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Plankton Research

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ORIGINAL ARTICLE
Diel, seasonal and vertical changes in the
pelagic amphipod communities in thesubarctic Paciﬁc: insights from imaging
analysis
RYO TANIGUCHI1,† , KANAKO AMEI2,‡,§ , KOKI TOKUHIRO2, , YUICHIRO YAMADA3 , MINORU KITAMURA4 AND
ATSUSHI YAMAGUCHI5,6, *1

school of fisheries sciences, hokkaido university, 3−1−1 minato-cho, hakodate, hokkaido 041−8611, japan, 2 graduate school of fisheriessciences, hokkaido university, 3−1−1 minato-cho, hakodate, hokkaido 041−8611, japan, 3 school of marine biosciences, kitasato
university, 1–15–1 kitasato, minami-ku, sagamihara 252–0373, japan, 4 japan agency for marine-earth science and technology, 2−15
natsushima-cho, yokosuka, kanagawa 237−0061, japan, 5 faculty of fisheries sciences, hokkaido university, 3−1−1 minato-cho, hakodate,hokkaido 041−8611, japan and 6 arctic research center, hokkaido university, kita-21 nishi-11 kita-ku, sapporo, hokkaido 001−0021, japan*corresponding author: a-yama@ﬁsh.hokudai.ac.jp† ryo taniguchi present address: nitori co. ltd., sapporo headquarters, 1−2−39 shinkotoni 7-jo, kita-ku, sapporo, hokkaido 001−0907,
japan.
‡ kanako amei present address: department of marine ecosystems dynamics atmosphere and ocean research institute, the university of
tokyo, 5−1−5, kashiwa, chiba 277−8564, japan.
§ kanako amei present address: graduate school of agricultural and life science, the university of tokyo, 7−3−1, hongo, bunkyo, tokyo
113−0033, japan.
|| koki tokuhiro present address: demonstration laboratory, marine ecology research institute, 4−7−17 arahama, kashiwazaki, niigata
945−0017, japan.
Received September 10, 2022; editorial decision March 15, 2023; accepted April 4, 2023
Corresponding editor: Marja Koski

Vertically stratiﬁed day and night samples were collected from a depth of up to 1000 m during four seasons at a single
station in the western subarctic Paciﬁc. Subsequently, the abundance, biovolume, community structure and population
structure of the pelagic amphipods were evaluated from the imaging analysis using ZooScan. The stable isotope ratio(δ 15 N) was also measured for each species. In total 10 amphipod species were identiﬁed in total, and their community
structures were separated into four groups. The four communities were characterized by the upper-layer community
dominated by Themisto paciﬁca, and the deep-water community that was characterized by the absence of T. paciﬁca.
The other two groups were observed for the intermediate depths at night only, which was characterized by the low

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J. Plankton Res. (2023) 1–17. https://doi.org/10.1093/plankt/fbad017

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KEYWORDS: ZooScan; St. K2; amphipoda; imaging analysis

INTRODUCTION

images and size data from one scan. Thus, its usefulness
has been applied to various regions (Gorsky et al., 2010;
Irisson et al., 2022). Pelagic amphipods have large bodies;thus, species identiﬁcation may be possible based on
their images. Based on morphology, developmental stages(juveniles, immature, mature females and males) (Yamada
et al., 2004) may also be identiﬁed. However, no study has
applied ZooScan to the community structure of pelagic
amphipods or the population structure of the dominant
species.
Various unique ecological characteristics of pelagic
amphipods have been previously reported. Thus, someHyperiidea species are known to attach to gelatinous zooplankton. As host gelatinous zooplankton for Hyperiidea,
taxa belonging to ctenophores, cnidarians, hydrozoans,salps and protozoan rhizarians have been reported (Harbison et al., 1977; Madin and Harbison, 1977; de Lima
and Valentin, 2001; Gasca et al., 2007; Nakamura et al.,2019). Species-speciﬁc associations are present between
the host and amphipod species; thus, Scina spp. and Vibilia
spp. are associated with hydrozoans and salps, respectively(Harbison et al., 1977; Madin and Harbison, 1977; deLima and Valentin, 2001; Gasca et al., 2007). Sexual
differences in associations with gelatinous zooplankton
exist within each species; for example, Hyperia galba lives
within the scyphozoans, feeding on the host tissue andtheir growth, reproduction, and early development are
made in the host scyphozoans, although their adult males
have no association with the scyphozoans (Fleming et al.,2014).
The feeding modes of pelagic amphipods vary withspecies and developmental stages and include herbivores
to carnivores (Sugisaki et al., 1991; Espinosa-Leal et al.,2020). As indices for evaluating the feeding modes ofamphipods, stable isotope ratios, especially δ 15 N, are valuable (Sugisaki et al., 1991; Søreide and Nygård, 2012;
Fleming et al., 2014). However, there is a lack of information on the stable isotope ratio of the whole pelagic
amphipod species, and inter-species comparisons havebeen performed on this regard in the western subarctic
Paciﬁc.
A long-term time-series station in the western subarctic
Paciﬁc, station K2 (St. K2) (47◦ N, 160◦ E, depth 5230 m)
was established by the Japan Agency for Marine-Earth

In oceans worldwide, pelagic amphipods associate fromthe sea surface to the benthopelagic layer of the deepsea (Vinogradov, 1999). Pelagic amphipods are known
to dominate zooplankton biomass, especially in higherlatitude oceans (Mayzaud and Boutoute, 2015). Themisto
japonica is the dominant species in the waters surrounding
Japan, speciﬁcally at Toyama Bay in the southern Japan
Sea. The growth rate based on laboratory rearing (Ikeda,
1990; 1992), the budget of the assimilated carbon (Ikeda,
1991), diel vertical migration (DVM) and life cycle ofthe ﬁeld population (Ikeda et al., 1992), and production estimation (Ikeda and Shiga, 1999) of this species
have been reported. For the second dominant species,
Primno abyssalis, the vertical distribution, growth, maturation, brood size and life cycle of the ﬁeld population
have also been reported (Ikeda, 1995). Further, in the
Oyashio region in the western subarctic Paciﬁc, ecologiesof the two sibling species, Themisto paciﬁca and T. japonica(Yamada et al., 2004; Yamada and Ikeda, 2004), and P.
abyssalis (Yamada and Ikeda, 2001; Yamada et al., 2002)
and Cyphocaris challengeri (Yamada and Ikeda, 2000; 2001)
have also been previously studied. In addition, chemicalcomposition, metabolic measurements and production
estimations were made for the above-mentioned four
dominant amphipod species (Yamada and Ikeda, 2003;
2006). Thus, the neighboring waters of Japan are characterized by intensively studied physiological and ecological characteristics of each dominant pelagic amphipod species. However, little information is available on
the community structure of pelagic amphipods and theecology of other minor pelagic amphipod species.
To evaluate the amphipod community and population
structures of the dominant species, species identiﬁcation
and body size measurements are required. However, thebody shapes of most amphipod specimens are rounded,making it difficult to measure their body size underordinary microscopic observations. Thus, body-size
measurements of amphipods are time-consuming, andthey provide scarce information despite their importance(cf. Yamada et al., 2004). Imaging analysis methods areavailable for accurate and rapid measurement of bodysizes. Within the imaging methods, ZooScan can obtaintaxonomic information (species identiﬁcation) based on

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abundance of T. paciﬁca performing diel vertical migration from those depths. The deep-dwelling species displayed
higher δ 15 N and positive relationships were detected with the habitat depth of each species. For the predominant T.
paciﬁca, population structure (cohort) analysis was possible based on equivalent spherical diameter data from ZooScan.
This study demonstrates that imaging analysis by ZooScan is applicable for analyses of minor taxonomic groups(amphipods) in zooplankton communities.

R. TANIGUCHI ET AL.

DIEL, SEASONAL AND VERTICAL CHANGES IN THE PELAGIC AMPHIPOD COMMUNITIES

Fig. 1. Location of the sampling station: St. K2 in the western subarctic
Paciﬁc (solid star). Approximate positions and directions of the major
current ﬂows are shown with the arrows (cf. Yasuda, 2003). EKC: East
Kamchatka Current, WSAG: Western Subarctic Gyre, DSW: Dense
Shelf Water, ESC: East Sakhalin Current, OSMW: Okhotsk Sea Mode
Water, OY: Oyashio, KE: Kuroshio Extension.

were measured using a CTD (SBE 911 plus; Sea-Bird
Electronics Inc.).

ZooScan measurement
In the land laboratory, amphipod specimens were sorted
from zooplankton subsamples at 1/2–1/64 based on thevolume. For the sorted amphipod samples, we performed
imaging analysis using ZooScan (ZooScan MIII, Hydroptic Inc.).
The protocols for sample measurement using ZooScan
were based on Gorsky et al. (2010). Dehydrated water
was used to examine the ZooScan cell, and a backgroundscan was conducted. Subsequently, the sorted amphipod
samples were ﬁlled for the scanning cell and images of thesamples were captured. To obtain accurate images of thesamples, ﬂoated samples and duplicated specimens were
removed using tweezers to collect the individual specimen
settled at the bottom of the scanning platform. The total
numbers of captured images of amphipods were 6737.
The scanned images were separated from the individual
images using ZooProcess with ImageJ, Eco Taxa was
updated (http://ecotaxa.obs-vlfr.fr/) via File Zila, andspecies identiﬁcation and measurement of the equivalent spherical diameter (ESD, in mm) were performed.
In addition to species identiﬁcation, the developmental
stages of the most abundant species (T. paciﬁca) were identiﬁed from the morphological characteristics mentioned
below (Yamada and Ikeda, 2004):
Juvenile: body size <3.0 mm.
Immature males: antennules were segmented but notextended, and body size was 2.7–4.7 mm.
Immature females: antennules were not segmented;
body size = 3.0–4.5 mm.

MATERIAL AND METHOD
Field sampling
Day and night vertically stratiﬁed oblique hauls of
a 1.5 m2 mouth opening Intelligent Operative Net
Sampling System (IONESS, SEA Co. Ltd) equippedwith 335 μm were made from eight depth strata (0–50, 50–100 100–150, 150–200, 200–300, 300–500,
500–750 and 750–1000 m) at St. K2 (47◦ N, 160◦ E,
depth 5230 m; Fig. 1) during four seasons over 1 year:
29 October 2010, 26 February, 22–23 April and 3–
4 July 2011 (Electronic Supplement 1). Zooplankton
samples were preserved in 4% formalin (v/v) immediately
after collection. At each sampling date, environmental
data [temperature, salinity and dissolved oxygen (DO)]3

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Science and Technology (JAMSTEC) (Honda et al., 2017).
Information on amphipods at St. K2 is limited due tovarious factors such as the DVM of the dominant species,
night: day zooplankton abundance ratio showing 3.6-folddifference at 0–150 m depths, mesopelagic occurrence ofPhrosina spp. and Primno spp. and C. challengeri exhibiting
DVM of up to 200 m (Steinberg et al., 2008). Other
than the information on the abundance and community
structure of amphipods, little information is available,
especially regarding the seasonal changes and population
structure of the dominant species.
In the present study, we used formalin-preserved samples collected from the day and night vertical stratiﬁcation
sampling at eight layers down to a depth of 1000 m
at St. K2 in the western subarctic Paciﬁc, covering four
seasons in 1 year. For the sorted amphipod samples fromthe whole zooplankton samples, imaging data were captured by ZooScan and species identiﬁcation and stage
identiﬁcation for T. paciﬁca were performed based on
the images. From imaging data, abundance, biovolume,community structure and population structure of thedominant species (T. paciﬁca) were made. Based on thesorted specimens, dried with the species, the stable isotope
ratio (δ 15 N) was measured and an inter-species comparison was made. For the gelatinous zooplankton taxa (Radiolaria/Phaeodaria, Cnidaria and Thaliacea) that havebeen reported as host associations for pelagic amphipods(Hyperiidea), their diel vertical distributions were conducted based on biomass data from the same samples(Kitamura et al., 2016). Through this study, we will test
whether we can obtain valuable information [abundance,
biovolume, taxon (species and developmental stage) andbody size] shortly and accurately by imaging analyses(ZooScan) on the sorted samples of the particular taxon(amphipods).

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50 − p1p2

where d1 is the upper depth (m) of the sampling layer
where 50% of the population is distributed, d2 represents
the sampling interval (m) where 50% of the population is
distributed, p1 is the composition (%) of the cumulative
abundance (ind. m−2 ) occurring in the upper layers of thesampling layer with 50% of the population distribution,and p2 is the composition (%) of the cumulative abundance (ind. m−2 ) of 50% of the population distribution
within the cumulative standing stock (ind. m−2 ) of thewater column.
For the most numerous pelagic amphipod species at St.
K2, T. paciﬁca, the cumulative numbers (n) of captured
images in day or night samples at each sampling datewere 93–1138 images, which allowed us to constructhistograms of ESD and developmental stage compositionin the population.

Based on the split factors and ﬁltered volumes of eachsample, the abundance (ind. m−3 ) and biovolume based on
ESD (mm3 m−3 ) were quantiﬁed for each species. Basedon the abundance and biovolume data, Shannon-weaver
species diversity (H ) and Pielou’s evenness index (J’) were
calculated using the following equations:pi × ln(pi)i=1J  = H  / ln S

Stable isotope ratio (δ 15 N)

where S is the number of species and pi is the relative
composition of species i in each sample (Morishita, 1996).
For the community structure of the pelagic amphipods,
Bray–Curtis (Bray and Curtis, 1957) cluster analysis
connected with the complete linkage based on theabundance data (ind. 1000 m−3 ) standardized by the
fourth root was performed. Similarities between thesamples were evaluated using a two-dimensional plot of
the nonmetric multidimensional scaling method (NMDS;Minchin, 1987), and interactions with environmental
parameters (depth, temperature, salinity and DO) wereanalyzed by multiple regression analysis. For temperature,salinity and DO, integrated mean values at each samplinglayer were calculated and applied for the multiple
regression analysis. The effect of spatial and temporalenvironmental parameters (season, day/night and depth)
and interactions within them (season × day/night, season
× depth and day/night × depth) on the occurrenceof each amphipod community was analyzed using
PERMANOVA. These analyses were conducted using
the PRIMERv7 software (PRIMER-E Ltd). Differencesin amphipod abundance between the clusters were
evaluated using one-way analysis of variance (ANOVA)
and the subsequent post-hoc test (Tukey–Kramer test).

To quantify the stable isotope ratio (δ 15 N: ), specimensfrom the samples with the highest biovolumes (mm3 m−3 ),which varied with species, were chosen. The specimens
were rinsed with distilled water and dried in an oven at
60◦ C for 5 h. After drying, the specimens were ﬁnely
ground using a mortar and pestle. The nitrogen stable
isotope (15 N and 14 N) was analyzed using an elemental
analyzer (Flash EA1112-Delta V Plus He-Flow System,
Thermo Fisher Scientiﬁc, Germany). The δ 15 N value wascalculated using the following equation.
δ 15 N = Nsample /14 Nsample /
15
Nstandard /14 Nstandard − 1 × 1000
15where 15 Nsample and 14 Nsample are the values of the samples and 15 Nstandard and 14 Nstandard are the values of 15 N
and 14 N of the standardized samples, respectively. Interspecies differences in δ 15 N were evaluated using oneway ANOVA and the Tukey–Kramer test. To evaluate
the effect of habitat depth on the δ 15 N value, linear
regression between δ 15 N () and nighttime D50% (m) was

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D50% = d1 + d2 ×Data analysis

SPAGES 1–17

These analyses were performed using the OriginPro
software (Light Stone Ltd).
The presence of DVM in pelagic amphipods was evaluated using the two-sample Kolmogorov–Smirnov test. To
evaluate the vertical distribution depth of each species,
the depths of 50% of the population (D50% ) were calculated using the following equation (Pennak, 1943):

Mature males: antennules were segmented andextended; body size = 4.1–6.0 mm.
Mature females: antennules were not segmented, andspaces were present on the basis of the swimming legs;
body size = 4.5–9.00 m.
These body sizes were used for the extended specimens(Yamada and Ikeda, 2004). While we did not measure
the body sizes of the amphipods in the extended state,using the scales obtained for each image as a guide,approximate body sizes were estimated. It should also
be noted that we applied ESD to the amphipod bodysize index. Images of the pelagic amphipods captured
in this study are available as electronic supplements(Electronic Supplements 2–15).

H = −NUMBER 00

R. TANIGUCHI ET AL.

DIEL, SEASONAL AND VERTICAL CHANGES IN THE PELAGIC AMPHIPOD COMMUNITIES

1000 m−3 ). T. paciﬁca comprised 85.5% (annual mean)of the amphipod abundance. The next most abundantspecies were P. abyssalis (20.0 ind. 1000 m−3 , 4.7%), Scina
borealis (12.4 ind. 1000 m−3 , 2.9%) and C. challengeri (10.0
ind. 1000 m−3 , 2.4%).
The abundance density of pelagic amphipods at eachsampling depth ranged between 4 and 17 057 ind.
1000 m−3 (Fig. 3). Based on abundance, species diversity(H ) was 0–1.9, and species evenness (J’) was 0–1.0.
Both values were lowest near the surface layer where thesingle species (T. paciﬁca) predominated. During the day,the highest densities were seen at 0–500 m and varied
seasonally. Thus, daytime abundance was high near thesurface in July and October while was stable at 0–500 m
in February and April. In contrast, the highest density
during the night was observed at the shallowest depth (0–50 m) throughout the four seasons. The proportion of thedominant T. paciﬁca was high at 0–500 m during the day,while it was high at 0–100 m during night and was low
below that layer at night. The shallowest depths (0–50 m)
were dominated by T. paciﬁca during both day and night,
which implied low species diversity (H ) and evenness (J’)
in that layer. At depths below 300 m, Koroga megalops, Rhachotropis natator and S. borealis were distributed throughout
the year, with high species diversity (H ) and evenness (J’).
In terms of biovolume, T. paciﬁca was also dominant(annual mean: 2931 mm3 1000 m−3 ), but its annual
mean composition (56.2%) was lower than that of theabundance (Table I). This was due to the dominance ofsmall specimens of this species. For the species showing

performed. Since diel rhythm is available for the feeding
activity of the amphipods (Froneman et al., 2000), weapplied the nighttime D50% (m) as the depths where they
perform the feeding.

RESULTS
Hydrography
Vertical changes in temperature, salinity and DO at St.
K2 during the four sampling dates are shown in Fig. 2.
Throughout the sampling layers and dates, temperature,salinity and DO ranged from 0.7–8.5◦ C, 32.5–34.5 and
0.3–7.5 mL L−1 , respectively. Seasonal thermoclines
developed at depths of ∼50 m in October and July,
while temperatures were homogenous in the upper 100 m
during February and April. For all sampling periods, thetemperature showed a sub-minimum at 100 m and submaximum at 200 m, and then decreased with increasing
depths below them. The salinity increased with increasing
depth throughout the sampling period. Low salinity (<33)
was observed in the upper 50 m in July and October. DO
decreased rapidly from the sea surface to 200 m, wasextremely low (2 mL L−1 ) below 200 m depth and formed
an oxygen minimum layer there.

Pelagic amphipod community
Throughout the year, 10 amphipod species belonging to
10 genera and 8 families occurred (Table I). The mostabundant species was T. paciﬁca (annual mean: 363.9 ind.

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Fig. 2. Vertical distribution of temperature, salinity and DO (DO, O2 ) at St. K2 in the western subarctic Paciﬁc from October 2010 to June 2011.
Circled numbers in the right column indicate sampling layers of oblique tows by IONESS.

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SuborderFamilySpecies

Abundance(ind. 1000 m−3 )(%)

Biovolume(mm3 1000 m−3 )(%)

C. scleroticus

3.9 ± 3.00.9

120 ± 107

2.3

H. galba
T. paciﬁca

1.1 ± 0.6
363.9 ± 289.1

0.3
85.5

141 ± 123
2 931 ± 2 202

2.7
56.2

P. abyssalis

20.0 ± 12.0

4.7

558 ± 235

10.7

S. borealis

12.4 ± 7.1

2.9

87 ± 20

1.7

V. caeca

1.2 ± 0.8

0.3

11 ± 90.2

C. challengeri

10.0 ± 6.4

2.4

588 ± 370

11.3

E. multicalceola
R. natator

1.2 ± 0.8
3.7 ± 2.00.3
0.9

29 ± 27421 ± 459

0.6
8.1

K. megalops

7.4 ± 1.9
0.7

1.7
0.0

313 ± 139
0.40

6.0
0.0

Hyperiidea
Oxycephalidae
Hyperiidae

Phrosinidae
Scinidae
Vibiliidae
Amphilochidea
Cyphocarididae
Eusiridae

Uristidae
OthersFig. 3. Vertical changes in amphipod abundance, species diversity, evenness and species composition at day (upper) and night (lower) at 0–1000 m
depths of St. K2 in the western subarctic Paciﬁc during four occasions (October 2010, February, April and July 2011). Note that scales of abundance
are in log scales.

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Table I: List of pelagic amphipod species occurred for the 0–1000 m water column at St. K2 in the western
subarctic Paciﬁc from October 2010 to July 2011. Annual mean abundance and biovolume (mean ± 1
SE: ind. 1000 m−3 or mm3 m−3 at 0–1000 m water column) and the species composition (%) are alsoshown

R. TANIGUCHI ET AL.

DIEL, SEASONAL AND VERTICAL CHANGES IN THE PELAGIC AMPHIPOD COMMUNITIESSpecies

Abundance (ind. 1000 m−3 )A (30)

C. scleroticus
H. galba
T. paciﬁca
P. abyssalis
S. borealis
V. caeca
C. challengeri
E. multicalceola
R. natator
K. megalops

a

0.1
1.9
1785.9
19.9a
0.3a
3.3
32.4b
0a
0.2a
0.3a

one-way ANOVA

B (8)

C (9)

D (17)

b

a,b

1.2a
0.1
1.8
1.3a
3.8a
0
0a
0.7a
4.6b
10.1b

10.7
2.4
61.9
59.4b
19.4a
3.5
5.4a,b
2.5b
3.7b
6.5b

4.1
0
0
72.1b
95.6b
0
14.9a,b
0a
0a
0a

∗∗∗

NS
NS

∗∗∗
∗∗∗

NS
∗∗

∗∗∗
∗∗∗
∗∗∗

The pelagic amphipod communities varied vertically.
Thus, throughout the season and day–night, only group
A was seen in the upper 0–100 m. For the deepest
layer (500–1000 m), group D was seen throughout theseason and day–night. The occurrence of groups B
and C was observed at intermediate depths of 100–
500 m. In terms of the season, group B was absent inJuly. On the other three sampling occasions, all fourgroups occurred. A diel change was observed in group
C. Thus, group C was speciﬁcally observed at 150–
300 m at night. The PERMANOVA indicated that thethree environmental parameters (day/night, depth andinteraction of day/night × depth) had a signiﬁcanteffect on the separation of each group (P < 0.001)(Electronic Supplement 17). Weak effects from the season
and the interaction of season and depth were also
observed (P < 0.05).
For the 10 amphipod species that occurred at St.
K2, the day–night vertical distributions during thefour seasons of the ﬁve major species and the ﬁveminor species are shown in Figs 6 and 7, respectively.
The vertical distribution center (D50% ) and magnitudeof DVM (D50% [D–N]) are presented in Table III.
Three species (T. paciﬁca, P. abyssalis and C. challengeri)
were distributed at depths of 0–500 m (Fig. 6a–c). For
T. paciﬁca, DVM characterized by nocturnal ascent
was observed for the three seasons (P < 0.05), andthe mean DVM magnitude was computed as 55 m
(Table III). For P. abyssalis, nocturnal ascent of the
DVM was observed in July, but no DVM behavior wasobserved in the remaining three seasons. For C. challengeri,
the nocturnal ascent of DVM was observed during
the three seasons, and their mean DVM magnitude
was 203 m that was the largest among the three
species.

high composition in biovolume, the large-sized two
species: C. challengeri (588 mm3 1000 mm−3 , 11.3%) and P.
abyssalis (558 mm3 1000 mm−3 , 10.7%) were marked. The
biovolume densities of the pelagic amphipods in eachsampling layer ranged between 0.1 and 130 mm3 m−3(Electronic Supplement 16). During the day, the highest
biovolume was observed at depths of 0–500 m and varied
seasonally. However, the highest night-time biovolume
was observed for the shallowest (0–50 m) throughout thefour seasons.
From the cluster analysis based on abundance, thepelagic amphipod community was divided into fourgroups (A–D) with 68% dissimilarity (Fig. 4a). Eachgroup contained 8–30 samples. In NMDS, each group
was plotted in different areas, and all environmental
parameters (temperature, salinity and DO) had a signiﬁcant relationship with the NMDS ordination (Fig. 4b).
For group A, the highest abundance and predominanceof T. paciﬁca (>95%) was characteristic of the group.
Abundances were low in groups B and C; group B was
dominated by T. paciﬁca and P. abyssalis, and P. abyssalis andS. borealis were dominant in group C. The lowest abundance was observed in group D. K. megalops, R. natator andS. borealis were considered the abundant species of group
D. Intergroup differences in abundance were observed
for most groups of pelagic amphipods (Table II). Thus,
C. challengeri was abundant in groups A–C, K. megalops wasmore abundant in groups B and D, P. abyssalis was high ingroups B and C and S. borealis was abundant in group C.

Vertical distribution of each pelagic
amphipod species
The seasonal, vertical and day–night occurrences ofeach pelagic amphipod group are shown in Fig. 5.

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Table II: Comparison of amphipod abundances at four groups (A–D) identiﬁed by Bray–Curtis dissimilarity (cf. Fig. 4). Values are mean abundances at 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, differences insuperscript letters indicate signiﬁcant differences (P < 0.05). Numbers in the parentheses indicate the numberof samples included in each group. ∗∗ : P < 0.01, ∗∗∗ : P < 0.001, NS: not signiﬁcant

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However, the remaining three species (S. borealis, Vibilia
caeca and H. galba) did not occur at the deepest depths ofthis study (750–1000 m) and had a D50% at the intermediate 150–300 m depths (Figs 6d, 7b and d). Among thethree species, S. borealis and H. galba displayed shallower
vertical distribution depths at night because of the smaller
abundance in the samples; it was not signiﬁcant in most of
the cases, and only one season of S. borealis was evaluatedas the nocturnal ascent DVM (Figs 6d and 7d). For V.

Except for the above-mentioned three species, theremaining seven species had no signiﬁcant DVM behavior
in either the whole season or day–night (Figs 6 and 7).
The vertical distribution of the remaining seven species
was classiﬁed into two patterns. Thus, the four species(K. megalops, Cranocephalus scleroticus, R. natator and Eusirella
multicalceola) that occurred at deeper depths (750–1000 m)
had broader vertical distribution depths and D50% at
depths of ∼400–500 m (Table III).

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Fig. 4. (a) Results of cluster analysis based on amphipod abundance at St. K2 in the western subarctic Paciﬁc. Four groups (A–D) were identiﬁed
at 68% Bray–Curtis dissimilarity connected with the complete linkage method. Numbers in the parentheses indicate the number of samples eachgroup contained. (b) NMDS plots of each group. Arrows indicate directions of signiﬁcant environmental parameters. (c) Mean abundance (whitecircle) and species composition of each group.

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DIEL, SEASONAL AND VERTICAL CHANGES IN THE PELAGIC AMPHIPOD COMMUNITIES

Table III: Summary of vertical distribution cores (D50% ) of the 10 amphipod species at St. K2 in thewestern subarctic Paciﬁc during four occasions between October 2010 and July 2011. Day and nightdifferences were tested by Kolmogorov–Smirnov test. ∗ : P < 0.05, ∗∗ : P < 0.01, ∗∗∗ : P < 0.001. Grandmean was calculated based on the data of day and night. Values are means ± SE. Species order was arranged
with the order of the grand mean of daytime D50% . For calculation of the grand mean, the datum shownwith the underline was omitted. - : no occurrence
SpeciesT. paciﬁca
V. caeca
P. abyssalis
H. galba
C. challengeri
S. borealis
E. multicalceola
C. scleroticus
R. natator
K. megalops

29 October 2010

26 February 201122–23 April 2011

3–4 July 2011

Grand mean (m)

Day

Night

Day

Night

Day

Night

Day

Night

Day

Night

D50% (D–N)

45
184
262
314
235
390
412
407
548
557

28∗

162
165
53
875
267
404
492
388
579
590

30∗

101
125
166
131
400
381
415
400
500
486

33∗∗

27
162
241
321
236
401
400
625
420
531

25
107
161∗∗∗
208
58∗∗
243
438
242
400
467

84 ± 26
159 ± 11181 ± 41255 ± 44285 ± 34394 ± 5430 ± 18455 ± 49512 ± 30541 ± 1929 ± 1133 ± 12176 ± 7134 ± 2682 ± 19261 ± 10492 ± 39330 ± 39488 ± 62527 ± 20

55
26
5
121
203
133
−62
125
24
14

164
192
103
60∗∗∗
252∗∗
429
391
533
576

129
186
92
62∗∗∗
293
625
422
670
526

166
149
254
477
266
350
540

caeca, their D50% was at restricted depths of 107–184 m(Table III) throughout the season and day–night (Fig. 7b).

and highest values were observed for C. challengeri and
R. natator, respectively (Fig. 8). Common for pelagic
amphipods, δ 15 N values were lower for the shallower
dwelling species and higher for the deeper dwelling
species. These depth-related trends in δ 15 N values
implied a signiﬁcant relationship between δ 15 N and nighttime habitat depth (D50% ): δ 15 N = 0.00904 × nighttime
D50% + 8.028 (r2 = 0.542, P < 0.0001, Fig. 8). While such

Nitrogen stable isotope (δ 15 N) of each pelagic
amphipod species
The δ 15 N values of each pelagic amphipod species at
St. K2 ranged between 6.8 and 14.0%, and the lowest

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Fig. 5. Seasonal, vertical and diel changes in the occurrence of the four amphipod community groups (A–D) identiﬁed by Bray–Curtis dissimilarity
based on their abundance (cf. Fig. 4a) at St. K2 in the western subarctic Paciﬁc during October 2010 to July 2021. D: day, N: night.

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Fig. 6. Day (open, left) and night (solid, right) vertical distribution of the ﬁve amphipod species (arranged with the order of abundance, cf. Table II):T. paciﬁca (a), P. abyssalis (b), C. challengeri (c), S. borealis (d) and K. megalops (e) at St. K2 in the western subarctic Paciﬁc during four sampling occasions
between October 2010 and July 2011. Triangles represent vertical distribution cores (D50% ). Diel changes were tested by Kolmogorov–Smirnov
test. ∗ : P < 0.05, ∗∗ : P < 0.01, ∗∗∗ : P < 0.001.

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Fig. 7. Day (open, left) and night (solid, right) vertical distribution of the ﬁve amphipod species (arranged with the order of abundance, cf. Table II):
C. scleroticus (a), V. caeca (b), R. natator (c), H. galba (d) and E. multicalceola (e) at St. K2 in the western subarctic Paciﬁc during four sampling occasions
between October 2010 and July 2011. Triangles represent vertical distribution cores (D50% ). Diel changes were tested by Kolmogorov–Smirnov
test. ∗ : P < 0.05, ∗∗ : P < 0.01, ∗∗∗ : P < 0.001.

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Fig. 8. Scatter plot between δ 15 N and grand mean of nighttime D50%of the 10 amphipod species at St. K2 in the western subarctic Paciﬁc.
Differences in symbols denote signiﬁcant differences in δ 15 N values (oneway ANOVA and Tukey–Kramer test). The line was regression based on
the whole species data. The shaded area represents a 95% conﬁdence
interval. T.p.: T. paciﬁca, C.c.: C. challengeri, H.g.: H. galba, V.c.: V. caeca,
P.a.: P. abyssalis, S.b.: S. borealis, C.s.: C. scleroticus, R.n.: R. natator, E.m.:
E. multicalceola, K.m.: K. megalops.

depth-related patterns were present, the δ 15 N values ofsome species were outside the 95% conﬁdence limit.
Thus, low δ 15 N values were observed in C. challengeri
and H. galba. For the high δ 15 N values, three species,
T. paciﬁca, V. caeca and R. natator, exhibited similar
patterns.

Population structure of the dominant
T. paciﬁca
ESD of T. paciﬁca was at 0.2–9.0 mm (Fig. 9a). For ESD ineach sampling period, two–three cohorts were identiﬁed.
The recruitment of the small-sized ESD was observed fortwo periods (October and April). The subsequent growthof each cohort was traceable for 9 months (October–July) or 1 year (April–April). The population structuresin February and April, with the small abundances of thesmall-sized ESD specimens, were characterized by thedominance of mature females and males (Fig. 9b). On
the other hand, juveniles composed more than half anabundance in July and October.

DISCUSSION
Community structure
There were three notable characteristics of the pelagic
amphipod community in this study. First, both abundanceand biovolume showed the highest values at the shallowest

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depths of 0–50 m at night, which is comparable with theother region (Espinosa-Leal et al., 2020). Secondly, thecommunity structure showed diel changes, particularly
at depths of 150–300 m. At that depth, the community
was dominated by T. paciﬁca during the day, whereas thecomposition of T. paciﬁca substantially decreased during
nighttime, and the composition of the other species thatremained stable occurred at the depth without increased
DVM. Such DVM behavior of T. paciﬁca in this region
has been reported (Yamada et al., 2004). Third, species
diversity had high values at 300–500 m during bothday and night. These depths are comparable with theother regions (Roe et al., 1984; Espinosa-Leal et al., 2020).
Among the three characteristics, the ﬁrst two are causedby the DVM behavior of T. paciﬁca, the dominant species
in both abundance and biovolume. The DVM behaviorof T. paciﬁca and T. japonica is well documented in the western subarctic Paciﬁc (Yamada et al., 2004; Hanamiya et al.,2020) and Japan Sea (Ikeda et al., 1992). Furthermore, thenocturnal ascent DVM of T. paciﬁca induces a decrease in
its composition at depths of 150–300 m during the night,
which causes diel changes in the community structure atthat layer. Finally, because both deep-water species andupper-layer species occurred at 300–500 m, the species
diversity may have peaked at that layer.
Evaluation of the separation of the pelagic amphipod
community into four groups (A–D) is also a notableﬁnding of this study (Fig. 4). The numbers of thepelagic amphipod community classiﬁcation have wellcorresponded with those in the worldwide oceans(Lavaniegos and Hereu, 2009; Burridge et al., 2017;
Espinosa-Leal et al., 2020; 2021). In this study, groupA, dominated by T. paciﬁca, was observed down to
300 m during the day, while their occurrence depth
was restricted to <150 m during the night. T. paciﬁca
dominated the pelagic amphipod community, comprising
86 and 56% of the total abundance and biovolume,
respectively. Thus, their dominance and DVM behavior(Yamada et al., 2004) alter the amphipod community.
At 150–300 m depth at night, group C, dominatedby S. borealis and P. abyssalis instead of T. paciﬁca, wasobserved. This is due to the upward migration of T.
paciﬁca at night, then the community at 150–300 m iscomposed of the remaining species at the depth during
the night. Deeper distribution of P. abyssalis than those of
T. paciﬁca has been reported (Ikeda, 1995; Yamada et al.,2002). The depths with high species diversity (300–500 m)
corresponded well with the depths of various zooplankton
communities (B, C and D). For groups B and D, thevertical distribution depths of the dominant species, E.
multicalceola, R. natator and K. megalops, corresponded wellwith those of a previous study (Barnard, 1964).

R. TANIGUCHI ET AL.

DIEL, SEASONAL AND VERTICAL CHANGES IN THE PELAGIC AMPHIPOD COMMUNITIES

Vertical distribution of each speciesof P. abyssalis and C. challengeri at St. K2 have also been
documented in a previous study (Steinberg et al., 2008).
Within the 10 pelagic amphipods presented in thisstudy, associations with gelatinous zooplankton have beenreported for all three species. Thus, Scina spp. have beenreported to attach to jellyﬁshes (Madin and Harbison,
1977; Gasca et al., 2007), Vibilia spp. have been reported
to attach to salps (Harbison et al., 1977; Gasca et al., 2007;
Quigley et al., 2015), and H. galba has also been reported
to attach to jellyﬁshes (Madin and Harbison, 1977; Gasca
et al., 2007; Quigley et al., 2015). The D50% of these three

As new ﬁndings of this study, evaluation of the dielvertical distribution and magnitude of DVM for all
10 amphipod species is also important (Figs 6 and
7). For dominant amphipod species, DVM behavior
characterized by nocturnal ascent has been reported
for T. paciﬁca/japonica (Ikeda et al., 1992; Yamada et al.,2004), P. abyssalis (Ikeda et al., 1995; Yamada et al., 2002)
and C. challengeri (Yamada and Ikeda, 2000). Among thethree species, the magnitude of the DVM was the largest(203 m) for C. challengeri (Table III). The DVM behaviors

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Fig. 9. Seasonal changes in the histogram on ESD (a) and developmental stage composition (b) of T. paciﬁca at St. K2 in the western subarctic
Paciﬁc. The triangles in (a) show the means of each cohort in ESD, and solid and open triangles represent possible differences in generations.
Numbers in the parentheses in (a) indicate the number (n) of captured images.

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As feeding modes of these species, small-sized juvenilesof Themisto spp. are reported to become carnivores as theygrow (Sugisaki et al., 1991; Pakhomov and Perissinotto,
1996; Froneman et al., 2000; Haro-Garay, 2003). Thus,
based on gut pigment and δ 15 N values, Sugisaki et al.
(1991) reported that the feeding modes of T. japonica
change from herbivores to carnivores as they grow. For C.
challengeri, carnivorous (Haro-Garay, 2003) or scavenging(Yamada and Ikeda, 2003) feeding modes have been
proposed. H. galba has been reported to be associatedwith jellyﬁsh (Madin and Harbison, 1977; Gasca et al.,2007; Fleming et al., 2014; Espinosa-Leal et al., 2021).
Associations with salps have been reported for V. caeca(Harbison et al., 1977; Roe et al., 1984; Gasca et al., 2007;
Quigley et al., 2015). R. natator is reported to be distributedat depths of 930–5500 m in the Gulf of Alaska (Barnard,1964).
Thus, while the δ 15 N values of the pelagic amphipods
showed a clear depth-related relationship, the feeding
modes of the species plotted out of the regression did
not correspond with the reported feeding modes of eachspecies. As an alternative explanation, the δ 15 N valuesof the species with exoskeletons are reported to havelower values of the exoskeleton, whereas internal tissues
may have relatively high δ 15 N values, and the internal
tissue values may express the feeding modes of eachspecies. Therefore, the low δ 15 N values observed for C.
challengeri and H. galba might reﬂect the development of
the exoskeleton of these species, while the high δ 15 N
values of T. paciﬁca, V. caeca and R. natator might reﬂect
the thinner exoskeleton of these species. Because of thesmaller body sizes of the target species, we did not separate the exoskeleton and internal tissues in this study
for measurement of δ 15 N values that is termed the “bulkmethod” for the pelagic amphipods (Søreide and Nygård,2012). Thus, for evaluation of the exact trophic levels,
measurements that separate the exoskeleton and internal
tissue, and measurement of δ 15 N only on the internal
tissue might be required for pelagic amphipods in futurestudies.

Nitrogen stable isotopes (δ 15 N)
The nitrogen stable isotopes (δ 15 N) of the pelagic
amphipods have a linear depth-related relationship:
they increase with increasing depth (Fig. 8). δ 15 N is anindex of the trophic level, and their differences of 3–4%
suggest differences in trophic levels (Aita et al., 2011). The
depth-related increase in δ 15 N of mesozooplankton has
been reported for the Mediterranean and the ArabianSea. Moreover, δ 15 N values near the surface layer (2%)
are reported to increase ∼12% at 4000 m, and it
is interpreted that the particulate organic materials
reach deeper depths through several-time prey-predationinteractions (Koppelmann and Weikert, 2000; 2003;
Koppelmann et al., 2009).
Bearing this in mind, the depth-increasing patterns
observed for δ 15 N in the pelagic amphipods in this study
may be related to the accumulation of prey-predationinteractions that may increase with increasing depth.
Interestingly, several amphipod species had extremely
low (C. challengeri and H. galba) or high (T. paciﬁca, V.
caeca and R. natator) δ 15 N values than the regression line
(Fig. 8). Since the δ 15 N values are indices of trophic levels,
the former species may have a herbivorous tendency,
whereas the latter species would have a carnivorous
tendency.

Population structure of the dominant
speciesIn the present study, using the images captured by
ZooScan, developmental stages of the dominant amphipod species, T. paciﬁca, were identiﬁed, and histogram
drawing applying the ESD as an index of the bodysize of the individuals, and cohort analyses on the ESD
were possible (Fig. 9). Because of their rounded body
shapes, body size measurements of pelagic amphipods
are time-consuming. However, with the initially sorted
taxa samples, captured zooplankton images and species

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species occurred mainly at 150–300 m (Table III). These
three species did not occur at the sea surface or the deepest
depths in this study, and their vertical distribution patterns
were classiﬁed for the same, occurring at intermediate
depths (Figs 6d, 7b and d).
The zooplankton biomass of each taxon used in
the samples in this study has been previously reported(Kitamura et al., 2016). The day/night vertical distributions of radiolarians/phaeodarians, cnidarians andthaliaceans reported by Kitamura et al. (2016) are shown
in Electronic Supplement 18. The D50% of the abovementioned three species was 133–159 m (V. caeca), 134–
255 m (H. galba), 261–394 m (S. borealis) and shallower
at night (Table III). The D50% of cnidarians was 102–
154 m and that of thaliaceans was 200–250 m. Thus,
the vertical distributions of the host and three amphipod
species nearly correspond. However, clear associations
between them (i.e. occurrence of amphipod species ingelatinous zooplankton) were not observed in this study. It
is possible to drop off the amphipods from the gelatinous
zooplankton during oblique net towing of IONESS. To
evaluate the intensity of pelagic amphipod attachment
on gelatinous zooplankton, an in-situ observation system
made by nondestructive visual devices such as a video
plankton recorder may be a suitable instrument for thispurpose (Takahashi et al., 2013; 2015a; b).

NUMBER 00

R. TANIGUCHI ET AL.

DIEL, SEASONAL AND VERTICAL CHANGES IN THE PELAGIC AMPHIPOD COMMUNITIESACKNOWLEDGEMENTS
The zooplankton samples used in this study were collected from theR/V Mirai of the JAMSTEC. We appreciate Dr Hiromichi Ueno forproviding valuable guidance on the water mass classiﬁcation.

SUPPLEMENTARY DATA
Supplementary data can be found at Journal of Plankton Research online.

FUNDING
Part of this study was supported by Grant-in-Aid for Challenging
Research (Pioneering) 20 K20573, Scientiﬁc Research 22H00374 (A),
20H03054 (B) and 19H03037 (B) from the Japan Society for the Promotion of Science (JSPS). This study was partially conducted for the Arctic
Challenge for Sustainability II (ArCS II; JPMXD1420318865). This
research was also supported by the Environment Research and Technology Development Fund (JPMEERF20214002) of the Environmental
Restoration and Conservation Agency of Japan.

DATA AVAILABILITY
Data will be provided upon request from the corresponding author.

REFERENCES
Aita, M. N., Tadokoro, K., Ogawa, N. O., Hyodo, F., Ishii, R., Smith,
S. L., Saino, T., Kishi, M. J. et al. (2011) Linear relationship between
carbon and nitrogen isotope ratios along simple food chains inmarine environments. J. Plankton Res., 33, 1629–1642. https://doi.org/10.1093/plankt/fbr070.

CONCLUSION
This study revealed the ecology of pelagic amphipods
in the western subarctic Paciﬁc by applying imagescanned data of the sorted pelagic amphipod samples
from the day/night samples collected between 0 and1000 m depths on four occasions covering 1 year.
Through the analytical methods used in this study,
the abundance, biovolume and community structureof pelagic amphipods were evaluated. In addition,
the day/night vertical distribution patterns of all 10
amphipod species were evaluated and classiﬁed into

Barnard, J. L. (1964) Some bathyal Paciﬁc Amphipoda collected by the
U.S.S. Albatross. Pac. Sci., 18, 315–335.
Bray, J. R. and Curtis, J. T. (1957) An ordination of the upland forest
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three patterns. For the most dominant pelagic amphipod
species (T. paciﬁca), estimation of life cycle patterns is
possible by using ESD data as an index of body size.
Vertical changes in δ 15 N of all species are novel attempts
and ﬁndings in this ﬁeld. For example, the alternative
nitrogen stable isotope (δ 15 N) analyses showed increasesin δ 15 N values with increasing habitat depths at night.
In this study, imaging analyses of the sorted samples
with taxa were helpful for species identiﬁcation, size
quantiﬁcation and estimation of the accurate biovolumeof each individual.

or stage identiﬁcation performed on the images, they
are relatively easy and rapidly analyzed (Irisson et al.,2022). Thus, this study showed the usefulness of ZooScan
analyses for community and population structure analysesof dominant zooplankton taxa. When sorted samples
on each taxon are available, ZooScan analysis allows
us to obtain each species’ abundance and biomass(biovolume) data by capturing images. The biovolume
is easily converted to ESD, which is used as an index ofbody size. It should be noted that the numbers in bodysize measurements in Fig. 9a were maximum of 1138
individuals per one occasion. Measuring their body lengthwith a microscope is very time-consuming, and accuracy
and precision may be similar to those of the ZooScan
data (Gorsky et al., 2010). Because of these reasons, theusefulness of ZooScan using sorted samples on speciﬁctaxon is easily understood.
For the population structure data of T. paciﬁca, the main
recruitment of juveniles was observed in July–Octoberwhich corresponded to the period in the Oyashio region(Yamada et al., 2004). While each cohort of ESD seems
to be traceable from small juveniles to adults, it should
be noted that the population structure analyses based on
the more frequent sampling interval (16 times per 2 years:
8 times per year) showed that the recruitment of young
T. paciﬁca in the Oyashio region and their generation
length varies with temperature, and 32 days at 12◦ C
and 224 days at 2◦ C have been reported (Yamada et al.,2004). Considering these time scales, the rough samplinginterval of this study (four times per year) may make it
difficult to accurately trace the cohort of T. paciﬁca inthis region. Thus, while the cohort trace of this study
in Fig. 9 is doubtful, the sampling interval of the timeseries samples applied for this study is not adequate; if
the samplings were conducted at a sufficient time interval,
population structure analyses using ZooScan may provide
solid insight into their life cycles. Thus, this study indicatesthe usefulness of ZooScan for community and population
structure analyses of certain zooplankton taxa.

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BF00349122.

Espinosa-Leal, L., Escribano, R., Riquelme-Bugueño, R. and CorredorAcosta, A. (2021) Distribution and biodiversity patterns of hyperiid
amphipods across the coastal–offshore gradient of the sub–tropicalSoutheast Paciﬁc. Mar. Biodivers., 51, 13. https://doi.org/10.1007/
s12526-020-01152-x.

Ikeda, T., Hirakawa, K. and Imamura, A. (1992) Abundance, population structure and life cycle of a hyperiid amphipod Themisto japonica(Bovallius) in Toyama Bay, southern Japan Sea. Bull. Plankton Soc.
Japan, 39, 1–16.
Ikeda, T. and Shiga, N. (1999) Production, metabolism and production/biomass (P/B) ratio of Themisto japonica (Crustacea: Amphipoda)in Toyama Bay, southern Japan Sea. J. Plankton Res., 21, 299–308.
https://doi.org/10.1093/plankt/21.2.299.

Fleming, N. E. C., Harrod, C., Griffin, D. C., Newton, J. and Houghton,
J. D. R. (2014) Scyphozoan jellyﬁsh provide short–term reproductive
habitat for hyperiid amphipods in a temperate near–shore environment. Mar. Ecol. Prog. Ser., 510, 229–240. https://doi.org/10.3354/
meps10896.

Irisson, J. O., Ayata, S. D., Lindsay, D. J., Lee, K. B. and Stemmann,
L. (2022) Machine learning for the study of plankton and marine
snow from images. Annu. Rev. Mar. Sci., 14, 277–301. https://doi.org/10.1146/annurev-marine-041921-013023.

Froneman, P. W., Pakhomov, E. A. and Treasure, A. (2000) Trophic
importance of the hyperiid amphipod, Themisto gaudichaudi, in the
Prince Edward archipelago (Southern Ocean) ecosystem. Polar Biol.,23, 429–436. https://doi.org/10.1007/s003000050464.

Kitamura, M., Kobari, T., Honda, M. C., Matsumoto, K., Sasaoka, K.,
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