Progress in Oceanography 219 (2023) 103155

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

Vertical changes in zooplankton abundance, biomass, and community
structure at seven stations down to 3000 m in neighboring waters of Japan
during the summer: Insights from ZooScan imaging analysis
Kunito Yamamae a, 1, Yasuhide Nakamura b, Kohei Matsuno a, c, Atsushi Yamaguchi a, c, *abcFaculty/Graduate School of Fisheries Sciences, Hokkaido University, 3-1-1 Minato-cho, Hakodate, Hokkaido 041-8611, Japan
Estuary Research Center, Shimane University, 1060, Nishikawatsu-cho, Matsue 690-8504, Japan
Arctic Research Center, Hokkaido University, Kita-21 Nishi-11 Kita-ku, Sapporo, Hokkaido 001-0021, JapanA R T I C L E I N F O

A B S T R A C T

Keywords:
Size spectrum
NBSS
Inter-oceanic comparison
ZooScanSize diversity

The imaging device ZooScan is used to examine net-collected zooplankton samples. ZooScan has been applied toregional and seasonal changes in the zooplankton community, but it has rarely been used to characterize verticalchanges, especially down to the deep sea. In this study, we report a ZooScan analysis of vertically stratified
zooplankton samples collected by collected by Vertical Multiple Plankton Sampler down to 3000 m at sevenstations near Japan in the Okhotsk Sea, Japan Sea, East China Sea, and subarctic, transitional, and subtropicalNorth Pacific. Throughout the region, both abundance and biomass, as indicated by aggregate zooplankton
volume decreased with increasing depths. ANCOVA analysis revealed that factors linked to vertical changes
varied with location. Depth and region were the primary determinants of abundance and biomass, respectively.
Cluster analysis based on abundance delineated 8 distinct zooplankton community groups. The occurrence ofeach group varied regionally and 3–5 groups were vertically stratified at each station. Across all stations,
Normalized Biomass Size Spectra (NBSS) and size diversity showed pronounced change around 150–500 m
depths. At shallower depths, the NBSS slope was steep, the intercept was high, and size diversity was low while,at deeper depths the opposite was true for each of those parameters. Generalized additive models showed that
depth, temperature, and salinity had a significant effect on NBSS and size diversity. This study indicates that the
ZooScan imaging approach may be useful in the analysis of deep-sea zooplankton communities.

1. Introduction
In aquatic ecosystems, zooplankton play a key role in mediating thetransfer of energy as organic materials from primary producers to higher
trophic levels (cf. Lalli and Parsons, 1997; Miller and Wheeler, 2012). In
addition, zooplankton egests fecal pellets and performs diel verticalmigration, which promote vertical material fluxes in a process termed
the “Biological pump” (Ducklow et al., 2001; Steinberg et al., 2008a).
Diet composition and feeding modes vary greatly across zooplankton
taxa (cf. Lalli and Parsons, 1997; Miller and Wheeler, 2012). In turn,zooplankton size shape the community of vertebrate predators thattarget particular taxa (Nunn et al., 2012). Finally, zooplankton sizes also
affect the fecal pellet sizes, which are directly related to the sinking ratesof the fecal pellets (Stamieszkin et al., 2015). Thus, zooplankton size andtaxa are the two most important factors in determining their quantita­
tive functional roles in marine ecosystems.
ZooScan is a device that allows simultaneous determination of size
and taxonomic affinity of zooplankton (Gorsky et al., 2010; Irisson et al.,2022). ZooScan measurements can be used to obtain indices ofzooplankton size spectra, and conduct analyses based on Normalized
Biomass Size Spectra (NBSS) (Schultes and Lopes, 2009; Kwong andPakhomov, 2021). Both the slope and intercept of NBSS are known tovary in response to bottom-up or top-down controls. Where high pri­mary productivity induces a high abundance of the small-sized
zooplankton (i.e., bottom-up conditions), the intercept and slope of
NBSS are high and steep, respectively. On the other hand, under highpredation pressure conditions on small zooplankton (i.e., top-down
conditions), the intercept and slope of NBSS change to low and flat,* Corresponding author at: Faculty/Graduate School of Fisheries Sciences, Hokkaido University, 3-1-1 Minato-cho, Hakodate, Hokkaido 041-8611, Japan.
E-mail address: a-yama@fish.hokudai.ac.jp (A. Yamaguchi).
1
Present address: Ishikawa Prefecture Fisheries Research Center, 1-1 Kuratsuki, Kanazawa, Ishikawa 920-858, Japan.
https://doi.org/10.1016/j.pocean.2023.103155
Received 26 May 2023; Received in revised form 26 June 2023; Accepted 18 October 2023
Available online 23 October 2023
0079-6611/© 2023 Elsevier Ltd. All rights reserved.

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Progress in Oceanography 219 (2023) 103155

respectively (Moore and Suthers, 2006; Suthers et al., 2006; Zhou, 2006;
Zhou et al., 2009). The application of ZooScan data in NBSS studies has
been limited to investigations on seasonal changes (Vandromme et al.,2012) and spatial changes in epipelagic depths (Naito et al., 2019;
Kwong and Pakhomov, 2021). To date, few studies have used ZooScan to
examine vertical changes in zooplankton size and community
composition.
Japan’s neighboring waters include subarctic, transitional, andsubtropical regions of the western North Pacific and three marginal seas:
Okhotsk Sea, Japan Sea, and East China Sea, all of them having different
oceanographic characteristics. Studies on zooplankton size compositionin the neighboring waters of Japan have focused on latitudinal differ­ences (Yokoi et al., 2008; Shiota et al., 2013; Mishima et al., 2019),

inter-oceanic comparisons including marginal seas (Sato et al., 2015),
and localized seasonal changes (Yamaguchi et al., 2014; Hikichi et al.,2018). These studies were based on measurements collected by Optical
Plankton Counter (OPC; Herman, 1988), which does not produce taxo­
nomic information. It also should be noted that they focused mainly on
epipelagic depths. No attempt was made to characterize vertical changes
in zooplankton size composition, especially down to the greater depths.
Studies of vertical changes in zooplankton community down to great
depths in the neighboring waters of Japan have focused on latitudinalchanges in zooplankton biomass in the subarctic, transitional, andsubtropical regions of western North Pacific (Yamaguchi et al., 2002b,
2004, 2005), species-specific distributions of copepods (Yamaguchi
et al., 2002a), and on chaetognath abundance and community

50 ˚N
Okhotsk Sea

hio

as
Oy

OK

SA
Japan Sea

40

ima
h
s
Tsu rent
cur

30

JS1

rm

wa

TR

ECS

Kur
osh
io

East
China
Sea

JS2

ST

20

Western North Pacific Ocean
10
120

130

140

150

160˚E

Fig. 1. Location of the seven sampling stations neighboring waters of Japan. OK: Okhotsk Sea, JS1: Japan Sea station 1, JS2: Japan Sea station 2, ECS: East China Sea,
SA: subarctic Pacific, TR: transitional Pacific, ST: subtropical Pacific. Approximate flow directions of the major currents are shown with the arrows in the panel.
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composition (Ozawa et al., 2007). While providing valuable insights,
these studies do not add to our understanding of vertical variation
among whole zooplankton communities the waters around Japan.
Here we report ZooScan analyses on vertically stratified zooplankton
samples down to a maximum of 3000 m from seven stations covering
subarctic, transitional, and subtropical regions of the western North
Pacific, and three marginal seas: Okhotsk Sea, Japan Sea, and the East
China Sea. Zooplankton abundance, biovolume, community structure,size composition, and NBSS were characterized, and their geographicaland vertical changing patterns were evaluated. For abundance andbiovolume, their vertical changing patterns were evaluated by analyzing
the regressions with depth and comparing their regressions with thosefrom the previous studies. Based on the abundance of each taxon,
zooplankton community structures were analyzed by cluster analyses,
and their spatial and vertical distributions were conducted. As indices ofzooplankton size compositions, intercept and slope of NBSS, and size
diversity were analyzed for each sample, and the effects of the envi­
ronmental parameters (depth, temperature, and salinity) on them wereanalyzed by the Generalized Additive Models (GAM).

(Hydrooptic Inc.) following the protocol of Gorsky et al. (2010). First, abackground scan of distilled water in the scanning cell was conducted.
Whole or subdivided zooplankton samples were placed on the ZooScan
scanning cell using a wide-bore pipet. The resulting images were used toisolate each individual using ZooProcess and ImageJ software. The im­ages were digitized at 2400 dpi resolution, which corresponded to 10.6
µm per pixel. Images were uploaded to the website EcoTaxa, and semiautomated identifications were made for each image (Picheral et al.,2017; Irisson et al., 2022).
Imaged individuals were assigned to one of the following categories:
protozoan; Phaeodaria, Foraminifera, Tintinnida, and metazoan; Cni­
daria, Hydrozoa, Scyphozoa, Siphonophorae, Annelida, Gymnosomata,
Ostracoda, Calanoida, Cyclopoida, Harpacticoida, Poecilostomatoida,
Mysidacea, Amphipoda, Euphausiacea, Calyptopis, Cladcera, Chaetog­
natha, Doliolida, Appendicularia, Ophiuroidea, Mollusca, Decapoda,
Crustacean nauplius, and others; fecal pellet, fragment, detritus. For thenumerical dominant Calanoida, more detailed identifications werepossible for the following genera: Acartia spp., Eucalanus bungii, Gaeta­
nus spp., Metridia spp., Neocalanus spp., Paraeuchaeta spp., Pseudocalanus
spp. Samples assigned to non-living fractions (i.e., fecal pellet, fragment,
and detritus) were not included in the following analyses.
From ZooScan images, the volume (Volume, mm3) of each specimen
was calculated from major axis length (Lmajor, mm) and minor axis
length (Lminor, mm) using the following equation:

2. Material and methods
2.1. Field sampling
Vertically stratified zooplankton sampling was conducted at sevenstations in the western North Pacific and marginal seas around Japan in
cruises of the T/S Oshoro-Maru from 11 June to 2 August 2011 and
10–15 June 2014. Station codes and sampling depths are as follows: St.
OK in the southern Okhotsk Sea (45˚24′N, 145˚02′E) from 0 to 3000 m, St.
JS1 (41˚45′N, 138˚30′E) and JS2 (41˚45′N, 139˚47′E) in the Japan Sea bothfrom 0 to 750 m, St. ECS (27˚18′N, 126˚48′E) in the East China Sea from0 to 1500 m, St. SA (43˚39′N, 154˚07′E) in the subarctic western North
Pacific from 0 to 3000 m, St. TR (36˚30′N, 155˚00′E) in the transitional
domain of the western North Pacific from 0 to 3000 m, and St. ST(20˚47′N, 135˚29′E) in the subtropical western North Pacific from 0 to1000 m. Samplings were conducted with a Vertical Multiple Plankton
Sampler (VMPS) equipped with 63 µm mesh with 0.25 m2 mouth
opening (Tsurumi Seiki Co. Ltd., Terazaki and Tomatsu, 1997) with
twelve maximum stratifications (Fig. 1, Table 1). Zooplankton samples
were preserved with 5 % borax-buffered formalin seawater on board
immediately after collection. Hydrographic data (temperature, salinity,and dissolved oxygen concentration [DO]) were obtained by CTD (SBE
911 Plus, Sea–Bird Electronics Inc.) casts at each station.

Volume = 4/3 × π × (Lmajor /2) × (Lminor /2)2
The equivalent spherical diameter (ESD, mm) of each specimen wasderived from calculated volume using the following equation:√̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅
3 Volume × 3
ESD =4π
Using sampled numbers (n), specimen volume (Volume, mm3), and net
filtered volume (F: m− 3), abundance (Abu: ind. m− 3), and biovolume(Bio: mm3 m− 3) estimates were obtained using the following equations:
Abu =

n
F×s

Bio =

VolumeF×s

where s is the splitting factor of the samples during the ZooScan
measurements.
2.3. Data analysis

2.2. ZooScan measurement

In this study, we examined zooplankton larger than 200 µm ESD,
which is significantly larger than the diagonal length (89 µm) of theZooplankton images from field samples were captured by ZooScan

Table 1
Sampling data on vertical stratified samplings by VMPS equipped 63 µm mesh at the seven stations located various regions of the neighboring waters of Japan. Notethat the depth strata was varied with the region.
Area

Abbreviation

Position

Sampling
data

D/N

Depth strata (m)Okhotsk Sea

OK

45˚24́N, 145˚02́ E

Night

Japan Sea (Station 1)

JS1

41˚45́N, 138˚30́ E

Night

0–25, 25–50, 50–75, 75–100, 100–150, 150–250, 250–500, 500–750, 750–1000,
1000–1500, 1500–2000, 2000–3000
0–50, 50–150, 150–250, 250–550, 550–600, 600–750

Japan Sea (Station 2)

JS2

41˚45́N, 139˚47́ E

Night

0–50, 50–150, 150–250, 250–400, 400–600, 600–750

East China Sea

ECS

27˚18́N, 126˚48́ E

11 June2011
11 June2014
14 June2014
4 July 2011Day

NW Pacific: subarctic
regionNW Pacific: transitional
regionNW Pacific: subtropicalregionSA

43˚39́N, 154˚07́ E

31 July 2011

Night

TR

36˚30́N,155˚00́ E

27 July 2011

Day

ST

20˚47́N,135˚29́ E

11 July 2011Night

0–25, 25–50, 50–75, 75–100, 100–150, 150–250, 250–375, 375–500, 500–750,
750–1000, 1000–1250, 1250–1500
0–25, 25–50, 50–75, 75–100, 100–150, 150–250, 250–500, 500–750, 750–1000,
1000–1500, 1500–2000, 2000–3000
0–25, 25–50, 50–75, 75–100, 100–150, 150–250, 250–500, 500–750, 750–1000,
1000–1500, 1500–2000, 2000–3000
0–25, 25–50, 50–75, 75–100, 100–150, 150–250, 250–500, 500–750, 750–1000

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mesh size (63 µm) used for field sampling We used smaller mesh size infield collections to avoid the effects of collection efficiency of smaller
specimens due to the abundance of seston or detritus as reported in
Makabe et al. (2012).
We performed regression analysis with abundance (Abu: ind. m− 3) or
biovolume (Bio: mm3 m− 3) as dependent variables and depth (D: m) as
the independent variable to assess vertical changes in abundance andbiovolume,. For regressions, we used log–log transformed values foreach variable and perform the analyses using the relevant functions as
implemented in MS-Excel:

log10 Bio = a × log10 D + b
where a is the slope and b is the intercept of the regression. We con­ducted an analysis of covariance (ANCOVA) by applying target variables
such as abundance and biovolume and explanation variables such as
depth and location to assess the relationship between these factors andthe zooplankton assemblages.
We performed cluster analyses of zooplankton community for all 69
samples using Bray-Curtis similarities and mean-connecting methods
based on values transformed to the fourth root of the abundance esti­mates (Abu: ind. m− 3). Inter-group differences in zooplankton abun­dance were analyzed by one-way ANOVA and post hoc test (Tukey-

log10 Abu = a × log10 D + b

Fig. 2. Vertical changes in temperature, salinity and dissolved oxygen at the seven stations neighboring waters of Japan. OK: Okhotsk Sea, JS1: Japan Sea station 1,
JS2: Japan Sea station 2, ECS: East China Sea, SA: subarctic Pacific, TR: transitional Pacific, ST: subtropical Pacific. Symbols denote mean values for the sampling
depths of VMPS at each station.
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Kramer test). To explore the effects of environmental variables (latitude,
depth, temperature, salinity, and dissolved oxygen), we produced twodimensional non-metric multidimensional scaling (NMDS) ordination
based on the Bray-Curtis analysis.
To obtain normalized biomass size spectra (NBSS), we usedzooplankton biovolume estimates for zooplankton between 0.2 and 5.0
mm ESD binned in 0.05 mm intervals. Specifically, we used log10
zooplankton biovolume (mm3) in each size class for the X-axis and thelog10 zooplankton biovolume (mm3 m− 3) / Δbiovolume (mm3) for the Yaxis. Biovolume was divided by the biovolume interval (Δbiovolume[mm3]) and log-transformed. Then, the NBSS linear model was calcu­
lated as follows:
Y = aX + b
where a and b are the slope and intercept of the NBSS, respectively.
Zooplankton size diversity was examined applying measures of
species diversity (H’) (Morisita, 1996). For evaluation of the effects ofthe environmental variables (depth, temperature, and salinity) on theslope, the intercept of the NBSS, and size diversity, analyzed by thegeneralized additive model (GAM), were made for each target variable
using functions implemented in R.
3. Results
3.1. Hydrography
Fig. 3. T-S diagram at the seven stations neighboring waters of Japan. OK:
Okhotsk Sea, JS1: Japan Sea station 1, JS2: Japan Sea station 2, ECS: East China
Sea, SA: subarctic Pacific, TR: transitional Pacific, ST: subtropical Pacific.
Symbols denote mean values for the sampling depths of VMPS at each station.

Vertical changes in temperature, salinity, and DO at each station are
shown in Fig. 2. Across stations, temperatures ranged from –1.2 to
29.4˚C. Inter-oceanic differences in temperature were prominent in theupper 1500 m. The warmest conditions were found in the subtropical
Pacific and the East China Sea, while the coldest condition was observedin the Okhotsk Sea. Temperature below 0˚C was measured between 50
and 100 m depths in the Okhotsk Sea. Such “intermediate cold water”(Takizawa, 1982) was also seen in the subarctic Pacific. The otherdistinct water mass, the “Japan Sea proper water,” which is character­ized by extremely cold temperature (0–1˚C) (Sudo, 1986), was seen
below 300 m depths of the Japan Sea.
Salinity ranged between 32.6 and 34.9 across stations. Regionalchanges were notable above 1500 m depths and fell into three patterns:
subarctic, subtropical, and Japan Sea. For the subarctic (St. OK, SA),salinity was low at the near-surface layer and then increased withincreasing depth. For the subtropical (St. ECS, TR, ST), the high salinity
near the surface overlayed a subsurface minimum betwen 200 and700
m, then increased with increasing depths below that layer. For the Japan
Sea (St. JS1, JS2), salinity was within a narrow range (34.0–34.3) anduniform throughout the layers.
DO concentration ranged between 0.85 and 7.90 ml L–1 across sta­tions. Common for all stations, [DO] had a minimum at around 1000 m
depths. For shallower depths, especially above 200 m, [DO] was highest
in subarctic waters (St. OK, SA), lowest in subtropical ones (St. ECS, TR,ST), intermediate in the Japan Sea (St. JS1, JS2).
A T-S diagram plotting sampling stations shows extensive environ­mental variation (Fig. 3). In the subarctic (St. OK, SA), temperatures
were cold and similar throughout sampled depths while salinities
increased with increasing depths. While in the subtropical stations (St.
ECS, TR, ST) and the Japan Sea (JS1, JS2), salinities were high andsimilar throughout the layer, but temperatures decreased withincreasing depths.

30 % of the community across stations and depths. For the 0–250 m ofthe subarctic stations (St. OK, JS1, JS2, SA), Cyclopoida was also an
important community component. For the deeper layers below 250 m of
St. OK and SA and all depths of subtropical stations (St. ECS and ST),
Poecilostomatoida was also important and composed more than 30 % inabundance.
Zooplankton biovolume (mm3 m− 3) and their taxonomic composi­tion at each layer are shown in Fig. 5. For biovolume, high contributions
from Euphausiacea were seen at 50–150 m of St. JS1 and 150–250 m of
St. JS2. Overall, the most dominant taxon was Calanoida. The second
dominant taxa varied with station: Chaetognatha (St. OK, SA, and ST),
Doliolida at the deep layer of St. TR. Phaeodaria dominated the deep
layer of St. JS1 which was also true for their abundance at those depths.
Vertical changes in zooplankton abundance and biovolume, alongwith the increasing depths, are shown in Fig. 6. These vertical changes
were fitted to the power regressions, and their slopes and intercepts areshown in Table 2. For abundance, significant regressions were observed
for all seven stations, and their slopes were between − 0.531 and − 1.379(Table 2). For the regressions On bio volume, their fittings were lower
than those of the abundance considering r2 and p-values (Table 2). For
two stations in the Japan Sea (JS1 and JS2), regressions were not sig­
nificant likely due to sampling depths being limited between 0 and 750
m and low number of stratification (six layers) within the stations. A
notable observation of biovolume variation was a sharp decrease inmagnitude of approximately 90 % at 75–100 m depths in St. OK and SA(Fig. 6b). It also should be noted that the depths corresponded with thedepths observed in the intermediate cold water at these stations (Fig. 2).
Results of ANCOVA applying abundance and biovolume as target
variables and region and depth as dependent variables are shown in
Table 3. The effects of these two factors on abundance and on biovolume
varied. Specifically, depth was the only environmental factor to affectabundance. Since there was no effect of interactions of region × depth
on abundance, the regressions of the abundance of the seven stations
were not varied and treated as having the same slopes. On the other
hand, biovolume was affected by region, while the other factors (i.e.,

3.2. Abundance and biovolume
Zooplankton abundance (ind. m− 3) and taxonomic composition ateach sampling layer are shown in Fig. 4. At most stations, abundance
was highest near the surface layer and then decreased with increasing
depths. Calanoida was widely abundant and comprised approximately
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Fig. 4. Vertical changes in zooplankton abundance and their taxonomic composition at the seven stations neighboring waters of Japan. Note that abundance scales
are in log-scales. OK: Okhotsk Sea, JS1: Japan Sea station 1, JS2: Japan Sea station 2, ECS: East China Sea, SA: subarctic Pacific, TR: transitional Pacific, ST:
subtropical Pacific.

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Fig. 5. Vertical changes in zooplankton biovolume and their taxonomic composition at the seven stations neighboring waters of Japan. Note that biovolume scales
are in log-scales. OK: Okhotsk Sea, JS1: Japan Sea station 1, JS2: Japan Sea station 2, ECS: East China Sea, SA: subarctic Pacific, TR: transitional Pacific, ST:
subtropical Pacific.

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Fig. 6. Vertical changes in zooplankton abundance (a) and biovolume (b) at the seven stations neighboring waters of Japan. OK: Okhotsk Sea, JS1: Japan Sea station
1, JS2: Japan Sea station 2, ECS: East China Sea, SA: subarctic Pacific, TR: transitional Pacific, ST: subtropical Pacific.
Table 2
Regression statistics of abundance (Abu: ind. m− 3) and biovolume (Bio: mm3m− 3) along with depth (D: m) for the seven stations neighboring waters of Japan.
As regressions, power models were used: log10Abu = a log10D + b or log10Bio = alog10D + b, where a and b were fitted constants. For details of data, see Fig. 6. *:p < 0.05, **: p < 0.01, ***: p < 0.001, ns: not significant.
Unit
Abundance

Biovolume

Station

a

b

r2

OK
JS1
JS2
ECS
SA
TR
ST

− 0.774− 0.755− 0.531− 1.277− 1.107− 1.379− 1.108

8.996
9.204
8.157
11.11910.89812.3349.827

0.925***
0.909**
0.7839*0.863***
0.961***
0.923***
0.868***

OK
JS1
JS2
ECS
SA
TR
ST

− 0.586− 0.306− 0.249− 1.088− 0.602− 0.465− 0.621

7.940
6.238
5.927
8.589
8.624
6.196
6.056

0.466*
0.479 ns0.099 ns
0.764***
0.501**
0.533**
0.648**

Table 3Results of ANCOVA on zooplankton abundance and biovolume, with the sam­pling depth (m) and region (station) (cf. Table 1) applied as independent vari­ables. df: degree of freedom, SS: sum of squares.
Unit

Parameter

Abundance
Depth
RegionDepth × Region
Error
Biovolume
Depth
RegionDepth × Region
Error

df

SS

F-valuep-value1
6
6
55

1,939,593
2,839,226
667,003
22,035,058

4.841
1.181
0.277

0.032
0.32990.9452

1
6
6
55

174,728
3,773,762
899,340
11,438,501

0.84
3.024
0.721

0.36340.0126
0.6346for group IV, and Cnidaria for group V.
Zooplankton communities were plotted at different locations evenfor the NMDS plot, and various environmental parameters (temperature,salinity, DO, depth, and latitude) had significant interaction with theplotted area of each sample in the NMDS plot (Fig. 8). From directions ofeach environmental variable and plotted area of each zooplankton
community in the NMDS plot, following interactions were evidenced:
thus, group D was seen at the high latitude, group F was seen at hightemperature regions, group G was at the high DO region/depths, andgroup H was seen at the deep and high salinity region and depths.
Results of abundance differences between zooplankton groups
evaluated by one-way ANOVA and post hoc Tukey-Kramer test are
shown in Table 4. Overall, copepods (Calanoida, Cyclopoida, and Poe­cilostomatoida) were dominant among zooplankton species/taxa,
throughout all communities. Calanoid copepods Metridia spp. wereabundant in the zooplankton communities of groups A, B, G, and H(Table 4). Phaeodaria and Ostracoda were abundant in group D. For

depth and interactions of region × depth) had no effect on this measure(Table 3).
3.3. Zooplankton community
Based on abundance data, zooplankton taxa were classified into fivegroups (I–V) at a 28 % similarity level, and their communities wereclustered into eight groups (A–H) at a 68 % similarity level (Fig. 7).
Group I is mainly composed by copepods such as Calanoida, Cyclopoida,
and Poecilostomatoida. Major components of other groups were: Mol­lusca and Doliolida for group II, Euphausiacea for group III, Phaeodaria
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Fig. 7. Result of cluster analysis based on the mesozooplankton abundance of each sample collected from 0 to 3000 m strata of the seven stations neighboring watersof Japan. OK: Okhotsk Sea, JS1: Japan Sea station 1, JS2: Japan Sea station 2, ECS: East China Sea, SA: subarctic Pacific, TR: transitional Pacific, ST: subtropical
Pacific. For samples, numbers after underbar represent depth layers (m).

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Fig. 8. Two-dimensional map by non-metric multidimensional scaling method (NMDS) of zooplankton communities specified by the depth-station complex data.
Eight groups (group A-H) that clustered according to the Bray-Curtis similarity index (Fig. 7) are shown by the different symbols. Arrows indicate directions ofsignificant environmental parameters. Lat.: latitude, Dep.: depth, Temp.: temperature, Sal.: salinity, DO: dissolved oxygen.

even in the surface layer of St. SA.
Scatter plots of the three parameters: slope and intercept of NBSS,
and size diversity are shown in Fig. 12. Across stations, it is noted thatthe slopes of NBSS at 200–1000 m and 1000–3000 m depths are mod­erate and circumscribed to a subarea in the scatter plot. While plot areaof the NBSS slope at 0–200 m depth was broad and varied with thestation. Steep slopes of NBSS were seen at subtropical stations, while
moderate slopes of NBSS were the case at subarctic stations.
Results of GAM analysis applying target variables as slope andintercept of NBSS, and size diversity and explanation variables asenvironmental parameters: depth, temperature, and salinity are shownin Fig. 13. The slope of NBSS had a significant relatioinship with tem­
perature, with warm conditions linked to steep slopes and cold condi­
tions associated with moderate slope. The intercept of NBSS hadsignificant interactions with depth and salinity. The intercept of NBSS
was high at shallower depths and low at the deeper depths. The intercept
of NBSS was high in low salinity conditions and low in high salinity
conditions. Size diversity had significant interaction with depth being
low at shallower depths and increasing with depth. This relationshipbetween depth and size diversity was highly significant (p < 0.001).
Results of inter-group differences in slope and intercept of NBSS andsize diversity tested by one-way ANOVA and post hoc test (TukeyKramer) are shown in Table 5. For the slope of NBSS, the groups E and F
observed at the epipelagic zones of the subtropical stations (Fig. 9) were
evaluated to have steep slopes. As groups having a high intercept of
NBSS, groups F and G were prominent. These two groups were seen at
surface 0–75 m of the subtropical (group F) or subarctic (group G) re­gions. As groups having high size diversity, groups A and D were pre­sent. These two groups were the deep-sea communities observed below
500 m depths. Thus, the three indices of zooplankton size: slope andintercept of NBSS, and size diversity varied greatly in the zooplankton
communities examined.

group F, Appendicularia was abundant, and dominance of calanoid
copepod Pseudocalanus spp. was observed for zooplankton group G.
Occurrences (geographical and vertical distribution) of eachzooplankton community are shown in Fig. 9. Each group occurred atconsecutive regions and depths. Broadly, occurrences of eachzooplankton group can be categorized into the subarctic stations (St. OK,
JS1, JS2, SA) and transitional and subtropical stations (ECS, TR, ST). For
the subarctic station, group G was seen at the shallower 0–50 m depths,
then group C was seen at 50–500 m, and group A dominated below thatlayer (>500 m) (Fig. 9). Group D was only seen for the deep layer (>500m) of the Japan Sea, and it should be noted that these depths correspondwith the occurrence of “Japan Sea Proper Water” (Fig. 2). For stations intransitional and subtropical areas, group E and F were seen at theshallower 0–300 m depths, and group B was seen for 200–500 m depths,
while groups A and H were present in the deepest layer (>500 m)(Fig. 9).
3.4. Zooplankton NBSS and size diversity
Results of NBSS based on zooplankton biovolume at each samplinglayer of the seven sampling stations are shown in Fig. 10. Common for
the whole region and depths, biovolume changes along with the sizes
were generally smooth, and significant NBSS was obtained for all thesamples. The vertical changes in slopes and intercepts of NBSS and size
diversity of each sample are shown in Fig. 11. Slopes of NBSS were zeroor positive for the surface layer (0–50 m) of the subarctic stations (St. OK
and SA). It also should be noted that the prominent decrease of the slope,the intercept of NBSS, and size diversity were observed for subsequent
100–150 m depths. As the common patterns observed for the whole
region, the three parameters: slope and intercept of NBSS, and size di­versity showed great changes around 150–500 m depths. Thus, above
150–500 m depths, the slopes of NBSS were steep, intercepts of NBSS
were high, and size diversity was low, while the moderate slope of NBSS
and low intercept of NBSS, and high size diversity were the cases of
below 150–500 m depths (Fig. 11). Such vertical changes in slope andintercept of NBSS, and size diversity were prominent, especially at St.
TR, ST, and ECS. On the other hand, the slope of NBSS was moderate,
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Table 4
Mean abundance (ind. m− 3) of each zooplankton taxon at eight clustered groups (A-H) identified by Bray-Curtis similarity analysis (cf. Fig. 7). The numbers in theparentheses indicate the number of samples included in each group. Differences between groups were tested by one-way ANOVA and post hoc Tukey-Kramer test. For
the results of the Tukey-Kramer test, any groups not connected by the underlines are significantly different (p < 0.05). -: no occurrence, *: p < 0.05, **: p < 0.01, ***: p< 0.001, NS: not significant. For abundance, the upper three most dominant taxa/species are shown by the bold and underlines.

4. Discussion

documented (Yamaguchi et al., 2002a; Nishibe and Ikeda, 2004). In thesubtropical Pacific, attachment of Poecilostomatoida to discarded
appendicularian structures is reported (Nishibe et al., 2015).
In terms of biovolume, in addition to Calanoida, sporadic high con­tributions from Euphausiacea (Fig. 5) were observed. The dominant
species of Euphausiacea in the western North Pacific, and their marginalseas are reported to be Euphausia pacifica and Thysanoessa spp. both ofwhich are reported to perform diel vertical migration (DVM) (Iguchi
et al., 1993; Taki, 2006, 2011). Stations where Euphausiacea wasobserved above 250 m depths corresponded night collections (Table 1).
For the other prominent taxa contributing to overall biovolume:
Phaeodaria, is important in deeper layers of the Japan Sea reportedly to
due to the prevalence of Aulographis japonica in the cold Japan Sea
Proper Water (Nakamura et al., 2013).
To assess the depth decrease of zooplankton abundance and biomass,
various regressions such as an exponential model (logY = a Depth + b),
power model (logY = a log Depth + b), and regression with an intercept
at 100 m (Y = Y100 (Depth/100)b) have been reported(Yamaguchi et al.,2002a, 2002b, 2004, 2005). Here, we report power regression to both4.1. Abundance and biovolume
In abundance terms, three orders of Copepoda (Calanoida, Cyclo­
poida, and Poecilostomatoida) contributed significantly to community
composition. Within them, Calanoida contains various feeding modes:
particulate feeders, detritivores, and carnivores, and they have impor­tant roles as mediators of energy transfer to higher trophic levels and invertical material flux (Mauchline, 1998). For the small-sized copepod,
Cyclopoida was dominated at 0–250 m of the subarctic stations (Fig. 4).
Cyclopoida feeds mainly on microzooplankton such as ciliates and areconsidered to have an important role in the transfer of the microbial
production to the higher trophic levels (Nishibe et al., 2010). The othersmall-sized copepod Poecilostomatoida is considered to be a detritivorethat feeds on detritus and is attached to the marine snow (Turner, 2004).
Poecilostomatoida was abundant below 250 m of the subarctic stations
and the whole water column of the subtropical stations. The dominanceof Poecilostomatoida at the deep layer of the subarctic Pacific is well11

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Fig. 9. Spatial and vertical distribution of zooplankton community groups identified by Bray-Curtis similarity index (cf. Fig. 7). Sampling depth at each station isshown by the symbols. Note that depth scale is in log-scale. OK: Okhotsk Sea, JS1: Japan Sea station 1, JS2: Japan Sea station 2, ECS: East China Sea, SA: subarctic
Pacific, TR: transitional Pacific, ST: subtropical Pacific.

abundance and biovolume. Yamaguchi et al. (2002a) also employed
power regressions to examine depth-decreasing rates of Copepoda in thewestern subarctic Pacific and reported that the slope (a) of the regres­sion is steep (range − 1.41– − 1.52) for abundance and moderate forbiomass (range − 1.10 – − 1.32). A steeper regression slope for abun­dance than that of biomass (as biovolume) was also observed in thisstudy (Table 2).
Biovolume decrease at the cold intermediate water at St. OK and SA
was strong. The cold intermediate water is brine water that originatedduring ice-forming last winter and is characterized by extreme cold (<0˚C) and the development of a strong pycnocline (Takizawa, 1982). At theintermediate cold water, the DVM of zooplankton is prevented, and thedecrease of zooplankton biovolume at that layer has been well docu­
mented (Yamaguchi, 2015). These factors may have induced the abrupt
decrease of biovolume at intermediate cold water observed for St. OK
and SA (Figs. 5, 6b).
Taxonomic differences in rates of biomass decrease with depth were
and the decreasing rates with more rapid rates for higher trophic level
organisms than for those from lower trophic levels (Yamaguchi et al.,
2002b, 2004). In this study, the depth-related decreasing rate andintercept of abundance were similar throughout all stations. This resultin abundance contrats the general patterns of zooplankton biomass:
depth-decreasing rates are similar but intercepts vary (Vinogradov,
1968; Table 3 of this study). These differences would be due to thedifferences in the units of analysis (abundance or biomass [biovolume]).
As a comparable study, Yamaguchi et al. (2015) conducted depthdecreasing rates of Copepoda of 0–2615 m depths based on thevertically stratified samples collected at 16 stations covering tropical tosubarctic regions (0˚to 56˚N in latitude) of the North Pacific. In that
expansive dataset, the abundance of Copepoda decreases withincreasing depth throughout the stations, but differences in regressions
were not observed (Yamaguchi et al., 2015). Thus, while comparable
information concerning biomass is scarce, the depth-related decreasingrate and intercept of zooplankton abundance seem to be similar
throughout the whole North Pacific and also the marginal seas.
For biovolume, regional (station-to-station) differences were prom­
inent, while depth related changes were minor (Table 3). Rates ofbiomass decrease with depth are similar throughout the regions, while
regional differences in intercept at the surface layer are foundthroughout the depths (Vinogradov, 1968; Yamaguchi et al., 2005).
These patterns likely reflect the fact that the origin of energy forzooplankton starting from primary productivity centers at the sea sur­face. Thus, regions with high productivity and high biomass at thesurface layer contain high values of both even in the deep layer, while
the regions with low productivity and biomass at the surface layer havelow values of both in the deep layer. Studies quantifying biogeochemical
amounts and fluxes in the subarctic and subtropical Pacific indicate mostof the parameters vary regionally approximately two-fold; however,mesozooplankton biomass is reported to be 10 times larger for thesubarctic than that in the subtropical region (Steinberg et al., 2008b;
Kitamura et al., 2016; Honda et al., 2017). Thus, the results on
zooplankton biovolume in this study (regional differences were promi­
nent and high in the subarctic region) correspond well with results ofregional comparisons between the subarctic and subtropical Pacific.
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Fig. 10. Vertical changes in normalized biovolume size spectra (NBSS) at various depth strata of the seven sampling stations neighboring waters of Japan. Note that
NBSS regressions are highly significant (r2 = 0.15–0.9, p < 0.05) for all sampling depths. OK: Okhotsk Sea, JS1: Japan Sea station 1, JS2: Japan Sea station 2, ECS:
East China Sea, SA: subarctic Pacific, TR: transitional Pacific, ST: subtropical Pacific.

4.2. Zooplankton communityof the subtropical region, and group G was seen for the cold surface layerof the subarctic region (Fig. 9). The same directions of depth and salinity
in NMDS panel are interpreted that the salinity was high for deeper
depths of most of the stations (Fig. 2). The zooplankton groups A and H
which observed for high depth values in NMDS panel were restricted todeep layers (Fig. 9). Thus, plotted areas of each zooplankton group anddirections of environmental parameters in NMDS are well correspondedwith the regional and vertical distributions of each zooplankton group.
Beyond the dominant Copepoda (Calanoida, Cyclopoida, andThis study examines zooplankton from the sea surface down to 3000
m at seven stations covering the subarctic and subtropical Pacific andtheir three marginal seas. Because of the study targeting broader region
and depth, zooplankton community was classified into eight groups(Fig. 7). Various environmental parameters are linked with the differ­entiation of zooplankton groups, (Fig. 8). Among zooplankton groups
observed in high DO regions, group F was seen for the warm sea surface
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Fig. 11. Vertical changes in slope and intercept of the normalized biovolume size spectra (NBSS) and size diversity at various depth strata of the seven samplingstations neighboring waters of Japan. OK: Okhotsk Sea, JS1: Japan Sea station 1, JS2: Japan Sea station 2, ECS: East China Sea, SA: subarctic Pacific, TR: transitional
Pacific, ST: subtropical Pacific.

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Fig. 12. Scatter plots between slope and intercept of NBSS (a), size diversity and slope of NBSS (b), and size diversity and intercept of NBSS (c) at seven stationsneighboring waters of Japan. OK: Okhotsk Sea, JS1: Japan Sea station 1, JS2: Japan Sea station 2, ECS: East China Sea, SA: subarctic Pacific, TR: transitional Pacific,
ST: subtropical Pacific. Differences in colors represent sampling depths (0–200, 200–1000, and 1000–3000 m).

Poecilostomatoida), Metridia spp., the large-sized calanoid copepod
genus, were notably abundant for the zooplankton groups A, B, G, and H(Table 4). Within these groups, group G was seen for the surface layers of
the subarctic Pacific, Japan Sea, and Okhotsk Sea (Fig. 9). Metridia is
known to perform DVM (Padmavati et al., 2004) and M. okhotensis is themost common species in the Okhotsk Sea (Yamaguchi, 2015; Arimaet al., 2016), M. pacifica in the Japan Sea (Hirakawa and Imamura,1993), and M. okhotensis and M. pacifica in the subarctic Pacific (Pad­mavati et al., 2004; Takahashi et al., 2009). The boreal large-body-sized
copepod species are known to be transported to the deeper layers of thetransitional and subtropical regions through the submergible cold-water
Oyashio (Omori and Tanaka, 1967; Kobari et al., 2008). The dominanceof the deep-sea Metridia species (M. venusta) in deep layers at lower
latitudes (<30˚N) has been reported (Yamaguchi et al., 2015). Thus, inthe transitional and subtropical regions, the groups dominated by Met­
ridia spp. (groups A, B, H) were seen only for the deeper layers.
For the other zooplankton groups, with particular dominant
zooplankton taxa/species, Phaeodaria and Ostracoda primarily
comprised group D (Table 4), which was seen in the deeper layers of theJapan Sea representing cold Japan Sea Proper Water (Fig. 9). In theJapan Sea Proper Water A. japonica has been well documented and theirbiomass is reported to be second to that of copepods at these layers(Nakamura et al., 2013). For the Japan Sea Proper Water, the dominanceof the ostracod Conchoecia pseudodiscophora has also been reported(Ikeda, 1990; Ikeda and Imamura, 1992). The distinct zooplankton
community in the cold Japan Sea Proper Water is confirmed by ourfindings.
For the other zooplankton groups dominated by the specificzooplankton taxa, group F, dominated by Appendicularia, was seen at
the surface layers of the ECS and TR (Table 4, Fig. 9). Appendicularia
filter feeds on pico- and nano-sized particle, reproduces asexually, and is
known to show outbreaks at the surface layer of the transitional region(Yokoi et al., 2008). Appendicularia creates a “house” structure for filter
feeding, which it sheds frequently, and Poecilostomatoida is known toattach to the discarded “houses” of Appendicularia and use them as
feeding and living places (Nishibe et al., 2015). For zooplankton group
F, Appendicularia and Poecilostomatoida are the dominant groups(Table 4). This suggests that Appendicularia dominated zooplankton
communities at surface layers of ECS and TR where it feeds on smallsized particles, then Poecilostomatoida would attach on the discarded
appendicularian houses.
Here we examined geographical and vertical distribution of
zooplankton communities from the sea surface to the deep sea, including
subarctic to subtropics of the western North Pacific (Fig. 9). In this re­gion, vertical distribution of planktonic communities has been reported
for the pelagic copepods (Yamaguchi et al., 2015) and chaetognaths(Ozawa et al., 2007). Copepod communities were segregated into sur­face and deep sea vertically and into subarctic and subtropics horizon­tally (Yamaguchi et al., 2015), a pattern corroborated in this study.
Chaetognath deep-sea communities have been reported to be the samefrom the Bering Sea to the subtropics, while those in the Japan Sea havebeen reported to be markedly distinct from other regions (Ozawa et al.,2007). These substantial differences in the zooplankton community ofthe deep sea of the Japan Sea characterized by the Japan Sea Proper
Water were confirmed in this study (Fig. 9). The basin area of the Japan
Sea is deep (maximum at 3700 m and mean 1350 m), while depths of its
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Fig. 13. Result of GAMs based on anomalies of the slope and intercept of NBSS and size diversity with environmental paraments (depth, temperature and salinity).
**: p < 0.01, ***: p < 0.001.
Table 5Inter-group differences in zooplankton size related variables (slopes and intercepts of NBSS and size diversities) evaluated for zooplankton samples collected from 0 to3000 m depths of the seven sampling stations at neighboring waters of Japan. For details of the location of the stations and distribution of each zooplankton community
clustered by the zooplankton abundance data, see Figs. 1 and 9, respectively. For detailed data of NBSS and size diversity see Figs. 10 and 11, respectively.

connections other outer oceans are shallow (<130 m), which leads to a
disconnection of the waters in the deep layer with the neighboring North
Pacific, East China Sea, and Okhotsk Sea, and forming the Japan Sea
Proper Water, and thus the presence of a specialized deep-sea fauna(Zenkevitch, 1963; Vinogradov, 1968).

(Moore and Suthers, 2006; Suthers et al., 2006; Zhou, 2006; Zhou et al.,2009). In this study, NBSS slopes had positive values for certain stations
and depth combinations: 25–75 m of OK and 0–75 m of SA (Fig. 10). This
was the result of higher biomass of the large-sized zooplankton in thosesamples. These stations/depths clustered in groups C and G in thezooplankton community mentioned before (Fig. 9). The groups C and G
are characterized by the dominance of the large-body-sized copepod
Neocalanus spp. (Table 4) suggesting that the positive slopes of NBSS ofthese stations/depths may be due to the smaller size ranges of thesampled zooplankton, as pointed out for the zooplankton community inthe eastern North Pacific by Kwong and Pakhomov (2021). Since wehave abundance and biovolume data of each taxon, added to slopes and4.3. NBSS and size diversity of zooplankton
We measured slopes and intercepts of NBSS and size diversity of all
the sampled examined in this study. The slopes of NBSS are expected tohave a negative value (e.g. low biomass at the large-sized higher trophic
organisms) and a value of − 1 expected in stable marine ecosystems
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intercepts of NBSS, we can discuss the causes of the unexpected NBSS
values in detail.
The slopes of NBSS observed in this study were between − 0.143 and− 0.51 for the mean values of each zooplankton community (Table 5). An
NBSS analyses by OPC was conducted on zooplankton samples collectedfrom 0 to 150 m using 335 µm mesh NORPAC net on the same cruise on
which this study is based (Sato et al., 2015). In that study, the NBSS
slope were reported as –0.90 for the areas dominated by large-sized
copepod Neocalanus spp. and as − 1.11– − 1.24 for other regions suchas subtropical Pacific (Sato et al., 2015). On the other hand, the samplesof this study were collected by the vertically stratified samplings of
VMPS down to 3000 m equipped with a smaller mesh of 63 µm, thenmeasured by ZooScan. Thus, greater differences were available between
the two studies (Sato et al., 2015 and this study) in terms of the target
depth (0–150 m vs. 0–3000 m), applied mesh size (335 µm vs. 63 µm),
and measurement devices (OPC vs ZooScan).
The differences in mesh sizes of the plankton net would provide
differences in net clogging or filtering efficiencies. However, thefiltering efficiencies measured by the flowmeter reading were high (>85%) for both mesh sizes (Electronic Supplement 1). Thus, the differencesin net filtering efficiency are not considered to cause the differences in
NBSS slopes between the two studies (Sato et al., 2015 and this study).
Since this study applied smaller mesh sizes (63 µm), it may allow us tocollect smaller-sized zooplankters and broader target size ranges for
NBSS analysis and then produce steeper slopes of NBSS than thosequantified by the large mesh size (335 µm) samples. But the results were
the opposite: NBSS slopes of this study were more moderate than thoseby Sato et al. (2015). Thus, the differences in net mesh size are notconsidered to be a cause of the differences in NBSS slopes. These facts
suggest that the different instruments (OPC vs. ZooScan) led to differ­ences in NBSS.
OPC quantifies all the particles contained in a sample, while ZooScan
can differentiate zooplankton based imagery. Thus, ZooScan candistinguish zooplankton from non-living particles such as fecal pellet,
fragment, and detritus, and not include those non-living particles insubsequent analyses as was the case in the present study (Vandromme
et al., 2012). NBSS derived from OPC includes all the particles, living
and non-living. Because the non-living particles (fecal pellet, fragment,
detritus) may be altered by fragmentation, coprophagy, and coprorhexy
by zooplankton and bacterial decomposition, their sizes are generally
smaller than the zooplankton (Turner, 2002, 2015). Thus, whenmeasuring the same zooplankton samples, data from OPC contains
small-sized non-living particles, and their intercept and slope of NBSS
would be higher and steeper, respectively, than those from ZooScan
which calculated only on zooplankton data.
Several studies have compared ZooScan with other instruments,
including ZooScan with LOPC (Schultes and Lopes, 2009) and ZooScan
with OPC (Naito et al., 2019). Since LOPC and OPC include small-sized
non-living particles, their NBSS slope tended to be steep, while for
ZooScan, the biovolumes of the large-sized gelatinous zooplankton (e.g.
jellyfishes, doliolids, and salps) have been reported to be overestimated,thus their NBSS slope tends to be more moderate (Schultes and Lopes,
2009; Gorsky et al., 2010; Vandromme et al., 2012; Naito et al., 2019;
Kwong and Pakhomov, 2021). Regardless of instrumental biases, whenmeasuring the samples with a common methodology it should bepossible to detect and test for community structure changes withgeographical, horizontal, or spatial factors (Schultes and Lopes, 2009,2012; Naito et al., 2019). Thus, in this study, we will make a comparisonof the values of the NBSS slope or intercept obtained from this study
only. For the other studies, we will make comparisons on thegeographical patterns and not include NBSS values for the inter-study
comparison.
For the latitudinal changes of NBSS slope of zooplankton in thesubarctic-subtropical North Pacific, there are several studies based on
OPC analyses, and the NBSS slope has been reported to moderate for thesubarctic region where dominated by the large-sized Neocalanus

copepods (Fukuda et al., 2012; Shiota et al., 2013; Sato et al., 2015;
Mishima et al., 2019). Within the region, seasonal changes in NBSS slope
have also been reported, and moderate NBSS slopes in summer whendevelopment for the late copepodite stages have been observed for thelarge-sized Neocalanus copepods (Yamaguchi et al., 2014; Hikichi et al.,2018). Zooplankton biomass in the subarctic Pacific is predominated by
the large-sized Neocalanus copepods (Ikeda et al., 2008). These facts
suggest that moderate NBSS slopes are available for the region or season
where and when dominated by the large-sized Neocalanus copepods.
Significant relationships were observed between NBSS slope andtemperature, with moderate slopes under low temperature, and steep
slopes under high temperature (Fig. 13). The moderate NBSS slope ofcold condition is due to the dominance of the large-sized copepods
Neocalanus spp. especially in the epipelagic zones of the subarctic Pacific(Ikeda et al., 2008). Even for the subtropical region, the temperature of
the deep-sea is low, and the deep-sea copepods inhabiting under suchcondition contain lipids in their body, have long longevity, and largebody sizes (Mauchline, 1998). Thus, under low-temperature condi­
tions, NBSS may tend to have moderate slopes. On the other hand, underwarm conditions, acceleration and high metabolism of zooplankton
would occur, and large-sized copepods with diapause phases in their life
history are absent (Mauchline, 1998). The steepest slopes of NBSS of thisstudy were seen from the groups E and F which were observed for the
epipelagic zones of the subtropical region (Table 5). These facts suggestthat high temperatures under these conditions may prevent the occur­
rence of large-sized zooplankton there.
Depth and salinity had significant negative relationship with the
NBSS intercept (Fig. 13). Intercept of NBSS is reported to reflect primary
productivity at the given region and depth (Moore and Suthers, 2006;
Zhou, 2006; Zhou et al., 2009; Gomez-Canchong et al., 2013). Since
primary productivity centers at sea surface, the NBSS intercept would behigh at the shallower depth. Since zooplankton biovolume decreased
with increasing depth (Fig. 6), the NBSS intercept would be decreased
with increasing depth. These depth trends of primary productivity andzooplankton biovolume induce negative relationships of NBSS intercept
and depth mentioned above. For the interaction of NBSS intercept andsalinity, the NBSS intercept was high (=high biovolume) under low
salinity conditions, while the NBSS intercept was low (=low biovolume)
under high salinity conditions (Fig. 13). In this study, low salinity con­ditions were seen for two stations in the subarctic Pacific and Okhotsk
Sea (Fig. 3). The zooplankton biovolume of the epipelagic zones of thesestations was high, especially at the near surface (Fig. 6b). These highzooplankton biovolumes there would produce high NBSS intercept
under low salinity conditions. Salinity increased with increasing depths
throughout the stations (Fig. 3). The decreasing NBSS intercept withincreasing salinity would be analogous to the NBSS intercept decrease
with increasing depths, as described above.
Depth had a strong significant effect on size diversity, and the size
diversity was low at the shallower depths and increased with increasing
depths (Fig. 13). In terms of the zooplankton community, size diversity
was high for groups A and D (Table 5) which were observed in the deep
layer of the subarctic region (Fig. 9). These facts suggest that size di­versity would be high at depths where zooplankton covering the broader
size ranges occur.
In the present study, all parameters on zooplankton size spectra:intercept and slope of NBSS, and size diversity showed large
geographical and vertical changes. Especially, vertical change was
detected at 150–500 m depths for all parameters, and these shifts weremost prominent in the transitional region and subtropical North Pacific,
and East China Sea (Fig. 11). For these regions, depths of 150–500 m
were serve as the boundaries to separate epipelagic zooplankton com­munity and deep-sea zooplankton community, and below that layer,since zooplankton community was characterized with the that in thecold condition, intercept of NBSS would be lower, high size diversity due
to dominance of the large-sized zooplankton (Fig. 13), then the mod­erate slope of NBSS may present (Fig. 11). While the narrower treated17

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size ranges should be noted (Kwong and Pakhomov, 2021), NBSS andsize diversity of this study clearly showed reflect of geographical andvertical changes in zooplankton community in the subarctic, transi­
tional, and subtropical regions of the western North Pacific, and its threemarginal seas: Okhotsk Sea, Japan Sea, and East China Sea.

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5. Conclusions
Based on the vertically stratified net samples collected down to thedeep layer (3000 m), regional and vertical changes in zooplankton
abundance, biovolume, community structure, NBSS, and size diversity
were evaluated at seven stations covering subarctic, transitional, andsubtropical regions of western North Pacific and its marginal seas:
Okhotsk Sea, Japan Sea, and East China Sea. Both abundance and bio­volume decreased with increasing depths. Their depth-decreasing rates
were more rapid for abundance than those in biovolume. The mostimportant environmental determinant of zooplankton abundance wasdepth, while region was the most prominent for their biovolume. Basedon the abundance data, zooplankton communities were clustered into
eight groups. Each group was distributed in adjacent regions and depths,
and the occurrence of a distinct community dominated by Phaeodaria
and Ostracoda was seen for the deep layer of the Japan Sea. NBSS andsize diversity showed clear vertical changes around 150–500 m depths.
Above that layer, the intercept and slope of NBSS were high and steep,
respectively, and linked with low size diversity there. On the other hand,contrating patterns: low NBSS intercept, moderate NBSS slope, and highsize diversity were seen below that layer. This study showed regionaland vertical changes in zooplankton abundance, biovolume, community
structure, NBSS, size diversity, and its governing environmental pa­
rameters clearly.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgements
The zooplankton samples used in this study were collected by T/SOshoro-Maru of the Faculty of Fisheries, Hokkaido University. We ex­press sincere thanks to the captain, crew, and scientists who onboard thecruise for their great help in collecting samples and obtaining hydro­
graphic data used in this study. Dr. Juan Andrés López of University of
Alaska Fairbanks kindly provided English editing. Part of this study was
supported by Grant-in-Aid for Challenging Research (Pioneering) 20
K20573, Scientific Research 22H00374 (A), 20H03054 (B), 19H03037(B), and 17H01483 (A) from Japan Society for the Promotion of Science(JSPS). This study was partially supported by the Arctic Challenge for
Sustainability II (ArCS II; JPMXD1420318865) and the Environmental
Research and Technology Development Fund (JPMEERF20214002) ofthe Environmental Restoration and Conservation Agency of Japan.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.pocean.2023.103155.
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