Polar Biology
https://doi.org/10.1007/s00300-023-03174-0

ORIGINAL PAPER

Interannual and spatial variation in small zooplankton off Vincennes
Bay, East Antarctica
Aiko Tachibana1· Yuri Ohkubo1 · Kohei Matsuno2 · Keigo D. Takahashi3 · Ryosuke Makabe1,3,4 · Masato Moteki1,4Received: 2 May 2022 / Revised: 9 June 2023 / Accepted: 28 June 2023
© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2023

Abstract
Although small zooplankton are an important component of both the classical food web and microbial loop, fundamental
information about small zooplankton in the Southern Ocean is lacking. This study presents the interannual and horizontal
variabilities of small zooplankton and the population structure of the key small copepod species Ctenocalanus citer off Vincennes Bay, East Antarctica. Zooplankton were sampled with a 100 µm mesh net during austral summer from 2016 to 2018.
Small copepods numerically dominated all samples, with Oithona spp., Oncaeidae, C. citer and nauplii being particularly
abundant (> 75% of total zooplankton abundance). Community structure analysis revealed annual and latitudinal changes in
the community, which were driven by the timing of sea-ice retreat and associated with the phytoplankton bloom. The population structure of C. citer showed variability not only with latitude but also between eastern and western areas. The watertemperature gradient formed by cyclonic eddies likely influences the developmental period of C. citer, thereby generating
the east–west difference in population structure. Spatial differences in the population structure of copepods attributable tocyclonic eddies are likely common during summer in East Antarctica. Our results demonstrate that the development of C.
citer population structure is synchronised with short-term fluctuations in phytoplankton size composition following sea-ice
retreat, suggesting that the phytoplankton bloom is efficiently used for population growth in the seasonal ice zone. These
data suggest that small zooplankton respond rapidly to local environmental changes.
Keywords Ctenocalanus citer · Phytoplankton bloom · Sea-ice retreat · Small zooplankton · Vincennes eddy

Introduction
Small copepods (< 1.5 mm) are abundant in the zooplankton
community and are important links in marine food webs
(Turner 2004). Nevertheless, most research on zooplankton
abundance and distribution has been based on net samples,* Aiko Tachibana
atachi0@kaiyodai.ac.jp
1

Department of Ocean Sciences, Tokyo Universityof Marine Science and Technology, 4‑5‑7 Konan, Minato,
Tokyo 108‑8477, Japan

2

Faculty/Graduate School of Fisheries Sciences,
Hokkaido University, 3−1−1 Minato‑Cho, Hakodate,
Hokkaido 041‑8611, Japan3

Department of Polar Science, Graduate University
for Advanced Studies, SOKENDAI, 10‑3 Midori‑Cho,
Tachikawa, Tokyo 190‑8518, Japan

4

National Institute of Polar Research, 10‑3 Midori‑Cho,
Tachikawa, Tokyo 190‑8518, Japanin which the mesh sizes are often too coarse to capture small
copepods (≥ 200 µm). Hence, this group is significantly
underestimated in most current and historical datasets (Gallienne and Robins 2001; Turner 2004; Pansera et al. 2014).
In the Southern Ocean, small cyclopoid (Oithona, Oncaeidae) and calanoid (Clausocalanus, Microcalanus) copepods,
as well as juvenile forms of larger copepods, are abundant in
the micro- and meso-sized zooplankton communities (Hopkins and Torres 1988; Schnack-Schiel et al. 2008; Stevens
et al. 2015; Ojima et al. 2015; Takahashi et al. 2017; Makabe
et al. 2017), although fine-mesh plankton nets (100–200 µm
mesh size) have rarely been used to study the zooplankton
community.
Small zooplankton link lower and higher trophic levels
via both the microbial loop and the classical food chain(Turner 1984; Atkinson 1998). Feeding by small copepod
species on the phytoplankton, protozoans and zooplankton
within the epipelagic layers of the Southern Ocean controls
lower trophic levels and carbon uptake efficiency (Atkinson
1996; Dubischar et al. 2002; Smetacek et al. 2004; Halfter

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et al. 2020). In addition, zooplankton respond rapidly toenvironmental change, and their community structure andabundance are influenced by organisms at higher trophic levels through the food chain (Atkinson et al. 2012). Therefore,
investigating the zooplankton community, including small
copepods, is essential for elucidating the ecosystems andbiogeochemical cycles in the Southern Ocean.
Ecosystem dynamics in the seasonal ice zone (SIZ) are
driven by the Antarctic Circumpolar Current (ACC) andrelated frontal systems, as well as the annual advance andretreat of sea ice (Hunt and Hosie 2005; Massom and Stammerjohn 2010; Nicol and Raymond 2012). The macro-zooplankton community, including krill and large copepods,
changes with the position of these frontal systems (Huntet al. 2007; Ward et al. 2012b; Tachibana et al. 2017). In particular, the distribution patterns of some large zooplankton
species are affected by the position of the southern boundary(SB) of the ACC (Hunt et al. 2007; Tanimura et al. 2008).
Small zooplankton communities are affected by sea-ice
dynamics associated with the seasonal phytoplankton bloom(Takahashi et al. 2017; Makabe et al. 2017). Higher primary
production at sea-ice edges (ice-edge blooms) observed during sea-ice retreat in spring and summer generally affects thedevelopment of small copepods, such as Ctenocalanus citerand Oithona similis (Atkinson 1998). The timing of sea-ice
melting and the occurrence of phytoplankton blooms varyinterannually and are subject to climate change (MontesHugo et al. 2009; Stammerjohn et al. 2012; Rohr et al.
2017). However, information about the interannual variability of the small zooplankton community related to sea-ice
dynamics is scarce.
Among the small zooplankton communities in the Southern Ocean, C. citer is a common species distributed in theupper 200 m during summer (e.g. Schnack-Schiel and Mizdalski 1994; Schnack-Schiel 2001). The reproductive period
begins in early spring, and the seasonal vertical migration
occurs during the spring–summer transition (Schnack-Schiel
and Mizdalski 1994). Although regional differences in thetiming of their seasonal ascent behaviour are observed off
Lützow-Holm Bay in the Indian Ocean sector during summer, the factors affecting these differences have not been
elucidated (Makabe et al. 2017). Furthermore, the relationship between phytoplankton abundance by the size fraction
and distribution of C. citer, which prefers smaller (< 10 µm)
phytoplankton (Pasternak and Schnack-Schiel 2007) is lessdocumented. Information on the spatial variability of the
population structure and vertical distribution in relation toenvironmental factors, including prey size composition, arelimited, although this species is potentially important in theSouthern Ocean ecosystem.
We conducted transect observations in January
2016–2018 in the SIZ along the 110°E meridian off Vincennes Bay, East Antarctica (Fig. 1). The transect is spanned

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by major fronts, namely, the SB of the ACC and the Southern ACC Front (SACCF). In addition, a series of cycloniceddies occurs off Wilkes Land, East Antarctica (Mizobata
et al. 2020). This eddy circulation transports warm circumpolar deep water (CDW) poleward on the eastern side of theeddy, and transports cold water equatorward on the westernside (Mizobata et al. 2020). This means that this physicalprocess forms, not only north–south, but also east–west
water temperature gradients in the water where the eddy islocated. Characteristics of these local oceanographic circulation patterns may influence the small copepod community
and its population structure; however, little is yet known
about the effects of these local hydrographic structures. This
study investigated the annual and spatial variation in community structure of small zooplankton in the SIZ to clarify
the influence of local eddies and sea-ice dynamics on that
community. In addition, for the key small calanoid copepod
C. citer, environmental variables, including the influence of
local eddies, were examined to explain the spatial variationin their population structures, providing information about
the life cycle strategies of copepods in the Southern Ocean.

Materials and methods
Field sampling and environmental data collection
Zooplankton were sampled from a transect along 110°E in
the SIZ off Vincennes Bay during three voyages each January from 2016 to 2018 aboard the training vessel Umitakamaru of the Tokyo University of Marine Science and Technology (Fig. 1). During the 2016 voyage, vertical tows from
200 to 0 m depth at a speed of approximately 1 m ­s−1 usinga Norpac net (100 µm mesh size, 45 cm mouth diameter)with an attached flow meter (Rigo Co. Ltd.) were conducted.
For sampling in 2017 and 2018, a vertical multiple plankton
sampler (VMPS, Tsurumi-Seiki Co. Ltd.) with a 0.25 ­m2mouth area and 100 µm mesh was used. Discrete depth samples were collected from three (200–100, 100–50, 50–0 m)
or four layers (200–150, 150–100, 100–50, 50–0 m) using a
multiple-net opening/closing system at a speed of approximately 1 m ­s−1 (Table 1). The filtered volume was determined using a digital flow meter installed on the net system.
In 2017, a latitudinal transect of seven stations along 63.5°S,
crossing the Vincennes eddies, was sampled to investigate
the interactions of zooplankton community structure withoceanographic conditions. Hydrographic information, particularly regarding eddies in 2017 along the latitudinal transect, was described by (Mizobata et al. 2020). A total of 21
zooplankton samples (including six samples using a Norpac
net in 2016 and 15 samples using a VMPS in 2017 and 2018)
were collected and immediately preserved with buffered 5%formaldehyde and seawater solution. Although the net mouthPolar Biology
Fig. 1  Zooplankton sampling
locations off Vincennes Bay,
East Antarctica, in Januaryfrom 2016 to 2018. a Overall
view of Antarctica, with extent
of image b indicated by blue
square. b Map of the study area.
Legends (pulses, red circles
and blue triangles) indicate thesampling location in each year.
Green x indicates CTD stations.
Circulation arrows denote theVincennes eddy, drawn withreference to Mizobata et al.
(2020)

area was slightly larger in the latter between the Norpac net
and the VMPS (0.16 vs. 0.25 ­m2, respectively), we assumed
that there was no difference in net avoidance of small zooplankton because the same mesh size (100 µm) and towing
speed were used. Therefore, we considered that biases due
to differences in sampling methods would be negligible, andused the data collected by the Norpac net and the VMPS
together in the analysis of interannual variability of the small
zooplankton community. Additional information is provided
in Online Resources 1 and 2.
Vertical temperature and salinity profiles were obtainedusing a conductivity, temperature and depth profiler system(CTD; SBE 9plus, Sea-Bird Electronics, Bellevue, WA,USA) at all sampling stations. Detailed information on the
CTD data is available in the reports of the Polar Data Journal(Shimada et al. 2020) and the Polar Science Data Archives(JARE57; http://​polar ​is.​nipr.​ac.​jp/​~parc/​usr/​di_​list.​php?​
pid=2​ 71). The Southern Ocean is characterised by the ACC,
which separates different water masses (Orsi et al. 1995).
The positions of the oceanic fronts were determined froman underwater environmental monitoring system (ETSG 2
Thermosalinograph, Falmouth Scientific, Inc., Procasset,

MA, USA) in combination with the CTD data, following
the definitions of (Orsi et al. 1995) and (Sokolov and Rintoul
2002). We defined the region north of the northern branch of
the Southern ACC front (SACCF-N) as the Northern Antarctic Zone (AZN), the region between the SACCF-N andthe southern boundary of the ACC as the Southern Antarctic
Zone (AZS) and the region south of the southern boundaryof the ACC as the SB, according to (Hunt and Hosie 2005).
The surface mixed layer depth (MLD) at each location wasdetermined according to the criteria of (Aoki et al. 2006).
Water samples were collected with a CTD multi-bottlerosette sampler equipped with 24 12-L Niskin bottles (General Oceanics, Miami, FL, USA) at all sampling stations
and then filtered through membrane filters (pore sizes 10
and 2 µm) and onto grass-fibre filters (Whatman GF/F) toobtain > 10 (Chl_10), 2–10 (Chl_2) and < 2 µm (GF/F) size
fractions, respectively. Chlorophyll a (chl a) was extractedwith N,N-dimethylformamide (Suzuki and Ishimaru 1990),
and its concentration was determined using a Turner fluorometer (AU-10, Turner Designs, San Jose, CA, USA).
Detailed information on chl a is available in the reports of
the Polar Data Journal (Makabe et al. 2019, 2020). Ice-free

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KC5
C02
C03
C04
C05
KC6
KC5
KM4
C03
C05
C06
C07
KC6
C09
C10
C11
C14
C15
KC5
B01
KC6

16_60S
16_61S
16_62S
16_63S
16_64S
16_65S
17_60S
17_61S
17_62S
17_63S
17_63.5S110E
17_64S
17_65.5S
17_106E
17_107E
17_108E
17_111E
17_112E
18_60S
18_63.5S
18_65S23-01-2016
24-01-2016
25-01-2016
25-01-2016
26-01-2016
27-01-2016
07-01-2017
08-01-2017
09-01-2017
16-01-2017
17-01-2017
10-01-2017
11-01-2017
13-01-2017
14-01-2017
15-01-2017
18-01-2017
19-01-2017
08-01-2018
10-01-2018
11-01-2018

Data (UTC)60.00061.00062.00063.00164.00064.97359.99960.99662.00063.00063.47564.25065.28463.49363.49863.50063.50063.50059.99963.49864.690Latitude (S)110.002110.002110.001
109.993109.998
109.018110.005
110.005
110.001
109.996109.980109.999109.998105.966
106.996107.997111.329112.662110.000
110.049
109.877

Longitude (E)

AZN
AZS
AZS
AZS
SB
SB
AZN
AZN
AZS
AZS
AZS
SB
SB
SB
SB
SB
AZS
AZS
AZN
AZS
SB

Zone

0.61
0.74
0.59
0.65
0.03
− 1.69
0.80
0.37
0.49
0.52
0.43
− 0.50− 1.13− 0.35− 0.61− 0.88
0.89
0.66
0.62
0.56
− 1.56

Temp200

33.7
33.6
33.3
33.5
33.4
32.9
33.7
33.7
33.7
33.5
33.6
33.9
33.7
33.6
33.6
33.7
33.7
33.6
33.6
33.6
33.1

Sal200

0.66
0.34
0.23
0.55
1.37
0.92
0.06
0.05
0.09
0.04
0.05
0.59
0.10
0.06
0.08
0.04
0.05
0.08
0.66
0.15
0.09

Chl_10
0.17
0.15
0.20
0.17
0.21
0.66
0.05
0.05
0.06
0.04
0.05
0.01
0.13
0.05
0.07
0.08
0.04
0.05
0.11
0.02
0.36

Chl_2
0.05
0.04
0.04
0.07
0.04
0.10
0.02
0.03
0.03
0.03
0.03
0.16
0.05
0.02
0.04
0.06
0.02
0.03
0.03
0.25
0.05

GF/F

Size-fractionated chlorophyll aof surface

69
55
48
41
30
26
41
36
29
40
39
51
30
38
30
36
38
38
47
34
12

MLD

93
112
83
77
45
21
97
62
63
66
67
51
0
51
54
61
62
63
98
44
29

IFD

NORPACNORPACNORPACNORPACNORPACNORPAC
VMPS
VMPS
VMPS
VMPS
VMPS
VMPS
VMPS
VMPS
VMPS
VMPS
VMPS
VMPS
VMPS
VMPS
VMPS

Gear

0–200
0-200
0-200
0-200
0-200
0-200
0-50-100-200
0-50-100-200
0-50-100-200
0-50-100-150-200
0-50-100-150-200
0-50-100-200
0-50-100-200
0-50-100-200
0-50-100-200
0-50-100-200
0-50-100-150-200
0-50-100-150-200
0-50-100-150-200
0-50-100-150-200
0-50-100-150-200

Layer

AZN Northern Antarctic Zone, which was located north of the northern branch of the Southern ACC front (SACCF-N); AZS Southern Antarctic Zone, which was located between the
SACCF-N, the southern boundary of the ACC; SB South of the Southern Boundary, Temp200 = Average water temperature from 0 to 200 m, Sal200 = Average water salinity from 0 to 200 m,
Chl_10 =  > 10 µm chlorophyll a concentration, Chl_2 = 10–2 µm chlorophyll a concentration, GF/F =  < 2 µm chlorophyll a concentration, MLD = surface mixed layer depth (m) and IFD = Icefree days at each location was defined as the number of days after the sea-ice concentration became less than 20%

StationSample name

Table 1  List of sampling locations and their environment information

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days (IFDs) at each location were defined as the numberof days after the sea-ice concentration (SIC) became lessthan 20%. Daily SIC data were determined using a bootstrap algorithm (Comiso et al. 1984; Comiso 1986) fromthe Advanced Microwave Scanning Radiometer 2 (AMSR2),
obtained from the Japan Aerospace Exploration Agency
website (http://s​ uzaku.e​ orc.j​ axa.j​ p/G​ COM_W/d​ ata/d​ ata_w_​
use.​html). Daily mean SIC data were mapped on a polarstereographic grid with a spatial resolution of 10 km and a
0.1° × 0.1° Mercator grid.

Laboratory procedures
All zooplankton samples were split into two aliquots usinga Motoda plankton splitter (Motoda 1959) in the laboratory,
one of which was used for further analysis. Large specimens(≥ 1.5 mm total length, i.e. Calanoides acutus, Calanus propinquus, Calanus simillimus, Metridia gerlachei, Metridia
lucens, Rhincalanus gigas and other large zooplankton;
Cnidaria, Amphipoda, Ostracoda, Euphausiacea, Polychaeta, Chaetognatha, Pteropoda and Appendicularia) wereidentified and counted under a stereomicroscope in one
sub-sample. The sub-sample in which large specimens were
excluded was further subdivided and at least 200 individualsof small specimens (< 1.5 mm) were counted and identified
under a stereomicroscope (SMZ18, Nikon, Tokyo, Japan)
and upright microscope (80 IE, Nikon, Tokyo, Japan). All
calanoid copepods were identified to the lowest possible
taxonomic level (generally species or genus), and then theirdevelopmental stages were determined under a stereomicroscope. The first copepodite (CI) stages of C. acutus and C.
propinquus were combined. The older copepodite (> CIII)
stages of Clausocalanidae (including C. citer, Clausocalanus
laticeps and Clausocalanus brevipes) except for Microcalanus pygmaeus were highly dominated by C. citer (96%);
therefore, we presumed that stages CI–CIII of Clausocalanidae were C. citer in further analysis. M. pygmaeus was identified to all copepodite stages. Cyclopoids and poecilostomatoids (genus Oithona and family Oncaeidae) were identified
to the genus or family level. Other zooplankton (Cnidaria,
Amphipoda, Ostracoda, Euphausiacea, Polychaeta, Chaetognatha, Pteropoda and Appendicularia) were not identified tothe species level. Abundance was calculated as the numberof individuals per ­m3 (Online Resource 3).

Data analysis
Cluster analysis was employed using 3 years of data to elucidate interannual and spatial variation in the SIZ zooplankton community structure. The zooplankton data from 2017and 2018 were converted to an integrated average abundance of 0–200 m (ind. m­ −3) for comparison with 2016.
The Bray–Curtis similarity and unweighted paired-groupaverage linkage indices were used for these analyses (Field
et al. 1982). Abundance data for each taxon were root transformed before the cluster analysis to reduce the effect ofunderestimating large zooplankton due to net avoidance.
Subsequently, permutational analysis of variance (PERMANOVA) and pairwise comparisons were conducted
to identify differences among the clustered groups. PERMANOVA was conducted using type III sums of squares
and the unrestricted model. Similarity percentage analysis(SIMPER) was performed to quantify the contribution ofa species to the dissimilarity among the clustered groups.
The environmental variables explaining the zooplankton
community were analysed using the distance-based linear
model permutation test (distLM). The best models wereselected through a stepwise selection procedure based on the
Akaike information criterion (AICc) with a correction forsmall sample size. The environmental factors included average water temperature (0–200 m; Temp200), average watersalinity (0–200 m; Sal200), photosynthetically active radiation (PAR), size-fractionated chl a concentrations (Chl_10,
Chl_2, GF/F) on the surface, MLD and IFDs. We measured
chl a via water sampling in nine layers primarily from thesurface to 200 m, including the subsurface chl a maxima(SCM), although data from several sampling layers in 2016
were lost due to sampling error. Because the surface chl avalues were significantly correlated with the integrated chl avalues from 0 to 200 m depth (r = 0.906–0.840, p < 0.0001),
we used the surface chl a values as representative in thewater column (to 200 m depth) for the environmental factors
in the zooplankton community analysis. To remove multicollinearity between environmental parameters, varianceinflation factors (VIFs) were calculated for each parameter.
If the VIF exceeded 6, it was removed from the explanatory
parameters. This is well below the suggested threshold of 10,
indicating that the correlation between variables is low andthat the parameters can be interpreted individually (O’brien2007). Community analyses were conducted using PRIMER
software version 7 with the PERMANOVA + add-on (Anderson et al. 2008; Clarke and Gorley 2015). All permutationbased tests were conducted using 999 permutations. Differences in mean abundance between groups were tested by
one-way analysis of variance, and the Tukey–Kramer post
hoc test was used to distinguish differences between thegroups.
The effects of environmental parameters on the population structure of C. citer were investigated using canonical correspondence analysis (CCA) for the untransformed
proportions of each developmental stage (CI–CVI) at eachstation in 2017 and 2018, along with normalised environmental variables. The 2016 samples were not stratified andwere excluded from this analysis. The environmental variables used were the same as those in the previous section(except for surface chl a), with the addition of the mean

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value of the size-fractionated chl a concentrations (Chl_10,
Chl_2, GF/F). The optimal subset of variables identified by
the model was selected using forward selection for adjusted­R2 values as the selection criterion. This analysis was run
using the cca and ordiR2step functions of the R packagevegan (Oksanen et al. 2019; R Core Team 2020). The significance of the model was analysed through permutation testing (permutations = 999) at a significance level of p < 0.010.

Hydrography
The water mass distributions along the 110°E transect
were generally similar in all 3 years. Fresher water spreadalong the surface mixed layer from the surface to approximately 30–50 m depth across the entire study area, reflecting the melting of sea ice (Fig. 2). Subsurface temperature
minimum layers were observed below the mixed layer.
Relatively warm, saline layers were found below the temperature minimum layer and identified as CDW. Alongthe 63.5°S transect, CDW was located in the eastern area

Temperature (℃)

Salinity
Depth (m)Depth (m)(a) 2016

Results(b) 2017(c) 2018

LatitudeLatitudeLongitude

Longitude(d) 2017

Fig. 2  Temperature and salinity contours in January of 2016 to 2018 along the 110°E (a–c) and 63.5°S (d) transect lines off Vincennes Bay, East
Antarctica. SACCF-N denotes the northern branch of the Southern ACC front. SB indicates the southern boundary of the ACC​

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below about 100 m depth, while cold water occurred atthese depths in the western area. This environmental gradient formed due to the Vincennes eddy (Fig. 1; (Mizobata
et al. 2020). SACCF-N was identified between 60° and
62° S (Table 1). SB was located between 63.5° and 64°S
every year along the 110°E transect. The MLD varied withlatitude, with the deepest value each year observed at thenorthernmost station (Table 1). The number of IFDs was
slightly higher in the eastern area than on the western side,(a) 2016 110

E transect
Chl_2 (2-10 µm)

GF/F (< 2 µm)

Chlorophyll a (µg L-1)

Chlorophyll a (µg L-1)

Depth (m)Chl_10 (> 10 µm)
Chlorophyll a (µg L-1)

E transect

Depth (m)(b) 2017 110

S transect

Depth (m)(c) 2017 63.5(d) 2018 110

E transect

Depth (m)Fig. 3  Vertical distribution of
the chlorophyll a concentrationin various size fractions of 2016
to 2018 along the 110°E and63.5°S transect lines. a: 110°E
transect in 2016, b: 110°E transect in 2016, c: 63.5°S transect
in 2017 and d: 110°E transect in2018. The dashed lines indicate
the zooplankton sampling layer

and was also higher in 2016 than the other 2 years, likely
because the survey was conducted about 2 weeks later.
The chl a concentration of each size fraction varied
according to year and location (Table 1 and Fig. 3). Surface chl a concentrations in the larger two size fractions(Chl_10 and Chl_2) were higher at the southern stations(64 and 64.5°S) in 2016 than in the other 2 years (Table 1).
At the northernmost station (60°S), the chl a concentration of the largest fraction (Chl_10) was relatively high inall years. The chl a concentration of the smallest fraction

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Polar Biology(GF/F size fraction) was highest at 63.5°S in 2018. Alongthe 63.5°S transect in 2017, chl a concentration in all size
fractions were less than 0.1 µg ­L−1 throughout the transect, and spatial variation was lower than along the 110° E
transect. The SCM varied latitudinally (Fig. 3). In the twosize fractions, Chl_10 and Chl_2, in 2017 and the large
size fraction, Chl_10, in 2018, SCM were shallower in thenorth (< 50 m) and deeper in the south (50–100 m). The
size fractions, Chl_2 and GF/F, in 2018 were shallower at
the southern station (65°S) than those at northern stations.
Along the 63.5°S transect in 2017, SCM were observed at
depths of 50–100 m, with fewer differences between stations. In the latitudinal and longitudinal transects, SCM
depths tended to be shallow in the larger fractions.

Fig. 4  Horizontal variation in
total zooplankton and copepod
abundances and compositions inJanuary of 2016 to 2018 alongthe 110°E (a, c) and 63.5°S (b,d) transect lines off Vincennes
Bay, East Antarctica

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Abundance and species composition of zooplankton
Summarising the 3 years, the total zooplankton abundance
ranged from 236 to 16,429 ind. ­m−3, with the lowest abundance in the southern area along 110°E, which was locatedin the SB area, while the highest abundance was observedat the northernmost station (AZN) in each year. The abundance was much lower along both 110°E and 63.5°S transects in 2017 than in other years (Fig. 4a, b). Copepods,
including nauplii, were dominant at all stations, accounting for 81–99% of total zooplankton abundance (Fig. 4a,b). The relative abundance of copepod nauplii was higher
in the southern area, with a maximum of 53% of the totalabundance at 63°S. Appendicularia were abundant around
63–64°S. Other plankton, including Polychaeta, Pteropoda,
Chaetognatha, Ostracoda, Cnidaria, Euphausiacea andPolar Biology

Amphipoda, accounted for a maximum of approximately
6% of the total abundance.
Along the 110°E transect, Oithona spp. was the predominant copepod taxon throughout the survey area (30.7–82.2%,
Figs. 4c, d); in particular, high abundances were recordedat the northern stations. Oncaeidae were the second mostabundant copepod at southern stations (south of 63°S,
2.5–52.0%). C. citer occurred throughout the survey area.
Microcalanus pygmaeus occurred south of 63°S. Large
copepods were observed at low abundances of less than
5% at all sampling stations. Oithona spp. was the dominanttaxon along the 63.5°S transect, followed by Oncaeidae C.
citer and M. pygmaeus were more dominant west of 110°E.
At the northernmost station, Oithona spp. was most abundant at 0–50 m depth among all depth layers in 2017. At
other stations, it was found mainly at 50–100 m, although
the differences among layers were smaller at 63.5°S(Fig. 5a). A similar pattern was observed in 2018 (Fig. 5c).
Along the 63.5°S transect, Oithona spp. was distributed in
the 50–100 m layer, except at 110°E (Fig. 5b). Although
Oncaeidae were abundantly distributed in the 0–100 m layers at 60°S in both 2017 and 2018 (Fig. 5a, c), this taxon wasless abundant in the surface layer (0–50 m) at other stations
and was distributed mainly at 50–200 m along the 110°E
transect and at eastern stations along the 63.5°S transect(Fig. 5a, b). At the western four stations, higher abundanceswere recorded in the deeper layer of 100–200 m. The distribution pattern of C. citer showed a higher abundance inthe shallowest layer (0–50 m) only at 60°S, while at stations south of 60°S, higher abundances were apparent at
50–200 m (Fig. 5a). This distribution pattern corresponds
to that observed in 2018 (Fig. 5c). No east–west trend in
the surface layer (0–50 m) was found along 63.5°S transect,
although this species was distributed in the 50–200 m layer
throughout the transect (Fig. 5b).

Statistical analyses of the small zooplankton
community
The overall zooplankton community was divided into one
sample (B; 65°S in 2016) and three groups (A, C and D)
at 65% similarity through cluster analysis based on the
root-transformed zooplankton abundances of each sample(Fig. 6a; PERMANOVA: p < 0.001). The one sample (B)was characterised by very low abundance and low diversity(Fig. 6b). Clear annual differences were observed between
2016 and 2017. In addition, latitudinal changes wereobserved for 2017 samples between groups C (60–62°S)
and D (63–65.5°S and 63.5°S transect). The 2018 samples
were separated into two groups. The northernmost station
was placed in group A, consisting of the 2016 group, andthe remaining two stations were in group D. The abundanceof group A was significantly higher than groups C and D

Fig. 5  Vertical distributions of three major copepod taxa (Oithonaspp., Oncaeidae and Ctenocalanus citer) in the upper 200 m along the
110°E (a) and 63.5°S (b) transect lines in January 2017 and along the
110°E transect line in January 2018 (c) off Vincennes Bay, East Antarctica(p < 0.0001). Small copepods, including Oithona spp., nauplii and C. citer, were important contributors to the totalabundance of each group (Fig. 6b). Oithona spp., C. citerand copepod nauplii had a high contribution in average dissimilarity in all comparisons between groups (Table 2).
The average abundance of these taxa and Appendicularia
was higher in group A than in groups C or D (p = 0.024
and 0.004, respectively). The taxa contributing to the13Polar Biology

dissimilarity between groups C and D were small copepodsof M. pygmaeus, Oithona spp. and C. citer. The first species
was more abundant in group D, while the latter two species
were much more abundant in group C. The best model ofenvironmental factors describing the zooplankton community included IFDs (p = 0.001) and chl a concentration of thelargest fraction (Chl_10, p = 0.007; Table 3). IFD and large
Chl_10 were factors explaining 34.0 and 12.9% of the variation in the zooplankton community, respectively.

Population structure of Ctenocalanus citer and its
environmental drivers

Fig. 6  Results of cluster analysis. a: Dendrogram based on abundances of the zooplankton community over 3 years. Each group wastested with PERMANOVA. b: Abundance and species compositionof each group identified in cluster analysis

Table 2  Species abundance(root) and their contributions
as average dissimilarities (Av.
Dis) to the overall average
dissimilarity between each pairof groups, as indicated by the
SIMPER analysis

The vertical distributions of each developmental stage of
C. citer differed spatially (Fig. 7), with C. citer being distributed in the surface layer in the north and in the deeper
layers towards the south. Along the 110°E transect, the highest abundances of copepodite stages CI–CIV were observedin the upper 50 m at 60°S (Fig. 7a). At 61°S–63°S, earlylife stages (CI–CII) occurred in the 50–100 m layer at highabundances. South of 63°S, these populations were concentrated in layers deeper than 50 m. Males were foundin the 50–100 m and 100–200 m layers at 60°S and 64°S,
respectively, at low abundances. In 2018, high abundancesof all stages except adult males were observed in the upper
50 m at 60°S (Fig. 7c). At 63.5°S and 65°S, early stages(CI–CIII) occurred in deeper layers of 50–200 m, while notrends were observed for middle stages (CIV and CV) andadult females. Along the 63.5°S transect, a high abundanceof adult females was observed in the 50–100 m layer ofwestern stations (106°E–108°E; Fig. 7b). Other stages also
occurred, mainly at 50–100 m. Adult males occurred only
at 100–200 m throughout the transect. There were no clear

Taxa/ Species

Average abundance

Average dissimilarity = 48.68
Copepod nauplius
Oithona spp.
Ctenocalanus citer
Appendicularia
Average dissimilarity = 54.82
Oithona spp.
Copepod nauplius
Ctenocalanus citer
Average dissimilarity = 35.11
Oithona spp.
Ctenocalanus citer
Copepod nauplius
Microcalanus pygmaeusGroup A
46.8
64.4
35.1
19.2
Group A
64.4
46.8
35.1
Group C
33.8
17.1
14.3
0.7

Group C
14.3
33.8
17.1
1.7
Group D
18.1
15.3
7.3
Group D
18.1
7.3
15.3
5.5

Av. Dis% Contribution

Cumulative %

9.0
8.5
5.8
5.3

18.5
17.5
12.0
10.8

18.5
36.1
48.0
58.8

13.4
9.4
7.8

24.4
17.2
14.2

24.4
41.6
55.8

8.6
5.1
3.2
2.5

24.5
14.6
9.0
7.0

24.5
39.1
48.1
55.1

Species contributing to the first 50% of the dissimilarity are shown in decreasing order of percentage contribution

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Table 3  Results of distance-based linear model (DistLM) analyses
on the relation of environmental variables to the community structure(Bray–Curtis) based on root transformed zooplankton abundance
Selected variables

Pseudo-F P-value Variation (%) Cumulative (%)

IFDs
Chl_10

9.8
4.4

0.001
0.007

34.1
12.9

34.1
47.0

The best model of variables was selected based on the Akaike information criterion (AICc) for all locations. The pseudo–F, P–value
were obutained by permutation (n = 999). IFDs was defined as thenumber of days after the SIC became less than 20%. Chl_10 was indicated > 10 μm chlorophyll a concentration

east–west differences in vertical distribution of C. citer at
any of the developmental stages.
The developmental stage composition of the C. citerpopulation varied spatially (Fig. 8a, b). The northernmost
station was dominated by early–middle copepodite stages(CI–CIV), with very small contributions of adult stages(CVI_F and M). Early stages (CI–II) were present at highproportions in the northeast area, while the lowest proportion of these stages was found in the western area. Older
stages (CV–CVI) were widely distributed throughout the
study area, and the relative contributions of these stages
were highest in the western area in 2017. In 2018, the population structure was similar to that observed in 2017, except
at the southernmost station, which was dominated by earlystages and adult females.
The best CCA model of relative stage composition wasconstrained by Temp200, Chl_10 and Chl_2, and explained
30% of the total inertia in the dataset (p = 0.001; Fig. 8c andOnline Resource 4). The first axis, which accounted for themost variability (21%), was strongly correlated with average water temperature, which was inversely correlated witha large contribution of adult stages. Large proportions ofearly life stages were positively correlated with the Chl_2.
Stations dominated by middle stages (CIII–CIV) had thehighest Chl_10.

Discussion
Effects of interannual environmental variation
on small zooplankton
Small copepods were numerically abundant at all stations,with particularly high abundances of Oithona spp., Oncaeidae, C. citer, M. pygmaeus and nauplii. These findings
confirm a previous study on the oceanic zone of the Southern Ocean (Atkinson et al. 2012). Our results demonstrate
a consistent latitudinal pattern across the 3 years. Spatial
variations in abundance, with high abundances of small

copepods in the AZN and Polar Front (north of SACCF)
and much lower abundances in the southern area of the AZS
and coastal areas, are typically observed in East Antarctica(Dubischar et al. 2002; Hosie et al. 2014; Ojima et al. 2015;
Takahashi et al. 2017, 2021; Makabe et al. 2017).
Despite this spatial variation, the zooplankton abundancein summer was highly variable among years. High abundance north of the SACCF reached 16,000 ind. m­ −3 in 2016
and 2018, which was four times greater than the abundance
observed in 2017. The abundance in 2017 fell within thepreviously reported ranges obtained using 100 µm meshnets (Dubischar et al. 2002; Ward et al. 2012a; Ojima et al.
2015). The abundance in the AZS was higher in 2016 thanin the other 2 years and previous studies (Ojima et al. 2015;
Takahashi et al. 2017; Makabe et al. 2017). The cluster analysis conducted in the present study supports these annual
differences. The zooplankton community is strongly influenced by sea-ice dynamics, which often drives phytoplankton blooms, as indicated by the best model of zooplankton
community composition. The sampling period was approximately 2 weeks later in 2016 than in the other 2 years, so
the IFDs were longer in 2016. Previous studies have shownthat zooplankton abundance increases with the phytoplankton bloom after sea-ice retreat, with a peak in fall (Huntand Hosie 2006; Yang et al. 2011). During summer, blooms
along with the sea-ice melt are the starting point for the
recruitment of new generations of zooplankton and growthof these populations, which lead to increases in abundance(Ward et al. 2012a). Therefore, the observed differences inabundance between the 3 years are likely to be understoodby the number of days between sea-ice retreat and sampling.
Zooplankton community structure is likely to be affectedby phytoplankton in ice-edge blooms associated with thetime of sea-ice retreat. This possibility was confirmed using
the distLM procedure, which revealed that the variation inzooplankton community structure was correlated with the
Chl_10 concentration and IFDs. To determine how the phytoplankton and ice-edge bloom changed after the sea-ice
melted, we compared the monthly average chl a concentrations from November to January between the 3 years basedon satellite ocean colour images of the Southern Ocean(Online Resource 5). Monthly mean chl a concentrations
were highly variable among years in our research area. In
January 2016, higher chl a concentrations were detected
throughout the observation period across all sampling sites,
while smaller blooms and low chl a concentrations wereobserved in 2017 and in the southern area in 2018. Ice-edge
blooms are temporary events that disappear within several
weeks (Arrigo et al. 2008). The high phytoplankton biomass (including released ice algae) provides a food resourcefor zooplankton (Kawall et al. 2001; Kohlbach et al. 2019).
In this study, abundance and the egg production rate werepositively correlated with chl a concentration for the most13

Polar Biology

17_60S 17_61S 17_62S 17_63S 17_63.5S 17_64Sb

17_106E 17_107E 17_108E 17_110E 17_111E 17_112Ec

18_60S 18_63.5S 18_65S

17_65S

Developmental stagesaDevelopmental stages

Developmental stages

Fig. 7  Horizontal and vertical
distribution of developmental
stages (CI–CVI) of Ctenocalanus citer in the upper 200 m.
a: 110°E transect in 2017, b:
63.5°S transect in 2017 and c:
110°E transect in 2018. The
histogram shows the percentages of total abundance for eachdevelopmental stage in threelayers. The solid line denotes
the log-transformed abundanceof each developmental stage

Abundance of developmental stages (%)

13

Polar Biologya2017 Jan

Stage

Fig. 8  Population structure (developmental stage composition) of
Ctenocalanus citer at each location in January of 2017 and 2018 (a,b) and the results of canonical correspondence analysis (CCA) for
relative developmental stage abundance in C. citer (c). In panels aand b, circulation arrows denote the Vincennes eddy. In panel c, thecolour of the centre of each pie chart denotes sampling year (black:b2018 JanStage

2017; red: 2018). Arrows denote significant environmental factors
with length representing the strength of the correlation to the ordination. Temp200 indicate average water temperature (0–200 m), Chl_10
indicate > 10 µm chl a. CI–CVI indicate the centroids for each developmental stage. (Color figure online)

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Polar Biology

dominant taxon, Oithona spp. (probably O. similis) (Wardand Hirst 2007; Pinkerton et al. 2020). In addition, Appendicularia was a major contributor to the dissimilarities ingroup A. In polar regions, Appendicularia respond rapidly tophytoplankton growth by altering the timing of their reproduction, resulting in peaks of abundance coincident with
the ice-edge bloom (Acuña et al. 1999; Spinelli et al. 2018).
Our results suggest that the abundance of small zooplankton
increased owing to favourable feeding conditions and formed
a consistent community throughout the SIZ in years withhigh primary production. However, the lower chl a concentrations observed in our study were associated with a lower
abundance of zooplankton and with latitudinal variationsin the zooplankton community (groups C and D). Most of
the species contributing to the dissimilarity between thenorthern (group C) and southern (group D) communities
were more abundant in the north, while M. pygmaeus wasmore abundant in the south. These species, except M. pygmaeus, are widely distributed in subantarctic and Antarctic
waters (Atkinson and Sinclair 2000), and ubiquitous northand south of the SB-ACC (Hunt and Hosie 2006; Ojima
et al. 2015). M. pygmaeus is an abundant species in Antarctic waters and is the most dominant species in the sea icecovered western Weddell Sea during spring (Schnack-Schiel
et al. 2008). The gradient in the distribution pattern of small
zooplankton species is likely to be more enhanced during
years with low food availability.
The abundance of small zooplankton and community
structure varied annually, and were affected by the chl aconcentration of the larger phytoplankton fraction associatedwith sea-ice retreat. The effects of hydrographic structure
and local eddies were less apparent for small zooplankton.
Small copepods have greater tolerance to changes in thephysical environment, including frontal structures in the
SIZ, than large zooplankton (Takahashi et al. 2017). These
results suggest that small zooplankton respond to primary
production through the food chain more quickly than large
zooplankton. Therefore, regional effects of climate have thepotential to affect the small zooplankton community in east
Antarctica more rapidly than large zooplankton (Nicol et al.
2000).

Effects of environmental variations
on the population structure of Ctenocalanus citerIn this study, the vertical distribution pattern and developmental stage of C. citer varied gradually with latitude. C.
citer was distributed in shallower depths during both years at
the northernmost station, with the intermediate stage dominating, while the vertical distribution of C. citer was deeper
towards the south, with the adult stage dominating. In contrast, the east–west difference in the vertical distribution of
C. citer was unclear, but the developmental stages differed,13

with the younger stages dominating in the east and the adultstage dominating in the west.
The surface distribution of C. citer during summer has
been reported in various regions of the Southern Ocean,such as the Scotia Sea (Atkinson and Sinclair 2000), theLützow-Holm Bay region (Makabe et al. 2012; Takahashi
et al. 2017) and the Polar Frontal Zone (Dubischar et al.
2002). C. citer migrates to the surface to graze on phytoplankton, which increases with sea-ice melting in the surface
layer. Sea-ice melting proceeds from the north, suggestingthat the time lag in melting is a potential factor causing thenorth–south difference in the vertical distribution. In addition, the vertical distribution of phytoplankton is likely toaffect the vertical distribution patterns of C. citer. The depthof the SCM increased southwards during the study period.
Thus, the spatial variation in the vertical distribution of C.
citer during summer is also likely to depend on food availability in the water column.
The development of the C. citer population structure in
the eastern Weddell Sea has previously been characterised(Schnack-Schiel and Hagen 1994; Schnack-Schiel 2001).
The average population stage of C. citer is early copepodite (CI–CII) in late spring/summer, with rapid progression
through the stages through winter. Although all developmental stages except adult males occur during all seasons,female gonads develop in late winter, coinciding with theoccurrence of males. Females with mature gonads occur athigh proportions in spring, which are maintained throughautumn. C. citer exhibits seasonal migration, graduallyascending from November to February and spending thesummer in the upper 100 m, where young generations arerecruited (Schnack-Schiel and Mizdalski 1994).Therefore,
analysis of the composition of developmental stages of copepods allows for the estimation of their population status.
The dominance of younger developmental stages(CI–CII) indicates the addition of new generations throughreproduction. Likewise, the occurrence of middle stages(CIII–CVI) demonstrates a transition to adult stages in the
population. Dominance of adult stages indicates a population just before or during the reproductive period. The developmental stage composition varied spatially. Middle stages
dominated populations in the northern area, younger stages
prevailed in the eastern area and adult stages predominatedin the western area as well as in the southern area in 2017.
These spatial differences in population structure are likely
generated not only by oceanic frontal systems, such as the
SACCF or SB-ACC, but also by the local east–west environmental gradient. Similar distribution patterns of copepod
population structures were observed in Lützow-Holm Bay,
East Antarctica (Makabe et al. 2017).
The CCA model revealed that the development of C. citerwas controlled by average temperature and food availability. Water temperature in the epipelagic layer is negatively

Polar Biology

correlated with the proportion of adult stages, suggestingthat higher temperatures promote development in this species. This finding is consistent with previous studies, whichshowed that low temperatures resulted in longer egg hatching times and higher mortality of each stage for the marine
copepod species (Ward and Shreeve 1998; Shreeve et al.
2002; Hirst and Bunker 2003). The water temperature differences between eastern and western areas along 63.5°S
are likely driven by the Vincennes eddy circulation, whichtransports warm CDW poleward on the eastern side of theeddy and transports cold water equatorward on the westernside (Mizobata et al. 2020). Thus, the environmental gradient formed by the cyclonic eddy affects the reproductive
period of the dominant small copepod, C. citer, leading toan east–west difference in population structure. In addition,
Mizobata et al. (2020) reported the presence of a cycloniceddy train consisting of the Vincennes eddy, the Poinsett
eddy and the Sabrina eddies in East Antarctica. These
results indicate that local spatial differences in the population structure of copepods are common during summer in
East Antarctica.
However, the population structure was slightly different
in 2018, with no adults dominating anywhere. The dominantdevelopmental stage was younger towards the south, which
was probably related to the size composition of the phytoplankton. C. citer is predominantly herbivorous throughout
the year (Hopkins and Torres 1988; Pasternak and SchnackSchiel 2007). According to Pasternak and Schnack-Schiel(2007), and the largest size class of food items (> 25 μm)
is rarely found in the guts of younger stages, and increases
with C. citer stage. This finding is consistent with our CCA
results, suggesting that it is difficult to assess the population
dynamics of this species based on bulk chl a concentrations.
The latitudinal changes in phytoplankton composition in
the Indian sector of the Southern Ocean have been reported
previously (Takao et al. 2014; Takahashi et al. 2022). In
the study of Takahashi et al. (2022), which was conductedduring the same voyage in 2018, the small diatom Fragilariopsis cylindrus was dominant at the sea-ice edge station,
while larger diatoms, such as Pseudo-nitzschia prolongatoides/subcurvata and Fragilariopsis kerguelensis, wereprevalent at the northern station. These latitudinal changes
in phytoplankton species composition are a common feature in the SIZ of the Indian sector (Takahashi et al. 2017).
These results suggest that shifts in phytoplankton composition (= latitudinal variation) in the SIZ after sea-ice melt aresynchronous with the development of the C. citer population
structure. This finding is also consistent with the summer
surface distribution of C. citer (Schnack-Schiel and Mizdalski 1994; Schnack-Schiel 2001). It has been reported thatfeeding (Pasternak and Schnack-Schiel 2007), reproduction(Niehoff et al. 2002) and development of C. citer (SchnackSchiel and Mizdalski 1994) are at least partially decoupledfrom phytoplankton blooms, as they are observed outside
the bloom period. Nevertheless, our results and those of aprevious study in which C. citer abundance increased during
the summer indicate that C. citer uses blooms efficiently forthe growth of newly recruited populations during summer
in the SIZ (Schnack-Schiel and Mizdalski 1994; Atkinson
et al. 2012).

Conclusion
In this study, we examined the community structure andabundance of small zooplankton in SIZ off Vincennes Bay,
East Antarctica, during summer (January 2016–2018). The
small zooplankton community was highly variable among
sampling periods in 2016, 2017 and 2018, and these patterns were likely driven by the abundance of large-sized
phytoplankton and IFDs. Our results indicate that small
zooplankton communities respond rapidly to changes infood availability after sea-ice melt. In contrast, the effect ofhydrographic structure, such as fronts and local eddies, on
small zooplankton community structure was unclear.
The population structure of C. citer, a key component of
the small copepod community in the study area, was examined in relation to environmental factors. The developmental stage distribution pattern varied latitudinally and also
between eastern and western areas. These spatial differences
are likely to be driven by a local east–west environmental
gradient. We suggest that the environmental gradient formedby cyclonic eddies influences the developmental period of C.
citer, which in turn leads to the east–west difference in population structure. Local spatial variation in copepod population structure due to cyclonic eddies is likely to be common
during summer in East Antarctica. The population structureof C. citer is also related to the spatiotemporal variationin the composition of primary producers after sea-ice melt,
suggesting that the development of population structure isclosely linked to the dynamics of the ice edge and phytoplankton blooms during summer.
Global warming is expected to cause changes in theSouthern Ocean ecosystem as the extent and thickness of
sea ice decreases (Arrigo and Thomas 2004; Constable et al.
2014). Our study demonstrated that small zooplankton species respond rapidly to these environmental changes in theSouthern Ocean.
Supplementary Information The online version contains supplementary material available at https://d​ oi.o​ rg/1​ 0.1​ 007/s​ 00300-0​ 23-0​ 3174-0.
Acknowledgements We are grateful to Captain Akira Noda and allcrew of the training vessel Umitaka-maru, and all cadets on board
participating in the Advanced Course for Marine Science and Technology of TUMSAT, for their invaluable assistance during oceanographic observations. We also thank researchers and graduate students for their excellent support during voyages of Kaiyodai Antarctic

13

Polar Biology
Research Expedition (KARE-19, 20 and 21). We would like to thankDr. Haruhiko Kashiwase for sharing his dataset of SIC with us. We
are very grateful to the reviewers who provided valuable feedback on
my paper. We dedicate this manuscript to the late Dr. Tsuneo Odate,
who had led the Japanese Southern Ocean ecosystem research teamfor many years. This study was supported by a Grant-in-Aid for Scientific Research (Grant nos. 15H05239 and 17H06319, PI: M. Moteki),
Research Project Funds of NIPR (Grant No. KP308, PI: T. Odate),
JARE (Grant No. AP0923 and AP0939, PI: M. Moteki) and Overseas
Research Fellowships (K. Matsuno).
Author contributions AT conducted data analyses and wrote the main
manuscript text. YO and KM conducted sampling and microscopic
analysis. KDT analysed satellite data and prepared Supplementary data.
RM and MM conceived of research plan and designed this research. All
authors contributed to discussion based on the results and to improving
the manuscript.
Funding Overseas Research Fellowships,Research Project Funds of
NIPR (KP308) and JARE (AP0923 and AP0939), Grant-in-Aid for
Scientific Research (15H05239 and 17H06319)

Declarations
Competing interests The authors declare no competing interests.

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