Polar Science 24 (2020) 100509

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Regional comparison of seasonal changes on copepod community structurein the Arctic Ocean
Koki Tokuhiro a, *, Yoshiyuki Abe b, Jonaotaro Onodera c, Makoto Sampei a, Amane Fujiwara c,€thig e, Atsushi Yamaguchi a, dNaomi Harada c, Kohei Matsuno a, d, Eva-Maria NoaGraduate School of Fisheries Science, Hokkaido University, 3-1-1 Minato-cho, Hakodate, Hokkaido, 041-8611, Japan
Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba, 277-8564, Japan
Institute of Arctic Climate and Environment, Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka, Kanagawa, 237-0061, Japand
Arctic Research Centre, Hokkaido University, Kita-21 Nishi-11 Kita-ku, Sapporo, Hokkaido, 001-0021, Japane
Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research, Am Handelshafen 12, DE-27570, Bremerhaven, Germanybc

A R T I C L E I N F O

A B S T R A C T

Keywords:
Sediment trap
Zooplankton swimmer
Arctic copepods seasonality

The Arctic Ocean is characterized as the greatly variable oceanic environment both seasonality and regionally.
Such environmental variability would affect regional differences in the respective copepod community struc­tures, though it has not been reported so far. In this study, we analyzed time-series zooplankton samples withfocus on large copepods collected by sediment traps moored in three different regions of the Arctic Ocean at
approximately 72–260 m water depth, and seasonality of copepod community structures were compared.
Remarkable seasonality in the copepod community structure around Molloy deep in the eastern Fram Strait were
due to the influence of endemic species transported by the West Spitsbergen Current. In contrast, in the southern
Canada Basin (Northwind Abyssal Plain, Hanna Canyon and Barrow Canyon), the community structure of pre­dominant large copepods showed less seasonality due to low primary production. In the MacKenzie Trough, thenumber of copepod swimmers were greater than those in all other regions investigated, which cooccur withmuch higher primary production in that area. These spatial differences in seasonality of copepod swimmer
community structure were thought to be caused by various factors, not only sea ice seasonality but also dif­ferences in current patterns, endemic species and the magnitude of primary production.

1. Introduction
In the Arctic Ocean, increase of air and sea water temperatures due toglobal warming induce rapid sea-ice reduction during summer (Markus
et al., 2009). The concurrent drastic change of the marine environmentis thought to critically affect marine ecosystems in the Arctic Ocean(Wassmann et al., 2011; Grebmeier, 2012). In the pelagic system,
zooplankton organisms represent the most important prey of various
higher trophic levels (Lowry et al., 2004; Wassmann et al., 2006). For
instance, they are the main food source for polar cod (Boreogadus saida),
which is an important commercial species in the Arctic Ocean (Brad­
street and Cross, 1982). Copepods can also be regarded as important
indicators of currents, water mass and marine environments because of
their low swimming ability and short life cycle compared to other or­
ganisms (e.g., fish) (Wassmann et al., 2006). Because of their dominancein the marine pelagic realm, it is an important topic to clarify thephenology of copepods. However, year-round ship-board observation isdifficult in the deep Arctic Ocean because of the seasonal ice coverage
lasting for eight months minimum. Due to this restriction, almost all
studies investigating copepods in the Arctic Ocean have been carried out
mainly during summertime when sea ice is very thin or melted (e.g.,
Springer et al., 1989). Thus, knowledge about seasonal changes withincopepod community structures is still scarce.
Automatic sediment traps programmable to collect samples are amarine observation equipment to collect sinking particles in the watercolumn over a certain time period when mooring at fixed depths. Since
automatic sediment traps can collect one-year-round or even longer,
they were used in the open ocean and the Arctic Ocean where it isdifficult to collect year-round samples by ship-board expeditions (Mat­suno et al., 2015; Makabe et al., 2016).
It has been reported that zooplankton actively swim into the trap andare killed by the preservation fluid filled in the cups (Knauer et al., 1979;* Corresponding author.
E-mail address: k.tokuhiro0319@fish.hokudai.ac.jp (K. Tokuhiro).
https://doi.org/10.1016/j.polar.2020.100509
Received 15 November 2019; Received in revised form 15 January 2020; Accepted 4 February 2020
Available online 6 February 2020
1873-9652/© 2020 Elsevier B.V. and NIPR. All rights reserved.

K. Tokuhiro et al.

Polar Science 24 (2020) 100509

Strait located at the entrance of the Atlantic sector to the Arctic Ocean(Kraft et al., 2012; Bauerfeind et al., 2014). In the Fram Strait, seasonalchanges in the community structures of pelagic amphipods (Themisto
libellula, T. abyssorum and T. compressa) were reported (e.g., Kraft et al.,€ter et al., 2019). The long-term seasonal changes of com­2012; Schromunity structures of pteropods (Limacina helicina and L. retroversa) wererevealed (Bauerfeind et al., 2014). Several studies have reported about
seasonal changes of copepod community structures also for the Pacificsector of the Arctic such as for the Beaufort Sea (Makabe et al., 2010,2016) and the Canada Basin (Matsuno et al., 2014, 2015, 2016). How­ever, those investigations were limited to only a specific region of the
Arctic Ocean and thus it is still unclear how the seasonality of copepod
community structures differs among various regions pan-Arctic Ocean

Ota et al., 2008). Zooplankton species composition in sediment trapsamples have usually been excluded from analysis. They were picked outof the samples to avoid an overestimation of sinking particles in watercolumn. No attention had been drawn to the picked-out swimmers inmost cases. Additionally, the zooplankton collected by sediment traps isthought to be semiquantitative because they are deployed at fixed
depths (Seiler and Brandt, 1997). However, in recent years that attitude
has changed, seasonal changes of the zooplankton community structure
have been reported after having analyzed zooplankton that swam orsunk into the collecting jars of sediment traps (Makabe et al., 2010; Kraft
et al., 2012; Bauerfeind et al., 2014; Matsuno et al., 2014).
Studies evaluating seasonal changes on zooplankton community
structures by means of sediment traps have been conducted in the Fram

Fig. 1. Location of the 3 mooring sites: Fram Strait, Canada Basin, MacKenzie Trough. Fram Strait was sampled at two stations (St. N-4 and St. HG-IV) from 10 July2010 to 15 June 2014. Canada Basin was sampled at three stations (St. NAPt, St. NHC and St. NBC) from 04 October 2010 to 10 September 2016. MacKenzie Troughwas sampled two stations (St. MG and St. MA) from 14 September 2011 to 02 September 2012. West Spitzbergen Current, WSC; Return Atlantic Current, RAC; East
Greenland Current; EGC.
2

K. Tokuhiro et al.

Polar Science 24 (2020) 100509(e.g., Fram Strait, MacKenzie Trough and Canada Basin). Periods ofsea-ice coverage, amount and timing of primary production, daytime
hours and the feeding environment affecting copepod community
structure. Seasonal changes of these environmental factors are different
between Arctic regions (Conover, 1988; Harada, 2016), eventually
resulting in different copepod communities in each region. Until now,there is no comparative study describing differences of seasonal changes
in copepod community structures in high Arctic marine environments.
In this study, we compared seasonal changes of the community
structures of dominant large copepods collected with time-series sedi­ment traps moored in three different Arctic regions: Fram Strait,
MacKenzie Trough and Canada Basin in order to understand the com­munity compositions as well as to clarify what environmental factors
can affect the observed differences in seasonal changes of the domi­
nating copepod community structures.

depths were 190–205 m at St. N-4 and 200–205 m at St. HG-IV,
respectively. The cups of sediment traps were automatically rotatedand replaced at 5–59 days (St. N-4) and 7–59 days (St. HG-IV), respec­tively. Twenty collection cups were used to collect samples per year.
However, 13–19 samples per year in N-4 and 17–20 samples per year in
HG-IV were used for analysis because of sediment trap funnel clogging
during few summer sampling intervals.
Canada Basin: In total three trap arrays were moored. A time-series
sediment trap (SMD26S-6000, open mouth area 0.5 m2, Nichiyu Giken
Kogyo, Co. Ltd.) was moored at St. NAPt (75.0� N, 162.0� W, 1910 mbottom depth) of Northwind Abyssal Plain of Canada Basin from 4
October 2010 to 10 September 2014 (Fig. 1 and Table 1). Range of thesediment trap depths were 186–260 m. The cups of sediment traps were
replaced at 10–15 days, and twenty-six collection cups were used per
year. Another time-series sediment trap (SMD26S-6000, open mouth
area 0.5 m2, Nichiyu Giken Kogyo, Co. Ltd.) was moored at a different
location within the Canada Basin during 1-year at St. NHC (73.3� N,
160.8� W, 426 m bottom depth) of North of Hanna Canyon in Canada
Basin from 28 September 2015 to 10 September 2016 (Fig. 1 andTable 1). The sediment trap depth was deployed at 170 m. Collection
interval were 7–14 days and twenty-six collection cups were used. But
twenty-four samples were used for analysis because of sediment trap
funnel clogging during few summer sampling intervals. A third timeseries sediment trap (SMD26S-6000, open mouth area 0.5 m2, Nichiyu
Giken Kogyo, Co. Ltd.) was moored at St. NBC (72.5� N, 155.4� W, 2000
m bottom depth) of North of Barrow Canyon in Canada Basin from 21
September 2015 to 9 September 2016 (Fig. 1 and Table 1). The deployed
trap depth was approximately 250 m. Collection interval were 12–14
days and twenty-six collection cups were used. Again, only twenty

2. Material and methods
2.1. Field sampling
Time-series sediment traps were moored at seven stations in three
Arctic regions (eastern Fram Strait, Canada Basin and MacKenzie
Trough) collecting samples throughout several seasons between 2010
and 2016 (Fig. 1 and Table 1).
Fram Strait: Two time-series sediment traps (K/MT 234, open mouth
area 0.5 m2, Kiel) were moored at St. N-4 (79.7� N, 4.5� E, 2670 m bottom
depth) and St. HG-IV (79.0� N, 4.3� E, 2600 m bottom depth) in eastern
Fram Strait from 15 July 2010 to 15 June 2014 and from 10 July 2010 to
15 June 2014, respectively (Fig. 1, Table 1). Range of the sediment trap

Table 1
Information of trap deployments and collected samples by means of sediment traps at each investigated station in the Arctic Ocean.
Mooring point

Mooring period

Lat.

Long.

Water depth(m)Trap depth(m)Open area(m2)

Collection
days

No. ofcups

Fram Strait (St. N-4)

1st year(15.07.2010–30.06.2011)
2 nd year(01.08.2011–15.07.2012)
3rd year(27.07.2012–30.06.2013)
4th year(05.07.2013–15.06.2014)79.74N

4.50E

2677

190

0.5

5–59

20

79.74N

4.51E

2667

200

0.5

10–32

20

79.74N

4.51E

2667

205

0.5

10–31

20

79.74N

4.50E

2675

205

0.5

7–31

20

1st year(10.07.2010–30.06.2011)
2 nd year(01.08.2011–15.07.2012)
3rd year(29.07.2012–30.06.2013)
4th year(10.07.2013–15.06.2014)

79.00N

4.33E

2604

200

0.5

10–59

20

79.01N

4.33E

2605

200

0.5

10–32

20

79.01N

4.51E

2642

205

0.5

10–31

20

79.06N

4.03E

2577

205

0.5

7–31

20

1st year(04.10.2010–28.09.2011)
2 nd year(04.10.2011–18.09.2012)
3rd year(04.10.2012–18.09.2013)
4th year(10.09.2013–10.09.2014)75.01N

162.17W

1973

186

0.5

13–15

26

75.11N

175.00W

1975

260

0.5

10–15

26

75.00N

162.00W

1975

222

0.5

10–15

26

74.33N

161.58W

1715

189

0.5

14–15

26

North of Hanna Canyon (St. NHC)

1st year(28.09.2015–10.09.2016)73.30N

199.22W

426

170

0.5

7–14

26

North of Barrow Canyon (St. NBC)

1st year(21.09.2015–09.09.2016)72.47N

204.59W

2000

250

0.5

12–14

26

MacKenzie trough off the coast (St.
MG)

1st year(20.09.2011–02.09.2012)

71.00N

135.29W

705

125

0.5

8–16

24

MacKenzie trough off the coast (St.
MA) shallow

1st year(14.09.2011–02.09.2012)70.45N

136.00W

659

72

0.125

8–17

24

MacKenzie trough off the coast (St.
MA) deep

1st year(14.09.2011–02.09.2012)70.45N

136.00W

659

172

0.125

8–17

24

Fram Strait (St. HG-IV)

Northwind Abyssal Plain (St. NAPt)

3

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Polar Science 24 (2020) 100509

samples were used for analysis because of sediment trap funnel clogging
during few summer sampling intervals.
MacKenzie Trough: In total two moorings were deployed over a timeinterval of one year only. At St. MG (71.0� N, 135.3� W, 700 m bottom
depth) of MacKenzie Trough off the coast in Beaufort Sea, a time-series
sediment trap (PPS. 6/2, open mouth area 0.5 m2, Technicap) wasmoored at 125 m depth from 20 September 2011 to 1 September 2012
(Fig. 1 and Table 1). Collection interval days were 8–16 days andtwenty-four collection cups were used. In addition, at St. MA (70.5� N,
136.0� W, 680 m bottom depth) of MacKenzie Trough, two time-series
sediment traps (PPS. 3/3, open mouth area 0.125 m2, Technicap)
were moored at 72 and 172 m depths from 14 September 2011 to 1
September 2012 (Fig. 1 and Table 1). Collection interval days were 8–17
days and twenty-four collection cups were used each depth.
Fixation of collected material was different: The sample cups of thesediment traps at St. N-4 and St. HG-IV were filled with mercuric chlo­ride (0.14% final solution) and 5% buffered formalin seawater was used
all the other stations to preserving sinking particle and zooplanktonswimmer.

sediment trap and d is the collection interval (days).

2.2. Environmental data from satellite

3.1. Hydrography

The weekly average of sea-ice coverage near each station during themooring periods were calculated at 25-km resolution from the sea-ice
concentration dataset (National Snow and Ice Data Center). MODIS/
Aqua Level 3 binned chlorophyll a data were downloaded from theDistributed Active Archive Center (DAAC) of the Goddard Space Flight
Center (GSFC) of NASA and a running mean of 9 days were calculated by
9-km resolution. Daytime hours at each station were calculated ac­
cording to Brock (1981).

In the Fram Strait, polar night occurred from mid-October to midFebruary, and midnight sun was observed from mid-April to midAugust. The sea ice concentration (SIC) around St. N-4 of eastern
Fram Strait showed no clear seasonal changes related with seasonality ofsun and low coverage (4-years average 8.79%) throughout the year
(Fig. 2a). SIC increased during October and March of 1st, 3rd and 4thyear, but during September and March of 2nd year was very low. Surface
chlorophyll a (Chl. a) concentration ranged between 0.05 and 3.87 mg
m 3 and showed peaks from May to June. The SIC around St. HG-IV ofeastern Fram Strait was even lower than St. N4 and reached about 40%
in spring (Fig. 2b). Also, SIC was increasing in October and June of 3rdyear. Surface Chl. a concentration ranged between 0.02 and 16.7 mg
m 3, which was 4 times higher than these of St. N-4, but the timing of
the peaks was similar at the both stations.
The SIC around St. NAPt of Canada Basin showed clear seasonalchanges (4-years average 76.2%), and sea ice completely melted from
August to October and rapidly increased from October to November(Fig. 2c). Surface Chl. a concentration increased when sea ice melting,and the values were much lower than at all the other stations (0.02–0.35
mg m 3). Midnight sun occurred from late April to early August, andpolar night was observed from late October to early February. Sea ice
concentration at St. NHC (1-year average 72.6%) was increasing rapidly
from mid-October and melted mid-June, and completely sea-ice melting
period was observed in August (Fig. 2d). Only 7 valid surface Chl. a was
detected during open ocean period because of a lot of clouds. Polar night
was observed from early November to early February, and midnight sun
occurred from early May to early August. Rapid freezing was observed
from mid-October to mid-November, and gradual melting occurred frommid-May at St. NBC (1-year average 68.4%) (Fig. 2e). Surface Chl. a
could be detected only 1 time in September because of a lot of clouds.
Polar night and midnight sun period were almost same as St. NHC.
The SIC of St. MG and St. MA of MacKenzie Trough increased rapidly
from late October to mid-November and it was more than 90% from
mid-September to mid-May, and sea ice rapidly decreased from midMay to mid-June (Fig. 2f and g). 1-year average of SIC is 59.3% at St.
MG and 58.3% at St. MA, respectively. Surface Chl. a concentration wasincreased during open water period (from July to August), and thevalues were higher than at all other stations (0.03–38.9 mg m 3). Polarnight and midnight sun occurred from mid-November to mid-January
and early May to late July, respectively.

2.4. Data analysis
Flux data (ind. m 2 day 1) of large copepods (prosome width >1.41mm) for each station were forth root transformed. Similarities between
samples were examined using a Bray-Curtis similarity index anddendrogram created using Unweighted Pair Group Methods using
Arithmetic mean (UPGMA) were punctuated arbitrary similarity togroup samples (Field et al., 1982). According to these groups, average
flux (ind. m 2 day 1) and contribution percentage (%) of the dominantlarge copepods of each group were calculated by similarity percentages(SIMPER). Besides, nonmetric multidimensional scaling analysis(NMDS) was carried out using same similarity to confirm relationshipbetween groups and environmental factor (sea ice concentration, sur­face chlorophyll a and daytime). All these analyses were carried out
using PRIMER 7 software (PRIMER-E Ltd.).
3. Results

2.3. Sample analysis
The zooplankton samples from eastern Fram Strait (St. N-4 and HGIV) were gently filtered with a 0.5-mm mesh net, and the organisms
retained on the mesh net (>0.5 mm size) were treated as zooplanktonswimmers. Large copepods (prosome width >1.41 mm) were identified
to species level according to Brodsky (1967) and counted under a stereo
microscope. Because species identification using morphological features
between three Calanus developmental stages (Calanus hyperboreus, Cal­
anus glacialis and Calanus finmarchicus) was difficult, we identified themusing prosome length of each copepodite stage (Hirche et al., 1994;
Kosobokova and Hirche, 2016; Table 2). In addition, species identifi­
cation for the younger than copepodite stage 5 of Paraeuchaeta glacialis
and Paraeuchaeta norvegica was not possible (Auel, 1999), we treatedthese species as Paraeuchaeta spp.
The samples from the other station (St. NAPt, NHC, NBC, MG andMA) were gently filtered through a 1-mm mesh net, and the organisms
retained on the mesh net (>1 mm size) were treated as zooplanktonswimmers. Large copepods fraction of the zooplankton swimmers was
identified at species level and counted according to Brodsky (1967).
The flux (F, individuals m 2 day 1) of zooplankton swimmers wascalculated using the following equation:
F¼N �

1 1
�
O d

where N is the number of individuals, O is the mouth area (m2) of theTable 2Size categories of the prosome length for identifying the Calanus species in the
Fram Strait (cf. Hirche et al., 1994; Kosobokova and Hirche, 2016).
Species

Females

C5

C4

C3

C. finmarchicus
C. glacialis
C. hyperboreus<3.1 mm>3.1 mm<2.9 mm>2.9 mm<2.2 mm>2.2 mm>3.0 mm<1.7 mm>1.7 mm>2.0 mm

3.2. Community structure
In the eastern Fram Strait, C. finmarchicus, C. glacialis, C. hyperboreus,
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Polar Science 24 (2020) 100509

Fig. 2. Seasonal changes in sea ice concentration and surface Chl. a at each mooring station. Open and solid bars indicate the period of the midnight sun and polarnight, respectively. (Pay attention to the different scales on y-axis).

Metridia longa, Paraeuchaeta spp. and Heterorhabdus norvegicus domi­
nated. Flux of these dominant large copepods changed from 1.25 to 164
ind. m 2 day 1 (mean � sd: 25.9 � 28.3 ind. m 2 day 1) at St. N-4 and0.93 to 128 ind. m 2 day 1 (36.4 � 35.0 ind. m 2 day 1) at St. HG-IV(Fig. 3a and b). The flux of the large copepods in St. N-4 showed two

peaks every year, first peak was from March to May and second peak wasfrom August to October. The flux of the second peak was higher thanthat of the first peak. The flux at St. HG-IV showed two peaks every year,
first peak was from March to May and second peak was from August to
October. The flux of the first peak and the second peak were almost
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Polar Science 24 (2020) 100509

Fig. 3. Seasonal changes on copepods abundance and community structure in the Arctic Ocean. (Pay attention to the different scales on y-axis).

equal, but the species composition changed: the composition of
C. finmarchicus was high in the first peak despite 1st year, while M. longa
and Paraeuchaeta spp. were dominant in the second peak.
In the Canada Basin, C. glacialis, C. hyperboreus, M. longa, Para­
euchaeta spp., H. norvegicus and Gaetanus tenuispinus were observed at St.

NAPt (Fig. 3c). The flux of these large copepods changed from 1.29 to
36.9 ind. m 2 day 1 (10.8 � 5.93 ind. m 2 day 1). Seasonal fluctuationof the flux throughout year was smaller than those in the Fram Strait, but
the flux showed two small peaks in March–August and September–Oc­
tober with increasing share of the composition by C. hyperboreus. At St.
6

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Polar Science 24 (2020) 100509

NHC, C. glacialis, C. hyperboreus, M. longa, Paraeuchaeta spp.,
H. norvegicus and Chiridius obtusifrons were abundant and the flux ofthese large copepods ranged between 2.15 and 42.7 ind. m 2 day 1(9.05 � 8.72 ind. m 2 day 1) (Fig. 3d). Two peaks of the flux wereobserved from April to June and October with dominance of Para­
euchaeta spp. and M. longa. At St. NBC, C. hyperboreus, M. longa, Para­
euchaeta spp., H. norvegicus, G. tenuispinus and Aetideopsis spp. occurred(Fig. 3e). The flux of these large copepods changed from 0.71 to 21.4
ind. m 2 day 1 (8.23 � 4.86 ind. m 2 day 1). The peaks on the flux wereobserved in March–May and September–November, and composition of
C. hyperboreus was high at the spring peak. In addition, share of
H. norvegicus on the flux was higher than that of at St. NHC.
In the MacKenzie Trough, C. glacialis, C. hyperboreus, M. longa, Par­aeuchaeta spp, G. tenuispinus and C. obtusifrons dominated at St. MG(shallow) (Fig. 3f). The flux of these copepods ranged from 0.30 to 268
ind. m 2 day 1 (45.8 � 63.1 ind. m 2 day 1) and showed a peak in
September–October with dominance of Paraeuchaeta spp. and M. longa.
At St. MA (shallow and deep traps), C. glacialis, C. hyperboreus, M. longa,
Paraeuchaeta spp., H. norvegicus and G. tenuispinus were abundant(Fig. 3g and h). The flux of the copepods at St. MA (shallow) changed
from 38.7 to 1440 ind. m 2 day 1 (295 � 290 ind. m 2 day 1) andmaximum flux was the highest comparing to all other stations. The flux
showed a peak in September–October and low in November–January
and no clear seasonal change from February to August. With the sea­sonal change of the flux, dominant species changed: Paraeuchaeta spp.
dominated in the peak of September–October, C. glacialis occurred in
January–April and M. longa were abundant from May to July. The flux ofthe copepods at St. MA (deep) ranged from 3.23 to 126 ind. m 2 day 1(25.6 � 23.7 ind. m 2 day 1). Similarity was observed in seasonalchange on flux between shallow and deep traps at St. MA, but
C. hyperboreus and H. norvegicus were higher in deep trap than these ofshallow.
To clarify seasonal change and comparison between stations ofcopepod community structure, copepod communities were divided into
10 groups (A-J) with 74% similarity using cluster analysis based on flux
(Fig. 4a). Then, we classified groups including less than 2 samples as notavailable group (NA) and did not use it for later analysis. Average fluxes
in the order of group A to J were 250, 22.5, 10.9, 5.88, 7.28, 9.96, 19.3,
39.8, 61.1 and 39.3 ind. m 2 day 1 (Fig. 4b). The average flux of group
A was the highest, and group D had the lowest in all groups. As results of
SIMPER (Table 3), Paraeuchaeta spp. (contribution percentage: 58.5%),
M. longa (19.8%) and C. glacialis (13.2%) dominated in group A, and theshare of C. glacialis was higher than those of the other groups. M. longa(52.7%), H. norvegicus (26.8%) and Pseudocalanus spp. (12.0%) domi­
nated in group B, and Pseudocalanus spp. was only found in the group B
as dominant species. In group C, M. longa (30.4%), H. norvegicus (26.8%)
and Paraeuchaeta spp. (11.9%) were dominant. Similar to group C,
M. longa (40.8%), Paraeuchaeta spp. (27.5%) and H. norvegicus (18.8%)
dominated in group D. Dominant species of group E were M. longa(60.1%), Paraeuchaeta spp. (17.0%) and H. norvegicus (11.4%), andM. longa occupied more than half on total of flux. Paraeuchaeta spp.
(70.1%) dominated, and M. longa (24.7%) and C. hyperboreus (3.4%)
predominated in group F. M. longa (50.7%), Paraeuchaeta spp. (28.1%)
and C. hyperboreus (9.6%) occurred in group G. In the group H, dominant
species were Paraeuchaeta spp. (52.2%), C. finmarchicus (33.7%),
M. longa (6.1%) and many C. finmarchicus were observed comparing tothe other groups. Paraeuchaeta spp. (55.5%), M. longa (29.9%) andC. glacialis (5.0%) occurred in group I. Paraeuchaeta spp. (43.5%),
M. longa (34.3%) and C. hyperboreus (16.0%) dominated in group J. To
analyze relationship between copepods assemblage and environmental
factor, NMDS was carried out. But this result wasn’t used according to
Clarke and Warwick (2001) because stress value was 0.22.
Seasonal changes on copepod groups identified by cluster analysis on
flux at each station were shown in Fig. 5. Seasonal changes were clearlyobserved in the eastern Fram Strait (St. N-4 and St. HG-IV). Groups E, F
and H occurred in winter (January–March), groups E, F and J were

Fig. 4. Dendrogram showing the Bray-Curtis similarity results based on
zooplankton flux (a). Ten groups (A–J) were identified at 74% similarity.
Numbers in parentheses indicate the number of stations included in each group.
NA: not available. The mean flux and species composition of each group (b).

shown in spring (April–June), group I was observed in summer(July–September) and group I and E occurred in autumn (October–De­
cember). Groups E, H, I and J were observed only in eastern Fram Strait.
In the St. NAPt, copepods community showed no clear seasonal change
and group C was mainly dominant. At St. NHC, occurrences of thegroups C, D, F and G changed within short periods (monthly or every
two weeks). Seasonal change of community structure in NBC was similar
to that of St. NAPt. In the MacKenzie Trough, groups A, B, C, E, F and G
were observed at St. MG and the copepods community exchanged in the
short periods (monthly or every two weeks). At St. MA (shallow), group
B occurred only in winter, and the other seasons were occupied by group
A. In the St. MA (deep), group A and B occurred from autumn, but theoccurrences of groups C, D, F and G were exchanged complexly fromwinter to summer. The groups A and B were observed only in the stationsof MacKenzie Trough (St. MA and St. MG).
4. Discussion
4.1. Zooplankton sampling by sediment trap
For quantitative evaluation of abundance, biomass and distributionof zooplankton species, plankton net sampling is the common method (e.
g., Darnis and Fortier, 2014), although it is known that some large
zooplankton may avoid the net. While zooplankton collected by net
reflect most of the zooplankton in the towed water layers, sediment trapsampling of zooplankton is believed to reflect only the organisms
occurring around the sediment trap depth layer because the sediment
trap depth is fixed at a certain depth (Seiler and Brandt, 1997). This isregarded as a disadvantage and it is argued that sediment trap sampling
therefore does not reflect the zooplankton community as a whole. In
addition, zooplankton seems to be attracted by the trap’s abundancesand by the respective preservatives so that collecting zooplankton withtraps can only be regarded as a semi-quantitative method (see also Lee
7

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Polar Science 24 (2020) 100509

Table 3
Mean flux and contribution in percent for species in clustering groups (cf. Fig. 4a) in the Arctic Ocean. The dominant species were shown based on the contribution
percent according to SIMPER.
Group

Species

Mean flux (ind. m-2 day-1)

Contribution (%)

GroupSpecies

Mean flux (ind. m-2 day-1)

Contribution (%)

A

Paraeuchaeta spp.
M. longa
C. glacialis
C. hyperboreus
Pseudocalanus spp.

156.69
38.82
33.88
7.92
7.33

58.52
19.77
13.21
5.57
1.41

F

Paraeuchaeta spp.
M. longa
C. hyperboreus
C. glacialis
C. finmarchicus

6.28
2.70
0.33
0.46
0.05

70.13
24.68
3.40
1.35
0.29

B

M. longa
H. norvegicus
Pseudocalanus spp.
G. tenuispinus
C. glacialis

9.49
3.47
2.78
1.36
0.67

52.73
20.46
11.97
4.96
4.39

G

M. longa
Paraeuchaeta spp.
C. hyperboreus
H. norvegicus
C. glacialis

7.81
5.66
2.75
1.01
1.06

50.66
28.13
9.55
5.98
4.11

C

M. longa
H. norvegicus
Paraeuchaeta spp.
C. hyperboreus
G. tenuispinus

2.60
2.32
1.82
1.52
0.57

30.38
26.75
11.89
11.80
6.42

H

Paraeuchaeta spp.
C. finmarchicus
M. longa
C. hyperboreus
C. glacialis

16.73
17.41
1.94
1.82
1.78

52.20
33.67
6.06
4.67
3.34

D

M. longa
Paraeuchaeta spp.
H. norvegicus
Chi. obtusifrons
C. hyperboreus

1.36
1.93
0.63
0.45
1.40

40.84
27.49
18.80
12.35
0.52

I

Paraeuchaeta spp.
M. longa
C. glacialis
C. finmarchicus
H. norvegicus

33.92
18.29
3.03
2.76
1.50

55.52
29.94
4.96
4.52
2.46

E

M. longa
Paraeuchaeta spp.
H. norvegicus
G. tenuispinus
C. finmarchicus

4.08
1.50
0.84
0.55
0.14

60.09
16.98
11.43
9.15
1.55

J

Paraeuchaeta spp.
M. longa
C. hyperboreus
C. finmarchicus
H. norvegicus

17.10
13.46
6.26
1.78
0.60

43.52
34.25
15.94
4.52
1.52

Fig. 5. Seasonal changes in occurrence of copepod groups identified by cluster analysis on flux (cf. Fig. 4) at each station in the Arctic Ocean. Copepods groups wereidentified 10 groups (A–J) by Bray-Curtis similarity (cf. Fig. 4). Cross: no data, slash: not available, blank: no sampling.

et al., 1992). However, since high-frequency investigations using
research vessels are very difficult and expensive in the Arctic Ocean
because of sea-ice coverage, very low temperatures and the Polar Night
samples collected by sediment trap is an effective method to clarify
seasonal changes on zooplankton communities in certain depth andallow to explain ecological phenology like life cycles of copepods in the
Arctic Ocean (Tokuhiro et al., 2019). The few studies of zooplankton
collected by means of sediment traps in the Arctic Ocean, reveal

reproducible seasonal changes on community structure of, for instancepelagic amphipods, like Themisto spp. and pteropods Limacina spp. in theeastern Fram Strait (Kraft et al., 2012; Bauerfeind et al., 2014) andseasonal changes on copepod community structure in the Chukchi Sea
and the Beaufort Sea (Makabe et al., 2010; Matsuno et al., 2014, 2015;2016; Tokuhiro et al., 2019). Thus, despite the disadvantages, thesampling of zooplankton swimmers with sediment traps have been
gradually recognized as an approach for evaluating seasonal change of8

K. Tokuhiro et al.

Polar Science 24 (2020) 100509

copepod community in recent years. In this study, seasonal changes in
the copepod community clearly showed different patterns in eachregion.

Fram Strait and the MacKenzie Trough. M. longa is omnivore,
H. norvegicus and Paraeuchaeta spp. are carnivore (Conover and Huntley,
1991; Nishida and Ohtsuka, 1996; Dvoretsky and Dvoretsky, 2015).
Paraeuchaeta spp. have a large body mass and thus need much moreenergy for growth compared with M. longa and H. norvegicus (Ashijian
et al., 2003; Kosobokova et al., 2007; Dvoretsky and Dvoretsky, 2015).
In this region, seasonality of sea ice concentration was like observed in
the MacKenzie Trough, but surface Chl. a concentration was much lower
than that of the Fram Strait and the MacKenzie Trough, as primary
production is also thought to be low in the Canada Basin (Arrigo et al.,2008; Pabi et al., 2008). Therefore, Paraeuchaeta spp. could eventually
not obtain enough food for completing their life cycle because of too few
small copepods as a prey due to low primary production. This might be
the reason why flux and abundance of Paraeuchaeta spp. was low in the
copepod community.
Short-term seasonal change was observed only at St. NHC in the
Canada Basin. Mooring condition (bottom depth and sediment trap
mooring depth) and seasonal change of copepod communities of St. NHC
was like St. MA and St. MG in the MacKenzie Trough rather than St.
NAPt and St. NBC. Moreover, surface zooplankton is transported by aneddy from the continental shelf to the Canada Basin during summer(Llin�
as et al., 2009) and the continental species C. glacialis appeared at
St. NHC in this study. Lane et al. (2008) also reported that high abun­dances of zooplankton around St. NHC was observed due to horizontal
inflow from the continental shelf. Therefore, the observed complex
changes in community structures within the large copepods may becaused by these transport mechanisms of zooplankton from the conti­
nental area. In summary, due to influence of bottom depth, sediment
trap depth and transportation from the continental area, the copepod
community structure of St. NHC exhibits the most complex resembling
short-term changes of the here investigated Arctic regions.

4.2. Fram Strait
In the eastern Fram Strait, the copepod community changed clearly
during the season. The group H was observed during spring only ineastern Fram Strait and was characterized by a dominance of
C. finmarchicus. C. finmarchicus is known to be distributed in the Atlantic
sector (e.g., Barents Sea) of the Arctic Ocean, but does not occur in the
Pacific sector (Conover, 1988). However, only a few populations were
found near St. N-4 and St. HG-IV (Conover, 1988; Hirche and Kosobo­
kova, 2007) originally. In addition, copepodite stage 6 male (C6M) was
dominant (maximum 76%) when the peak of this species was observed(data not shown). In the Barents Sea, C6M in C. finmarchicus occur fromFebruary to March, but they did not dominate the population and they
disappeared quickly (Tande, 1982). This may show that adult males
have a short life-period. Fram Strait is affected by inflow of the East
Greenland Current (EGC) from the north, the West Spitzbergen Current(WSC) from the south and the Return Atlantic Current (RAC) from theEast, and these currents (WSC and RAC) were most intense during spring€ller et al., 2012; Armitage et al., 2017). From these(Beszczynska-Mo
facts, C6M of C. finmarchicus is thought to be transported from coastal
areas of Greenland and/or Svalbard archipelago by WSC and RAC dur­ing spring, and they eventually reached the end of their life-period, andweakened individuals finally sunk and were collected by the traps.
Paraeuchaeta spp. and M. longa always appeared in the trap samples
because the distribution depth of P. norvegica and P. glacialis in eastern
Fram Strait is between 0 and 200 m depth (Laakmann et al., 2009) and
M. longa mainly occurs at 100–500 m water depth (Conover and Hunt­ley, 1991; Ashjian et al., 2003). C. hyperboreus appeared in spring andautumn. It is known that this species conducts seasonal vertical migra­
tion (Hirche, 1997), therefore, this movement seems to affect theirappearance in the trap samples. In contrast, C. glacialis was mainly
observed during autumn. This species usually occurs over continental
shelves (Darnis et al., 2008), but few individuals of the population
appear in this study area during sampling (Conover, 1988; Hirche et al.,1991). Whereas many C. glacialis were observed at a 1500 m depth layer
in late autumn in southern Greenland Sea (Hirche, 1991). Thus, thisspecies may have been transported by currents from coastal areas (e.g.,
Svalbard archipelago) and must also perform vertical migration in lateautumn. Therefore, movement and distribution depth of respective
species may cause clearly seasonality of copepods community.
In the Fram Strait, a strong seasonality of sea ice concentration
wasn’t observed, thus Chl. a was detected for a long time only inter­
rupted by short sea ice coverage periods. It is reported that sea ice in the€ller et al.,Fram Strait is affected by the Atlantic Water (Beszczynska-Mo2012). Although a relationship between environmental factors (SIC and
Chl. a) and copepod community structure wasn’t analyzed statistically
due to lack of environmental data in this study, obvious relationships
were not observed by comparing with figures except for current. Thismeans that there are several steps in the process until copepod com­munities get effected by sea ice melting and freezing. Thus, since only
relationship between current and copepods community structure wasthought to be observed in this study, seasonality as well as variability ofcurrent patterns may have affected the variability of copepod commu­
nities in the Fram Strait the most.

4.4. MacKenzie TroughIn the MacKenzie Trough, group A occurred frequently, and group B
was observed only during winter. Average flux of group A was higher
than those of the other groups. Paraeuchaeta spp., M. longa andC. glacialis were characteristically dominated in group A. Because
C. glacialis is a continental shelf species (Darnis et al., 2008), they were
thought to be observed in St. MA and St. MG where are shallow bottom
depth and locate near continental shelf. According to Darnis et al.
(2008), large copepods composed in order to C. glacialis, C. hyperboreus,
M. longa and P. glacialis using plankton net samples in continental shelfof the Beaufort Sea, and P. glacialis showed low abundance andH. norvegicus did not occur. In the slope area, however, the large co­pepods were abundant in order to M. longa, C. hyperboreus, C. glacialis,
P. glacialis and H. norvegicus, and the numbers of P. glacialis andH. norvegicus were low. In contrast, during this study, Paraeuchaeta spp.
and C. glacialis were dominant in group A and M. longa was abundant ingroup B, and composition of Paraeuchaeta spp. was much greater thanthat of net sampling (Darnis et al., 2008). This species is known to be a
cruising feeder swimming actively when they feed on small copepods(Almeda et al., 2017), and this behavior may be a positive factor to becollected by sediment traps.
Moreover, we compared samples among St. MA (shallow, 72 m), St.
MG (shallow, 125 m) and St. MA (deep, 172 m) to analyze effect of trap
depth because St. MA and St. MG deployed near and mooring period
were same. Group A occurred when the sediment trap depth was shal­
lower, and the other groups (e.g., group G and group F) were observed as
the sediment trap depth was deeper. Also, Paraeuchaeta spp. andC. glacialis showed higher abundances at shallow depth and that of
M. longa and C. hyperboreus increased with deeper sediment trap depth.
These facts mean that vertical distribution of the various species over­lapped at deep sediment trap depth. Thus, community structure inshallow depth of the MacKenzie Trough showed no seasonal changes inthe dominance of Paraeuchaeta spp. and C. glacialis because all the other

4.3. Canada Basin
Seasonal changes of community structure in St. NAPt and NBC were
not observed, and group C occupied the water column close to the trap
during almost during all periods. Average flux of group C was low andpercentages of M. longa and H. norvegicus were high. Also, share of
Paraeuchaeta spp. in St. NAPt and St. NBC were lower than those in the9

K. Tokuhiro et al.

Polar Science 24 (2020) 100509

large species (C. hyperboreus and M. longa) didn’t overlap in the shal­
lower layer. Flux of Paraeuchaeta spp. and C. glacialis decreased withincreasing depth and distribution depth of the other species overlapped.
Hence complex seasonal changes of copepod community structures wereobserved at deeper layers.
In the MacKenzie Trough, sea ice concentration changed like in the
Canada Basin and surface Chl. a was higher than the other regions.
Neither remarkable (St. MA shallow) nor short-term (St. MG and St. MAdeep) seasonality of community structure was observed in this region.
Especially, high-flux group A was observed throughout the year, whichwasn’t observed in the other regions. This may be induced by small
sediment trap open area (0.125 m2).
Since only one-year observation was performed in the MacKenzie
Trough, we cannot consider the observed species compositions found in
the trap samples as the usually occurring structure. Based on same thesampling program in 2009–2010, maximum flux of Paraeuchaeta spp.
was 971 ind. m 2 day 1 at St. MA (shallow) and 701 ind. m 2 day 1 St.
MG (shallow), and Paraeuchaeta spp. dominated (data not shown)similar to results of this study. In addition, Dezutter et al. (2019) re­
ported that high flux of C. glacialis was observed in sediment trap sam­ples at the MacKenzie Trough, although interannual variability wasobserved. Thus, the tendency we found is thought to be a common
feature of sediment trap samples over the MacKenzie Trough eventuallycaused by high concentrations of surface Chl. a across the MacKenzie
Trough compared to all other regions investigated in this study.

copepods community structures in all region.
Seasonal changes of copepod community structures within Arctic
Ocean was shown to be quite different between the three regions in thisstudy. It was additionally discussed that these differences were influ­
enced by several environmental factors (sea ice concentration, current
patterns, endemic species occurrence and the amount of primary pro­duction). These discussions couldn’t be obtained when only using
plankton net sample collected during the short Arctic summer. However,also variations of mooring situations (e.g., mooring periods, depth andsite) between regions seemed to affect the seasonal change of large co­pepods community structure in this study. Therefore, for more robust
comparison, exhaustive observation webs of sediment traps and com­
parison of seasonal changes within same deployment depths and same
sampling periods are required for different regions in the Arctic Ocean.
Acknowledgements
We would like to thank captain and crew of Japan agency for MarineEarth Science and Technology RV Mirai, Alfred Wegener InstituteHelmholtz Centre for Polar and Marine Research (AWI) RV Polarstern
and Canadian Coast Guard RV Amundsen and IB S.W. Laurier. We also
thank Nadine Knüppel at the AWI for picking copepods in Fram Strait
samples. We also express our sincere thanks to support Program forOverseas Visits by Young Researchers of Arctic Challenge for Sustain­
ability (ArCS). Part of this study was supported by a Grant-in-Aid for
Scientific Research 19H03037 (B), 18K14506 (Early Career Scientists)
and 17H01483 (A) to KT, 22221003 (S), 15H05712 (S) to NH,
15H01736 to JO from the Japan Society for the Promotion of Science(JSPS).

4.5. Regional comparison
Seasonal changes of copepods community structure obtained withsediment trap samples showed large variations among the investigatedregions, and in summary, three patterns of seasonal changes wereobserved in this study: clear seasonal changes (eastern Fram Strait), no
seasonal change (Canada Basin) and changes within short periods(MacKenzie Trough). The following three points could be mentioned asfactor of these differences. First point is the influence of the sediment
trap depth. With or without seasonal change we found differences only
due to the chosen sediment trap depth in the MacKenzie Trough sam­ples, and group A which showed a high flux rate, was observed mainly atshallow depths. Therefore, effects of sediment trap depth should not beignored for evaluating zooplankton community by sediment traps.
Second point is horizontal transportation of copepods by currents.
Ocean-specific community (e.g., group H) characterized by
C. finmarchicus was observed only in the Fram Strait due to the inflow of
the Atlantic water. Also, transportation from shelf areas led to specificshort-term changes in community structures at St. NHC even in Canada
Basin where usually little seasonality is reported. Third point is thehydrographic environment and related to this as biological factor,
especially primary production here expressed as surface Chl. a concen­
tration. The latter was quite high over the MacKenzie Trough, but low inthe eastern Fram Strait and the Canada Basin (Arrigo et al., 2008; Pabi
et al., 2008; in this study), and copepod fluxes showed the same pat­terns. In addition, dominant species of group A, which had the highest
flux of all samples examined, were observed in the eastern Fram Strait
and Canada Basin, but they were especially abundant in group A. If thisfact is true, not only flux but also dominant species of copepods would be
driven rather by the feeding environment (primary production) than by
anything else between regions in the Arctic Ocean. However, in thisstudy, relationship between seasonal change of sea ice concentrationand copepods community structure was complex. In the Fram Strait, sea
ice concentration showed diffuse seasonal changes, but the copepods
community structure exhibited a clear seasonality. In the Canada Basin,seasonal change of sea ice concentration was evident and copepods
community structure didn’t show any variation. In the MacKenzie
Trough, remarkable seasonal changes of sea ice concentration andshort-term seasonal change of copepods communities were observed.
Thus, seasonality of sea ice concentration may not affect directly large

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