TYPE Original Research
PUBLISHED 24 April 2023
DOI 10.3389/fmars.2023.1174940

OPEN ACCESSEDITED BY

Andrea Cucco,
National Research Council (CNR), Italy
REVIEWED BY

Emmanuel Hanert,
Université Catholique de Louvain, Belgium
Yang Ding,
Ocean University of China, China*CORRESPONDENCE

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

This article was submitted to
Coastal Ocean Processes,
a section of the journal
Frontiers in Marine Science

Quantifying connectivity
between mesophotic andshallow coral larvae in Okinawa
Island, Japan: a quadruple
nested high-resolution
modeling study
Kimika Takeyasu 1, Yusuke Uchiyama 1* and Satoshi Mitarai 2
1
Department of Civil Engineering, Kobe University, Kobe, Japan, 2 Marine Biophysics Unit, Okinawa
Institute of Science and Technology Graduate University, Okinawa, JapanRECEIVED 27 February 2023
ACCEPTED 05 April 2023
PUBLISHED 24 April 2023
CITATION

Takeyasu K, Uchiyama Y and Mitarai S(2023) Quantifying connectivity between
mesophotic and shallow coral larvae in
Okinawa Island, Japan: a quadruple nested
high-resolution modeling study.
Front. Mar. Sci. 10:1174940.
doi: 10.3389/fmars.2023.1174940
COPYRIGHT© 2023 Takeyasu, Uchiyama and Mitarai.
This is an open-access article distributed
under the terms of the Creative Commons
Attribution License (CC BY). The use,
distribution or reproduction in otherforums is permitted, provided the original
author(s) and the copyright owner(s) are
credited and that the original publication inthis journal is cited, in accordance withaccepted academic practice. No use,
distribution or reproduction is permitted
which does not comply with these terms.

Coral bleaching has recently been occurring extensively across the world’s
oceans, primarily because of high water temperatures. Mesophotic corals that
inhabit depths of approximately 30–150 m are expected to survive bleaching
events and reseed shallow water corals afterward. In Okinawa, Japan,
mesophotic coral ecosystems have been reported to serve as a refuge forpreserving the genotypic diversity of bleaching-sensitive corals. The
connectivity of larval populations among different habitats is a key elementthat determines the area to be conserved in desirable coral ecosystems. Because
coral larvae are largely transported passively by ambient oceanic currents,
particularly in the horizontal direction, numerical ocean circulation models
greatly help to quantify connectivity with detailed spatiotemporal network
structures. The present study aimed to quantify the short-distance connectivityof shallow and mesophotic coral larvae in reef areas on the northwest coast of
Okinawa Island. To this end, a quadruple nested high-resolution synoptic ocean
model at a lateral spatial grid resolution of 50 m was developed, which wascapable of realizing detailed coastal currents inﬂuenced by complex nearshore
topography, and coupled with an ofﬂine 3-D Lagrangian particle-tracking model.
After validating the developed model, short-distance horizontal coralconnectivity across reef areas on the northwest coast was successfully
evaluated. The alongshore lateral connectivity had apparent asymmetry caused
by depth-dependent horizontal currents, whereas the larvae spawned at shallow
and mesophotic depths were reachable to each other. Such across-depth larval
dispersal was attributable to the mixed-layer depth in the spawning period, viz.,the boreal spring, which approximately coincides with the boundary between
shallow and mesophotic coral, leading to the intensive vertical exchange ofvirtual larvae.
KEYWORDS

mesophotic coral, connectivity, ocean circulation and particle tracking model,
advective and dispersive effects, mixed layer

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Bongaerts et al. (2010) proposed the ‘deep reef refugia hypothesis’,
which suggests that deep reef areas are protected or dampened fromdisturbances that affect shallow corals and may provide a viablereproductive source for shallow reef areas after disturbance.
Recently, mesophotic coral ecosystems (MCEs; e.g., Kahng et al.,2014) that inhabit intermediate depths, ranging from approximately
30–150 m, called the mesophotic zone (MPZ), have drawn attention
as potential refuges during high-temperature events under threatsof coral bleaching. Mesophotic coral ecosystems consist ofgenetically similar species to shallow coral ecosystems and are
expected to survive bleaching events due to the colder ambient
temperature in the mesophotic depths and to reseed shallow corals
afterward (e.g., Lesser et al., 2009; Bongaerts et al., 2010; Slattery
et al., 2011). Similarly, MCEs are expected to be less susceptible toanthropogenic impacts and higher temperatures (Glynn, 1996;
Hughes and Tanner, 2000; Lesser et al., 2009).
The Ryukyu Islands in the East China Sea (Figure 1) are located ata relatively high latitude compared with other coral habitats, hosting
abundant coral reefs because of the inﬂuence of the warm Kuroshio
Current (Ikeda et al., 2006). The archipelago was also affected bybleaching events in 2016. Kayanne et al. (2017) reported that ~90% ofcoral reefs at Ishigaki Island and 50–80% of coral reefs in Sekisei

1 Introduction
Coral reefs are widely distributed along tropical and subtropicalcoasts and are composed of over 90,000 species that maintain a highbiodiversity, resulting in coral reefs being recognized as one of themost important marine ecosystems on Earth. However, in recent
years, overﬁshing, eutrophication, erosion, and climate change have
led to the degradation of coral ecosystems globally (e.g., HoeghGuldberg et al., 2007; Carpenter et al., 2008; Hoegh-Guldberg et al.,2017; Hughes et al., 2018). High water temperatures occasionallylead to coral bleaching, which occurs extensively worldwide; forinstance, in the Indian Ocean, Paciﬁc Ocean, Red Sea, Caribbean
Sea, and Great Barrier Reef (e.g., Lafratta et al., 2016; DeCarlo et al.,2017; Hughes et al., 2017).
Most coral research has focused on shallow corals, which areseverely vulnerable to near-surface high temperatures, partly
because they are more accessible and much less costly to observe
than deep corals (e.g., Menza et al., 2008). Nevertheless, coral
habitats have been conﬁrmed to extend to deeper zones (Lesser
et al., 2009; Hinderstein et al., 2010; Kahng et al., 2010), where thelight intensity is only a fraction of that at the surface but is sufﬁcientfor zooxanthellae to live in symbiosis with corals for photosynthesis.

A

B

C

D

FIGURE 1(A) The study area encompassing the entire Ryukyu Islands with the perimeter of the ROMS-L1, -L2, and -L3 models (black boxes), (B) and the ROMS-L4
model domain (red box) in the L3 domain (black box). Blue circles indicate the three tide gauge stations at Naha, Okinawa, and Nakagusuku discussed in
section 2.4. (C) An enlarged plan view of the area around Okinawa Island with the source sites for particle tracking experiment Case 1 (shallow release from adepth of 2 m). The circles indicate 57 source and destination patches with a diameter of 500 m, which are further grouped into areas s1–s6. The pink squares
indicate the virtual tide gauge stations for comparisons between the L3 and L4 tides in section 2.4. (D) Same as (C), but for Case 2 (mesophotic release froma depth of ~30 m). The circles indicate 54 source and destination patches to be grouped into areas m1–m5. The black solid line is the isobath at a 30 m
depth. The red rectangles correspond to the L4 domain in (B–D). Colors show bathymetry in m.

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horizontal connectivity (Holstein et al., 2016; Garavelli et al., 2018),
and more importantly, studies on 3-D coral larval transport released
from different depths are scarce and nil for Okinawa.
Connectivity has been evaluated based on population genetics, inwhich genetic similarities among individual corals sampled at different
locations are diagnosed. On the other hand, a numerical ocean
circulation model and Lagrangian particle-tracking model enable thequantiﬁcation of connectivity with detailed spatiotemporal network
structures. Uchiyama et al. (2018c) investigated the large-scaleconnectivity of coral larvae in reef areas across the Ryukyu Islands
by focusing primarily on horizontal transport. Although the Kuroshio
Current is expected to play a signiﬁcant role in long-distance larvaltransport, where ~10% of the released larvae are transported
extensively across the Ryukyu Islands, they showed that shortdistance connectivity is quantitatively predominant for regional coralconnectivity. However, they focused only on depth-integrated
horizontal larval transport, thus, 3-D connectivity among multiple
depths, including the MPZ, was not considered.
Based on the above arguments, this study aims to 1) investigate
the 3-D, local, and short-distance transport of coral larvae released
from different depths across coral reef areas on the northwest coastof Okinawa Island, including Seseko Island, where abundant
mesophotic corals have been conﬁrmed (Sinniger et al., 2017;
Sinniger and Harii, 2018); 2) evaluate the vertical connectivity
between shallow nearshore areas and mesophotic intermediate
depth zones to demonstrate how signiﬁcantly mesophotic corals
are sustained by neighboring shallow corals, and vice versa; and 3)
examine the mechanisms behind the formation of connectivity due
to regional 3-D advective transport and vertical mixing effects. To
this end, we conducted a quadruple nested high-resolution synoptic
ocean modeling based on a highly sophisticated, state-of-the-art
downscaling system (e.g., Kamidaira et al., 2017; Uchiyama et al.,2018c) coupled with a 3-D Lagrangian particle tracking model. An
experiment was carried out for approximately 2 months, including
the coral spawning period in the region, to quantify the shortdistance and vertical transport of coral larvae in nearshore reef areasat a lateral spatial grid resolution of 50 m.

Lagoon (Figure 1A) were damaged by this bleaching. The corals
around Sesoko Island, located off the west coast of the Motobu
Peninsula at Okinawa Island (Figures 1C, D), were critically affectedby bleaching events in 1998 and 2001, resulting in the disappearanceof bleaching-sensitive species, such as Seriatopora hystrix, fromshallow water areas (van Woesik et al., 2011). However, Sinniger
et al. (2013; 2017) found a brooding coral S. hystrix in the MPZ
around Sesoko Island and speculated that MCEs could function as abuffer against thermal stress, thus, serve as a refuge to preserve thegenotypic diversity of bleaching-sensitive corals. A vast area acrossthe Ryukyu Islands is covered by bottom topographies suitable for thedevelopment of MCEs, such as deep terraces, banks, and pinnacles,
potentially providing larger habitats than those for shallow corals.
Indeed, multiple MCEs have been found in the Ryukyu Islands(Kimura et al., 2011; Fujita et al., 2012; Ohara et al., 2013; Sinniger
et al., 2017), including those around Sesoko Island. Extensive surveys
of deep corals could provide information regarding mesophotic
corals around the Ryuku Islands, such as their distribution area,
species, and connectivity (Sinniger and Harii, 2018).
A healthy and continuous supply of eggs and larvae is essential
for coral persistence. It is necessary not only to maintain deterioratingcoral habitats but also to preserve their spawning origins, as sufﬁcientamounts of larvae must be recruited to sustain abundant coralecosystems. Therefore, priority should be given to coral areas with
ample and stable larval supplies. Population connectivity (or‘connectivity’ for brevity) represents the statistical linkage of corals
inhabiting different locations, evaluated based on the probability of
their displacement due to Lagrangian advection by ambient oceanic
currents (e.g., Mitarai et al., 2009). Thus, the connectivity of corallarval populations among different habitats is viewed as a key element
determining the areas to be conserved (Munday et al., 2009). In
particular, for mesophotic corals, vertical connectivity with shallow
corals is an important factor that determines the health and fragilityof MCEs. For instance, genetic analyses of in situ corals have veriﬁed
vertical connectivity between shallow and mesophotic corals in
Bermuda (Bongaerts et al., 2010), western and eastern Australia(Van Oppen et al., 2011), and the Red Sea (Kramer et al., 2019).
Bongaerts et al. (2010) found that the reseeding potential of deep reefs
varied among species and habitats and concluded that deep refugia
should not be regarded as a broader ecosystem-wide phenomenon.
Coral larvae are generally passively transported to thesurrounding currents in the ocean for days or even weeks after
spawning because of their subtle swimming ability. Although thedrifting larvae may be preyed on during this period, the survivors
may sink to the ocean ﬂoor and attach themselves to hard surfaces,such as rocks and other hard corals, by chance. Hence, speciﬁcationof the origin of the coral spawn as well as their habitat is essential topreserve coral ecosystems. Although numerical ocean models havebeen used to identify connectivity to complement genetic analyses,
Thomas et al. (2015) ﬁrst simulated larval dispersal and settlement at
different depths, followed by Holstein et al. (2016) who used abiophysical model of larval dispersal to analyze the verticalconnectivity of broadcasting and brooding species in the U.S.
Virgin Islands and suggested the signiﬁcance of mesophotic
subsidies for shallow recruitment. However, there has been
considerably less research on vertical connectivity than on

Frontiers in Marine Science

2 Methods
2.1 Downscaling 3-D ocean
circulation model
Regional Oceanic Modeling System (ROMS; Shchepetkin and
McWilliams, 2005; Shchepetkin and McWilliams, 2008) was used todevelop a very high-resolution synoptic ocean model, viz., the
ROMS-L4 model, at a lateral grid resolution of 50 m for thenorthwest coastal area of Okinawa Island (Figure 1). This
resolution is required to represent detailed 3-D currents on thecomplex nearshore topography and bathymetry around the reefareas that are anticipated to inﬂuence short-distance and verticallarval transport. The outermost 3-D pelagic oceanic dynamics were
provided by the assimilative Japan Coastal Ocean Experiment(JCOPE2) reanalysis product (Miyazawa et al., 2009). The oneway off-line nesting approach described in Mason et al. (2010) and03

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resultant intrinsic baroclinic tides, which successively propagate
into the child L3 and L4 models through the open boundaries. A
short-term reanalysis was conducted for the 3-month period
beginning on April 20, 2013 to properly include the timing of thesynchronized mass spawning of coral in Okinawa, which typicallyoccurs from late May to early June, excluding a model spin-up timeof approximately 1 month prior to the main computation. Other
computational conditions of the ROMS model suite for the Ryukyu
Islands, including the present ROMS-L4 model, are summarizedin Table 1.

Uchiyama et al. (2018a) was applied to accomplish seamless multidomain nesting with the combined Orlanski-type radiation
condition and inﬂux nudging condition towards the parent model
output. This JCOPE2-ROMS downscaling system (Uchiyama et al.,2017b; Uchiyama et al., 2018a) has been used for several different
Asian marginal seas with extensive validations against satellite andin situ observations (e.g., Kamidaira et al., 2018; Masunaga et al.,2018; Tada et al., 2018; Kamidaira et al., 2019; Kurosawa et al., 2020;
Kamidaira et al., 2021; Zhang et al., 2022) and has been successfully
extended to quadruple nested conﬁgurations with further
downscaling (e.g., Uchiyama et al., 2018d; Zhang et al., 2019;
Uchiyama et al., 2022).
The present ROMS-L4 model is embedded in the JCOPE2ROMS model developed for the East China Sea, including the
Ryukyu Islands, in double (Kamidaira et al., 2017; Uchiyama et al.,2018c; Takeda et al., 2021) and triple (Uchiyama et al., 2018b)
nested conﬁgurations. The ROMS-L4 model was designed toencompass the northeast coast of Okinawa Island by 1386 × 800
horizontal grid cells and 32 vertically stretched terrain- and surfacefollowing s-layers, covering an area of approximately 69.3 × 40 km.
The model topography was obtained from the Shuttle Radar
Topography Mission at 30-arc-sec resolution (SRTM30_Plus;
Rodrı́guez et al., 2005; Becker et al., 2009), which covers theglobal ocean at 30 geographic arc-sec, supplemented by the Japan
Oceanographic Data Center (JODC)-Expert Grid data for
Geography at a 500 m resolution (http://www.jodc.go.jp/jodcweb/
JDOSS/infoJEGG.html) for the coastal region. Surface wind stresses
were imposed using the grid-point value mesoscale model (GPVMSM), an operational atmospheric product of the Japan
Meteorological Agency (JMA), at a horizontal resolution of 0.05°
× 0.0625°. Net heat, freshwater, and radiation ﬂuxes at the ocean
surface were obtained from the Comprehensive Ocean-Atmosphere
Data Set (COADS) of the National Oceanic and Atmospheric
Administration (NOAA), a monthly climatology data with ﬂux
bias correction. Ten principal tidal constituents from the TPXO 7.0
global tidal reanalysis (Egbert et al., 1994; Egbert and Erofeeva,
2002) were additionally imposed on the sea-surface height along theperimeter of the ROMS-L2 model to include barotropic tides and2.2 Ofﬂine Lagrangian particle tracking
model for ROMS
The 3-D Lagrangian transport of coral larvae was thennumerically simulated using the precomputed 3-D ﬂow ﬁeld of
the ROMS-L4 model output provided at 2 h intervals. An ofﬂine 3D Lagrangian particle tracking model for ROMS was exploited(Carr et al., 2008), which has frequently been used in numericalstudies on Lagrangian dispersal of virtual ﬂuid parcels (e.g., Romero
et al., 2013; Romero et al., 2016; Masunaga et al., 2022), larvae andeggs of marine fauna (Mitarai et al., 2009; Uchiyama et al., 2018b;
Uchiyama et al., 2018c; Takeda et al., 2021), and even microplastic
particles (Matsushita et al., 2022) with ample validations against in
situ datasets of Lagrangian ﬂoats and drifters. Corals have various
biological characteristics, such as larval behavior, larval precompetency period, and larval reproduction duration, dependingon their species, habitat, and other conditions (Shlesinger and Loya,
1985; Baird et al., 2009). However, little is currently known about
corals in the study area, particularly mesophotic corals.
Consequently, following on from previous researches of the study
area (e.g., Uchiyama et al., 2018b; Uchiyama et al., 2018c), speciﬁcbehavior models, such as diel vertical migration, mortality, or
random walk subgrid-scale diffusivity, were not introduced to
avoid further complexity and uncertainty. The present analysis
purely pursued the advective effects of ambient ﬂow ﬁelds on 3-D
larval transport as simply as possible, as if coral larvae are passively

TABLE 1 Numerical conﬁgurations for the suite of the quadruple nested ROMS system.

Model

ROMS-L1

ROMS-L2

ROMS-L3

Computational period

1/1/2008 - 11/2/2015

12/27/2010 - 11/2/2015

10/11/2012 - 1/31/2014

4/20/2013 - 7/20/2013

Grids (x × y × z)

768 × 768 × 32 layers

1280 × 1120 ×32 layers

1088 × 1120 × 32 layers

1376 × 800 × 32 layers

Horizontal grid size

3.0 km

1.0 km

250 m

50 m

Baroclinic time step

240 s

40 s

15 s

1.5 s

Lateral B.Cs.

JCOPE2 (daily)

L1 (daily update)L2 (2-hourly update)

L3 (2-hourly update)

Surface wind stress

GPV-GSM (6-hourly)

GPV-MSM (hourly)

GPV-MSM (hourly)

GPV-MSM (hourly)

Sea surface ﬂuxes

COADS (monthly climatology)

SST and SSS
Tides
Topography

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ROMS-L4

JCOPE2 (10-day averaged)
–

TPXO7

L2 (2-hourly update)

SRTM30_PLUS

L3 (2-hourly update)

SRTM30_PLUS (~1 km) + J-EGG500 (0.5 km)

04

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transported by oceanic currents. This approach is viewed as a basis
for future research with detailed larval behaviors, such as verticalmigration and subgrid-scale uncertainties.
The study area is topographically characterized by the Motobu
Peninsula located in the middle of the model domain, which
separates two sheltered shallow seas on both sides: Nago Bay on
the left and Haneji Inland Sea on the right. For connectivity
evaluation, coral habitats in the study area were deﬁned as sourceand sink patches, as shown by the circle marks with a radius of
500 m in Figure 1. Approximately 500 virtual larvae were evenly
distributed in each circular patch and were released from a depth of
2 m to represent shallow corals (Case 1) and from a depth of ~30 m
to represent mesophotic corals (Case 2) by referring to the previous
study (e.g., Holstein et al., 2016). Overall, 57 source patches were
deployed in Case 1 (Figure 1C) and 54 in Case 2 (Figure 1D).
Considering the regional topographic features, the 57 and 54
patches were grouped into six (Case 1) and ﬁve areas (Case 2) to
identify the connectivity between the areas.
Releases of Lagrangian particles, viz., virtual coral spawning,occurred once a day at 00:00 for 1 month from May 20, 2013, whichis the typical spawning time of corals in the study area. Hence, thetotal number of released Lagrangian particles was approximately
800,000 in each case. In general, the planula larvae of the corals
survive for a few days to a few months before settlement. Nishikawa
et al. (2003) reported that only 10% of the larvae of typical coral
species in the study area can survive for 30 days after spawning.
Therefore, particle tracking was conducted for up to 30 days after
each release, until they were beached on a land grid, or until theyexited the study area.

fx (x; t, a) ≈Cij (t) = fx (x = xj ; t, a = xi )(pR2 ),1 N
d (X n (t, a) − x),N on=10Z

The parent models of the present multi-nested downscaling
JCOPE2-ROMS system for the Ryukyu Islands have beenthoroughly validated in previous studies to show the satisfactory
reproducibility of the synoptic oceanic state and mesoscalevariability (Kamidaira et al., 2017; Uchiyama et al., 2018c). The
child ROMS-L4 model inherits a quantitatively similar
reproducibility to that of its parent models. For instance, themodeled temperature was compared to observation to show highaccuracy with the root mean square error of 0.906 °C and the model
skill score of 0.935 (not shown). Here, the validation result of highfrequency tidal variability, which is a predominant driver ofnearshore larval dispersal, is brieﬂy presented. In situ tidal data at
three tide gauge stations in Naha, Okinawa, and Nakagusuku wereobtained from the JODC. Tidal harmonic analysis was thenconducted for the data from January 1 to December 31, 2013.
Figures 2A, B show scatterplots of the amplitudes and phase epochsof the four major principal tidal constituents (M2, S2, K1, and O1)computed from the observed data and the ROMS-L3 model output.
The tidal amplitude and phases are well represented by the ROMSL3 model, with correlation coefﬁcients of 0.952 for the amplitude
and 0.997 for the phase epoch. Subsequently, as no observed tidal
data were available within the ROMS-L4 domain, another harmonic
analysis was performed to compare the results of L3 and L4 models
for 1 month of June, 2013 and showed extremely high correlations:
0.992 for amplitude and 1.000 for phase (Figures 2C, D). While thevalidation was conducted indirectly due to a shortage of in situ data,
this result clearly shows that the ROMS-L4 model can reproduce
tidal variability with high accuracy.

(1)0

fx (x; t, a + r)dr,(2)

jr j≤R

where R is the radius of the release site a. The ﬁnal form of thediscrete Lagrangian PDF is obtained by applying an isotropic spatial
Gaussian ﬁlter, G:

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2.4 Model validation

where N is the total number of particles, d is the Dirac delta
function, Xn is the position of the n-th Lagrangian particle, a is theinitial position of the particle of interest, and x is the sample-spacevariable for X. Both a and x encompass laterally over a circular
patch with an arbitrary depth range in z. Discrete Lagrangian PDFs
are evaluated from the center location of the release sites (patches)averaged over each site. Hence:fx (x; t, a) ≈ pR1 2(3)

where xi and xj are the source and sink patch locations, respectively,
and normalization by pR2 converts the PDFs into probabilities. The
vertical coordinate z of xi is 2 m (30 m) for shallow (mesophotic)
releases from s1–s6 (m1–m5) for Case 1 (Case 2), as shown in
Figure 1C (Figure 1D). The depth range of xj was deﬁned arbitrarily.
For the depth-integrated Lagrangian PDFs and connectivity
evaluated in section 3, xj was deﬁned with − h < z ≤ h, where his the local depth and h is the free surface height. On the other hand,in section 4, xj is deﬁned with − 30 < z ≤ h (m) as the favorable
depth zone to shallow corals and with − 150 < z ≤ −30 (m) as thatto mesophotic corals. Accordingly, the vertical connectivity between
the shallow zones and MPZs was computed by adequately imposing
the depth range constraints in xi and xj. For further details onmathematical representations and their physical interpretations,refer to Mitarai et al. (2009).

To quantify the dispersal of Lagrangian particles released fromsource patches, Lagrangian probability density functions (PDFs) wereanalyzed following the methodology described by Mitarai et al. (2009).
A Lagrangian PDF represents the PDF of particle displacement for agiven elapsed time (i.e., advection time) t as follows
0

−∞

0

G(x − x)fx (x; t, a)dx :Coastal connectivity Cij is deﬁned as the probability of
Lagrangian ﬂuid particles being transported from source site i tosink site j over a time interval t:

2.3 Lagrangian probability density
functions and connectivity

fX (x; t, a) =

Z ∞

05

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A

B

C

D

FIGURE 2

Scatter diagrams of the four major principal tidal constituents (M2, S2, K1, and O1) derived from harmonic analysis of the surface elevations. Upper
panels show (A) the amplitude and (B) phase epoch from the ROMS-L3 and in situ observation at three tide gauge stations around the Okinawa
Island shown by blue circles in Figure 1. Lower panels show (C) the amplitude and (D) phase epoch from the ROMS-L3 and ROMS-L4 models at thethree virtual tide gauge stations shown by pink squares in Figure 1. R in each plot indicates the correlation coefﬁcient.

extensive, and the released virtual larvae largely stay near the sourceareas for the ﬁrst 2 weeks. Particularly in highly sheltered areas,such as s2, m2 (Nago Bay), and s5 (Haneji Inland Sea), most larvae
remain near the source areas and self-recruitment is predominant.
Although they are dispersed gradually as the advection time
progresses, the larvae originating from the source areas s2, m2
and s5 are retained near the source area with a connectivity of over
10–3 even at Ta = 30 days.
A signiﬁcant difference between the two cases is found in thealong-isobath connectivity between the northeastern andsouthwestern areas of the Motobu Peninsula. The connectivity
near the lower right corners of the matrices (e.g., Cij with i = s4,
s5, and s6, and j = s1, s2, and s3) is generally small for shallow corallarvae (Case 1) at all three Ta, demonstrating that southwestward
larval transport beyond the Motobu Peninsula is rare. However, formesophotic coral larvae released from a depth of 30 m (Case 2), theconnectivity around the lower right corner of the matrices is higher
than that in Case 1, indicating that more larvae are transported
southwestward (i.e., from Haneji Inland Sea to Nago Bay) in the
MPZ. Therefore, this result suggests that horizontal larval
connectivity differs depending on the released depths, particularlyon the northern (Haneji) side of the Motobu Peninsula.

3 Horizontal larval transport
3.1 Horizontal connectivity matrices
Figure 3 shows area-integrated connectivity matrices Cij withthe x-axis showing the source areas and the y-axis showing thedestination areas on the labeled advection time (Ta ) in days. The
upper panels show the Lagrangian particles representing shallow
coral larvae released from a depth of 2 m (Case 1), while the lower
panels show the particles representing mesophotic coral larvae
released from a depth of 30 m (Case 2). For brevity, hereinafter,
the former particles are referred to as ‘(virtual) shallow coral larvae’,
while the latter is referred to as ‘(virtual) mesophotic coral larvae’.
For example, the combination of the x-axis of s4 and y-axis of s3 at
Ta = 5 days in Figure 3A shows yellowish green, viz., Cs4s3 ≅ 10−3 ,which can be interpreted as one coral larva out of 1,000 released
from the s4 area (northeastern shore of the Motobu Peninsula;
Figure 1) can be transported to the s3 area (the western shore ofMotobu Peninsula) in 5 days.
Both Case 1 and 2 initially exhibit higher connectivity aroundthe line with the 45° slope depicted by reddish colors until theadvection time of 14 days, showing that lateral dispersal is not that

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A

B

C

D

E

F

FIGURE 3

Horizontal connectivity matrices around the northwest coast of Okinawa Island for the advection times Ta of 5, 14, and 30 days. Colors indicate theprobability, viz., connectivity Cij . The x-axes show the grouped source areas, and the y-axes show the grouped sink areas shown in Figure 2. Upper
panels (A–C): shallow connectivity matrices for releases at a depth of 2 m (Case 1). Lower panels (D–F): mesophotic connectivity matrices forreleases from a depth of 30 m (Case 2).

transport in the deeper offshore areas, whereas the larvae from s6
are entrained in the shallower area in the Haneji Inland Sea aroundarea s5.
Figure 5 shows fractions of the virtual larvae transported fromthe northeastern side of the Motobu Peninsula (areas s4–s6 andm4–m5) to the other side (area A in Figure 6) as a function of theadvection time. The fractions of the reverse transport based on all
the released larvae (blue curves) from the shallow zones and the
MPZs increase in the ﬁrst few days, and then gradually decrease.
However, the difference is found to be insigniﬁcant by ~1%, or by~3,750 Lagrangian particles, because the majority of the larvae thatoriginate from the northeastern areas are transported
northeastward out of the study area through the eastern open
boundary. In contrast, the fractions based on the particles
remaining in the study area (red curves, Fremain) are found to besigniﬁcantly different between the shallow and mesophotic release
cases. At the advection time of 30 days, only ~12% of the larvae
released from the shallow areas (red dotted curve) reaches area A(see Figure 6) on the other side of the peninsula, whereas more
southwestward reverse transport beyond the peninsula is found forthe larvae released from the mesophotic areas of ~33% (red solid
curve). These results well-quantify the visual patterns of the
Lagrangian PDFs shown in Figure 5.

3.2 Depth-integrated Lagrangian PDFs
Figure 4 shows the temporal evolution of the depth-integrated(viz., x is deﬁned over the entire depth range − h < z ≤ h. See
section 2.3) Lagrangian PDF distribution of virtual larvae released
from areas s2 and s6 (at a 2 m depth) and area m5 (at a 30 m depth)
at advection times of 5, 14, and 30 days, illustrating depthindependent lateral transport patterns of shallow coral larvae (sixpanels in the upper two rows) and mesophotic coral larvae (bottom
panels). The higher the Lagrangian PDF, the more particles aretransported to that location. The vast majority of shallow corallarvae released from the semi-enclosed Nago Bay (area s2) remains
around the source area at Ta = 5 days (Figure 4, top panels),suggesting that short-term self-recruitment plays an important rolein the formation of recognizable local connectivity in such shelteredareas. Consistent with the temporal evolution of the connectivity
shown in Figures 3A–C, the larvae from s2 are transported anddispersed to surrounding areas gradually over the advection time inboth the northeastward and southwestward directions with
substantial retention to the source areas.
The middle and bottom panels of Figure 4 compare theLagrangian PDFs of the virtual larvae released from source areass6 (shallow corals) and m5 (mesophotic corals) located off thenortheastern coast of the Motobu Peninsula. Prevailingnortheastward transport and a subsequent exit from the L4
domain are evident regardless of the release depth, although there
is modest reversal of larval transport beyond the peninsula. This
reversed southwestward transport to the other side of the peninsula
is more apparent for the larvae from m5 (mesophotic corals) thanfor those from s6 (shallow corals) because of the along-isobath

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3.3 Horizontal current ﬁeld
In the preceding two subsections, the release depth wasdemonstrated to alter horizontal larval transport. To examine themechanism behind the difference in the horizontal transport

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FIGURE 4

Temporal evolution of depth-integrated horizontal Lagrangian PDFs (color) released from (top) areas s2, (middle) s6, and (bottom) m5 at the labeled
advection time Ta (days). Black circles indicate the source patches of each release area. The black solid contours are the isobaths of 30 and 100 m
depths. Arrows point to the true north as the panels are rotated relative to the geographical coordinates.

transport opposite to the mean current direction is induced byresidual and dispersive effects associated with tidal currents andother high-frequency factors. On the southwestern side of thepeninsula (Nago Bay), the surface currents are characterized bynearshore anticyclonic, clockwise circulation that extends to thenorthward ﬂow around the peninsular tip and is part of thenortheastward ﬂow on the other side (Haneji Inlans Sea).
Stagnated water is formed in Nago Bay, where shoreward
retention is promoted for the shallow larvae released from area s2
with overall northeastward transport to the other side of thepeninsula (Figure 4, top panels).
Meanwhile, the mesophotic current distribution at a depth of
40 m (Figure 6B) resembles the near-surface current distribution,although it is much weaker. The most striking difference is thebathymetric constraint at the peninsular tip, which blocks themesophotic currents from passing through. In turn, westward
currents are formed from the peninsular tip towards Ie Island(the island just off the peninsular tip), resulting in westward
elongated PDFs of the mesophotic larvae from m5 until Ta = 14days, followed by modestly higher PDFs in area A at Ta = 30 days
(Figure 4, bottom panels) than those of the shallow larvae from s6.
In addition, the mesophotic larvae from m5 are transported
shoreward to reach shallow areas of the Hanaji Inland Sea, where
the depth is shallower than 40 m, as depicted by the nil velocity
colored in white in Figure 6B. In addition to the bathymetricconstraint, the surface mixed layer plays an inevitable role indynamically decoupling shallow and mesophotic currents. The
surface mixed-layer depth H bls evaluated using the KPP
turbulence model in ROMS (Figure 6C) ranges 15–25 m inoffshore areas, which separated the near-surface currents andpatterns of the larvae released from the two depth zones, themonthly averaged ﬂow ﬁelds near the surface at a 5 m depth andaround the mesophotic layer at a 40 m depth are depicted in
Figures 6A, B. The near-surface currents (Figure 6A) indicate that apronounced northeastward velocity exceeding 0.2 m/s develops on
the northeastern side of the Motobu Peninsula, consistent with thedominant transport direction of the shallow coral larvae released
from area s6 (Figure 4, middle panels). It should be noted that larval

FIGURE 5

Fractions (%) of the virtual larvae transported from the northeasternside of the Motobu Peninsula (areas s4–s6 and m4–m5) to the otherside (area A in Figure 6C) as a function of the advection time. Fall (bluecurves): fractions of all the released larvae. Fremain (red curves):
fractions of the larvae that remain in the study area (viz., those thathave not exited). The dotted curves pertain to Case 1 (shallow release)and the solid curves pertain to Case 2 (mesophotic release).

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10.3389/fmars.2023.1174940

B

C

FIGURE 6

Time-averaged ﬂow ﬁelds based on the ROMS-L4 model output for the 1-month period of June, 2013. The horizontal velocity vectors (A) at a 5 m
depth (near-surface) and (B) at a 40 m depth (mesophotic zone), overlaid on their absolute values (m/s) indicated by color, are depicted. (C) The
surface mixed-layer depth Hbls (m) is indicated by color, with the two black rectangles showing areas A and B used for the analyses in sections 3.2
and 4.2. The black solid contours indicate the isobaths of 30 and 100 m depths. Arrows point to the true north.

areas m1–m5, but only within the mesophotic depth range of –150<
z ≤ –30 (m).
Table 2 clearly illustrates that vertical connectivity (3) and (4) issigniﬁcant, whereas horizontal connectivity (1) and (2) is 2–3 times
as large. All the 3-D connectivity values decrease with time, but at
Ta = 14 days, they are still 1/3–2/3 of those at Ta = 5 days. Then,these values further decrease to almost zero at Ta = 30 days, as thelarvae are mostly ﬂushed out of the study area, while the verticalconnectivity values (3) remain as large as those of horizontal
connectivity. More interestingly, the vertical connectivity from themesophotic to the shallow zone (4) is higher than that from theshallow to MPZ (3) until Ta = 14 days, and is quantitatively
comparable to the horizontal connectivity within the MPZ (2).
Therefore, the MPZ is deemed to be an important source for both
mesophotic and shallow coral ecosystems. Similarly, the shallow
zone could also be a source for both depth zones but to alesser degree.

associated shallow coral larval transport from those in themesophotic layer. In contrast, when Hbls< 10 m or Hbls ≈ h inshallow nearshore areas, vertical eddy mixing considerably
promotes vertical larval exchange.

4 Three-dimensional larval transport
4.1 Three-dimensional connectivity
between shallow zones and MPZs
In this study, the horizontal transport of virtual larvae released
from shallow source sites (s1–s6) and mesophotic source sites (m1–m5) were examined using depth-independent Lagrangian PDFs andassociated connectivity. To further understand the connection
between the two depth zones, the 3-D connectivity is evaluated atadvection times of 5, 14, and 30 days, as summarized in Table 2.
Here, the source/destination areas are s1–s6 for the shallow larvaeand m1–m5 for the mesophotic larvae, whereas the destination
areas are further restricted to the two depth zones. As explained in
section 2.3, the depth range of the destination patch xj was taken as–30 (m) < z ≤ h for the shallow coral settlement at s1–s6, and as –150< z ≤ –30 (m) for the mesophotic coral settlement at m1–m5(Figure 7). The 3-D connectivity is the area-integrated value for agiven depth range in xj. For instance, (3) shallow-mesophotic
connectivity is computed from the larvae released from the sourceareas s1–s6 (with a release depth of 2 m) that reach the destination

4.2 Vertical distribution of Lagrangian PDFs
To investigate a possible mechanism that promotes verticalconnectivity between the shallow zones and MPZs, temporal
evolutions of the vertical distribution of Lagrangian PDFs of thevirtual larvae integrated over areas A and B (see Figure 6C) aredepicted with the surface mixed-layer depth Hbls (solid line:
spatiotemporal average and dotted lines: standard deviations ± s)

TABLE 2 Three-dimensional connectivity between two depth zones at the advection times Ta of 5, 14, and 30 days.

Advection time, Ta
Source-destination types

5 days-2

14 days

30 days-2

1.24 × 10-3

(1)

Shallow-shallow

3.96 × 10

1.23 × 10(2)

Mesophotic-mesophotic

2.18 × 10-2

7.78 × 10-3

1.29 × 10-3

(3)

Shallow-mesophotic

6.13 × 10-3

4.41 × 10-3

9.83 × 10-4

(4)Mesophotic-shallow

1.84 × 10-2

6.21 × 10-3

4.39 × 10-6

(1) Source: shallow zone and destination: mesophotic zone, (2) source: mesophotic and destination: mesophotic, (3) source: shallow and destination: mesophotic, and (4) source: mesophotic anddestination: shallow. (1) and (2) represent horizontal connectivity, while (3) and (4) represent vertical connectivity.

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area B that lead to a shallower Hbls (Figure 6C), which impedes
downward larval transport.
However, for the mesophotic coral larvae released from a depthof 30 m (Case 2, Figures 8B, D), the Lagrangian PDF peaks at roughly
the same release depth. They are vertically dispersed to be extended
down to an ~80 m depth with PDFs of ~5.0 × 10–4, meaning that only
one larva out of 2,000 reaches this depth. Initial dilution takes place inapproximately 1 day when a small fraction of mesophotic larvae isentrained in the mixed layer and moves upward to the surface.
Because of the restricted downward transport of near-surface larvae
across Hbls, the surfaced mesophotic larvae dominate over the
subsurface larvae as the advection time progresses. This is moreevident in area B (Figure 8D), where shallow sheltered areas in the
Hanaji Inland Sea intensify near-surface retention (Figure 4).
Mesophotic coral spawning was set to occur at a depth of 30 mfrom May to June to suit the timing of mass spawning in the study
area, corresponding to the boreal spring when the surface mixedlayer develops to approximately 15–25 m from the surface. Thus,
the release depth of mesophotic coral larvae coincides with thevertical range of the seasonally varying surface mixed-layer depth in
the area. Therefore, the mixed layer plays two important roles in: 1)
acting as a barrier that prevents shallow (mesophotic) coral larvae
from being transported downward (upward), and 2) enhancing
near-surface vertical mixing to accumulate larvae near the surface.
If spawning occurs in the middle of summer, when Hbls is muchshallower, role 1) as a barrier prevails to diminish vertical larval
exchange between the shallow zones and MPZs.

FIGURE 7

Schematic diagram of four types of the horizontal and verticalconnectivity between the shallow corals and the mesophotic corals.
Blue and orange circles are the source patches used for Case 1(Figure 1C) and Case 2 (Figure 1D), respectively. In this study, theshallow zone is deﬁned from the surface down to 30 m depth, while
the mesophotic zone is from 30 m to 150 m depths. Mesophotic isabbreviated to “Meso” here. See also Table 2.

in Figure 8. Strikingly, the mixed layer constrains the vertical extent of
the virtual larvae. For the larvae released from a 2 m depth (Case 1,
Figures 8A, C), most of the larvae stay above the base of the mixed
layer at approximately –18< z ≤ –23 (m), which reduces the numberof near-surface larvae that sink. As a result, in both areas, theLagrangian PDFs near the surface are ~10-2, while they are lowered
to ~10–3 at ~40 m, which is one order of magnitude smaller. Nearsurface retention is more apparent with less downward dispersion inarea B than in area A because of extensive shallow nearshore areas in

A

B

C

D

5 Discussion
In the present study, the competency period was simply
considered for determining the analysis period, but other details

FIGURE 8

Hovmöller plots of the vertical distribution of the Lagrangian PDFs integrated over (A, B) area A and (C, D) area B (see Figure 6C for the deﬁnition) as
a function of the advection time until Ta = 14 days (colors). Left panels (A, C): Case 1 with shallow releases from a depth of 2 m. Right panels(B, D): Case 2 with mesophotic releases from a depth of 30 m. The solid black lines indicate the mean surface mixed-layer depth Hbls averaged
temporally for 1 month of June 2013 and spatially over each area A and B (see Figure 6C), and the dotted black lines indicate the ranges of theirstandard deviations, ± s .

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accurately. This will be pursued in the future with our ROMS
model, which has already been equipped with sophisticatedfunctionality to include wave effects to simulate nearshore
circulation (Uchiyama et al., 2010), thus, enabling more realistic
larval transport modeling across the inner and outer areas ofmultiple coral reefs.

of coral life history, such as vertical migration, mortality, anddensity, were not considered because of the high degree of
uncertainty involved. However, the density of coral larvae usuallychanges during their swimming period (Arai et al., 1993; Szmant
and Meadows, 2006; Vermeij et al., 2006), and a certain number oflarvae die while ﬂoating in the ocean without reaching the bottom(Graham et al., 2009). Biophysical particle tracking computationalmodeling studies have shown that incorporating a biological model
does not change relative connectivity patterns, but that diel verticalmigration and mortality signiﬁcantly affect absolute connectivity(Garavelli et al., 2018). In addition, we presumed mesophotic corals
are spawned at a depth of 30 m based on the preceding study by
Holstein et al. (2016), and vertical random-walk diffusivity is notconsidered for sake of simplicity, whereas these two factors may
affect vertical distribution to some extent. Although there remain
many unanswered questions regarding the effects on the vertical
distribution of coral larvae compared to those on the horizontal
distribution, it is possible that adopting the spontaneous verticalmigration pattern of larvae in the model could increase the numberof particles reaching the surface after spawning at depth and further
enhance connectivity between the shallow zones and MPZs.
Therefore, studies on the biology and life history of corals
inhabiting the study area are expected to enable more detailed
and realistic modeling studies, which could be accomplished by
improving the present particle tracking model to an individualbased biological model (e.g., Fujimura et al., 2014; Thomas
et al., 2015).
As a relatively high-resolution model was employed with ahorizontal grid resolution of 50 m here, our focus is on the threedimensional transport process among offshore areas rather than on
detailed behavior within the reef. Nevertheless, it is believed that
understanding inner reef circulation is also important for
estimating local coral recruitment. Indeed, it has been conﬁrmedthat nearshore circulation in many coral reefs, such as in the Indian
Ocean, Paciﬁc Ocean, and Caribbean Sea (Munk and Sargent, 1948;
Symonds et al., 1995; Hearn, 1999; Hench et al., 2008; Lowe et al.,2009), is mainly affected by breaking waves. Other wave effects, suchas Stokes drift, wave setup, wave-driven nearshore currents,
breaker-enhanced turbulent mixing, and wave-induced bottom
streaming (e.g., Uchiyama et al., 2009; Uchiyama et al., 2010;
Weir et al., 2011; Marchesiello et al., 2015; Uchiyama et al.,2017a; Akan et al., 2020; Wang et al., 2020; Wang et al., 2021),
are also anticipated to signiﬁcantly inﬂuence Lagrangian transport
in coastal areas. The linear addition of Stokes drift to the Lagrangian
equation of motion of the particle tracking models has beenreported to improve reproducibility in the open ocean to a certain
extent (e.g., Iwasaki et al., 2017; Matsushita et al., 2022). Nearshore
currents, in particular transient rip currents (e.g., Fujimura et al.,2017; Uchiyama et al., 2017a; Fujimura et al., 2018), which occur
intermittently and promote cross-shore exchange and dispersal
extensively, must be considered to represent inter-reef larvaltransport. However, the inclusion of wave effects is beyond thescope of the present study, partly because the present grid resolutionof 50 m is insufﬁcient to properly represent the surf zone, andfurther nesting should be conducted to develop a much higherresolution model that accounts for the surf zone dynamics

Frontiers in Marine Science

6 Conclusions
The 3-D inter-reef connectivity of coral larvae was numericallyinvestigated for the northwestern coastal area of Okinawa Island,
located in the East China Sea, using an ofﬂine Lagrangian particle
tracking model driven by a quadruple nested high-resolution
JCOPE2-ROMS downscaling model (e.g., Uchiyama et al., 2018c).
Coral larvae were modeled to inhabit the shallow zone at a depth of
2 m and the MPZ at a depth of 30 m. It was found that shortdistance, local connectivity within the source areas was as high as~10–2 in the ﬁrst few days, which was 10 to 100 times higher thanthe connectivity in other areas. This pronounced initial selfrecruitment gradually decreased as the advection time T a
progressed, and the virtual larvae were transported to other areas
away from the source areas. For example, the self-recruitment
connectivity within the southwestern-most shallow area s1(Figure 1C), Cs1s1 , was evaluated to be ~10–2 at Ta = 5 days, while
it decreased to ~10–4 at Ta = 30 days (Figure 3). Meanwhile, thehigh-resolution model allowing the representation of detailed
topographic features indicated the sizable entrainment of larvaein sheltered areas, such as Nago Bay (areas s2 and m2 in Figures 1C,D) and Haneji Inland Sea (area s5 in Figure 1C), where connectivity
remained as high as 10–3 even at Ta = 30 days.
For the horizontal transport of the shallow coral larvae,
northeastward inter-reef transport beyond the Motobu Peninsula(e.g., from s1–s2 to s5–s6) was predominant with a connectivity of~1–4 × 10–4 (Figure 3C) at Ta = 30 days, whereas the opposite
transport (e.g., from s5–s6 to s1–s2) barely occurred withconnectivity of less than 10–5 or a fraction of ~12% (Figure 5).
This signiﬁcant directional bias was well-explained by vigorous
mean northeastward near-surface currents at 0.1–0.2 m/s developed
more energetically on the northeastern side of the peninsula(Figure 4A). In contrast, for the mesophotic coral larvae, theopposite transport (e.g., from m4–m5 to m1–m2) occurred moreevidently by ~3 × 10–4 (Figure 3D) or ~33% (Figure 5) at Ta = 30days than the shallow coral larvae. Even with the subsurface
topographic barrier near the peninsular tip in the MPZ, lessenergetic northeastward currents on the northeastern side andmoderate westward currents near the tip (Figure 4B) jointly
promoted the southwestward transport of the larvae released
from the MPZ. Therefore, lateral connectivity was establishedasymmetrically in the alongshore direction around the peninsula,although the bias was largely inﬂuenced by the seasonal surface
mixed-layer (Figure 4C) and associated depth-dependent
horizontal currents.
It was also found that the virtual larvae released in the shallow
zones and MPZs were interchangeable (Table 2). The vertical rangeof the mixed-layer depth Hbls for the boreal spring in the study area

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NOAA at https://psl.noaa.gov/data/gridded/data.coads.1deg.html.
The present ROMS-L4 model was built upon parent models
developed with earnest assistance from Yuki Kamidaira, Sachika
Odani, and Tsubasa Miyagawa. Further inquiries can be directed tothe corresponding author.

and the presumed broadcast spawning depth of the mesophotic
coral overlapped at a ~30 m depth. This coincided with theenhanced upward entrainment of mesophotic coral larvae toemerge near the surface where shallow corals coexist (viz.,predominance of 3-D connectivity (4) from the MPZ to theshallow zone in Table 2) under the inﬂuence of intensive verticalmixing in the surface mixed layer (Figure 8). The larvae released
from the MPZ also dispersed vertically down to the deeper zone
below the mixed layer, while upward transport occurred to induce
both shallow and mesophotic corals to remain in the surface zone.
Conversely, the mixed layer extending to the MPZ promoted theshallow corals to sink down, leading to modest vertical connectivity
from the shallow zone to the MPZ (viz., 3-D connectivity (3) inTable 2) to a much lesser degree than (4). In conclusion, the above
results suggest the signiﬁcance of 3-D connectivity between
mesophotic and shallow coral ecosystems. Hence, yet with several
technical limitations argued in Section 5, the present study
conﬁrmed that the mesophotic coral ecosystem could serve as a
refuge from environmental stresses for shallow corals in the study
area under advective effects of the ambient 3-D currents.

Author contributions
KT: Investigation, Software, Validation, Visualization, Writing– original draft. YU: Conceptualization, Methodology, Supervision,
Software, Writing- Reviewing and Editing, Funding acquisition.
SM: Methodology, Investigation. All authors contributed to thearticle and approved the submitted version.

Funding
This research was ﬁnancially supported by the Japan Society for
the Promotion of Science (JSPS) Grant-in-Aid for ScientiﬁcResearch (Grant # 18H03798) at Kobe University.

Data availability statement

Conﬂict of interest

The ROMS 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 andTech no logy (JAM STEC) and are available at h t t p : / /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/JDOSS/
infoJEGG.html. The GPV-GSM and GPV-MSM atmosphericproducts were generated by JMA and are available from therepository at http://database.rish.kyoto-u.ac.jp/arch/jmadata/data/
gpv/original/. The COADS data are maintained and distributed by

The authors declare that the research was conducted in theabsence of any commercial or ﬁnancial relationships that could beconstrued as a potential conﬂict of interest.

Publisher’s noteAll claims expressed in this article are solely those of the authorsand do not necessarily represent those of their afﬁliated organizations,or those of the publisher, the editors and the reviewers. Any productthat may be evaluated in this article, or claim that may be made by its
manufacturer, is not guaranteed or endorsed by the publisher.

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