Introduction
Marine primary production (PP) by phytoplankton is a key factor
controlling the strength of the oceanic biological carbon pump and the
amount of CO2 that is stored in the ocean . PP is controlled by light and nutrients, such as nitrogen,
phosphorus or iron, necessary for the production of
phytoplankton. These nutrients are supplied to the light-lit surface
waters by upwelling, turbulent entrainment of subsurface water,
riverine inputs, biological nitrogen fixation, atmospheric deposition
and benthic remineralisation .
Model structure. The model domain comprises five boxes representing
the top 100 m of an upwelling region (U), the underlying oxygen minimum zone
(UM), and an adjacent open-ocean basin divided into a surface (S) and an
intermediate-depth box (I). A deep box (D) underlies both the upwelling
region and the open ocean. The large-scale circulation is represented by deep
(A) and shallow (B) convection (thick grey lines). Mixing between boxes is
implemented via mixing coefficients (K). Remineralisation derived from
primary production by ordinary (Phy) and diazotrophic (NF) phytoplankton in
the surface boxes consumes oxygen. Under anoxic conditions remineralisation
is fuelled by anaerobic remineralisation (Denif). In the configuration
employed in this study, the model domain exchanges nutrients and oxygen with
the Southern Ocean (right, denoted as “SO”). Nitrogen deposition and
benthic remineralisation are included additionally to represent their
influence on the local water-column nutrient concentrations (thick light blue
arrows). The graph above is a schematic figure of our model domain; the graph
below shows the surface of our model domain, and the colour bar is nitrate
concentration in µ mol L-1.
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Nitrogen is often the limiting nutrient for phytoplankton in the ocean
. On the other hand, oceanic nitrogen is thought to
adjust, via nitrogen gain and loss processes, to the marine phosphorus
inventory on geological timescales, making phosphorus the ultimate
limiting nutrient and nitrogen the proximate limiting nutrient
. The ocean's nitrogen inventory has a turnover
time of a few thousand years, being affected by relatively large
interacting nitrogen sinks and sources. The exact mechanisms and
timescales of the interactions are not well understood. Estimates of
oceanic nitrogen fixation, the main fixed-N source into the ocean,
vary from 106 to 330 TgNyr-1 based on both in situ
observations and models . Water-column denitrification
and anaerobic ammonium oxidation (anammox) in oxygen minimum zones
(OMZs), accounting for 100–300 TgNyr-1, and benthic
denitrification, estimated as 95–300 TgNyr-1, mainly
determine the oceanic fixed-N sink . Due to the
large uncertainties in the major sources and sinks of the global
nitrogen cycle, the balance of the nitrogen inventory in the ocean is
still a matter of debate .
Phosphate can be the ultimate limiting nutrient on geological timescales even in regions with fixed-nitrogen deficits with respect to
the Redfield equivalent of the phosphate concentration
. The ocean's phosphorus
budget has been suggested to be unbalanced in the modern ocean with
sedimentary burial as the major sink exceeding phosphorus sources
. This condition might be alleviated by benthic
phosphorus regeneration, which can be enhanced under low-oxygen bottom
waters (O2<20 µmolL-1)
. Input of bioavailable phosphorus
into the ocean stimulates primary production, and decomposition of
subsequent export production enhances O2 consumption in the
ocean, in turn increasing the volume of oceanic oxygen-deficit water
and the fixed-N loss. Consequently, phosphorus regeneration is expected
to be enhanced by enlarging OMZs, possibly leading to a positive
feedback loop .
Iron (Fe) limitation has been suggested to exert some control on both
primary production and N2 fixation in the eastern
tropical South Pacific (ETSP) , possibly related to relatively low rates of
atmospheric Fe deposition in this area in comparison to the eastern
tropical North Atlantic . However, ambient
Fe concentrations are relatively high, allowing complete utilisation
of phosphate in the upwelling region of the ETSP .
Also, the stimulation of N2 fixation due to Fe enrichment
reported by appears positively related to ambient
Fe concentration. This is counter to what would be expected if
N2 fixation was mainly Fe limited. Thus, the role of Fe
limitation in the ETSP remains unclear, and we have excluded Fe
dynamics from this work, which also facilitates focusing on the influence of
benthic nitrogen and phosphate remineralisation in the ETSP.
OMZs also play an important role in the global marine fixed-N budget
as they are responsible for a large fraction of total marine fixed-N
loss . The relative contribution of heterotrophic
denitrification and autotrophic anammox to the total oceanic
fixed-nitrogen sink remains debated . Anammox has
been observed to be a major fixed-N loss process in the ETSP . However, the essential substrates for
anammox are ultimately provided by heterotrophic processes ,
such as organic-matter remineralisation or dissimilatory nitrate reduction to ammonium (DNRA). Thus,
both denitrification and anammox are driven by the flux of organic matter into the OMZ.
For simplicity, heterotrophic denitrification is
considered to be the major fixed-N loss process in the present study. Continental
shelves and the upper continental slopes are the most important sites for
benthic fixed-N loss . However,
found that the continental shelf and upper continental
slope of the ETSP across a section at 11∘ S are sites of nitrogen
recycling rather than fixed-N loss because of relatively low rates of
denitrification and high rates of NH4+ release from DNRA. This illustrates that the NH4+
released from DNRA should be taken into account when the benthic fixed-N sink
is estimated.
In the last few decades, a number of model- and data-based investigations
have been carried out on the importance of atmospheric fixed-N input into the
ocean for marine biogeochemical cycles
. suggest that
anthropogenic nitrogen deposition is rapidly approaching estimates for global
oceanic N2 fixation, while preindustrial deposition was an order of
magnitude lower. However, the response of nitrogen fixation and
denitrification to atmospheric nitrogen deposition remains an open question.
Atmospheric nitrogen inputs into the global ocean are dominated by inorganic
nitrogen from anthropogenic sources . The
exact magnitude of organic nitrogen deposition and its bioavailability are still under appraisement due to a lack of enough observations
. Therefore, we apply the finding of
and that DON accounts for 30 % of total
nitrogen deposition in our model and investigate its role on the nitrogen
budget of the ETSP with the bioavailability measured by .
Several scenarios with different DON bioavailability are assessed to analyse
uncertainties regarding the bioavailability of DON.
Various biogeochemical models have addressed the effects and feedbacks
between the major sources and sinks in the marine nitrogen cycle
. However, most of them have explored only a subset of the
atmospheric, pelagic and benthic nitrogen sources and sinks. Using
a conceptually simple and computationally efficient box model, we here
attempt a synthesis considering all essential sources and sinks and their
mutual interactions, with the only exception of riverine input, which is
excluded from our model analysis because it contributes negligibly to the
nitrogen inventory in the ETSP .
Model description
Circulation and biogeochemical model
The circulation model is the same as in , which is
a prognostic five-box model to explore the interactions among oceanic
circulation, nitrogen fixation and water-column denitrification in the
OMZ of the ETSP. Briefly, the physical parameters were calibrated to fit the average δ14C
of each box and biogeochemical parameters are constrained by literature data.
δ14C is the 13C fractionation-corrected ratio of 14C / 12C,
which is commonly used in ocean modelling to evaluate and calibrate model physics because it tends to cancel the effect of the biotic downward transport of 14C with
the rain of organic particles produced by marine organisms. All the simulations in
this manuscript employ the Open-boundary + Reduced-denitrification (OBRD) configuration of , which allows for the exchange of
deep and intermediate ETSP waters with the Southern Ocean (“SO” in
Fig. ) and applies reduced remineralisation
rates under suboxic conditions. The model domain consists of five
boxes representing the water column of an upwelling region and an
adjacent ocean basin. The U box represents the upper upwelling
region. The UM box is the OMZ below, where suboxia is expected to
develop. The S box represents the surface ocean away from the
upwelling zone. Below the S box sits the I box, which represents water
of intermediate depth and exchanges water with UM. D is the deep box,
which represents water deeper than 500 m (model configuration shown
in Fig. ).
We represent two phytoplankton types in the biogeochemical model: ordinary
phytoplankton (Phy) and nitrogen fixers (NF) as defined in .
Both Phy and NF concentrations are determined by the steady-state balance
between net primary production (NPP) and mortality (M), respectively, in the U and S boxes.
Phy requires both phosphate and nitrate, and growth of Phy is described
by a Blackman-type dependence on the nitrate and phosphate limitation terms. NF can
fix N2 as long as PO43- is available. A quadratic mortality term is adopted for both Phy and
NF, considering possible viral lysis, phytoplankton aggregation or a feedback between zooplankton
grazing and phytoplankton concentration. N2 fixers are given a lower maximum growth rate, which is one third of the maximum growth rate of
ordinary phytoplankton, in order to account for the high cost of nitrogen fixation .
Dead phytoplankton is immediately remineralised in the surface layer and
underlying boxes according to the predefined remineralisation
fractions. Remineralisation occurs preferentially via aerobic
respiration, with anaerobic denitrification and the associated
nitrogen loss setting in only when all O2 has been consumed by
aerobic respiration. When oxygen is exhausted in the OMZ,
remineralisation is assumed to slow down by a factor of 5, and
accordingly denitrification within the UM box is responsible for one fifth of the remaining organic-matter remineralisation, and the remainder
will be remineralised in the D box.
In order to represent the nitrogen and phosphate fluxes across the
water–sediment interface, remineralisation of particulate organic carbon
reaching the sediment (POC rain rate, RRPOC) is included additionally in the
UM and D boxes. RRPOC is calculated according to the method introduced in
Sect. , and we assume that all the POC is buried in the
sediment.
Summary of model configurations including different processes.
Process abbreviations are “N-DEP”, “Model BD”, “Data BD”, “Model PR”
and “Data PR”. N-DEP represents the atmospheric nitrogen input into the
surface ocean according to the estimate by ; Model BD
and Data BD represent model- and data-based benthic denitrification,
respectively; Model PR and Data PR are model- and data-based benthic
phosphorus regeneration, respectively.
Configuration
Processes
N-DEP
Model BD
Data BD
Model PR
Data PR
Control
NDEP
+
MBD
+
MPR
+
DBD
+
DPR
+
Synthesis configurations
MBD+MPR (Syn1)
+
+
DBD+DPR (Syn2)
+
+
MBD+MPR+NDEP (Syn3)
+
+
+
DBD+DPR+NDEP (Syn4)
+
+
+
+ Indicates that the process is included.
Model configurations
The above descriptions define the control configuration. In order to
investigate the model sensitivity to atmospheric nitrogen deposition
and benthic remineralisation, we employ another nine model
configurations incorporating either a subset or all of these
processes, which are summarised in Table .
In the NDEP configuration, atmospheric nitrogen input into the surface ocean according to the estimate by is included;
MBD and DBD are configurations in which model- and data-based benthic denitrification rates are included in the control configuration; MPR and
DPR represent configurations with model- and data-based benthic phosphorus regeneration, respectively. Detailed information of all processes is presented in
Sects. , and ; the configuration names are summarised in Table 1.
Nitrogen deposition, benthic denitrification and phosphate
regeneration are integrated into the synthesis model configurations to
explore the model sensitivity to each process and their mutual
interactions in the ETSP. Synthesis configuration Syn1 includes model-based benthic
denitrification and phosphorus regeneration; Syn2 includes the data-based benthic
denitrification and phosphorus regeneration; Syn3 includes atmospheric deposition in addition to the processes in Syn1; Syn4
includes atmospheric deposition in addition to the processes in Syn2.
The synthesis configurations Syn1 to Syn4 are summarised in
Table .
Atmospheric nitrogen deposition
Years 2000–2009 levels of dry and wet inorganic nitrogen deposition
following the RCP 4.5 scenario are examined in
our work. Inferred atmospheric inorganic nitrogen deposition rates are
0.081 and 1.4 TgNyr-1 (73.1 and
64.9 mgNm-2yr-1) for the U and S box,
respectively. Note that the circulation remains constant in our model,
and only atmospheric nitrogen deposition fluxes are included as an
additional annual nitrogen input into the surface (U and S) boxes.
Atmospheric phosphorus deposition is excluded from our analysis
because its amount is much smaller than the Redfield equivalent of nitrogen atmospheric deposition .
This results in N / P (mole / mole) ratios of more than 100, much higher than the average elemental
N / P ratio required by phytoplankton .
Benthic denitrification
The empirical transfer function of is applied to
predict benthic inorganic nitrogen loss (LDIN in
µmolNm-2d-1) through benthic denitrification,
which can account for the net loss of dissolved inorganic nitrogen
(DIN) from the sediment.
LDIN=0.06+0.19⋅0.99(O2-NO3-)bw⋅RRPOC,
where NO3- and O2 are bottom-water nitrate and oxygen
concentrations in µmolkg-1, and the RRPOC is in µmolCm-2d-1. Since the bottom-water
NO3- and O2 concentrations are well known in the
ETSP, the uncertainty in our estimation of benthic denitrification
comes mostly from uncertainties in the rain rate, which, in turn,
depends on biological production, as a function of phytoplankton
biomass and its physiological status. Simulated phytoplankton
concentrations in the surface boxes of the model roughly agree with
estimates by from Aqua-MODIS satellite data
and the Redfield C : N ratio (U box:
1.06 µmolNkg-1 simulated
vs. 0.68 µmolNkg-1 from Aqua-MODIS; S Box:
0.23 µmolNkg-1 simulated
vs. 0.28 µmolNkg-1 from Aqua-MODIS).
Model-based estimation of benthic denitrification
Fixed-N losses via benthic denitrification (LDIN) in the
UM and D boxes are obtained according to Eq. (), with the
respective simulated actual NO3- and O2
concentrations taken as the bottom-water concentrations, and RRPOC is
estimated from the export production from of the U and S boxes
(EPU and EPS) and the Martin
curve (Eq. ) :
RRPOC=F⋅z100-b,
where RRPOC is the rain rate, F is the export production from both
surface boxes and z is the water depth. The bathymetry of the
regions of the UM and D boxes is derived from the 2-minute gridded global relief dataset ETOPO2 (http://www.ngdc.noaa.gov/mgg/gdas/gd_designagrid.html). We
apply b=0.82 in Eq. (), which is the global
average according to and also close to his
estimate for the ETSP. An exponent of 0.4 for
Eq. () in suboxic water is implied by
. Therefore, sensitivity experiments are performed
with b=0.4. From Eq. () and the fraction of
the lower boundary of the respective box in contact with the seafloor,
the RRPOC at the sediment surfaces of the UM and D boxes is calculated
according to Eqs. ()
and ():
RRPOCUM=EPU⋅SDUM⋅AMCUM,RRPOCD=(EPU+EPS)⋅SDD⋅AMCD,
where EPU and EPU+EPS represent the export production (F in Eq. )
in the upwelling region and the whole model domain, respectively; AMCUM and
AMCD ((z100)-b in Eq. ) are the average Martin curve values corresponding to
the actual water depth (z) in the ETOPO2 data; SDUM and SDD
represent the percentages in contact with the sediment in the UM and D boxes, respectively (Table ).
Data-based estimation of benthic denitrification
For a second and independent estimate of LDIN, we combine
observations from different datasets. O2 and NO3-
concentrations for our model domain are obtained from the annual objectively
analysed mean concentrations of the WOA 2009 1∘×1∘
data and interpolated over the region
of our model domain to match the resolutions of the other datasets.
RRPOC is estimated from primary production following .
According to the carbon-based approach of , average
annual primary production is derived from photosynthetically available
radiation (PAR), the diffuse attenuation coefficient at 490 nm
(K490), chlorophyll a (Chl a) and mixed layer depth (MLD). PAR, K490 and
Chl a are from the Aqua-MODIS satellite data (2005–2010)
(http://oceancolor.gsfc.nasa.gov/), and MLD is from the Hybrid
Coordinate Ocean Model (HYCOM,
http://orca.science.oregonstate.edu/1080.by.2160.monthly.hdf.mld.hycom.php).
Export production is estimated from primary production and
sea-surface temperature (SST) , where SST is from the WOA
2009 annual average 1∘×1∘ temperature data
. The rate of particle transport at each grid cell to the
seafloor is calculated using the Martin curve (Eq. )
. To obtain more accurate estimates for RRPOC of our
regional box model, all data processed in this experiment are interpolated on
a grid of 2′×2′ in the UM box and 20′×20′ in the D box, and
the ETOPO2 data (2′×2′) are averaged within each 20′×20′
grid cell in the D box. The Aqua-MODIS data (5′×5′) and
NO3- and O2 concentrations from WOA 2009 dataset are
interpolated or averaged horizontally to match these resolutions. The
vertical resolution of the NO3- and O2 concentrations are
interpolated to resolve the bathymetry of the ETOPO2 data, and the
NO3- and O2 concentrations closest to the sediment are
applied in Eq. () for the bottom-water NO3- and
O2 concentrations.
Finally, the LDIN derived from observational datasets is averaged over the regions represented by UM and D boxes to produce an
annual NO3- loss term.
Phosphorus regeneration
Phosphorus regeneration is estimated according to
and , with both model- and data-based estimates for
the rain rate. We estimate benthic PO43- regeneration
(resupply of benthic PO43- to the water column,
BenDP) from the RRPOC degradation ratio
(rREG) and the POC burial rate in the sediments (BURPOC)
according to
BenDPUM=RRPOCUM-BURPOCUMrREG,BenDPD=minRRPOCD-BURPOCDrREG,RRPOC106,
where RRPOC is estimated with the methods described in
Sections. and . A minimum
condition is introduced in the D box to prevent
BenDP exceeding the rain rate of particulate
organic phosphate (RRPOP = RRPOC / 106) to the deep ocean but
not for the UM box because there are possible extra sources of RRPOP,
such as inputs via weathering or eolian deposition, for the
continental shelf, which is contained in the UM box in our model.
BURPOC is estimated from Eq. () for the continental shelf
(UM box) and Eq. () for the deep-sea sediment (D box), and
rREG is the C : P regeneration ratio estimated via
Eq. () following the empirical relations of
.
BURPOCUM=0.14⋅RRPOCUM1.11,BURPOCD=0.014⋅RRPOCD1.05,rREG=123+(-112)⋅exp-O232,
where O2 is the oxygen concentration in the ambient bottom
water (in µmolkg-1). rREG in
Eq. () is higher than the Redfield ratio in oxic water,
resulting in preferential P burial under oxic conditions; rREG is much
smaller than the Redfield ratio when O2<20 µmolkg-1, indicating excess phosphate release
from the sediment under suboxic conditions.
Summary of data-based flux estimates. “N deposition” is the annual
nitrogen input via atmospheric deposition; “Sediment percentage” is the
percentage of the surface areas of the UM and D boxes in contact with the
sediment; “Average Martin curve fraction” represents the average fractions
(calculated from the Martin curve) of export production reaching the sediment
for each grid point of the topography data; “NPP” is the net primary
production estimated from Aqua-MODIS satellite data; “Data BD” and “Data
PR” represent fixed-N loss via benthic denitrification and phosphate release
via phosphorus regeneration in the UM and D boxes, respectively. High-BD
indicates that the full sediment of the D box is included to estimate
NO3- loss via benthic denitrification and phosphate release via
phosphorus regeneration.
N deposition
Sediment
Average Martin
NPP
Rain rate
Data BD
Data PR
percentage
curve fraction
(Tg N yr-1)
(SD, %)
(AMC, %)
(mg C m-2 d-1)
(Tg N yr-1)
(Tg P yr-1)
U box
0.081a
0.12±0.052b
S box
1.4a
1.6±0.63b
UM box
0.81c
53.04c,d
1374.7e
148.4f
0.17g
0.058h
D box
2.25c
12.51c,d
873.9e
12.2f
0.82g
0.056h
D box (high-BD/PR)
873.9e
12.2f
8.8g
0.56h
Equations
Eq. 2
Eqs. 3, 4
Eqs. 1
Eqs. (5–9)
a Nitrogen deposition estimated from a
chemistry–climate model by . b Average
nitrogen deposition estimated from 23 atmospheric chemistry transport models
by . c Two-minute Gridded Global Relief Data
(http://www.ngdc.noaa.gov). d
The Martin curve exponent b=0.82 is from .
e NPP is estimated according to . PAR,
K490 and Chl a are from the Aqua-MODIS satellite data
(http://oceancolor.gsfc.nasa.gov/); MLD data are from the Hybrid
Coordinate Ocean Model
(HYCOM, http://orca.science.oregonstate.edu).
f Export production is estimated from NPP and SST according to
; SST is from the World Ocean Atlas annual average
1∘×1∘ temperature . g
BD is estimated from RRPOC applying the empirical transfer function of
. h PR is estimated from RRPOC following the
empirical relationship of and .
Model sensitivity experiments
Since the atmospheric nitrogen deposition data from
only include results of a single chemistry–climate model, a multi-model
perspective could offer additional insights into the influence of
uncertainties in nitrogen deposition on our model results. Three recent
inter-model comparisons show
very similar performance over our model domain; therefore, we choose the
results from , which is also applied in a number of
benchmark papers such as . The influence of DON from the
atmospheric nitrogen deposition on the nitrogen budget is investigated by
applying the fact that DON accounts for
30 % of the total dissolved nitrogen deposition suggested by and . The bioavailability of the deposited DON
is also considered by assuming that 30 % of it is available to primary producers according to . In addition, 10 and 50 % bioavailability is also
applied in our model to account for the underlying uncertainties. Considering the rapid rise of nitrogen deposition , we also apply the
RCP 8.5 scenario for the year 2100 predicted by in our model domain.
reported a large quantity of aphotic nitrogen fixation in
the ETSP, which can account for as much as 90 % of the total fixed-N input
via nitrogen fixation there. To test the effect of aphotic nitrogen fixation
on the nitrogen budget of the ETSP, we include the aphotic nitrogen fixation
rate measured by as additional NO3- input in
two sensitivity experiments: AphoticNfix1 and AphoticNfix2. Due to the very
low sampling density of their data, we extrapolate their data to our model
domain and assume that the nitrogen fixation rate in the open ocean is the
same as that measured at the coast. Aphotic nitrogen fixation is responsible
for 0.0711, 0.0528 and 0.0528 µmolNkg-1yr-1 (0.44,
6.5 and 25.6 TgNyr-1) fixed-N input into the UM, I and D
boxes, respectively, with estimates from the 2010 cruise (AphoticNfix1). It
contributes 0.0109, 0.0057 and 0.0059 µmolNkg-1yr-1
(0.067, 0.70 and 2.9 TgNyr-1) when applying estimates for the
2011 cruise (AphoticNfix2).
Since our model domain only includes the top 2000 m of the
water column, the sediments only account for a small portion of the
whole sediment of the ETSP
(Table. ). A sensitivity experiment “high-BD/PR” is
performed with the assumption that all of the bottom of the D box is
in contact with the sediment below 500 m (high benthic
denitrification (high-BD), or high phosphorus regeneration (high-PR))
including all NO3- losses by benthic denitrification and
phosphate release by phosphorus regeneration in the sediment.
The original work of and
indicates a lower value for the exponent b of
Eq. () in suboxic water. We perform an additional
sensitivity experiment with b=0.4 according to the suggestion by
to explore the influence of benthic
denitrification and phosphorus regeneration under conditions of slower
POC remineralisation.
We perform another sensitivity experiment to explore the influence of organic-matter remineralisation
on the benthic denitrification and phosphorus regeneration with more recent findings , where we apply the
variable Martin curve exponent b values in our model domain. In the UM box, b=0.83, which corresponds to the Peru–Chile upwelling
region, is applied, whereas b=0.85 is applied in the D box, which is the average of the b values for the regions named Chile–Peru Current Coastal (CHIL),
Pacific Equatorial Divergence (PEQD), South Pacific Subtropical Gyre (SPSG) and Western Pacific Warm Pool (WARM) in .
Results
Nitrogen deposition
Due to the low NO3- concentrations in the surface U and S boxes, the
annual nitrogen input by atmospheric nitrogen deposition accounts for 63 and
10 %, respectively, of nitrogen inventories of the U and S boxes.
Figure indicates that the extra bioavailable nitrogen
input by nitrogen deposition reduces the growth of nitrogen fixers in the
surface ocean mainly in the U box, even though more nitrogen is deposited
in the S box. Nitrogen fixation is reduced by about 0.7 and
0.1 TgNyr-1, respectively, in the U and S boxes (about 18 and
5 % of the total). The reduction in nitrogen fixation accounts for about
48 % of the total bioavailable nitrogen inputs into surface waters from
atmospheric deposition (1.5 TgNyr-1).
Nitrogen fluxes after including atmospheric nitrogen deposition in
the control, Syn3 and Syn4 configurations defined in Table .
Lateral-flux is the nitrogen efflux or influx through the southern boundary;
NfixU and NfixS represent the nitrogen fixation rate by
NF, respectively, in the U and S boxes; WC-denif is water-column
denitrification; NdepU and NdepS are the nitrogen input
into surface U and S boxes via nitrogen deposition.
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Water-column denitrification stays almost unchanged because the increase in
export production (EP) by Phy (ordinary phytoplankton) is almost exactly
compensated for by the decrease in EP of NF, resulting in
essentially unchanged total EP. As a result of the ≈50 % of the
nitrogen deposition not compensated for by lower nitrogen fixation, the model
domain becomes a larger fixed-N source (Fig. ). The
fixed-N loss through the lateral boundary increases from
0.93 TgNyr-1 in the control configuration to
1.7 TgNyr-1 in the configurations including nitrogen
deposition, leading to about 0.78 TgNyr-1 extra fixed-N loss
from the model domain, i.e. about 50 % of the total bioavailable
nitrogen input from atmospheric deposition. Thus, almost all the extra
nitrogen input into the model domain via nitrogen deposition is offset by
reduced nitrogen fixation and enhanced lateral transport out of the model
domain.
Nitrogen deposition has no significant influence on biogeochemical tracer
concentrations of the model in steady state: Phy concentration increases by
3 % in the U box and even smaller changes occur in the S box, which can
be attributed to the stronger nitrogen deficit in the region above the OMZ (U
box) than in the open ocean (S box) (Fig. S2 in Supplement). The largest
effect is a decrease by about 9 % of the concentration of NF in the U box, partly counteracting the nitrogen input via nitrogen
deposition (Fig. ). NF concentration stays almost
unaltered in the S box (Fig. ). Slight variations of the
NO3- concentration occur in the UM box and of O2
concentrations in the I and D boxes (Fig. S2).
Benthic denitrification
The data-derived benthic denitrification and phosphorus regeneration in the UM
and D boxes are shown in Table . Modelled NPP in the surface ocean above the UM and D boxes is,
respectively, 1.4 and 0.87 gCm-2day-1, indicating higher
NPP in the coastal upwelling region and lower NPP in the open ocean adjacent
to the upwelling region, which is consistent with the estimate by
. Due to the small sediment-area percentages, the
annual nitrogen loss by benthic denitrification is 0.17 and
0.82 TgNyr-1 in the UM and D boxes, accounting for only about
0.14 % and 5.1 × 10-3 %yr-1, respectively,
of the NO3- inventories in these boxes (Table ).
The higher sedimentary NO3- sink in the UM box can be attributed to
the anoxic conditions and larger RRPOC.
Our simulated biogeochemical tracer concentrations in steady state are quite
robust with respect to benthic denitrification (Fig. ).
Including benthic denitrification causes only minor deviations in the MBD and
DBD configurations compared to the control run. Nitrogen fixation rates
increase by about 2.9 and 5.8 %, respectively, in the MBD and DBD
configurations (A bars in panels MBD and DBD of Fig. ).
Most of this increase occurs in the U box, which receives water with a strong
N deficit via upwelling.
Sensitivity of simulated steady-state concentrations of nitrogen
fixers NFU and NFS in the U and
S boxes, respectively. Horizontal grey and light blue lines represent the
NFU and NFS concentrations in the
control configuration, respectively. Syn1, Syn2, Syn3 and Syn4 denote the
“MBD + MPR”, “DBD + DPR”, “MBD + MPR + NDEP”, and
“DBD + DPR + NDEP” synthesis configurations defined in
Table .
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Nitrogen fluxes after including benthic denitrification and/or
phosphorus regeneration. Lateral-flux is the nitrogen efflux or influx
through the southern boundary; NfixU and NfixS represent
the nitrogen fixation rate by NF in the U and S boxes, respectively; WC-denif
is water-column denitrification; Benthic-denif represents the fixed-N loss
via benthic denitrification in the model domain. Bar labels: A, main
experiments; B, sensitivity experiments with high-BD; C, sensitivity
experiments with Martin curve exponent b=0.4.
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Obviously, the response is stronger in the DBD configuration than in the MBD
configuration because fixed-N loss via benthic denitrification in the DBD
configuration is approximately 5 times larger (A bars in
Fig. ). The DBD configuration results in a stronger responses
of nitrogen fixation and lateral fluxes to benthic denitrification: the increase
in nitrogen fixation cannot fully compensate for the nitrogen loss by benthic
denitrification. Thus, the model domain becomes a smaller fixed-N source, about
25 % of that in the control configuration. In other respects, the
steady-state solutions of the MBD and DBD configurations are almost identical to
those of the control configuration after including benthic denitrification (Fig. S3). The
temporal development of biogeochemical tracer concentrations is also insensitive
to the presence or absence of benthic denitrification (Fig. S3).
Phosphorus regeneration
Phosphate release by phosphorus regeneration accounts for about 0.23 %
and 2.2 × 10-3 %yr-1, respectively, of the
total phosphate inventories in the UM and D boxes (Table ).
The higher sedimentary PO43- source in the UM box can be
attributed to the anoxic conditions and larger RRPOC. The
phosphate release associated with benthic phosphorus regeneration can
stimulate nitrogen fixation and EP from the surface ocean, followed by higher
water-column denitrification, owing to enhanced decomposition of exported
organic matter (A bars in MPR and DPR panels in Fig. ).
In the MPR configuration, nitrogen fixation increases by about 18 % in the
U box and stays almost unchanged in the S box. In the DPR configuration,
nitrogen fixation also increases by about 23 % in the U box when benthic
phosphate release is included (Fig. ). Water-column
denitrification increases by 10 and 14 %, respectively, in the MPR and DPR
configurations (Fig. ).
Compared to the MBD and DBD configurations, benthic phosphorus regeneration does
not turn our model domain into a smaller fixed-N source, in spite of higher
water-column denitrification because enhanced nitrogen fixation compensates for
the extra nitrogen loss (A bars in Fig. ).
While changes in nitrogen deposition and benthic denitrification are to a
large extent compensated for by adjustments in nitrogen fixation, phosphate is
the ultimate limiting nutrient in our model domain . Hence,
the extra phosphate input into the model domain by benthic phosphorus
regeneration has a more significant influence on the steady-state model
results than the perturbations of the nitrogen inputs or losses
(Fig. ). Phy concentration in the DPR configuration
decreases in the U box but remains unchanged in the S box (Fig. S2). Phy
concentrations in the U and S boxes remain almost unaltered in the MPR
configuration. Compared with the control configuration, NF concentrations in
the U and S boxes increase by 11 and 1.6 %, respectively, in the MPR
configuration and by 14 and 1.6 %, respectively, in the DPR configuration
(Fig. ). The nitrate concentration in the UM box decreases
by about 4.2 % in the MPR configuration and 5.2 % in the DPR
configuration (Fig. S2). The temporal development of biogeochemical tracer
concentrations appears robust to benthic phosphorus regeneration (Fig. S4).
Synthesis configurations
In the synthesis configurations (Table ), phytoplankton,
nutrient and oxygen concentrations are quite robust with respect to the
various fluxes associated with nitrogen input or removal and phosphate
release from the sediment into the water column (Fig. S2). However, the
interactions among nitrogen fixation, water-column denitrification, and
benthic denitrification and phosphorus regeneration result in different
sensitivities of nitrogen fixation and of the lateral fluxes to atmospheric N
deposition in the presence of benthic denitrification and phosphorus
regeneration (Fig. ). In contrast to the NDEP
configuration, nitrogen fixation rates in the Syn3 and Syn4 configurations
increase by about 1.7 and 8.5 %, in spite of the additional nitrogen
input into the model domain by atmospheric nitrogen deposition.
Most of this increase occurs in the U box, whereas almost no change happens in
the S box.
The lateral fixed-N flux out of the model domain (NO3- source)
increases by about 0.97 TgNyr-1 in the Syn3 configuration, which
accounts for about 65 % of the total atmospheric nitrogen deposition; i.e.
more than half of the extra nitrogen supplied by nitrogen deposition is not
utilised locally. However, in the Syn4 configuration, the increase in lateral
NO3- efflux only accounts for about 25 % of the total nitrogen
deposition, with 75 % of the deposited nitrogen utilised within the model
domain. Less fixed N is lost laterally from the model domain in the
configurations including data-based estimates than in those including
model-based estimates, due to more NO3- loss within the model domain
(Fig. ). Thus, the sensitivity of lateral fluxes and the
fixed-N budget to nitrogen deposition is strongly controlled by benthic
denitrification and phosphorus regeneration.
Model sensitivity
The nitrogen deposition rate estimated by is about 48
and 14 % higher, respectively, in the U and S boxes than the estimate of
. However, this increase induces only a 3.1 % decrease
in nitrogen fixation in the U box and a 5.9 % increase in lateral nitrogen
flux, while water-column denitrification and nitrogen fixation in the S box
remain unchanged (A and B bars in panel NDEP of Fig. ).
Whereas the uncertainty associated with the nitrogen deposition estimate of
amounts to about ±40%, the nitrogen fixation rate
in the U box and lateral flux only vary by about ±9.7 and ±20%, respectively (panels NDEP-low and NDEP-up in
Fig. ). Effects of accounting for atmospheric deposition
of bioavailable DON are investigated in three sensitivity experiments with
different scenarios for DON bioavailability (panels NDEP-DON(10 %),
NDEP-DON(30 %) and NDEP-DON(50 %) in Fig. ). Including
bioavailable atmospheric DON in addition to DIN deposition causes only minor
changes, i.e. slightly lower nitrogen fixation and slightly higher lateral
nitrogen efflux. The RCP 8.5 scenario projects about a 7.2 % increase in
nitrogen deposition for the year 2100 compared to our main experiment
(2000–2009 average according to the RCP 4.5 scenario), causing only
negligible changes to the nitrogen budget in our model domain (A bars in
panels NDEP and NDEP-2100 of Fig. ). These sensitivity
experiments show that variations in nitrogen deposition are largely offset by
changes in nitrogen fixation and lateral nitrogen flux out of the model
domain, tending to keep a balanced nitrogen inventory.
Sensitivity of nitrogen fluxes to atmospheric inorganic and organic
nitrogen deposition and associated uncertainties. Lateral-flux is the
nitrogen efflux or influx through the southern boundary; NfixU and
NfixS represent the bioavailable nitrogen fixation rate by NF in
the U and S boxes, respectively; WC-denif is water-column denitrification;
NdepU and NdepS are the nitrogen input into surface ocean
(U and S boxes) via nitrogen deposition. Bar labels: A, nitrogen deposition
data from ; B, nitrogen deposition data from
. In NDEP-low and NDEP-up, the lower and upper limit of
nitrogen deposition fluxes are included; in NDEP-DON(10 %),
NDEP-DON(30 %) and NDEP-DON(50 %), the bioavailability of deposited DON
is assumed to be 10, 30 and 50 %, respectively; in NDEP-2100, nitrogen
deposition is estimated according to the RCP8.5 scenario projections for 2100
.
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The effect of aphotic nitrogen fixation is investigated in the AphoticNfix1
and AphoticNfix2 configurations, where photic nitrogen fixation decreases by
39 and 15 %, respectively (Fig. S5). Water-column denitrification remains
unchanged because more nitrogen input by aphotic nitrogen fixation does not
increase export production to the OMZ. The lateral fixed-N effluxes in the
AphoticNfix1 and AphoticNfix2 configurations are about 33 and 4 times those in the control configuration, accounting for about 91 and 78 %,
respectively, of extra nitrogen input by aphotic nitrogen fixation (Fig. S5).
Aphotic N2 fixation has little effect on most tracers except
NO3-, which increases by 110 and 87 %, respectively, in the UM box
and the whole model domain for AphoticNfix1, which is a strong overestimate
compared to WOA 2009 data (Fig. S6). The lower estimate of aphotic N2
fixation (AphoticNfix2) brings the NO3- concentrations closer to the
WOA 2009 data (Fig. S6), and the associated changes in nitrogen fluxes are
similar to our other sensitivity configurations (Figs.
and S5). As for the sensitivity with respect to atmospheric nitrogen
deposition, these changes are largely compensatory, leading to only small
changes in the nitrogen budget of our model domain.
Figure shows the results of the sensitivity
experiments with high-BD and high-PR. Compared with
Fig. , the influence on the biogeochemical tracer
concentrations in steady state is stronger, due to the larger
NO3- loss via benthic denitrification and PO43-
release via phosphorus regeneration
(Table ). High-BD or high-BD together with
high-PR can even turn our model domain into an NO3- sink
(B bars in panels DBD and DBD+DPR of Fig. ).
Sensitivity of simulated steady-state concentrations of nitrogen
fixers (NFU and NFS) in the U and S boxes, respectively, after incorporating high-BD and high-PR. Horizontal grey and
light blue lines represent the NFU and
NFS concentrations in the control configuration.
![]()
Applying the Martin curve exponent b=0.4 also amplifies the influence
of benthic denitrification and phosphorus regeneration on phytoplankton
and biogeochemical tracers, although the effect is weaker than in the
high-BD and high-PR configurations. For example,
NFU increases by as much as 33 % in the DBD+DPR
configuration, and NFS increase about 15 % (Fig. ). Compared with A bars in
Fig. , this enhanced influence results from the
higher NO3- loss through benthic denitrification and
phosphate input via phosphorus regeneration (C bars in
Fig. ).
Sensitivity of simulated steady-state concentrations of nitrogen
fixers (NFU and NFS) in the U and S boxes, respectively, after applying b=0.4 for Eq. ().
Horizontal grey and light blue lines represent the NFU and
NFS concentrations in the control configuration.
![]()
Spatial variations in the Martin curve exponent b as suggested by
result in nitrogen fluxes and concentrations in steady state which are in good agreement with those in our main
configurations (A and C bars in Figs. S7 and S8) because the b values from
are all very close to b=0.82, as used in our main
configurations.
Due to the higher RRPOC reaching the sea floor under suboxic conditions,
benthic denitrification increases by about 42
and 198 % (A and C bars of panels MBD and DBD in
Fig. ) and phosphorus regeneration increases by about
36 and 200 %, respectively, in model- and data-based estimations in
the sensitivity experiments with Martin curve value b=0.4. Our model
domain switches to a NO3- sink in the DBD and DBD + DPR
configurations with b=0.4 (C bars in
Fig. ). Comparing the A and C bars of panel DBD in
Fig. , we find that higher benthic denitrification
can stimulate nitrogen fixation, but water-column denitrification
remains constant. However, comparing the A and C bars of panel DBD+DPR in
Fig. , we find that higher benthic denitrification
can increase nitrogen fixation and water-column denitrification,
indicating an important role of PO43- in balancing the nitrogen
inventory. This shows a positive feedback between water-column
denitrification in the OMZ and benthic denitrification below, caused
by slower remineralisation under anoxic conditions, which results in
more RRPOC reaching the sea floor. All above comparisons indicate that
phosphate limitation could be responsible for breaking this positive
feedback under the assumption of our model that PO43- is
the only limiting factor for the growth of nitrogen fixers.
Discussion and conclusions
The impact of nitrogen deposition on the ETSP has rarely been investigated so
far, since this region is believed to receive less bioavailable nitrogen from
atmospheric deposition than the coasts of western Europe, south and east Asia
. The influence of anthropogenic nitrogen
deposition on the biogeochemical cycles of the open ocean is increasing and
the increase in atmospheric nitrogen deposition will probably induce an
approximately 10 % rise in carbon sequestration on land and in the ocean
by 2030 . The ETSP, a typical N-deficit region
due to denitrification in the OMZ, is likely to be sensitive to anthropogenic
nitrogen deposition. We find that, in our model, nitrogen deposition can
inhibit N2 fixation by relieving nitrogen limitation for Phy, which
counteracts the effect of atmospheric nitrogen input. This is in line with
the finding that N2 fixation decreases with increasing nitrogen
deposition in global-scale models that use essentially the same assumptions
about the environmental controls on marine nitrogen fixation
.
Another portion of the deposited nitrogen is exported out of the model domain
since not all the deposited nitrogen can be taken up by Phy locally, owing to
phosphate limitation (Fig. ).
The coastal upwelling region (the U box) in our model is more sensitive to
nitrogen deposition due to the N-deficit water supplied by upwelling
(Fig. ). In spite of the uncertainties in the magnitude of
atmospheric bioavailable nitrogen deposition and the bioavailability of
deposited DON, atmospheric deposition appears unable to exert a strong influence
on the fixed-N budget of our model domain, as nitrogen deposition is mostly
counteracted by decreased nitrogen fixation and enhanced nitrogen export out of
the model domain.
Replacing obligate N2 fixation in our model by facultative N2
fixation slightly enhances the strength of the negative feedback between
nitrogen fixation and nitrogen deposition (see Sect. S1 in the Supplement for details).
Model flux comparison with model-based and observational estimates.
Reference
N2 fixation
WC-denif
BD
PR
(Tg N yr-1)
(Tg P yr-1)
U box
S box
This studya
2.8–6.7
1.9–3.2
4.9–6.6
0.19–9.0f,g
0.062–0.62f,g
a,b
0.086
4.4
5.7
0.86f
c
1.4–21e
a
2.0f
0.34f
c
10
1.0h
a,b
0.4 ± 0.1
13 ± 4.0
7.0 ± 2.0
6.0 ± 2.0f
c
0.023–0.30d
c
0.22–18.7d
a Model results. b Personal
communication. c Observational estimates. d Value
extrapolated to the area of the U box in our model. e Value
extrapolated to the area of the S box in our model.
f For the whole sediment area below our model domain. g Top 2000 m of our model domain. h Top 600 m of the OMZ region.
Schematic of the model sensitivity to different processes related to
the nitrogen budget of the ETSP. The red solid lines represent stimulatory
effects, and the black solid lines represent depressive effects.
![]()
The NPP estimated in our study is on average 1.4 and 0.87 g C m-2 d-1, respectively, in the surface ocean above
the UM and D boxes, according to the carbon-based approach of
. estimated NPP from
ship-collected data as, respectively, 1.2 and 0.67 g C m-2 d-1 for the surface ocean above the UM and D boxes, whereby the NPP for the
surface ocean above the D box could be somewhat overestimated because the
western boundary for their data is 140∘ W. Our estimates are about
17 and 30 % higher than those of for the surface
ocean above the UM and D boxes because the carbon-based approach of yields considerably higher values than other approaches
for tropical regions. Export production is linearly related to RRPOC
(Eq. ), as is RRPOC to BD (Eq. ). PR and
RRPOC are related through a power law with exponents of 1.11 and 1.05 for the
UM and D boxes, respectively (Eqs. –).
Fixed-N loss via BD and PO43- release by PR estimated with
ship-collected data should thus be within the range corresponding to the NPP
estimates from and . However,
in our data-based estimation of BD and PR, the fixed-N loss by BD and
PO43- release by PR is, respectively, 421 and 140 % higher than
our model-based estimates. Therefore, the NPP estimated from ship-collected
data lead to benthic remineralisation fluxes between our data-based and
model-based estimations.
Aphotic nitrogen fixation, i.e. below the euphotic zone, has been considered an
important contribution to the nitrogen budget of the ETSP .
Our model configurations including aphotic N2 fixation are in line with
this view, as the large amount of additional nitrogen input in the AphoticNfix1
configuration induces overestimation of NO3- concentrations in the
model domain, whereas NO3- concentration is closer to the WOA 2009 data
in the AphoticNfix2 configuration, which has a much lower aphotic nitrogen
fixation rate. Due to the very sparse data for aphotic N2 fixation, we
had to extrapolate the data for the coastal region to the vast open ocean of
the ETSP, which could have led to an overestimation of aphotic
nitrogen fixation. Thus, we expect that aphotic N2 fixation is likely
closer to the lower (2011) estimate of , as the resulting
NO3- concentrations are closer to the WOA 2009 data.
Table shows our modelled fluxes in comparison with other
model-based and observational estimates. N2 fixation in the upwelling
region of our model is higher than those reported by ,
, and but within the range
suggested by . However, the N2 fixation rate in the
open ocean of our model is lower than those by and
but within the range suggested by .
Water-column denitrification is comparable to and
but lower than that from . Our
predicted fixed-N loss by benthic denitrification is comparable to other
estimates. Phosphorus regeneration in our analysis spans a wide range but is
comparable to the evaluation of for the full depth
of the model domain. Major nitrogen and
phosphorus fluxes in our study also span wide ranges because fluxes both from
the upper 2000 m and full depth of the ocean are assessed with both data and
model-based evaluations, in each case accounting for organic-matter
remineralisation under different oxygen conditions
(Table ). Currently, both global and regional estimates of
nitrogen fixation and benthic remineralisation rates are rather uncertain,
owing to temporal and spatial variations and problems associated with
measuring methods e.g.. Thus, we had to apply rather
wide ranges in order to investigate the potential influence of these
processes on the nitrogen budget of our model domain.
Under the assumption that N2 fixation compensates for any fixed-N deficit
, nitrogen fixation can be stimulated by benthic denitrification.
found that benthic denitrification stimulates N2 fixation in their 3-D biogeochemical model,
which was tuned under the condition that the global fixed-N budget was balanced. Even
though we make no a priori assumption about the association between N2
fixation and fixed-N loss processes, we also find that a fixed-N deficit can
stimulate N2 fixation, thus compensating for the fixed-N loss.
We find that incorporating benthic phosphorus regeneration strongly increases
primary production, which is mainly attributed to nitrogen fixation (panels
MPR and DPR in Fig. ). Phosphorus regeneration is
enhanced under O2-deficit conditions, and the enhanced phosphate
release stimulates primary production, resulting in the expansion of OMZs and
possibly causing a positive feedback loop leading to more benthic phosphorus
regeneration . However, our model domain
only represents the upper 2000 m of the ocean and its sediments only
account for a small fraction of the total sediment area in the ETSP. The
model results incorporating benthic denitrification and phosphorus
regeneration, and assuming that all of the D box is in contact with the
sediment, are shown in Figs.
and . Our parameterisation allows nitrogen fixation to
be favoured in N-deficit waters, since the increase in water-column
denitrification can be compensated for by increased nitrogen fixation when
phosphorus regeneration is sufficient (panels MPR and DPR in
Fig. ).
The simplicity and computational efficiency of our box model facilitates
exploring model sensitivity to various processes related to the nitrogen
budget of the ETSP. Even though details of spatial and temporal variations
are missing compared with results from 3-D global circulation models
, we can efficiently
diagnose the regional impacts in steady state. We identify stimulatory
effects between nitrogen fixation and water-column
denitrification, phosphorus regeneration and nitrogen fixation, phosphorus
regeneration and water-column denitrification, and atmospheric deposition and
lateral NO3- transport (Fig. ). Depressive
effects occur between atmospheric deposition and nitrogen fixation and
between benthic denitrification and lateral NO3- transport
(Fig. ). The model sensitivity to processes related to
the nitrogen budget of the OMZ in the ETSP is illustrated in
Fig. . Nitrogen fixation can be enhanced by benthic
denitrification, compensating for part of the NO3- loss. The
stimulatory effect between nitrogen fixation and water-column denitrification
helps balance the fixed-N budget. The extra fixed-N input by nitrogen
deposition is partly counteracted by decreased nitrogen fixation and partly
removed by lateral flux. All of these local responses combined constitute a
nitrogen-balancing mechanism in the ETSP. Even though water-column
denitrification has been considered to be the major fixed-N loss process for
simplicity, the stimulatory effects between nitrogen fixation and fixed-N
loss and between phosphorus regeneration and fixed-N loss still apply even if
anammox replaced water-column denitrification as the fixed-N loss pathway.
Thus, the nitrogen-balancing mechanism in the ETSP should not depend on
whether the fixed-N is lost through denitrification or anammox.
In the high-BD sensitivity experiment, our model domain turns into an NO3- sink (Fig. ). The NO3- inventory in
the ETSP is determined by nitrogen fixation, water-column denitrification,
benthic denitrification and lateral NO3- flux. Since our model domain
(except in the high-BD sensitivity configuration) encompasses only the water
column and a small fraction of the corresponding sediment area, we cannot rule
out that the ETSP including sedimentary denitrification is an NO3- sink,
which is consistent with many model- or data-derived results
. Extra phosphate input into the model
domain via phosphorus regeneration can increase water-column denitrification
significantly due to the increase in EP from the surface ocean. However,
phosphorus regeneration alone cannot turn our model domain into an NO3-
sink.
The remineralisation rate of organic matter is thought to be reduced under
anoxic conditions , resulting in a higher RRPOC reaching the sediments. According to the analysis of
, benthic denitrification is very sensitive to RRPOC; i.e.
higher RRPOC results in higher benthic denitrification. Based on our findings that higher
benthic denitrification can increase nitrogen fixation, higher nitrogen fixation could result in
higher water-column denitrification and the expansion of the OMZ and hence a
positive feedback between water-column and benthic denitrification. But this
positive feedback is only observed in configurations with phosphate input via
phosphorus regeneration, which indicates that PO43- limitation could
play an important role in preventing this positive fixed-N loss feedback.