spatial and temporal relocation of “excess N”;
(3) spatial relocation and dilution of PP; (4) spatial shift and dilution and
vertical relocation of respiration; (5) weakening of stratification due to
plume mixing; (6) mitigating effect on the northern hypoxia core and the
Yangtze Bank; (7) no effect of P limitation on the southern hypoxia core; (8) nutrient sources from the Taiwan Strait and the Kuroshio as shown by
Große et al. (2020); (9) lower
denitrification represents a small positive feedback on eutrophication.
Vertical relocation
The change in primary production affected not only total respiration but
also its vertical distribution. POM aggregation, and thus sinking rate, is a
quadratic function of concentration in the model, and therefore, lower primary
production favors remineralization in the water column rather than in the
sediment. This vertical relocation was relatively small in comparison to the
dilution effect; the maximum change in the ratio WR : (WR + SOC) was
+11 %, +16 %, and -3 % in zones 2, 4, and 5, respectively (see
Supplement Fig. S5). The relative increase in SOC in zone 5 was due to the
additional primary production that led to increased deposition. This effect
was small in comparison to zones 2 and 4 partly because zone 5 is deeper
(zmean=75 m versus ∼ 37 m).
Positive feedback on eutrophication
The net increase in WR relative to SOC is important because of the
proportionality between sediment denitrification and SOC
(Fennel et al., 2009). Denitrification ranges from 0.7
(zone 5) to 2.9 (zone 2) mmol N m-2 d-1 in the baseline simulation
(annual average). This is within the lower range of recent observations in
the coastal ECS (Lin et al., 2017). The total annual
decrease in denitrification resulting from P limitation over the study area
(zones 1–6) was 75.0 × 108 mol N (-6.2 %). This effect is quite small
in comparison to the spatial relocation and dilution of O2 sinks but
nevertheless represents a positive feedback on eutrophication in the ECS.
Mitigating effect on the northern hypoxia core and the Yangtze Bank
SOC is an important process in the ECS (Zhou et al., 2017)
and the dominant O2 sink below the pycnocline
(Zhang et al., 2020). It is therefore not
surprising that the change in SOC around the northern hypoxic center and on
the Yangtze Bank in July–August, i.e., -11 and -10 mmol O2 m-2 d-1 (-15 % and -20 %) in zones 2 and 4, respectively, had a significant effect on hypoxia (Figs. 8a,
9). This effect varies spatially between the
two hypoxic centers. Around the northern hypoxic center, the lack of
PO4 limits the duration and the spatial expansion of hypoxic conditions
and therefore moderates hypoxia. This is where P limitation has the largest
effect on hypoxia.
P limitation also prevents the expansion of hypoxic conditions further
northwest, on the western side of the Yangtze Bank
(Fig. 8a). Hypoxia only occurs sporadically in
this region and in small patches (909 km2 on average; maximum extent:
3260 km2) that develop when the plume extends over the bank in
July–August. Without P limitation, hypoxia was more frequent and widespread
in this area, covering 5429 km2 on average when hypoxia occurs
(maximum: 12 375 km2). The effect on the Yangtze Bank can be related to
the lower SOC and a weakening of stratification as the plume mixes with
ocean waters downstream. The spatial distribution of the potential energy
anomaly (a proxy for stratification; see
Große et al., 2020, for details) in
summer illustrates this change in stratification over the western Yangtze
Bank (Supplement Fig. S6). This stratification effect is consistent with
the idea that hypoxia is tightly controlled by the pycnocline in the
northern region (Chi et al., 2017). It was also shown to
be an important controlling factor in the context of P limitation in the
northern Gulf of Mexico (Laurent and Fennel, 2014).
Overall, the area of the shelf that can be exposed to hypoxia decreases by
34 % with P limitation, whereas the size of the hypoxic zone in reduced by
48 % on average, mainly in August (Fig. 8a).
Conceptual model of the effect of P limitation in the ECS
To summarize our findings, we provide a conceptual model of P limitation in
the ECS (Fig. 11). Along the CE–Jeju Island it
follows the general framework of Laurent and Fennel (2017)
for multi-dimensional dispersive systems, in which the “excess” DIN
transported downstream results in a spatial shift and dilution of primary
production. The dilution and relocation of O2 sinks are added here, as
well as the weakening of stratification downstream. These processes were
implied originally. Based on our results, we also add several processes that
were not included in the original framework, namely the vertical relocation
of O2 sinks and the change in denitrification that represents a small
positive feedback on eutrophication. The lack of changes around the southern
hypoxic core is specific to the ECS.
Große et al. (2020) recently showed
with the same model that relative to the Changjiang, nutrient sources from
the Taiwan Strait and the Kuroshio are important contributors to O2
consumption along the Zhejiang coast (<30∘ N). This
process is added to the conceptual model. This source of nutrients
contributes to the occurrence of harmful algal blooms in the area
(Che et al., 2022).
As mentioned above, we found similarities in the effect of P limitation
between the ECS and other systems. Along the CE–JI line, the dispersive
conditions favor the dilution of eutrophication with a positive effect on
subsurface water oxygenation within the northern hypoxia core. The same
mechanism was found in the northern Gulf of Mexico
(Laurent and Fennel, 2014, 2017) and off the Pearl River
Estuary (PRE) under severe P limitation (Yu and Gan, 2022).
The “dilution effect” (Laurent and Fennel, 2017) is therefore
a prevalent consequence of P limitation that is applicable to other river
plume systems. We did not find a positive feedback of P limitation on
hypoxia as suggested by Yu and Gan (2022) for the PRE. Their
study indicates severe, widespread P limitation in offshore waters, which is
not in line with our findings for the ECS. This positive feedback may be
specific to the PRE system.
Sensitivity of hypoxia to altered nutrient loads
We carried out the first systematic analysis of the effect of nutrient
reduction strategies on hypoxia in the ECS.
Große et al. (2020) recently suggested
that N management in the Changjiang has the potential to mitigate hypoxia on
the shelf. However, they did not assess nutrient reduction strategies. Our
results are in line with Große et al. (2020) and further indicate that hypoxia can be eliminated on the shelf at
high nutrient reduction levels (Figs. 8,
10, and S4). This highlights
the direct link between cultural eutrophication and hypoxia in the ECS
(Li et al., 2011; Wang et al., 2016). The
simulations indicated that management effects vary with the level and type
of nutrient reduction, as well as the area of interest. The N + P
nutrient reduction strategy was the most effective to mitigate hypoxia, as
reported previously for other coastal systems
(Fennel
and Laurent, 2018; Kemp et al., 2005; O'Boyle et al., 2015; Paerl, 2009;
Scavia and Donnelly, 2007) and for their upstream freshwater systems
(Paerl et al., 2016). The dual
N + P reduction is generally accepted as the most effective strategy to
mitigate eutrophication and hypoxia (Wurtsbaugh et al.,
2019). Nonetheless, the efficiency of nutrient reduction strategies (N + P, N-only, or P-only) varied between the northern (zone 2) and southern (zone 3)
hypoxia cores and was related to the spatial distribution of P limitation.
Similar spatial variations in the effectiveness of nutrient reduction
strategies (P-only or N-only) were also reported elsewhere (e.g., Chesapeake
Bay; Kemp et al., 2005). In the southern zone 3, where P
limitation is not frequent, a N-only strategy was nearly as effective as a
N + P strategy in mitigating hypoxia, whereas its efficiency was low at
moderate levels of reductions in the northern zone 2
(Fig. 10). This spatially explicit response
differs from the northern Gulf of Mexico (Mississippi plume) mentioned
above, where nutrient limitation follows an upstream–downstream continuum,
as described here along the CE–JI transect.
According to the nutrient load experiments, the level of reduction that is
necessary to mitigate hypoxia in the ECS is somewhat moderate due to the
high efficiency of the N + P reduction strategy (Figs. 8, 10). Long-term
hypoxia mitigation goals are not in place in the ECS, and eutrophication is
expected to worsen in the future with the increased use of fertilizer for
agriculture (Strokal et al., 2014; Wang et al.,
2020). Nonetheless, we explore the feasibility of possible intermediate
(-50 %) and long-term (-80 %) goals to mitigate the hypoxic zone
(Figs. 9, S4). Our experiments showed that a 50 % decrease in the
hypoxic area would require a 28 % reduction in N + P loads (38 % for
N-only and 60 % for P-only), whereas an 80 % decrease in hypoxic area
would require a 44 % reduction in N + P loads. At such mitigation levels,
hypoxia still occurred over a large area in our model but was limited in
duration (Fig. 8). Since the sediment layer is not explicitly represented
in the model (instant remineralization), there is no “legacy” effect of
eutrophication on hypoxia that may be associated with long-term organic
matter accumulation in the sediment
(Turner et al., 2008; Van Meter et
al., 2018). The nutrient reduction levels mentioned above therefore
represent a lower limit to the necessary management measures.
In the Changjiang nutrient mitigation experiments we applied the same
reduction level to all nutrient subspecies (i.e., dissolved inorganic,
dissolved and particulate organic). Changjiang N is dominated by nitrate, with
particulate and dissolved organic N contributing only 8 %–13 % of total N
(Große et al., 2020). Most of the
mitigation efforts should therefore target the inorganic subspecies. More
efficient N recycling from sewage may be a short-term measure to limit DIN
load to the CE (Yu et al., 2019). The long-term goal for
N reduction may be more challenging due to diffuse sources of DIN in the
Changjiang basin (Chen et al., 2019b). Manure and
fertilizers are major nutrient sources to the Changjiang, and therefore,
nutrient reduction targets could partly be met through cost-effective
management such as increased manure recycling to cropland
(Strokal et al., 2020; Yu et al.,
2019), more efficient fertilizer application (e.g., by increasing farm size,
Wu et al., 2018), and, more generally, by
increasing nutrient recycling in the Changjiang basin
(Yu et al., 2019). Several strategies have been proposed
to enhance water quality in the Changjiang (Guo
et al., 2021; Yu et al., 2019); our experiments can help estimate their
effectiveness to mitigate hypoxia on the shelf. Further investigations of
the link between nutrient limitation in the coastal ECS and the change in
land cover and land use in the Changjiang basin over the last decades may
help refine nutrient management strategies.
Conclusions
We carried out the first systematic assessment of the effects of P
limitation and nutrient loadings in the Changjiang–ECS system. P limitation
modifies O2 sinks over a large area of the shelf by partly relocating
and diluting primary production offshore, away from the locations prone to
hypoxia outside the Changjiang Estuary. The resulting horizontal and
vertical relocations of O2 sinks drastically reduce the size of the
hypoxic area (by about half), mostly off the Changjiang Estuary and on the
Yangtze Bank. P limitation had only small effects along the southern
Zhejiang coast. The incremental decrease in river nutrients in the
Changjiang showed that despite the effect of P limitation on hypoxia, N + P
reductions remain the best strategy to mitigate hypoxia. Tentative goals for
intermediate (-28 %) and long-term (-44 %) N + P load reductions were
proposed to reduce the hypoxic zone by 50 % and 80 % of its current
area, respectively.
Code and data availability
The ROMS source code is available from http://myroms.org,
last access: 10 August 2019 (Haidvogel et al., 2008). Model results are
available on request.
The supplement related to this article is available online at: https://doi.org/10.5194/bg-19-5893-2022-supplement.
Author contributions
AL and KF conceived the study. HZ set up the model. AL set up the
simulations and conducted the analyses. AL wrote the manuscript with input
from all co-authors.
Competing interests
The contact author has declared that none of the authors has any competing interests.
Disclaimer
Publisher's note: Copernicus Publications remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Acknowledgements
We thank Compute Canada for providing computing resources under the
resource allocation project qqh-593-ac.
Financial support
This research has been supported by the Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery program (grant no. RGPIN-2014-03938).
Review statement
This paper was edited by Tina Treude and reviewed by three anonymous referees.
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