TYPE Original Research
PUBLISHED 26 August 2022
DOI 10.3389/fmars.2022.990559

OPEN ACCESSEDITED BY

Makio Honda,
Japan Agency for Marine-Earth
Science and Technology (JAMSTEC),
Japan

Seasonal variability of upper
ocean primary production along
the Kuroshio off Japan: Roles of
eddy-driven nutrient transport

REVIEWED BY

Shinya Kouketsu,
Japan Agency for Marine-Earth
Science and Technology (JAMSTEC),Japan
Yoshikazu Sasai,Japan Agency for Marine-Earth
Science and Technology (JAMSTEC),Japan*CORRESPONDENCE

Yusuke Uchiyama
uchiyama@harbor.kobe-u.ac.jp

Xu Zhang 1, Yusuke Uchiyama 2*, Eiji Masunaga 3, Yota Suzue 4
and Hidekatsu Yamazaki 5,6,7
1
Laboratory for Climate and Ocean-Atmosphere Studies, Department of Atmospheric and Oceanic
Sciences, School of Physics, Peking University, Beijing, China, 2Department of Civil Engineering, Kobe
University, Kobe, Japan, 3Global and Local Environmental Co-creation Institute, Ibaraki University,
Hitachi, Japan, 4Construction Technique Institute Engineering Co., Ltd., Nagoya, Japan,
5
Department of Ocean Sciences, Tokyo University of Marine Science and Technology, Tokyo, Japan,
6
Alpha Hydraulic Engineering Consultants Co., Ltd., Tokyo, Japan, 7College of Marine Ecology andEnvironment, Shanghai Ocean University, Shanghai, China

SPECIALTY SECTION

This article was submitted toMarine Biogeochemistry,a section of the journal
Frontiers in Marine Science
RECEIVED 10 July 2022
ACCEPTED 09 August 2022
PUBLISHED 26 August 2022
CITATION

Zhang X, Uchiyama Y, Masunaga E,
Suzue Y and Yamazaki H (2022)
Seasonal variability of upper ocean
primary production along the Kuroshio
off Japan: Roles of eddy-driven
nutrient transport.
Front. Mar. Sci. 9:990559.
doi: 10.3389/fmars.2022.990559
COPYRIGHT© 2022 Zhang, Uchiyama, Masunaga,
Suzue and Yamazaki. This is an openaccess article distributed under theterms of the Creative Commons
Attribution License (CC BY). The use,
distribution or reproduction in otherforums is permitted, provided theoriginal author(s) and the copyrightowner(s) are credited and that theoriginal publication in this journal iscited, in accordance with accepted
academic practice. No use,
distribution or reproduction ispermitted which does not comply withthese terms.

We assessed spatial and seasonal variabilities of eddy-driven vertical nutrient
ﬂuxes, which are essential for maintaining primary production in the upper
ocean. A climatological model based on a Regional Oceanic Modeling System(Regional Oceanic Modeling System) coupled with a Nutrient Phytoplankton
Zooplankton and Detritus (NPZD) biogeochemical model at a submesoscale
eddy-permitting resolution was used to investigate the mechanisms drivingsuch variabilities around the Kuroshio, off the coast of Japan. The model
realistically reproduced the spatial segmentations in primary production on
both sides of the Kuroshio path with a higher chlorophyll-a concentration on
the northern side than the southern side. In winter, downward eddy-induced
nitrate ﬂux is predominantly provoked in the upstream Kuroshio region (KR),while upward nitrate ﬂuxes prevail in the downstream Kuroshio Extension (KE)region, due to both shear and baroclinic instabilities. Baroclinic instability plays
a crucial role in inducing seasonal variability, leading to enhancement(reduction) of the eddy ﬂux in winter (summer), particularly in regions awayfrom the Kuroshio axis. Furthermore, we found that the inﬂuence of the IzuOgasawara Ridge, located in the KR, on regional dynamics and resultant spatial
variability of the biogeochemical response are mostly conﬁned in the KR. The
Kuroshio is less turbulent in the upstream of the ridge, while it becomes
unstable to shed mesoscale eddies in laterally wider and vertically deeper
regions downstream. Consequently, although the near-surface nitrateconcentration is lower downstream, the upward eddy-driven nitrate ﬂux ismore effective in maintaining active primary production due to the shear andbaroclinic instabilities in winter.
KEYWORDS

primary production, seasonal variability, mesoscale and submesoscale eddies,
Kuroshio, Kuroshio extension, Regional Oceanic Modeling System (ROMS)

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carbon production rate of 40 g C m-2 y-1 in the Enshunada Sea(Kimura et al., 1997; Nakata et al., 2000). Kaneko et al. (2013)
reported that segmentation of vertical nitrate ﬂuxes on bothsides of the Kuroshio is observed in the Kuroshio region(hereinafter referred to as KR; see the thick black box in
Figure 1A). Kodama et al. (2014) analyzed seasonal and spatial
variabilities of nitrate concentration in the upper ocean along
138°E in the KR and demonstrated a higher value in winter. In
the eastern part of the KR, the Kuroshio passes over the IzuOgasawara Ridge, a unique shallow topography consisting of
two major island chains located off the south coast of Japan
along 140–141°E. Sugimoto and Hanawa (2012) reported that
the Kuroshio tends to be unstable downstream after it passes
over the shallower part of the ridge at a depth of ~1000 m,
leading to intense eddy mixing. Studies on the volume transportof the Kuroshio (e.g., Isobe and Imawaki, 2002) and thewestward propagation of eddies near the Izu-Ogasawara ridge(e.g., Ebuchi and Hanawa, 2001; Xu et al., 2016) have been
extensively conducted despite the lack of biogeochemical
connections. In contrast, in the Kuroshio Extension (KE)region (east of M5 in Figure 1B), primary production in springis occasionally lowered by a lack of nitrate and silicic acid
(Nishibe et al., 2015). Intermittent nutrient transport inducedby ageostrophic vertical circulation and mixing has been
detected on a timescale of a few days near the Kuroshio front
in the KE (Clayton et al., 2014) due to the combination of
diabatic turbulence and adiabatic subduction (Nagai et al., 2012).
The importance of cyclonic (anticyclonic) eddy generation andrelated eddy core migration for enhancement (reduction) of
phytoplankton production in the KE has been discussed (e.g.,
Sasai et al., 2010; Kouketsu et al., 2014). More recently, aclimatological model (Uchiyama et al., 2017) showedsigniﬁcant differences of the biogeochemical responses to eddy
activities in the KR and KE. In the KR, persisting cyclonic eddies
developed between the Kuroshio and coastline are responsible
for upwelling-induced eutrophication. However, the eddyinduced vertical nutrient ﬂux counteracts and promotes
pronounced southward and downward diapycnal nutrienttransport from the mixed-layer down beneath the main bodyof the Kuroshio, which suppresses the near-surface productivity.
In contrast, the KE has a 23.5% higher productivity than the KR,
even at comparable eddy intensity. Upward nutrient transportprevails near the surface due to predominant cyclonic eddies,particularly to the north of the KE, where the downward
transport barely occurs, except at depths deeper than 400 m
and to a much smaller degree than in the KR. In addition toabundant mesoscale eddies shed around the Kuroshio, smaller
but more intensive submesoscale eddies with sizes of O (110 km) are known to appear mainly in colder seasons due to themixed-layer deepening and surface cooling (e.g., Kamidaira
et al., 2018). Although submesoscale eddies are mostly
conﬁned in the surface mixed layer, they promote quiteenergetic vertical secondary circulations that are anticipated to

1 Introduction
Carbon exchange between the atmosphere and ocean
substantially regulates climate change. Previous studies havereported that approximately one-half of total CO2 emissions
are taken up by a combination of terrestrial and marine carbon
reservoirs (e.g., Schimel et al., 2001; Ballantyne et al., 2012).
Nellemann et al. (2009) reported that 55% of all biologicalcarbon is captured by marine organisms, commonly referred
to as “blue carbon”. Falkowski et al. (1998) showed thebiogeochemical controls and feedbacks on global ocean
primary productivity, which are responsible for pelagic blue
carbon. Meanwhile, carbon cycling in coastal waters is a major
component of global carbon cycles and budgets (Bauer et al.,2013). In general, localized upwelling due to mesoscale cycloniceddies brings nutrient-rich subsurface water to the surface toenhance near-surface primary productivity. Particularly inpelagic upper ocean, subsurface nutrients are the only source,which are greatly inﬂuenced by vertical transport due to eddyinduced localized upwelling (e.g., Falkowski et al., 1991). Satellite
observations revealed that spatial variability in surface
chlorophyll was distributed on both mesoscale andsubmesoscale. Numerical simulations have also been
conducted with particular concerns about biological responses
to mesoscale and submesoscale variability. It has beenrecognized that biogeochemical cycles could be affected bymesoscale eddies in the global upper ocean (e.g., Chelton et al.,2011; Gaube et al., 2013). For instance, Lee and Kim (2018)
investigated regional variability and turbulent characteristics ofsubmesoscale surface chlorophyll concentrations anddemonstrated that spring (fall) blooms are more active in the
coastal areas in the Japan sea because of the stronger
submesoscale horizontal shear and vertical processes that
increase vertical mixing. Liu and Levine (2015) also concluded
that the chlorophyll concentration was increased by 38% on
average (83% maximum) at submesoscales during the coldseason in the North Paciﬁc Subtropical Gyre. The offshoretransport of nutrients and carbon driven by ﬁlaments andmesoscale eddies in the California Current System wasdiscussed based on a coupled physical-biogeochemical modelin a climatological conﬁguration (Nagai et al., 2015).
The Kuroshio is one of the most energetic western boundary
currents accompanied by vigorous eddy activity at mesoscaleand submesoscale. It originates from the eastern area of
Philippines, drifts north along the East China Sea shelf, andveers northeast to ﬂow past the southern coast of Japan. The
Kuroshio then separates from the shelf near 140°E and 35°N,
forming a free jet known as the Kuroshio Extension, in the North
Paciﬁc Ocean (Kawai, 1972; Qiu, 2002). Both nutrient
concentrations and their inventories in the northern South
China Sea are affected by abrupt Kuroshio intrusions throughthe Luzon Strait on seasonal scales (Du et al., 2013). The total
annual nitrogen input due to the frontal eddies could result in a

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A

B

FIGURE 1(A) The ROMS-NPZD model domain encompassing the Kuroshio Region (KR) and the Kuroshio Extension Region (KE). The thick black box
indicates the KR, while the outer square corresponds to the perimeter of the model domain. The blue line annotated with N1 is the selectedtransect along 145°E, a representative of the KE, with three black dots on N1 showing the sampling locations for Hovmöller plots (Figure 4).
(B) The enlarged view of (A) corresponding to the black box in (A). The ﬁve blue lines represent the selected transects along 138°E, 138.9°E,
139.7°E, 140.5°E, and 141.4°E in the KR, named M1-M5, that are used for the subsequent analyses. The black dots on M1-M5 again show thelocations used for Hovmöller plots in Figures 3, 6–8. Red contours indicate the approximate Kuroshio path with surface velocity magnitudes ≥0.5 m/s at intervals of 0.3 m/s. Colors are bathymetry.

KE are limited, particularly in conjunction with the eddying
Kuroshio currents affected by the ridge topography in the KR.
In the present study, we aimed to analyze the seasonalvariability of eddy-driven vertical nutrient ﬂuxes that playessential roles in maintaining upper-ocean primary
production, as well as its driving mechanisms in the KR and
KE regions. To this end, we employed a high-resolution model
based on the Regional Oceanic Modeling System (ROMS;
Shchepetkin and McWilliams, 2005; Shchepetkin and
McWilliams, 2008) coupled with a nitrogen-based nutrient,
phytoplankton, zooplankton, and detritus (NPZD)
biogeochemical model described by (Fasham et al., 1990). The
model is initialized by the assimilative Japan Coastal Ocean
Predictability Experiments (JCOPE2) oceanic reanalysis(Miyazawa et al., 2009) and is run in a climatologicalconﬁguration for 10 years. This model was originallydeveloped and validated in a previous study (Uchiyama et al.,2017), where the annually averaged eddy-driven nitrate ﬂuxes
were discussed to highlight the opposing downward and upwardvertical nutrient supply in the KR and KE regions, emphasizingthat downward nutrient ﬂux suppresses primary production in
the KR. In contrast, the present study was focused on theseasonal variability of eddies and associated vertical nutrient
ﬂuxes along the Kuroshio path (or axis) around the KR and KE
regions with additional emphasis on the ridge topography. The
remainder of this paper is organized as follows. The design andconﬁguration of the coupled model are described in Section 2.
Section 3 introduces the model results including the seasonalenhance vertical transport of subsurface nutrient and thus toaffect upper-ocean primary production.
There are abundant studies concerning seasonal andinterannual variabilities of primary production and relatedparameterization, including those conducted by Uitz et al.
(2010), who analyzed seasonal and interannual variabilities ofglobal phytoplankton class-speciﬁc primary production.
Analyses in several speciﬁc regions have also been undertaken.
For example, subsurface chlorophyll maxima (SCM) areseasonal features and have strong effects on depth-integrated
primary production estimates in the Arctic Ocean when thesurface nitrate is depleted, while its interannual variability is very
limited (Ardyna et al., 2013). For SCM, Cullen (2015)
summarized that phytoplankton growth is controlled by abalance between available light intensity and nutricline depth,
presumably inﬂuenced by seasonal variations in vertical nitrate
ﬂux that could directly change the structure of SCM. Lomas et al.
(2012) reported seasonal primary production on the Eastern
Bering Sea shelf in spring and summer 2008 and 2009,concluding that the integrated rate of net primary production
is generally lower in summer, while phytoplankton growth rate
is higher. The pattern of seasonally integrated primary
production dynamics in the Kara Sea, Russia, was discussed
based on satellite data obtained in 2003–2015 (Demidov et al.,2017). Seasonal variability of the integrated net primary
production dominates over the interannual signal in the
Mediterranean Sea (Lazzari et al., 2012). However, studies on
the seasonal variability of the primary production in the KR and

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variability of surface biogeochemistry and eddy activity inrelation to the Kuroshio dynamics, as well as the effects of theoceanic ridge in the KR. The dynamics and the eddy generation
mechanisms are discussed in Section 4, followed by concludingsummary in Section 5.

et al., 2003) was used to improve the Kuroshio path
reproducibility, with a weak nudging inverse time scale of 1/20
per day. Table 1 summarizes the detailed numericalconﬁgurations of the ROMS models.

2 Methods

2.2 Biogeochemical model

2.1 Ocean circulation model

We employed a simple nitrogen-based pelagic NPZD
biogeochemical model based on (Fasham et al. 1990), with a
modiﬁcation described by Gruber et al. (2006), where we
consider ﬁve components: nitrate½NO−3 , ammonium ½NH4+ ,
phytoplankton [Phyt], zooplankton [Zoo] and detritus [Det].
The conservation equations are given as follows:

We exploited a downscaling ocean circulation model basedon the Regional Oceanic Modeling System (ROMS; Shchepetkin
and McWilliams, 2005; Shchepetkin and McWilliams, 2008),
coupled with a nitrogen-based pelagic NPZD biogeochemical
model (Section 2.2), encompassing both KR and KE regions(Uchiyama et al., 2017). The initial and side boundary
conditions for the ROMS were provided by monthly
climatology of the assimilative JCOPE2 oceanic reanalysis(Miyazawa et al., 2009). A one-way ofﬂine nesting technique
was employed to convey the parent JCOPE2 to the child
ROMS model with grid resolution reﬁnement (e.g., Mason
et al., 2010; Uchiyama et al., 2014; Kamidaira et al., 2017;
Uchiyama et al., 2017; Kamidaira et al., 2018; Uchiyama et al.,2018a; Uchiyama et al., 2018b; Uchiyama et al., 2018c; Tada
et al., 2018; Masunaga et al., 2018; Kamidaira et al., 2019;
Masunaga et al., 2019; Zhang et al., 2019; Kurosawa et al.,2020; Kamidaira et al., 2021; Takeda et al., 2021; Uchiyama
et al., 2022; Masunaga et al., 2022; Matsushita et al., 2022).
Therefore, the horizontal grid spacing was successfully reduced
from 1/12° (~10 km) of the JCOPE2 reanalysis to 3 km of the
ROMS model, and vertically into stretched 32 s-layers(Shchepetkin and McWilliams, 2005) with grid height
reﬁnement near the surface and bottom to adequately resolve
the boundary layers. We employed the K-ProﬁleParameterization (KPP) mixed-layer turbulence model
described in Large et al. (1994) and Lemarié et al. (2012) torepresent the vertical momentum and tracer mixing. With a 3km grid resolution, the present model is considered to be asubmesoscale eddy-permitting model, in which submesoscaleeddies are marginally represented (e.g., Uchiyama et al., 2017).
The SRTM30_PLUS product (Rodriguez et al., 2005; Rodriguez
et al., 2006; Becker et al., 2009) at a 30 arc second resolution
complemented by the J-EGG500 (http://www.jodc.go.jp/data_
set/jodc/jegg_intro.html) data set at a 500 m resolution was
utilized to represent the bathymetry. The ROMS model wasforced by the daily climatology of the GPV-GSM surface windstress (Roads, 2004) provided by the Japan Meteorological
Agency (JMA). The surface heat and freshwater ﬂuxes wereobtained from the monthly climatology of the Comprehensive
Ocean-Atmosphere Data Set (COADS; Woodruff et al., 1987).
Additionally, four-dimensional temperature and salinity (TS)nudging (also known as robust diagnostic; e.g., Marchesiello

Frontiers in Marine ScienceD½NO−3  = −Q1 ,
Dt

(1)

D
½NH4+  = −Q2 + m½Zoo½NH +  · ½Zoo + m½Det½NH +  · ½Det , (2)
4
4
Dt


D
½Phyt  = − m½Phyt  + m½Phyt ½Det  · ½Phyt  − G + Q1 + Q2 , (3)DtD½Zoo = − m½Zoo + m½Zoo½NH +  + m½Zoo½Det · ½Zoo + b · G,
4
Dt

(4)



D
½Det  = − m½Det  + m½Det ½NH +  · ½Det  + ð1 − b Þ · G
4Dt+ m½Phyt ½Det  · ½Phyt  + m½zoo½Det · ½Zoo,(5)

where D/Dt is the material derivative that includes 3-D
advection, vertical settling of [Phyt], [Zoo] and [Det], andvertical eddy diffusive ﬂuxes computed by the KPP model(Large et al., 1994). Q1 indicates the rate of nitrate uptake
by phytoplankton, Q2 denotes the rate of ammonium uptake

TABLE 1 Ocean circulation model conﬁgurations.

Model conﬁgurations

Data used

Computational period

Climatological 10 years

Grid cells

784 × 864 (× 32 layers)

Horizontal grid resolution

3 km

Baroclinic time step

150 s

Surface wind stress

JMA-GSM (daily climatology)

Surface ﬂux

COADS (monthly climatology)

Boundary/Initial condition

JCOPE2 (monthly climatology)

T-S nudging

JCOPE2 (10-day averaged climatology)

Topography

SRTM30+JEGG500

STRM30: SRTM30_PLUS (Rodriguez et al., 2005; Rodriguez et al., 2006; Becker et al.,2009).
J-EGG500 (http://www.jodc.go.jp/data_set/jodc/jegg_intro.html).

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oxidation as the energy. Yet photosynthesis and primary
production are not the same concept, Chl-a concentration andprimary production are closely related to each other. For
example, Behrenfeld et al. (1998) evaluated the primary
production from Chl-a concentration with an empirical relation:by phytoplankton, and G is the rate of phytoplankton grazing byzooplankton. These three terms are given by:
aJ · ½Phyt  · ½NO−3  · e− ∅ ·½NH4 ,
KNO−3 + ½NO−3 (6)aJ · ½Phyt  · ½NH4+ ,
KNH4+ + ½NH4+ (7)gmax · ½Phyt  · ½Zoo
:KPhyt + ½Phyt 

(8)

+

Q1 =

Q2 =

G=

log10 P = 0:559 log10 C + 2:793,

(9)
-2

-1

where P is primary production with the unit of mgC m d , C is
the Chl-a concentration with the unit of mgC m-3. Because P
could be evaluated more complicatedly with Chl-a speciﬁc
absorption coefﬁcient of phytoplankton, PAR, etc, Eq. (9) isjust a simpliﬁed representation. Although P may also be
evaluated from the nitrate and ammonium uptakes, viz., Eqs(6) and (7), with some assumptions such as the canonicalRedﬁeld C/N ratio of 6.625 (e.g., Koné et al., 2005), in-situ P is
still underway to be quantiﬁed precisely and universally (e.g.,Oschlies, 2001). Instead, we simply view Chl-a as a good proxyof P relying empirically on Eq. (9) in the present analysis bypresuming that spatiotemporal variabilities of P could be
qualitatively represented by surface Chl-a ﬁeld in the study
area. Hence, we leave the detailed quantiﬁcation of P to
future works.

where aj is the light limited growth rate, with unit of d-1, as afunction of photosynthetically active radiation (PAR) andmaximum growth rate (see Eqs. 4-5 in Fasham et al., 1990).
The other model parameters are summarized in Table 2.
The seasonal climatology of the World Ocean Atlas 2005
(WOA05. e.g., Garcia et al., 2006) and the monthly climatologyof the MODIS/Aqua satellite data (https://oceandata.sci.gsfc.
nasa.gov/MODIS-Aqua/) provided the initial and lateralboundary conditions for nitrate and phytoplankton. In thepresent study, we followed the conﬁguration described by
Gruber et al. (2006) and Uchiyama et al. (2017) to set
zooplankton to be proportional to chlorophyll-a (Chl-a)concentration for its initial and boundary conditions.
Meanwhile, ammonium and detritus were initialized to zero.
More details on the modeling approach of the current ROMSNPZD model are reported in Uchiyama et al. (2017). The model
was run for 10 years in a climatological mode, and the results forthe last (10th) year of data were used for the following analyses.
The present study investigates the upper-ocean primary
production, which is synthesis of organic compounds from
CO2, mainly by photosynthesis that uses light as its energy
while it often appears through chemosynthesis that relies on

3 Results
3.1 Surface Chl-a and eddy activity
The reproducibility of the hydrodynamic kernel of thepresent coupled ROMS-NPZD model has been extensively
conﬁrmed to show a good agreement in the annual andseasonally averaged values against satellite altimetry and sea
surface temperature (SST) data, in situ cross-sectional density
measurements, resultant 3D velocity ﬁelds, including theTABLE 2 Biogeochemical model conﬁgurations.

Parameter

Symbol

Value

Unit

Half-saturation for phytoplankton NO−3 uptake

KNO−3

1.5

mmol N m-3

Half-saturation for phytoplankton NH4+ uptake

KNH4+

0.5

mmol N m-3

Phytoplankton ammonium inhibition parameter∅

1.5(mmol N)-1

Phytoplankton loss to sink ratem[Phyt]0.01

d-1

Phytoplankton mortality to detritus ratem [Phy][Det]

0.072

d-1

Zooplankton maximum growth rate

gmax

0.75

d-1

Zooplankton assimilation efﬁciency

b

0.75

n.d.

Zooplankton half-saturation for ingestion

KPhyt

1.0

d-1

Zooplankton loss to sinkm[Zoo]

0.025

d-1

Zooplankton speciﬁc excretion ratem[Zoo] NH4+ ]

0.1

d-1

Zooplankton mortality to detritus

m[Zoo][Det]

0.025

d-1

Detrital loss to sink ratem[Det]

0.02

d-1

Detrital breakdown to NH4+ ratem[Det][ NH4+ ]

0.03

d-1

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study was to understand the inﬂuence of oceanic eddy dynamics
on vertical nutrient transport and their role in sustaining upperocean productivity, while avoiding terrestrial inﬂuences in theupper ocean that may introduce additional seasonality.
Figure 2 shows the spatial distributions of seasonallyaveraged surface Chl-a concentrations from winter (Dec.–Feb.)
to fall (Sep.–Nov.). An obvious spring bloom (Mar.–May) occurs
extensively on the northern side of the Kuroshio, between
Hokkaido Island (~144°E, 45°N) and the central Honshu
Island (~140°E, 35°N), because of abundant nutrient supply
from deeper layers to the surface in early spring (Figure 2B). By
contrast, although the Chl-a concentration on the southern sideof the Kuroshio is enhanced slightly, it remains lower than thaton the northern side. A possible reason is that the nitratedepleted subsurface mode water is dominant underneath thesouth of the Kuroshio (e.g., Nishikawa et al., 2013). The surface
Chl-a concentration is the lowest in summer (Jun.–Aug.;
Figure 2C), and then it generally increases in colder seasons
from fall to winter (Figures 2D,A). Meanwhile, the Chl-a
concentration is the highest in the Japan Sea in winter,compared to other seasons (Figure 2A), which is inconsistent
with observations (e.g., Yoo and Kim, 2003; Yamada et al., 2004;
Park et al., 2014), most likely due to the lack of the land-derived
nutrient input in the model. Nevertheless, the modeled seasonalvariability of surface productivity on the Paciﬁc side is largely
consistent with the MODIS/Aqua satellite data and previous
measurements (Sasai et al., 2007; Nagai et al., 2019). Qualitative

Kuroshio, and eddy intensity (Uchiyama et al., 2018b). More
importantly, the NPZD model was also validated with theclimatological satellite Chl-a data to show overall agreement,such as enhanced upper-ocean primary productivity enriched by
the nutrient stream accompanied by the Kuroshio (Uchiyama
et al., 2017; Nagai et al., 2019). Although this simpliﬁed
nitrogen-based pelagic model is not perfectly correct,
Uchiyama et al. (2017) concluded that the present model
performs reasonably well in diagnosing biological responses toeddy activities in the upper ocean around the Kuroshio.
However, there are several subtle discrepancies between themodel and observations, which are generally considered toplay minor roles in the present study. For example, modeled
primary production is slightly overestimated in the north of theKuroshio path in the KE compared to satellite observations,likely due to the use of a suboptimal set of the biologicalparameters and the biogeochemical model equations. Anotherpossible cause may be the lack of an iron limitation mechanism(e.g., Fiechter et al., 2009; Moore et al., 2013). In addition, theChl-a concentration near coastal areas is underestimatedbecause the model ignores land-derived nutrient input thatshould affect coastal productivity signiﬁcantly. In turn, as thecoastal Chl-a from the satellite is often contaminated byinﬂuences of suspended particulate matters (e.g., sediments),
the present inconsistency must be diagnosed carefully in future
works. It is worth noting that we intentionally excluded the landderived nutrient source because the primary aim of the present

A

B

C

D

E

F

G

H

FIGURE 2Upper panels: Seasonally averaged modeled surface chlorophyll-a (Chl-a) concentrations in four seasons. Note that we deﬁne four seasons as
winter (December-February), spring (March-May), summer (June-August), and fall (September-November), respectively. Lower panels: Daily
snapshots of relative vorticity normalized by the Coriolis parameter at the surface on the middle day of the four seasons. Note that we use
the Chl-a unit of mg/L here for comparisons to in-situ Chl-a data (e.g., Hsu et al., 2020). In contrast, phytoplankton concentrations shown in
Figures 3, 4 and 7 are depicted with the nitrogen unit of mmol N m-3 for comparisons to other nitrogen compartments such as phytoplankton
and nitrate to diagnose the nitrogen budget represented by the NPZD model. Nevertheless, the phytoplankton concentration can readily beconverted into the Chl-a unit with a Chl-a:N ratio of 2.0 (see Gruber et al., 2006).

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vertical structures across the Kuroshio path and at two
locations ±0.8° away from the path (Figure 1). Note that theKuroshio path is deﬁned by the maxima of the surface current
velocity. In the present model, we assume that the nitrogensource is distributed as nitrate in the subsurface, beneath themixed-layer (Sec. 2). Figure 3 shows Hovmöller diagrams of thenitrate concentration (left column), phytoplankton
concentration (middle column), and vertical eddy-induced
nitrate ﬂux (right column) in the northern, central, andsouthern sides of the Kuroshio, from the top to the bottom
rows along 138°E (M1, Figure 1B) in the KR. The magenta lines
indicate the corresponding mixed-layer depth determined by the
KPP boundary-layer sub-model of ROMS. To examine theimpacts of eddies on vertical nitrate transport, the verticalnitrate ﬂux F V was evaluated by applying Reynolds
decomposition of relevant variables into the mean and eddy
components using the following equation:evidence of the importance of eddies to seasonal productivity isdemonstrated in the lower panels of Figure 2, in which snapshotsof relative vorticity normalized by the local Coriolis parameter at
the surface are depicted for the four seasons in the enlarged area
(shown in the rectangular black boxes in the upper panels)around the KR and KE regions. While intensive mesoscalevortices are particularly signiﬁcant around the Kuroshio,
submesoscale eddies are generated more evidently in colder
seasons, with relatively smaller spatial scales in the northernarea (Figures 2E,F). In contrast, mesoscale eddies are more
predominant in warm seasons (Figures 2G,H). This area isknown to be occupied by intensive submesoscale coherent
structures in winter, mainly due to the mixed-layer deepening
and surface cooling (e.g., Kamidaira et al., 2018). Satellite ocean
color images have proven that such mesosocale andsubmesoscale structures signiﬁcantly affect the upper ocean
dynamics to alter surface Chl-a concentrations at these scales(e.g., Sangrà, 2015; Hsu et al., 2020).

w
 + N 0 w0 ,FV = Nw ≈ N|{z} |{z}mean

3.2 Comparison between Kuroshio
Region and Kuroshio Extension Region

(10)

eddy

where w is the upward vertical velocity, N is the nitrateconcentration ½NO−3 , the overbar denotes an ensemble (time)
averaging operator, and the prime indicates the ﬂuctuating(eddy) component for periods shorter than 90 days, calculatedwith a Butterworth frequency ﬁlter. Upward transport is deﬁned
as positive. We conﬁrmed the cross terms are sufﬁciently small.
As expected, intra-annual, seasonal variability is evident innitrate supply to the surface and the mixed-layer depth(Figures 3A-C). The mixed-layer deepens in colder seasons
from December to April, along with an enhanced nitrate
supply to the surface. This pattern is most signiﬁcant on the

3.2.1 Vertical structures and eddy-driven
nitrate ﬂux
The surface Chl-a in Figure 2 shows noticeable differences inspatial patterns between the upstream (i.e., the KR; e.g., M1
along 138°E, Figure 1) and downstream (i.e., the KE; N1 along
145°E) regions along the Kuroshio. In the KR, a shorewardconﬁned high Chl-a is formed, compared with that in the KE. To
understand the mechanisms of the different responses ofprimary production in the two regions, we investigated the

A

D

G

B

E

H

C

F

I

FIGURE 3

Hovmöller diagrams of nitrate concentrations (left column), phytoplankton concentration (middle column), and vertical eddy-driven nitrate ﬂux(right column) in the northern (top row), central (middle row) and southern (bottom row) locations along 138°E in the Kuroshio Region (KR, M1 asshown in Figure 1). The magenta lines are the corresponding mixed-layer depth determined by the K-Proﬁle Parameterization sub-model in ROMS.

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southern region. However, downward ﬂuxes appear in themixed-layer in winter along the Kuroshio path and its northside (Figures 3G, H), suppressing upper-ocean primary
production associated with eddy inﬂuences.
Chl-a within and around the mixed-layer appears to behigher in the KE, exhibiting a reddish color from April to June
(Figures 4E-F; up to ~1 mmol N m-3) than that in the KR(Figures 3E-F; ~0.4 mmolN m-3), except for the northernlocation where the nitrate concentration below the mixed-layer
is much higher in the KR (Figure 3A). The spring bloom is also
more remarkable in the KE than in the KR. The eddy-induced
ﬂux tends to exhibit upwelling at depths of ~100-300 m in theKE, particularly in colder seasons rather than warmer seasons, inthe northern location (Figure 4G). As the sign of eddy nitrate
ﬂux ﬂuctuates rapidly and repeatedly in time, we will look into
time-averaged spatial distributions later. It should be noted thata high correlation (a correlation coefﬁcient of ~0.62) between thenitrate concentrations and vertical eddy nitrate ﬂuxes in bothregions demonstrates that nitrate supply to the surface layer isstrongly inﬂuenced by mesoscale and submesoscale eddies. Sucha high correlation is more pronounced in the colder season,
particularly on the north side of the Kuroshio path (Figures 3A
and 4A). These results demonstrate that nutrient ﬂuxes from thenutrient-rich subsurface layer to the nutrient-depleted surface
layer are substantial for maintaining primary production near
the surface.
The other biological components (zooplankton, ammonium,
and detritus) are brieﬂy described below with the supplemental
Figures S1 and S2. Increase in zooplankton concentration on thenorth side of the Kuroshio is delayed for a month or two (Figures
S1A and S2A) compared with phytoplankton concentration,
while zooplankton concentration is fairly low along theKuroshio path and its south side (Figures S1B-C and S2B-C).

northern side of the path in the KR, where nitrate concentrationis the highest near the surface (Figure 3A). As the upper boundof the subsurface nitrate source (e.g., intermediate concentration
at ~15 mmolN m-3 depicted in cyan) is lowered in the southward
direction, as represented from Figures 3A-C, a meridionaltransition occurs with a southward upper-ocean decline innitrate concentration. Although the upper bound is elevated at
the northern location in warmer seasons from May to October,surface nitrate concentration is as low (Figure 3A) as those at thecentral and southern locations where the warm season upperbound is lowered (Figures 3B, C). Phytoplankton (viz., Chl-a
concentrations) ﬂuctuates quite sensitively in response toﬂuctuations in nitrate concentration in the mixed-layer(Figures 3D-F), depending on nitrate concentrations andgeographical locations relative to the Kuroshio axis. Chl-a isdistributed much deeper in colder seasons than warmer seasons
because of deep convective vertical mixing, indicated bydeepening of the mixed-layer, that promotes upward
entrainment of subsurface nutrient-rich water, thereby
maintaining high productivity.
Figure 4 shows the same plots as Figure 3, but along 145°E(KE, N1 in Figure 1A) to represent the KE region. Similar to the
KR in Figure 3, primary production is largest on the northernside of the Kuroshio, particularly in colder seasons with asouthward meridional phytoplankton downgradient(Figures 4D-F), where the nitrate upper bound descends(Figures 4A-B), even at the same distances from the Kuroshio
path as compared to those in the KR. The spring blooms occur
along the Kuroshio path and its south side from April to May(Figures 3E-F), while at the northern location, Chl-a
concentrations in colder seasons are occasionally as high as
those in spring (e.g., Dec. 20 and Feb. 10 in Figure 3D). The
vertical eddy-driven nitrate transport is positive (upward) in the

A

D

G

B

E

H

C

F

I

FIGURE 4

Same as Figure 3, but for 145°E in the Kuroshio Extension (KE, N1 as shown in Figure 1).

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colors; ~138°E–140°E & ~33°N–34°N; <~141°E & <~35°N)
ﬂuxes alternately occur along the Kuroshio path, with an
overall downward (upward) dominance in the KR (KE).
Coastline topographies are also responsible for magnifying theeddy ﬂux and enhance the complexity of the spatial distribution.
The Enshunada Sea, located in the north of the Kuroshio in 136°
E–140°E & 33.4°N–34.6°N, is characterized by a clear downward
eddy ﬂux in winter (Figures 5A, C), but by an overall positive(upward) ﬂux in summer (Figures 5B, D).
Seasonal differences in vertical eddy-driven nitrate ﬂuxes arealso apparent. The magnitude and extent of inﬂuences arelargely increased (decreased) in winter (summer) when verticalmixing is stronger (weaker). Focusing on differences in the KR
and KE regions, we note that the major trend of eddy nitrate ﬂux
is negative (downward) in the KR, particularly in the Enshunada
Sea in winter, which competes with coastal upwelling nitratetransport from the nutrient-rich subsurface water as downward
nitrate ﬂux serves to reduce productivity. The spatially averaged
eddy ﬂux in the KR is dominated by downward ﬂux, except
during summer because of the intensive subsurface downward
ﬂux underneath the Kuroshio axis, as illustrated by theprominent negative ﬂux in Figure 5 (see also Uchiyama et al.,2017). In contrast, the eddy nitrate ﬂux is broadly positive(upward) in the KE (Figure 5A), particularly during winter,
while it is negligibly small north of the Kuroshio during summer(Figure 5B). The sign change occurs around the Izu-Ogasawara
Ridge, where the negative downward eddy ﬂux in the upstream
region (<139°E) becomes positive over the ridge (139°E–140°E),
and then reverts back to negative in the downstream (140°E–
142°E), before reaching the KE, particularly in winter.

During the spring bloom, nitrate is mainly consumed byphytoplankton, which is subsequently grazed by zooplankton.
Nitrogen is mostly stored in phytoplankton and zooplankton
compartments in the KR and KE. Therefore, the nitrateconcentration decreases signiﬁcantly, exhibiting an obvious
negative correlation between plankton and nitrateconcentrations. Phytoplankton and zooplankton death further
enriches detritus sinking to ~100 m from the base of the mixedlayer (Figures S1D-F and S2D-F). Hence, the detritus
concentration is commonly distributed relatively deeper incolder seasons than in warmer seasons because of theenhanced vertical mixing in colder seasons. Detrital
decomposition and zooplankton death concurrently contributeto the increase of ammonium concentrations. Hence, inorganic
nitrogen deduced from detritus is the major source ofammonium in the deeper region below the mixed-layer,
especially on the northern side. Uptake of both nitrate andammonium by phytoplankton leads to the depletion ofammonium in the mixed-layer, particularly along theKuroshio path and on the southern side. The ammonium anddetritus concentrations are higher in the KE than in the KR. The
largest difference between the two regions is the subsurface
ammonium on the northern side, which is distributed to
300 m depth in the KE, while it exists down to ~100 m below
the mixed-layer base (Figure S2G). In addition, high-frequency
ﬂuctuations associated with eddy-driven nutrient transport are
signiﬁcant in all these compartments, showing substantial
impacts of eddies on the biogeochemistry to depths of several
hundred meters.

3.2.2 Averaged horizontal structures of verticaleddy-induced nitrate ﬂux

3.3 Effects of the oceanic ridge in the
Kuroshio Region: island mass effects

In the upper ocean, the transient (eddy) component of thevertical nitrate ﬂux dominates over the mean ﬂux, as mentioned
later. Therefore, we computed the vertically integrated eddyinduced nitrate ﬂux Fv (Eq. 10) from the surface to a depth of
300 m to examine seasonal patterns of the horizontal
distribution. We adapted 300 m here for the lower bound of
the vertical integral in both seasons because it mostly
encompasses highest productivity in winter (Figures 3 andFigure 4), whereas it shallows in summer that may lead tounderestimation of Fv. However, this choice does not actuallycause much problems according to our sensitivity tests withdifferent depths for the lower bound. The upper panels of
Figure 5 show the spatial distribution of vertically integrated
and seasonally averaged Fv for winter and summer, while thelower panels are the enlarged views of the KR, shown by the blueboxes in the upper panel. The mean eddy-induced nitrate ﬂux is
generally large around the Kuroshio path, with several signchanges occurring as the Kuroshio ﬂows northeastward inboth seasons. Downward (bluish colors; ~136°E–139°E & ~33°
N–34°N; ~140°E–142°E & ~34°N–35°N) and upward (reddish

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The Kuroshio ﬂows over an oceanic ridge (Izu-Ogasawara
Ridge; Figure 1B), located on the south coast of Japan in the KR,
meridionally stretching along 139–140°E. This uniquetopography is considered to have remarkable inﬂuences on the
Kuroshio and eddies, further affecting the associatedbiogeochemical responses. To examine changes inbiogeochemistry due to the ridge, we set four more crosssections along 138.9°E, 139.7°E, 140.5°E, and 141.4°E, both
upstream and downstream of the ridge (M2-5, Figure 1B).
Figure 6 illustrates Hovmöller diagrams of nitrateconcentrations on the time-averaged Kuroshio main axis, fromwest to east, and the two meridionally remote stations ±0.8°
from the axis. The sampled stations represented by black dots in
Figure 1B were selected on the M2-5 transects. Sets of the threevertically aligned panels, for example, Figures 6M2a-c (for M2),
are similar to Figures 3A-C (for M1). Note that the depths at thenorthern stations along M3 and M4 are ~300 m, and thus thedata below that depth are null. In addition, the northern station

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A

B

C

D

FIGURE 5

Upper panels: Spatial distribution of vertically integrated and seasonal averaged eddy-induced nitrate ﬂux to 300 m depth in winter and summer.
Lower panels: Enlarged plots of those shown in the upper panels for the Kuroshio Region (KR) shown by the blue boxes in the upper panels.

the reduced topographic constraint, to be a more freely
ﬂuctuating Kuroshio jet. Chl-a concentrations are also highest
in the northern stations with prominent spring blooms in Apr.–
Jun. (Figure 7M5A), consistent with the increased nitrate
distributions, with a lag of a few months. A strong eddy
nitrate ﬂux occurs in the mixed-layer during the colder season(Dec.–Apr.), followed by enhanced ﬂux mainly below the mixedlayer, but extended to the surface layer in the subsequent spring(Apr.–Jun.). Therefore, the increased vertical mixing due tosurface cooling in winter promotes upper-ocean eddy nitrate
ﬂuxes, bringing subsurface nitrate to the surface layer
persistently for a few months, which preconditions thealong M4 is so close to the shore, with a depth of ~100 m, that it
was replaced by a slightly offshore station at +0.4° (not +0.8°)
from the Kuroshio path. Figures 7, 8 show the same sets of plots
as Figure 6 but present phytoplankton concentrations (Figure 7)
and upward positive vertical eddy nitrate ﬂuxes Fv (Figure 8).
The general structure and variability are similar to thosealong M1, as discussed in Section 3.2.1. For instance, the mixedlayer deepens in colder seasons, thereby promoting nitrate
supply to the surface layer from the subsurface at all stations
except for the northern station along M5 (Figure 6M5A), where
nitrate concentration varies intermittently in the upper 300 m
layer, with a longer ﬂuctuation period, presumably as a result ofFrontiers in Marine Science

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FIGURE 6

Hovmöller diagrams of the nitrate concentrations in the northern (top row), central (middle row) and southern (bottom row) locations
represented by black dots Figure 1B along M2-5 in the KR. The magenta lines denote the corresponding mixed-layer depth.

the downstream region at the central and southern stations.
Primary production appears in spring along the eastern-mosttransect (Figures 7M5a-M5c), although the nitrate concentrationis relatively low (Figures 6M5a-M5c), again perhaps due to thenature of the Kuroshio jet that could promote abrupt vertical ﬂux
and horizontal nitrate transport from the upstream region (e.g.,
Nagai et al., 2019), thereby enhancing the production ofphytoplankton. Eddy-driven nitrate ﬂux is the strongest along
the main axis (Figures 8M2b-M5b), exhibiting considerable
vertically elongated structures, demonstrating the predominanceof quasi-geostrophic mesoscale eddies, especially around theoceanic ridge (Figure 8M3b). In turn, enhanced eddy ﬂuxes in
the mixed-layer in colder seasons indicate the emergence ofsusbmesoscale eddies, which can be marginally resolved in thepresent ROMS model (see Figure 2). Hence, the inﬂuence ofmesoscale eddies is most apparent on the Kuroshio path, near the
ridge, and within the downstream region on the north side of thepath, where the vertical Chl-a gradient is less obvious. For

subsequent Chl-a bloom under optimal radiation conditions inspring. During the spring bloom, the near-surface nitrate isconsumed by phytoplankton, leading to a depletion.
The ridge area (M3) is demonstrated to signiﬁcantly alter thenitrate distribution, where the near-surface nitrate is moderately
higher downstream compared to the upstream region, especiallyat the northern stations (Figures 6M2a-M5a). Phytoplankton is
distributed shallower in the upstream region, but is distributed
below the mixed-layer at a depth of ~200 m in the downstream
region. By contrast, at stations on the Kuroshio (Figures 6M2bM5b), near-surface nitrate concentration is higher in the upstream
region, while subsurface nitrate is lower, leading to steeper verticalnitrate gradients in the upstream region than downstream. Suchan increase in the vertically extended nitrate gradation in thedownstream region is also visible at the depths of ~100–300 m at
the southern stations (Figures 6M2c-M5c). Upper-ocean Chl-a isdistributed consistently with the vertically elongated nitrate,
leading to increased thickness of the high Chl-a water towards

FIGURE 7

Same as Figure 6, but for the phytoplankton concentrations.

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FIGURE 8

Same as Figure 6, but for the vertical eddy-driven nitrate ﬂuxes.

example, in winter and spring, the vertical eddy ﬂux is larger at thenorthern station in the downstream (Figure 8M5a) than that in
the upstream (e.g., Figure 8M2a) according to both mesoscale andsubmesoscale eddies that sustain local upwelling of nitrate,
resulting in surface-concentrated high nitrate (Figure 6M5a) andsubsequent spring blooms (Figure 7M5a).

along the Kuroshio path in winter (Figures 9A, C), consistent
with previous studies (e.g., Sasaki et al., 2014; Uchiyama et al.,2017; Kamidaira et al., 2018), which suggested that surface
cooling and associated mixed-layer deepening give rise tobaroclinic instability, resulting in the generation of vigorous
mesoscale and submesoscale eddies much more extensively incolder seasons in this area. The enhanced vertical eddy-driven
nitrate ﬂux in winter shown in Figures 5A, C is generally
collocated with the areas where large positive P e K e isdistributed. In contrast, PeKe decreases to narrow to the
Kuroshio path and is largely negative in summer (Figures 9B,
D), resulting in reduced eddy intensity; the vertical eddy nitrate
ﬂux is reduced accordingly (Figures 5B, D). In the KR, negative
PeKe appears near the Izu-Ogasawara Ridge in both seasons.
This ridge has a unique topographic feature, consisting ofmany islands and submerged seamounts, with depths
shallower than 1000 m. Therefore, the ridge is considered tointeract with the Kuroshio even at depths of ~800–1000 m(Figure 10), which inﬂuences subsurface water to a depth of1000 m in the KR, sometimes called island mass effects. Further
analyses of the inﬂuence of the ridge will be provided in thesubsequent section. It must be noted that the horizontal
distribution of KmKe is more or less similar to the distributionof PeKe in winter, with almost no clear seasonal variability, and istherefore not shown here.
To highlight the differences between the two EKE source terms in
the KR and KE regions, cross-sectional plots of seasonally averaged
KmKe (upper panels) and PeKe (lower panels) in winter along 138°E(KR; M1 in Figure 1) and 145°E (KE; N1 in Figure 1) are shown in
Figure 10. The associated mixed-layer depth is depicted by magentalines. The black dotted contours are the eastward velocity normal tothe cross-sections, representing the Kuroshio main body. In the KR,
eddies are generated by a combination of the positive KmKe and PeKearound the Kuroshio path in the upper ocean, while PeKe prevails
over KmKe within the mixed-layer, extending to ~32.1°N on thesouthern side of the path, as well as up to the coastline at ~34.6°N to

4 Discussion
4.1 Eddy generation mechanisms
To investigate the generation mechanism of eddies that playa central role in stimulating eddy nitrate ﬂuxes, we assessed theenergy conversion terms relevant to eddy kinetic energy (EKE).
We focus on KmKe, the conversion of mean kinetic energy to
eddy kinetic energy due to shear instability, and PeKe, theconversion of eddy potential energy to eddy kinetic energy due
to baroclinic instability, as deﬁned by the following equations(e.g., Klein et al., 2008; Oey, 2008):





∂u
∂u
∂u
∂ v
∂ v
∂ v
,
Km Ke = − u0 u0+ u0 v0+ u0 w0+ v 0 u0
+ v0 v0+ v 0 w0
∂x
∂y
∂z
∂x
∂y
∂z

Pe Ke = −

g 0 0
rw,
r0

(11)

(12)

where (x,y,z) are the horizontal and vertical coordinates, u and v
are eastward and northward horizontal velocities, P is thedensity of sea water, P0=1025.5kg m-3 is the reference density,and g is the gravitational acceleration. As KmKe and PeKe aredominant source terms in the EKE conservation equation, EKE
is increased (decreased) to let the mean ﬂow be unstable (stable)
when KmKe and PeKe are positive (negative).
Figure 9 is the same set of plots as Figure 5, but shows thehorizontal distributions of vertically integrated PeKe to a depthof 300 m in two seasons. Positive PeKe is distributed broadly

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A

B

C

D

FIGURE 9Same as Figure 5, but for the baroclinic conversion rate, PeKe.

the north, to a lesser degree (Figures 10A, B). Therefore, shear
instability (positive KmKe) due to the energetic Kuroshio mainly
promotes mesoscale eddies near the path (e.g., ~32.9°N–33.6°N &138°E) that leads to negative downward eddy-driven nitrate ﬂux inthe KR, i.e., the downstream region of the ridge, in winter (bluishareas: ~136°E–139°E & ~33°N–33.5°N, ~140°E–142°E & 33.5°N–35°
N. Figures 5A, C). Baroclinic instability (positive PeKe) in winter isalso important to the broadly distributed high EKE off the path,
resulting in the downward Fv near the coast to the north (~136°E–
140°E & ~33°N–34.5°N), and the upward Fv to the south (>~33°N)
in the mixed-layer (Figure 5C).
In contrast, in the KE region, the positive KmKe and PeKe
(Figures 10C, D) jointly give rise to upward eddy nitrate ﬂux

Frontiers in Marine Science(Figure 5A) in the upper ocean in winter along the N1 transect,maintaining near-surface primary productivity. Similar to theKR, shear instability occurs only near the Kuroshio, whereas
baroclinic instability is extensive along the meridional length
more evidently on the north side of the path, thereby promoting
eddy intensity and increased upward eddy ﬂux due to vigorous
vertical mixing that bring the subsurface nitrate to the upper
ocean, even away from the path. This meridional asymmetry of
PeKe distributions is key to the more active primary production
occurring broadly in the KE around the Kuroshio path and its
northern region in winter (Figure 5A), despite the upper boundof the subsurface nitrate source being located deeper in the KE(Figure 4), than in the KR (Figure 3).

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C

B

D

FIGURE 10

Cross-sectional plots of the seasonally averaged barotropic conversion rate, KmKe (top row), and baroclinic conversion rate, PeKe (bottom row),along 138°E (M1) in the KR (left column) and 145°E (N1) in the KE (right column) in winter. The magenta lines denote the mixed-layer depth
computed by KPP model. The black dotted contours show eastward velocity perpendicular to the transects, denoting approximate positions of
the Kuroshio.

Figure 11 shows the same plots as Figure 10, but in summer.
Compared to winter, the surface mixed-layer becomes thinner insummer, clearly reducing baroclinic instability as PeKe is only
signiﬁcant near the Kuroshio path in both KR and KE regions.
The summer KmKe is similarly distributed to that in winter, withalmost no obvious seasonal variability, as mentioned earlier inthis subsection. In the KR, positive PeKe (Figure 11B) promotes
the eddy-driven downward nitrate ﬂux (Figure 5B) throughbaroclinic instability only near the Kuroshio path (~136°E–
139°E & ~33°N–33.5°N) in summer, although positive PeKe in
the mixed-layer in winter (Figure 10B) is attributed to the muchwider appearance of non-trivial eddy ﬂuxes Fv (Figure 5B).
Likewise, in the KE, P e K e is considerably diminished,becoming negligible, while the development of positive KmKenear the path plays a role in maintaining modest eddy nitrate
ﬂux in this location. A sign of Fv largely depends on the
background nitrate distribution; Fv > 0 (upward) occurs if
eddy mixing reaches down to the subsurface nitrate reservoir,
otherwise Fv < 0 (downward) or if near-surface nitrate supply is
expected in case of coastal upwelling etc.
In summary, baroclinic instability is the most importantfactor accounting for seasonal variability in eddy generation. It
vitally stimulates the downward and upward eddy-induced
nitrate ﬂuxes in the upper ocean in the KR and KE in winter,
while its inﬂuence becomes much weaker in both regions
in summer.

A

C

B

D

FIGURE 11

Same as Figure 10, but in summer.

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and distributed not only near the surface but also at depth,
downstream along M5. A simple but plausible description of the
dynamical effects of the ridge on the Kuroshio and associatededdy activity is a squashing by islands and submerged
seamounts, as illustrated in Figures 12C, D, which
spontaneously accelerates and occasionally bifurcates theKuroshio, ampliﬁes the lateral velocity shear, and promotes
mesoscale eddies around the topographies, even at depth. Suchenhanced mesoscale eddies shed by the ridge make vertical andhorizontal mixing more energetic, thereby inducing verticallyextended intensive eddy ﬂux (Figure 11M3c). After passing over
the ridge, the squashed Kuroshio is relaxed to expand laterally
downstream, resulting in deceleration of the Kuroshio main
body and reduced eddying ﬂuctuations spreading over wider anddeeper areas (see Figures 12A, E).
It is noteworthy that the seasonal variability in these crosssectional structures is insigniﬁcant, except for a minor meridional
shift of the Kuroshio path up to ~0.4°, and a shallower mixedlayer, particularly in summer, as supplemented in Figure S4. As
shown in Figures 2 and Figure 11, the deepened mixed-layer isaccompanied by energetic submesoscale activities occurring
mostly within the mixed-layer in colder seasons, which are
attributed to additional near-surface eddy nitrate ﬂuxes that
promote upward nutrient supply through enhanced verticalmixing. These submesoscale eddies are primarily provoked bybaroclinic and mixed-layer instabilities, triggered by surface
cooling and down-front wind, which makes the Ertel potential
vorticity negative and preconditions symmetric instability in theupper ocean (Thomas and Lee, 2005; Thomas and Taylor, 2010;
Kamidaira et al., 2018; Nagai et al., 2019), regardless of theridge topographies.

4.2 Altered dynamics around theoceanic ridge
To investigate a possible mechanism responsible for spatialchanges in vertical nitrate transport in the KR, we examined thecross-sectional distributions of seasonally averaged values ofseveral variables in winter (Dec.–Feb.) along the threetransects (M1, M3, and M5, Figure 1B) in Figure 12 (moredetailed spatial structures are shown in Figure S3). The displayed
variables are EKE = ( = 12 (u02 + v02 ), colors) and eastward
horizontal velocity normal to the transects (white contours) in
the upper panel, while nitrate concentrations (colors) andpotential density sq (black contours) are shown in the lower
panels. The magenta lines are the seasonally averaged mixedlayer depth estimated by the KPP model. The Kuroshio main
body is inclined to extend southward to ~800 m depth. It is
shaped by topographic inﬂuences of the ridge near M3, as shownin Figure 12C. EKE peaks near the surface and slightly
northward of the maximum velocity of the Kuroshio, in
conjunction with the maximum horizontal velocity shear, withmagniﬁed complexity exhibited by two EKE peaks around theridge at ~34.4°N and ~33.7°N (Figure 12C). Similarly, nitrateconcentration and potential density are also inclined southward,
with elevated values near the coast inducing northward
upwelling of subsurface nitrate and potential energy from thebase of the Kuroshio main body to the coast. Mixed-layer depth
is consistently shallower on the shore side than offshore(magenta lines in Figure 12). Near-surface nitrate is higher inthe upstream region, whereas elevated nitrate does not reach thecoast along M5 (Figure 12F). The concentrated EKE peak along
M1 spreads meridionally in the upstream, while it is decreased

C

A

B

E

D

F

FIGURE 12

Cross-sectional plots of seasonally averaged EKE (upper) and nitrate concentrations (lower) along the transects M1, M3, and M5 in winter(colors). Contours are eastern velocity [m/s] normal to the transects (upper) and potential density sq [kg/m3] (lower). The magenta lines areseasonally averaged mixed-layer depths.

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extend on the north side of the Kuroshio. The vertical KmKe islargely centered on the path and near the topography but ismostly negative or weak (notice the different scales), indicatingthat horizontal shear instability dominates over the vertical shear
instability. All three conversion rates are signiﬁcantly energizedalong M3 (139.7°E) around the ridge. When the Kuroshio passes
over the ridge, it is squashed to enhance the horizontal velocity
shear and subsequent eddy shedding, mostly at mesoscale,except for the upper ocean, where baroclinic submesoscaleinstability takes over shear instability, as anticipated in thepreceding subsection. Moreover, an interaction between ridge
topography and the Kuroshio front at depth triggers pronounced
baroclinic instability below the mixed-layer along M3(Figure 13F), leading to continuous subsurface destabilizing
effects downstream (Figure 13I), with increased subsurface
EKE (Figure 12E). Therefore, the deeper ocean is inﬂuenced
by a combination of horizontal shear instability and baroclinic
instability, provoking signiﬁcant mesoscale eddy-driven nitratetransport downstream (Figures 8M4b, M5b), particularly on thenorthern side of the path (Figures 8M4a, M5a).
We should mention the distributions of conversion rate inwarmer seasons (data not shown). Similar to the mean structures
discussed in Section 4.2, the surface mixed-layer becomesthinner, resulting in considerable weakening of the nearsurface submesoscale baroclinic instability. In addition to the

4.3 Eddy generation by the oceanic ridge
Thus far, we have understood that spontaneous generationof mesoscale eddies by the Kuroshio shear and submesoscaleeddies by surface cooling are the two substantial elements that
affect eddy nitrate ﬂuxes responsible for sustaining primary
production in the KR and KE regions. An additional key
mechanism may be the topographically-generated mesoscalevariability due to the ridge. Therefore, we next examined theinﬂuences of the local topography on eddy generation bydecomposing the barotropic conversion rate K m K e into
horizontal and vertical components, as well as the baroclinic
conversion rate PeKe along the three transects (M1, M3, and M5,
Figure 1B) in winter (Figure 13) (more details are supplemented
in Figure S5). Consistent with the mean variables in Figure 12,
an apparent spatial asymmetry in the conversion rates isobserved between the upstream and downstream regions, withrespect to the ridge (M3; Figures 13D-F) as a pivot. In the
upstream region, the positive horizontal KmKe and PeKe due tohorizontal shear instability and baroclinic instability that
concurrently induce eddy-driven nitrate ﬂux near the
Kuroshio. Positive PeKe is induced in the upper ocean due tosubmesoscale eddies, particularly near and on the south side of
the path, with signiﬁcant ampliﬁcation in the downstream
region, where the near-surface PeKe is strengthened broadly to

D

A

G

E

B

C

H

F

I

FIGURE 13

Cross-sectional plots of seasonally averaged EKE source terms. Horizontal component of barotropic conversion rate KmKe (top row), verticalcomponent of KmKe (middle row), and baroclinic conversion rate, PeKe (bottom row), along the transects M1, M3, and M5 in winter. The
magenta lines show the mixed-layer depth computed by the KPP model. The black dotted contours show eastward velocity normal to thetransects, representing approximate positions of the Kuroshio.

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nutrient-rich subsurface to the nutrient-exhausted surface isimportant for maintaining near-surface primary productivity.
However, downward eddy nitrate ﬂuxes were apparent in winterin the upstream (Enshu-nada Sea region) and downstream regions,relative to the ridge in the KR. Eddy generation analysis indicatedthat, in winter, the topographic eddy shedding, positive barotropic
conversation rate (KmKe), and baroclinic conversion rate (PeKe)
jointly promoted eddy-driven downward nitrate ﬂuxes throughshear and baroclinic instabilities most vigorously in the mixed-layer
along the Kuroshio path and its northern side in the KR, which
eventually suppressed biological productivity. Positive PeKe leads toa relatively weak upward nitrate ﬂux that maintained primary
production on the southern side. In the KE, upward eddy ﬂux,
due to the combination of positive KmKe and PeKe, enhanced
primary production in the upper ocean. Inﬂuences ofsubmesoscale eddy-driven, near-surface baroclinic instability
extends broadly in the meridional direction, with a southwardbias in the upstream region, and a northward bias in thedownstream region, attributed to the spatially heterogeneous Chla distributions. By contrast, in summer, the mixed-layer depth
became very shallow, and thus the upper ocean PeKe almost
vanishes in both KR and KE. Positive KmKe and PeKe arise
mostly at depth beneath the mixed-layer, which stronglyinteracted with the ridge topography in the KR, increasing in the
upstream region and decreasing in downstream region. In the KE,
as PeKe was prominently reduced in summer, eddy nitrate ﬂux
decreased signiﬁcantly, particularly in the north of the Kuroshio.
Therefore, baroclinic instability is the key inﬂuencer on seasonalvariability in eddy generation near the surface, where vertical eddy
mixing is inevitably important to promote subsurface nutrient
supply to the upper ocean.
In terms of the topographic inﬂuences of the Izu-Ogasawara
Ridge, one essential regional difference is that the spatial
variability of the vertical eddy nitrate ﬂux ﬂuctuates more in
KR than in KE. The spatial variability of the eddy-driven nitrate
ﬂux, and the underlying eddy generation mechanism, aresigniﬁcantly altered by ridge topography, characterized by ﬂow
squash and mesoscale eddy shedding. Turbulence associatedwith the Kuroshio tends to be less energetic in the upstream,
while the ridge generates intensive eddy mixing more broadly
and deeply in the downstream, mainly due to the interaction
between the Kuroshio front and ridge topography, which results
in mesoscale eddy-generating baroclinic instability. Although
the near-surface nitrate concentration is lower in thedownstream, the upward eddy-driven nitrate ﬂux is stronger
in maintaining primary production due to shear and baroclinic
instabilities in winter. Quantitative comparison among the threemajor EKE source terms demonstrated that PeKe and thehorizontal K m K e dominate over vertical K m K e on eddy
generation in the KR. The horizontal KmKe increased in the
Kuroshio path and the region near the ridge, while PeKe wasintense and highly variable in time in the mixed-layer. The
seasonal meridional shift in the Kuroshio path was observed inmodest northward shift of the Kuroshio path that culminateswith the northward shift of the subsurface peak location of PeKealong M2, the overall patterns of the three conversion rates are
predominantly the same as those for winter (Figure 13).
However, the subsurface horizontal KmKe and PeKe are lesssigniﬁcant or even negative (for PeKe, i.e., stabilizing effects) inthe downstream region, particularly along M5 in warmer
seasons. Thus, the eddy ﬂuxes are weakened (Figures 8M5a-c).
Consequently, warmer seasons are characterized by a modest
northward shift of the Kuroshio by ~0.4° in the present
climatological model results. This subtly affects changes in theconversion rates, whereas the interaction between the Kuroshio
and the ridge topography is crucial to alterations in eddy
intensity in the downstream region. In turn, the warmed
upper ocean and increased incoming surface heat andradiation ﬂuxes greatly suppress near-surface submesoscale
ﬂuctuations, which resulted in reduced vertical mixing, eddy
nitrate ﬂuxes, and thus primary production in the upper ocean
in warmer seasons.

5 Concluding Summary
The Kuroshio has been recognized as a nutrient stream that
supplies nutrient-rich subsurface water to the upper ocean, mosteffectively by vertical eddy-driven nitrate ﬂuxes (e.g., Uchiyama
et al., 2017; Nagai et al., 2019). In the present study, weinvestigated seasonal variability of eddy ﬂuxes that sustain
upper ocean primary production, and the driving mechanisms
behind them in the Kuroshio Region (KR) and Kuroshio
Extension (KE) regions off the Paciﬁc coast of Japan by using
the JCOPE2-ROMS downscaling circulation modeling suite
coupled with an NPZD biogeochemical model. The upperocean primary production is found to be maintained by twocompleting effects associated with oceanic eddies: 1) the
downward eddy nitrate ﬂux that suppresses the production bynear-surface nitrate extraction, and 2) the upward eddy nitrate
ﬂux that promotes the production by localized upwelling of thesubsurface nutrients. The balance between these two effects varies
with seasons and areas due to the different eddy generation
mechanisms. In addition, we showed the shallow topography of
the Izu-Ogasawara Ridge, which lies underneath the Kuroshio
path, alters the eddy generation mechanisms signiﬁcantly.
We paid a particular attention to surface chlorophyll-a (Chl-a)
as the most important indicator of the upper-ocean primary
production. Its distributions demonstrated that the segmentationsin primary productivity occurred on both sides of the Kuroshio,with a higher Chl-a concentration in the northern area. An obvious
spring bloom occurred on the northern side of the KE and on themain path of the Kuroshio. Enhanced vertical mixing in winter andsubsequent improvement of the light environment in spring
resulted in enhanced primary production around the Kuroshio,
both in the KR and KE. The overall upward entrainment from the

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10.3389/fmars.2022.990559

JDOSS/infoJEGG.html. The GPV-GSM atmospheric productwas generated by JMA and is available from the repository at
http://database.rish.kyoto-u.ac.jp/arch/jmadata/data/gpv/
original/. The COADS and WOA05 data are maintained anddistributed by NOAA at https://psl.noaa.gov/data/gridded/data.
coads.1deg.html and https://www.nodc.noaa.gov/OC5/WOA05/
pr_woa05.html. The gridded MODIS/Aqua satellite surface chla product is available at https://oceandata.sci.gsfc.nasa.gov/
MODIS-Aqua/Mapped.

the present model, which introduced changes in the interaction
between the ridge and the front responsible for PeKe on an intraannual time scale.

Data availability statement
The original contributions presented in the study areincluded in the article/Supplementary Material. Further
inquiries can be directed to the corresponding author.

Conﬂict of interest
Author contributions
YS and HY are employed by Construction Technique
Institute Engineering Co., Ltd. and Alpha HydraulicEngineering Consultants Co. Ltd., respectively.
The remaining authors declare that the research was conductedin the absence of any commercial or ﬁnancial relationships that
could be construed as a potential conﬂict of interest.

XZ: investigation, software, validation, visualization, andwriting – original draft. YU: conceptualization, methodology,
supervision, software, writing - reviewing and editing, andfunding acquisition. EM: investigation. YS: investigation, software,and validation. HY: methodology and investigation. All authors
contributed to the article and approved the submitted version.

Publisher’s noteAcknowledgments
All claims expressed in this article are solely those of theauthors and do not necessarily represent those of their afﬁliatedorganizations, or those of the publisher, the editors and thereviewers. Any product that may be evaluated in this article, or
claim that may be made by its manufacturer, is not guaranteedor endorsed by the publisher.

This work was ﬁnancially supported by the Japan Society for
the Promotion of Science (JSPS) Grants-in-Aid for ScientiﬁcResearch 18H03798 and 19H00782 at Kobe University. The
ROMS-NPZD model used in this study is distributed by its
developers and is available at https://www.myroms.org/. The
JCOPE2 reanalysis data are available for scientiﬁc research
purposes from Japan Agency for Marine-Earth Science andTechnology (JAMSTEC) and are available at http://www.
jamstec.go.jp/jcope/htdocs/e/distribution/index.html. The
STRM30_Plus data are available at https://topex.ucsd.edu/
WWW_html/srtm30_plus.html. The J-EGG500 data set is
distributed by JODC at https://www.jodc.go.jp/jodcweb/

Supplementary material
The Supplementary Material for this article can be foundonline at: https://www.frontiersin.org/articles/10.3389/
fmars.2022.990559/full#supplementary-material

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