Deep–Sea Research II 181-182 (2020) 104901

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Deep-Sea Research Part IIjournal homepage: http://www.elsevier.com/locate/dsr2

Seasonal changes in the zooplankton community and population structurein the northern Bering Sea from June to September, 2017
Fumihiko Kimura a, *, Yoshiyuki Abe b, c, Kohei Matsuno a, d, Russell R. Hopcroft e,
Atsushi Yamaguchi a, daFaculty/Graduate School of Fisheries Sciences, 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
Research Development Section, Office for Enhancing Institutional Capacity, Hokkaido University, Kita 21, Nishi 10, Kita-ku, Sapporo, Hokkaido, 001-0021, Japand
Arctic Research Center, Hokkaido University, Kita-21 Nishi-11 Kita-ku, Sapporo, Hokkaido, 001-0021, Japane
Institute of Marine Science, University of Alaska, Fairbanks, AK99775-7220, USAbc

A R T I C L E I N F O

A B S T R A C T

Keywords:
Northern Bering sea
Seasonal changes
Zooplankton community
Population structure
Copepods
Chaetognaths
Appendicularians

Zooplankton community structure in the northern Bering Sea may change significantly over relatively shortperiods due to the inflow of different water masses and the seasonal release of meroplankton, although details ofthese changes are still unclear. We studied the zooplankton community in the northern Bering Sea from June to
September of 2017 and examined seasonal changes in the community structure and stage structure of thedominant species. Zooplankton abundance ranged from 41,000 to 928,000 ind. m− 2, with the greatest abun­dances near 174◦ W during July. Copepods were the dominant taxa, comprising 10–98% of zooplankton abun­dance, with benthic larvae such as bivalves dominant at some stations during July and August. Cluster analysis ofabundances divided the station/zooplankton communities into seven groups. West of 172◦ W, clear seasonalchanges were not observed, because the Bering Chukchi Winter Water persisted in the deep layer and sampling
was only conducted in this region in July and August. In contrast, the community structures east of 172◦ W
differed every month due to water masses changes, meroplankton release, and copepod production associatedwith the phytoplankton bloom. Despite the changes of water mass, development for the dominant large copepods(Calanus glacialis/marshallae, Eucalanus bungii and Metridia pacifica) was revealed from their population stage
structures. Seasonal shifts in species within Neocalanus and appendicularians were driven by water mass ex­changes. This study demonstrates that zooplankton community in the northern Bering Sea varies substantially ona monthly time scale. Therefore, to evaluate the impact of climate change on zooplankton, it is important toconsider both the seasonal period and the dominant water masses present.

1. Introduction
The northern Bering Sea is a shallow shelf-sea with a depth ofapproximately 50 m connecting the Arctic Ocean to the remainder of theBering Sea. It has high productivity that supports zooplankton, benthos,fish, marine mammals and seabirds due to its massive phytoplankton
blooms and advection of plankton in the Anadyr Water (Springer et al.,
1989, 1996; Springer and McRoy, 1993). In recent years, the magnitude
and timing of the phytoplankton bloom has changed with the timing of
the sea-ice retreat (Fujiwara et al., 2016). For instance, the timing of thesea-ice retreat was approximately two weeks earlier in 2018 than inprevious years, influencing the marine ecosystem; the magnitude of thebloom caused by ice algae was small and zooplankton abundance
decreased (Cornwall, 2019; Fukai et al., 2019). Decreased sea ice also
diminished the deep cold pool (<2 ◦ C) south of St. Lawrence Island andfish shifted northward and their abundance decreased in the south­
eastern region (Cornwall, 2019; Duffy-Anderson et al., 2019). Thus, themarine ecosystem of the northern Bering Sea is facing rapid changes
with sea-ice variations (Huntington et al., 2020).
The area has a complicated hydrographic environment due to the
inflow of multiple currents with different hydrographic features. Threetypes of water masses enter this region from the south (Springer et al.,
1989; Danielson et al., 2017) and are defined largely by salinity: Alaskan
Coastal Water (ACW; S > 31.8), Bering Shelf Water (BSW; 31.8 <S <* Corresponding author.
E-mail address: f.kimura@fish.hokudai.ac.jp (F. Kimura).
https://doi.org/10.1016/j.dsr2.2020.104901
Received 13 December 2019; Received in revised form 22 October 2020; Accepted 4 November 2020
Available online 13 November 20200967-0645/© 2020 Elsevier Ltd. All rights reserved.

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F. Kimura et al.

Fig. 1. Locations of the sampling stations in the Northern Bering Sea during June through September 2017. Color of the circles indicated spatial and vertical
distribution of the water mass as defined by Coachman et al., (1975) (cf. Fig. 3).
Table 1
Zooplankton samples used in this study. All samples were collected with vertical hauls of 150-μm mesh size nets but with slightly different net diameters on different
vessels (60 cm for R/V Sikuliaq, 45 cm for T/S Oshoro-Maru and R/V Mirai).
Date

D/N

StationLatitude (N)Longitude (W)Towed depth (m)VesselJune 23, 2017
June 24, 2017
June 24, 2017
June 24, 2017
June 25, 2017
June 25, 2017
June 25, 2017
July 11, 2017
July 11, 2017
July 12, 2017
July 18, 2017
July 18, 2017
July 19, 2017
July 19, 2017
July 22, 2017
August 26, 2017
August 26, 2017
August 27, 2017
August 27, 2017
August 27, 2017
August 27, 2017
September 20, 2017
September 20, 2017
September 20, 2017

Night
Day
Day
Day
Night
Day
Day
Day
Day
Day
Day
Day
Night
Day
Night
Day
Night
Night
Day
Day
Day
Day
Day
Day

CBW15
CBW13
DBO2.4
CBW9
CBW7
CBW5
CBW3
OS5
OS6
OS7
OS16
OS17
OS18
OS19
OS24
MR1
MR2
MR3
MR4
MR5
MR6
MR109
MR110
MR111

65◦ 30′65◦ 14′64◦ 58′64◦ 41′
64◦ 25′64◦ 09′63◦ 53′65◦ 45′65◦ 20′65◦ 03′64◦ 15′64◦ 00′63◦ 45′63◦ 30′63◦ 00′63◦ 06′63◦ 52′64◦ 43′65◦ 03′65◦ 16′65◦ 39′65◦ 39′65◦ 16′65◦ 04′168◦ 49′169◦ 21′169◦ 53′170◦ 26′170◦ 58′171◦ 31′172◦ 03′168◦ 09′168◦ 54′169◦ 38′171◦ 26′171◦ 57′172◦ 29′173◦ 00′174◦ 05′174◦ 01′172◦ 18′170◦ 21′169◦ 36′169◦ 03′168◦ 42′168◦ 43′169◦ 03′169◦ 36′

53
45
43
45
40
41
43
39
50
46
42
48
43
60
71
71
50
43
46
48
44
44
48
45

Sikuliaq
Sikuliaq
Sikuliaq
Sikuliaq
Sikuliaq
Sikuliaq
Sikuliaq
Oshoro-Maru
Oshoro-Maru
Oshoro-Maru
Oshoro-Maru
Oshoro-Maru
Oshoro-Maru
Oshoro-Maru
Oshoro-Maru
Mirai
Mirai
Mirai
Mirai
Mirai
Mirai
Mirai
Mirai
Mirai

2

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sizes by researchers has hampered prior attempts to examine season­
ality, but the recent panArctic adoption of the 150-μm mesh (Gill et al.,2011) by many researchers is resolving this limitation (e.g. Hopcroft
et al., 2010; Ershova et al., 2015b).
In this study, we collected zooplankton samples using plankton nets
with 150-μm mesh in the northern Bering Sea during 2017 to examine
seasonal changes in the structure of the zooplankton community. Hy­
drographic data and zooplankton samples were collected each monthfrom June to September (a total of 4 times). Zooplankton community
composition and its association with station location were analyzed. The
development and reproduction of copepods, chaetognaths and appen­
dicularians were evaluated based on seasonal changes in their popula­tion structure.
2. Materials and methods
A total of 24 zooplankton collections were taken by the T/S OshoroMaru, R/V Mirai, and R/V Sikuliaq in the northern Bering Sea (63◦ 65◦ 75′ N, 168◦ 09′ -174◦ 05′ W) during June 23–25, July 11–22, August
26–27 and September 20, 2017 (Fig. 1, Table 1). Zooplankton samples
were collected by vertical tows with a NORPAC net (mouth diameter: 45
cm; mesh size: 150 μm) or twin ring nets (mouth diameter: 60 cm; meshsize: 150 μm) from 5 m above the bottom to the surface during either day
or night. The volume of water filtered through the net was estimatedusing a one-way flow meter mounted in the mouth of the net.
Zooplankton samples were immediately preserved using 5% v/v borax
buffered formalin. At all stations, temperature, salinity and fluorescencewere measured using vertical casts of a CTD (Sea-Bird Electronics Inc.,
SBE 911 Plus) and a fluorometer package (Model FLRTD by Wetlabs Inc.
or Fluorometer by Seapoint Sensors, Inc.). Water masses were classified
by salinity according to Coachman et al. (1975).
Post cruise, zooplankton samples were split using a box splitter(Motoda, 1959). Zooplankton in the aliquots were identified andenumerated under a dissecting microscope. Calanoid copepods wereidentified to species and copepodid stage level. Identification of co­
pepods followed Brodsky (1967), Calanus glacialis and Calanus mar­shallae were treated as C. glacialis/marshallae in this study because of the
difficulty of species level identification (Frost, 1974). Gonad maturation
for adult females of the dominant copepod species was evaluated asstage I (immature), stage II (small oocytes in the ovary or oviduct) andstage III (large eggs or distended opaque in oviduct) (Miller et al., 1984;
Miller and Clemons, 1988; Niehoff, 1998). Mean Copepodid Stage (MCS)of the dominant large copepods (C. glacialis/marshallae, Eucalanus bungiiand Metridia pacifica) was calculated using the following equation:∑6i=1 i × Ai
MCS = ∑
6
i=1 AiFig. 2. Vertical sections of temperature, salinity and fluorescence across thetransects of the Northern Bering Sea during June through September 2017.
Solid triangles indicate the western end of the St. Lawrence Island.

32.5) and Anadyr Water (AW; S < 32.5) (Coachman et al., 1975). Since
zooplankton communities differ in each water mass (Springer et al.,1989), community composition changes longitudinally in this region(Ozaki and Minoda, 1996). Focusing on particular species, the appen­
dicularians Oikopleurea labradoriensis and O. vanhoeffeni may be in­dicators of Anadyr Water and Bering Shelf Water, respectively, because
their original distributions were different within the Bering Sea (Shiga,
1982, 1993a, 1993b). By contrast, Pacific copepods input to the north­ern Bering shelf are governed by the transport volume of Anadyr Water(Springer et al., 1989).
The species composition of the zooplankton communities can change
significantly with water mass and the sudden appearance of mer­
oplankton (Matsuno et al., 2011; Eisner et al., 2013). Barnacle larvae areoften the dominant meroplankton on the Bering Sea Shelf where they
may exceed 90% of zooplankton abundance (Matsuno et al., 2011). Witha planktonic period of only 2–3 weeks (Herz, 1933), meroplankton canchange the zooplankton community structure within a short period.
During the phytoplankton bloom in the Chukchi Sea, sudden increases inmeroplankton abundance can change the zooplankton community
structure in a period of weeks (Questel et al., 2013). The large seasonalvariations in the zooplankton community must be taken into account if
accurate evaluation of interannual changes compared to sea-ice extent
in the Chukchi Sea (Ershova et al., 2015a). In addition, despite reportsthat water masses change seasonally at Bering Strait (Woodgate et al.,2010), most studies of the zooplankton community in this region are
based on snapshot observations. To overcome these problems, at least
monthly sampling is needed. The use of inconsistent plankton net meshwhere i (1–6 indicate C1–C6) indicates the copepodid stage for a species,
Ai (ind. m− 2) is the abundance of a copepodid stage (cf. Marin, 1987).
Total lengths (TL, mm), from the top of the head to the end of the bodywithout the caudal fin, of the dominant chaetognath. Parasagitta elegans
was measured using calipers for large specimens (TL ≥ 10 mm) or an
ocular micrometer for small specimens (TL < 10 mm) to a precision of
0.1 mm. Based on gonadal maturation, P. elegans was classified into fivestages: juvenile, stages I, II, III, and IV (Terazaki and Miller, 1986). The
identification of appendicularians followed Shiga (1993a) and Choe andDeibel (2008). The trunk length of Oikopleura spp. was measured with a
precision of 0.1 mm using an ocular micrometer under astereomicroscope.
The nonparametric Mann-Whitney U test was carried out to test
whether there were significant difference in abundance (total abun­dance, copepod abundance and euphausiid abundance) between day
and night sampling times. This analysis was carried out using Statview(SAS Institute Inc.). Abundance data (X: ind. m− 2) for each species weretransformed to the fourth-root (X− 4) prior to cluster analysis in order to3

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Fig. 3. T-S diagrams from the Northern Bering Sea during June through September 2017. Numbers and isolines indicate water density. Data from specific stations
identified with labels. ACW: Alaskan coastal water, BSW: Bering Shelf water, AW: Anadyr water (cf. Coachman et al., 1975).

reduce the bias of abundant species. Similarities between samples were
examined using the Bray-Curtis index according to differences in species
composition. For grouping samples similarity indices were coupled withhierarchical agglomerative clustering and the complete linkage method(unweighted pair group method using arithmetic mean: UPGMA).
Nonmetric multidimensional scaling (NMDS) ordination was carried out
to delineate the sample groups on a two dimensional map. Multiple
regression analysis was carried out for dependent hydrographic vari­ables (latitude, longitude, depth, mean water column temperature,mean water column salinity and integrated water column fluorescence(the summation of the fluorescence values from the water column) andtwo dimensional NMDS as independent variables. PERMANOVA wascarried out to determine the variables that significantly affected clustergrouping. These included sampling day, water mass and their interac­tion. The analyses were carried out using Primer7 software (PRIMER-E
Ltd.). Intergroup differences in the abundance of each species andzooplankton taxon were tested with one-way ANOVA. If the ANOVA
identified statistically significant differences (p < 0.05), a Tukey-Kramer
post hoc test was carried out to clarify the interaction between groups.
To clarify the factors that governed the MCS of the dominant large co­pepods (C. glacialis, E. bungii and M. pacifica), an analysis of covariance(ANCOVA) was performed using Statview (SAS Institute Inc.), with the
day of the year and water mass as independent variables. A cohort
analysis was made of P. elegans TL data with the aid of Microsoft Excel

Solver (Aizawa and Takiguchi, 1999). It is difficult to quantitatively
capture euphausiids with nets due to net avoidance (Wiebe et al., 2004).
Therefore, euphausiids were not included in population and lifecycle
analyses.
3. Results
3.1. Hydrography
We identified three water masses in our study. Anadyr Water (AW,>32.5 salinity) was present every month, but dominated all layers
during June and in the eastern region during July. Bering Shelf Water(BSW, 31.8–32.5 salinity) was observed every month, particularly at
depth for the western stations during July and August. Alaskan Coastal
Water (ACW, salinity <31.8) was seen at the surface in the Bering Strait(stn. OS5) and west of St. Lawrence Island during July (stn. 16–24),
during August (stn. MR1 and MR2), and at the surface of stn. MR109
during September. Water temperature in the study ranged from − 1.4 to
10.1 ◦ C. A thermocline was present at approximately 20 m depth during
July and August and was particularly strong to the west of 172◦ W.
Salinity ranged from 31.3 to 32.9 and was freshest in the surface layerwest of 172◦ W. Chlorophyll fluorescence ranged from 0.09 to 4.94, witha phytoplankton bloom (>4) in the upper half of the water column
occurring to the east of 172◦ W during August and September (Figs. 2 and4

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abundance (total abundance, copepod and euphausiid abundance) be­
tween day and night. During June, abundances were similar between
stations (144,436–268,357 ind. m− 2) except stn. CBW15 that was
dominated by Anadyr Water. The zooplankton community structure
there was dominated by copepods, copepod nauplii and polychaeta(Fig. 4). During July, abundances varied greatly between stations, thegreatest (927,498 ind. m− 2) at 174◦ W and the lowest (41,127 ind. m− 2)
northwest of St. Lawrence Island near 172◦ W. Copepods still dominated,but bivalvia larva were the most dominant taxa at some of the stations.
During August, copepods comprised 98% of zooplankton abundance at
the most western station, but meroplankton (bivalvia larva, barnacle
larva and echinopluteus larva) dominated at the other stations. During
September, copepods and copepod nauplii dominated (Fig. 4). Twelve
genera of copepods were identified (Table 2). Among these species,
E. bungii, M. pacifica, N. cristatus, N. flemingeri and N. plumchrus werecategorized as Pacific species.
Based on the cluster analysis of taxa abundance, stations werecategorized based on zooplankton communities and separated into
seven groups (A–G) at 64 and 70% similarity (Fig. 5a). The environ­mental variables significantly affecting cluster analysis were longitude,
sampling depth, mean water column salinity and integrated water col­umn fluorescence (Fig. 5b). Mean group abundance was the highest forgroup G and the lowest for group B. Groups A, B, C and F were char­acterized by the dominance of copepods Pseudocalanus spp. and Cyclo­
poida, while Groups D, E and G were characterized by the dominance ofbivalvia and echinopluteus larvae (Fig. 5c). The distributions of eachgroup changed greatly during the year but not west of 172◦ W during
July and August (Fig. 6). To the east of 172◦ W, Group A occurred during
June, Groups A, B and C occurred during July, Groups D and E occurred
during August, and Group F occurred during September. On the other
hand, to the west of 172◦ W, Groups C and G occurred during July andAugust. The hydrography (salinity and temperature) was similar withineach group (Fig. 7). Note that there were no stations conducted to thewest of 172◦ W in September. The groups observed east of 172◦ W weremainly distributed in AW. PERMANOVA indicated that sampling day,water mass and their interaction significantly affected the clustergrouping (Table 3).
The one-way ANOVA test for intergroup differences identified thecharacteristic taxa within each station group (Table 2). Euphausiids
were important for Group A, Oikopleura vanhoeffeni for Group D, Acartia
spp. and cladocerans for Group E, and Calanus nauplii for Group F. Some
species were important in two groups including Limacina helicina inGroups B and D, barnacle nauplii in Groups D and E, and Centropages
spp. in Groups E and F (Table 2).
3.3. Copepod population structure
The population structures of C. glacialis/marshallae, E. bungii and
M. pacifica changed seasonally. For C. glacialis/marshallae, E. bungii and
M. pacifica, copepodid stages I (CI) to IV (CIV) were abundant during
June and decreased by August. In contrast, copepodid stage V (CV) was
dominant during August. All copepodid stages of Pseudocalanus spp.
appeared throughout the observation period but no clear change
occurred in their population structure (Fig. 8).
Calanus spp. and Pseudocalanus spp. nauplii occurred in June, Augustand September, Calanus spp. nauplii were greater in abundance during
September and Pseudocalanus spp. nauplii were greater during June in
the eastern region (Fig. 9). E. bungii nauplii abundances were greater inJune in the eastern region and near 172◦ W.
C. glacialis/marshallae adult females occurred in June, August and
September (Fig. 8), and reproductively mature adult females wereobserved each month (Fig. 10). Adult females of E. bungii andN. flemingeri occurred only in July, approximately 40–50% of whichwere reproductively mature. Adult females of M. pacifica occurred
during every month but reproductively mature females were seen onlyin September. Adult females of Pseudocalanus spp. with a high ratio ofFig. 4. Monthly changes in total zooplankton abundance and species compo­
sition in the northern Bering Sea during June through September 2017. Solidtriangles indicate the western end of St. Lawrence Island.

3).
3.2. Zooplankton community
The zooplankton community composition changed every month with
abundances ranging from 41,127 to 927,498 ind. m− 2. According to theMann-Whitney U test, there were no significant differences in5

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Table 2Comparisons of abundance in the northern Bering Sea during June through September of 2017. Values are mean abundance in eachgroup of stations. Differences between groups were tested using one-way ANOVA and the Tukey-Kramer HSD post hoc test. Groups notconnected by underlines are significant different (p < 0.05). *: p < 0.05, **: p < 0.01, ***: p < 0.001.

reproductively mature females occurred during every month. For
C. glacialis/marshallae, E. bungii and M. pacifica, the association of themean copepodite stage (MCS) with day of the year and water mass type
(ACW, BSW, AW) was evaluated using ANCOVA; none were associatedwith water mass, but all had a positive correlation with day of the year
(Table 4, Fig. 11). MCS indicated no significant difference within watermass, but large divisions might be affected by the difference in watermass. Notably, development of C. glacialis/marshallae was faster from
June to July and slower after August when most individuals had reachedCV.
Seasonal occurrence of the three species of Neocalanus spp. differedamong species: N. cristatus occurred during June through July,

N. flemingeri occurred from June to August, and N. plumchrus occurred
during September (Fig. 12). For these three species, CI–CIII were notobserved (Fig. 12). N. cristatus was composed of CIV-CV, N. flemingeri of
CIV, CV, adult male and adult females, and N. plumchrus of CIV-CV.
3.4. Chaetognatha
Parasagitta elegans was the predominant chaetognath species with
only trace occurrences of Eukrohnia hamata at several stations andabundance for the two species ranging from 90 to 2486 ind. m− 2 and
0–45 ind. m− 2, respectively. P. elegans TL separated into one or twocohorts (Fig. 13). The mean TL of each cohort ranged from 2.7 cm (small
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Fig. 5. (a) Dendrogram showing Bray-Curtis similarity results for zooplankton abundance. Eight groups (A–G) were identified at 64 and 70% similarity. (b)Nonmetric multidimensional scaling plots of the seven groups, with arrows indicating directions of environmental parameters. (c) The mean abundance andtaxonomic composition of each group; only groups with a high % composition are separated. Depth: sampling depth (5 m off of the sea floor), IF: integrated watercolumn fluorescence, MS: mean water column salinity, Lon.: longitude.

cohort in August) to 16.1 cm (large cohort in August). The abundance ofsmaller individuals was greater in June than in other months. Matureindividuals were typically over 22 mm length and occurred during
August and September.

water mass on the zooplankton community. In this study, by same
sampling for four straight months, we found that the zooplankton
community and population structure for dominant species vary sub­stantially on a monthly time scale in the northern Bering Sea.
Separate summer (Springer et al., 1989) and autumn (Pinchuk andEisner, 2017) communities have been reported previously in thenorthern Bering Sea, but seasonal changes in zooplankton during eachmonth have not been studied previously. In the southern Chukchi Sea,
the zooplankton community showed interannual changes with sea-ice
reduction and water mass changes (Ershova et al., 2015a). However,the sampling periods were different among years, creating unclear
long-term trends due to large yearly variation. The biomass of Pacificzooplankton carried onto the northern Bering shelf is governed by thevolume transport of Anadyr Water (Springer et al., 1989). According toMatsuno et al. (2011), the zooplankton community was changed byincreased Pacific Water inflow; however, monthly changes were notexplicitly evaluated in that paper. Resolving seasonal variability is
critical for evaluation of long-term trends for zooplankton influenced bysea-ice variation and climate change in the northern Bering Sea, as wellas in the Chukchi Sea.
In the northern Bering Sea, seasonal change patterns for water
masses were different east and west of 172◦ W. West of 172◦ W a twolayer structure was observed with dominance of ACW in the surface

3.5. Appendicularia
The appendicularians Fritillaria spp., O. labradoriensis andO. vanhoeffeni occurred in abundances ranging from 0 to 23,615, 0–4415
and 0–16,345 ind. m− 2, respectively. Fritillaria spp. was usually thedominant taxon. Species composition and trunk length of Oikopleura
showed that smaller individuals (less than 1 mm trunk length) pre­dominated (Fig. 14). A clear seasonal change in species composition wasobserved: O. labradoriensis dominated in June and July while
O. vanhoeffeni dominated in August and September (Fig. 14).
4. Discussion
4.1. Seasonal changes in community structure
Most of the previous studies of zooplankton community in thenorthern Bering Sea were based on snapshot observations, and becauseof this, it has been difficult to examine short term impacts of changes in7

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Fig. 6. Horizontal distributions of the seven station groups identified using Bray-Curtis similarity cluster analysis based on zooplankton abundance (cf. Fig. 5a) in thenorthern Bering Sea during June through September 2017.

layer and BSW in lower layers during July and August. It is unusual for
ACW to appear west of St. Lawrence Island. East of 172◦ W, AW was
dominant at lower depths during all seasons but the water masses in thesurface layer changed seasonally.
West of 172◦ W, only two zooplankton communities (Groups C and G)
occurred during July and August. Group G occurred most westerly andshowed the highest abundance through the sampling period. In theprevious studies, it was reported that zooplankton community structure
was strongly related to bottom water mass because large-sized
zooplankton were concentrated in the bottom layer (Coyle et al.,
1996; Eisner et al., 2013; Questel et al., 2013; Ershova et al., 2015a,
2015b). Therefore, the zooplankton community of the western region
may be affected by cold water masses that occur in the bottom layer inthis region. Although not significant, more C. glacialis/marshallae
occurred in Groups C and G than in other groups suggesting that these
species are mainly distributed in cold water masses in the bottom layer.
In the Bering and Chukchi seas, the biomass of C. glacialis is strongly
correlated with Bering Chukchi Winter Water, with temperatures lessthan 0 ◦ C (Pinchuk and Eisner, 2017). The population migrates down
into the lower layer by winter convection (Coyle et al., 1996).

Additionally, the towing depth of plankton nets at stations in Group G
were deeper than for the other groups (average 67 vs 45 m). Thus, theoccurrence of Group G could be associated with a deeper water mass
with high zooplankton density and the greater towing depth of the net.
In this study, since cold water masses occurred in the bottom layer of thewestern region during July and August, the community structures ofGroups G and C may have been greatly affected by these cold water
masses. Therefore, seasonal change in the community was not observedin the western region, presumably because a colder water mass with
abundant large copepods (i.e. C. glacialis/marshallae) was always present
in the bottom layer during July and August.
On the other hand, seasonal change in the community structure wasclearly observed east of 172◦ W. During June through July, Groups A and
B contained many Pacific copepods and euphausiids. This is induced byinflow of Anadyr Water, with high salinity and a greater abundance ofPacific copepods and euphausiids (Springer et al., 1989). In August,Group E contained many cladocerans, Acartia spp. and Centropages spp.,
characteristic species of ACW (Hopcroft et al., 2010). However, hy­drography of the station where Group E occurred had moderate salinity(32.2–32.3) and lower temperatures (0.5–0.9 ◦ C), suggesting that it was
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Fig. 7. T-S diagram with the seven groups identified from Bray-Curtis similarity based on zooplankton abundances (cf. Fig. 5a) in the northern Bering Sea during
June through September of 2017. The plot position is mean values in the water column. Circles indicate that the stations were located west of 172◦ W.

originated from Bering Sea Water. The onset of phytoplankton bloom isa key factor in the timing of barnacle larvae release from benthic adults(Crisp, 1962), consistent with presence of barnacle nauplii concurrent
with elevated August phytoplankton concentrations.
In September, Group F occurred with many Centropages spp. andCalanus nauplii. As mentioned above, Centropages spp. is abundant
within the ACW, suggesting that a similar water mass inflow occurred
during September and August. The reproduction of C. glacialis uses
mainly energy from feeding (Søreide et al., 2010) with the maximum
reproduction rate coincident with the phytoplankton bloom (Niehoff
et al., 2002). While the water mass did not change from August to
September, the influx of a large number of C. glacialis nauplii following
the phytoplankton bloom, resulted in a change in the community
composition.
The difference between taxa (barnacles vs copepods) in the timing ofabundance increases triggered by the phytoplankton bloom is thought toreflect differences in their reproductive timing and growth rates. Thus,barnacles rapidly reproduce releasing nauplii in associated with thephytoplankton bloom (Costlow and Bookhout, 1957; Crisp, 1962), but
copepods need time to grow large enough to be collected by nets after

Table 3Results of PERMANOVA on zooplankton community with day and water mass inthe northern Bering Sea during June through September of 2017.
Sourced.f.

SSF-valuep-valueDay
Water mass
Day × water mass10
1
2

13,7202839.71550.93.94014.0547
3.2373********d.f., degrees of freedom; SS, sum of squares.
***: p < 0.001; **: p < 0.01.

not ACW. Furthermore, because of the vertically similar water mass
structure, it is possible that strong vertical mixing was stimulated bywind and small eddies that resulted in a different zooplankton com­munity structure compared to adjacent stations. In addition, there weremany appendicularian O. vanhoeffeni in Group D, barnacle nauplii inGroups D and E, and the phytoplankton bloom was observed at the sametime in these groups. Because O. vanhoeffeni occurs mainly in Bering
Shelf Water (Shiga, 1993a, 1993b), Group D is believed to have9

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Deep-Sea Research Part II 181-182 (2020) 104901

Fig. 8. Monthly changes in abundance and population structure for the dominant copepods in the northern Bering Sea during June through September 2017.
Horizontal bars below the plots indicate the water masses (ACW, BSW and AW) were present for each station.

reproduction (Peterson, 1986). In summary, for seasonal changes in theeastern northern Bering Sea, the zooplankton community structurechanged every month due to differing advection of water masses anddifferent reproductive attributes of copepods and benthos in response to
the phytoplankton bloom.

stages were most abundant in June then matured throughout the sum­
mer so that the CV stage was most abundant in August, suggesting a
one-year life cycle in the northern Bering Sea. Calanus spp. has adiapause phase in their life cycle, with CV being the diapause stage for
Calanus glacialis/marshallae in the Bering Sea. Accordingly, delayeddevelopment at CV was observed. While the relationship between
developmental stage and day of the year is not a general method forevaluating the development of copepods, it has the advantage of using
field data directly without incubation experiments. A relational
expression in this study (June to August: MCS = 0.0183D ± 0.6215,
August to September: MCS = 0.0132D ± 1.786) showed a steeper slope
and faster development than previously observed in the Chukchi Sea(MCS = 0.012D ± 0.881, Matsuno et al., 2016). They sampled from Julyto October in the Chukchi Sea so the difference in rate between these twostudies may be due to environmental conditions (temperature, sea-ice
coverage) of the sampling region (Chukchi Sea vs northern BeringSea) or to observational periods.

4.2. Reproduction and development of dominant copepods
Based on population structure and nauplii occurrence, most of thedominant copepods in this ecosystem developed and reproduced during
the sampling period. In terms of their reproductive timing, C. marshallae
reproduces during early spring (April) in the southeastern Bering Sea(Vidal and Smith, 1986), and C. glacialis reproduces during March toJune in the Chukchi Sea (Ashjian et al., 2003). It is suggested thatC. glacialis/marshallae reproduces during a prolonged period in ourstudy area because nauplius and reproductively mature adult females
occurred from June to September in this study. Their early copepodite
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Deep-Sea Research Part II 181-182 (2020) 104901

Fig. 9. Monthly changes in abundance of nauplii of the dominant copepods
species in the northern Bering Sea during June through September 2017.

Fig. 10. Monthly changes in abundance and gonad maturation for adult fe­
males of the dominant copepods in the northern Bering Sea during June
through September 2017.

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Deep-Sea Research Part II 181-182 (2020) 104901

Table 4
Result of the ANCOVA for MCS of the dominant large copepods with Julian day
and water mass (cf. Fig. 7) applied as independent variables.
SpeciesParameters

d.f.

SS

F-valuep-value

C. glacialis/marshallae

Water
Day
Water × day
Error

2
1
2
31

0.205
2.652
0.207
5.738

0.553
14.328
0.560

N.S.
***
N.S.

E. bungii

Water
Day
Water × day
Error

2
1
2
21

0.546
13.3120.535
16.3110.351
17.139
0.344

N.S.
***
N.S.

M. pacifica

Water
Day
Water × day
Error

2
1
2
30

0.602
6.376
0.594
18.3120.493
10.446
0.486

N.S.
**
N.S.

d.f., degrees of freedom; SS, sum of squares.
N.S., not significant.
***: p < 0.001; **: p < 0.01.

E. bungii is mainly distributed in the subarctic North Pacific Ocean,with individuals occurring in the northern Bering Sea thought to betransported there in Anadyr Water (Springer et al., 1989). This species
has a one-year or two-year life cycle in the western and eastern North
Pacific Ocean, respectively (Miller et al., 1984; Shoden et al., 2005).
Reproduction is performed at the surface during the phytoplankton
bloom (Miller et al., 1984). The reproductive period of this species varies
according to the region, in the Oyashio region in April to May (Tsudaet al., 2004) and in the central Gulf of Alaska from June to July (Miller
et al., 1984). In the southeastern Bering Sea, reproduction is during April
to May and the early copepodite stages occur in early June (Vidal andSmith, 1986). In this study, nauplii occurred in June, suggesting that
reproduction occurred before June in this region. For this species, thedevelopment time from egg to C5 is 3–4 months at 5 ◦ C based on in­
cubation experiments in the laboratory (Takahashi and Ide, 2011). On
the other hand, Calanus finmarchicus, distributed in the subarctic
Atlantic Ocean, develops from egg to CV in 50 days at 5 ◦ C (Corkett,1986). Therefore, the development rate of E. bungii would not be fasterthan that of Calanus spp. at the same temperature based on previous
laboratory experiments. However, in this study, development of E. bungii
was the fastest among the dominant three large-bodied copepods. Thismight be caused by reproduction before our observation period or inputof nauplii and early copepodite stages since many early copepodite
stages occurred during June through July. Unfortunately, population
development could not be accurately evaluated due to seasonal changes
in water masses and low abundances with high variation for this species
compared to the other two species.
M. pacifica is distributed throughout the subarctic North Pacific
Ocean and does not have a diapause phase (Padmavati et al., 2004). This
species is believed to be transported to the study area in Anadyr Water
because it occurs mainly in Gulf of Anadyr and to the west of St. Law­
rence Island (Springer et al., 1989; Ozaki and Minoda, 1996). M. pacifica
reproduces from March through October, peaking with the spring bloomin the Gulf of Alaska (Hopcroft et al., 2005), develops during summer toautumn, then develops to adult during December to January (Nau­menko, 1979). In the northern Bering Sea, we hypothesize that they
reproduce though the observed period because early copepodite stages
and adult female occurred during June through September. This species
develops during June through August because the population compo­
sition of early copepodite stages was highest in June, while later cope­
podite stages dominated during August to September. The developmentof this species was the slowest among the dominant copepods. This may
be due to the continuous occurrence of adult females and reproduction.
Neocalanus spp. are known to be mainly transported in Anadyr Water(Springer et al., 1989). This genus diapauses at depth, with timing ofFig. 11. Relationships between mean copepodite stage and Julian day for thedominant copepods in the northern Bering Sea during June throughSeptember 2017.

diapause cessation and CV migration to the surface layer differing be­
tween the species: N. cristatus in May–July, N. flemingeri in April,N. plumchrus in July (Tsuda et al., 1999, 2004). In this study, the timingof the occurrence of N. plumchrus was later than for the other two spe­cies, with both CV and CIV observed.
Four species of Pseudocalanus genus are known to occur in the study
region (Ershova et al., 2016). Pseudocalanus acuspes, dominant in thisregion (Ershova et al., 2016), spawns throughout all seasons in the Baltic
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Deep-Sea Research Part II 181-182 (2020) 104901

Fig. 12. Monthly changes in abundance and population structure for the Neocalanus species in the northern Bering Sea during June through September 2017.
Horizontal bars below the plots indicate the water masses (ACW, BSW and AW) present for each station.

Sea (Renz et al., 2007). In this study, reproduction occurred over theentire observation period with Pseudocalanus nauplii occurred during in
June through September in the east region. We cannot comment on
population dynamics because we did not distinguish species.

4.4. Seasonal changes in Appendicularia
It is known that appendicularians rapidly reproduce by utilizing
phytoplankton blooms and that they have a short generation time
(Deibel and Lowen, 2012). In this study, while O. labradoriensis wasabundant in June and July, O. vanhoeffeni occurred in August and
September. In Conception Bay, Newfoundland, it has been reported thatthe occurrence of F. borealis, O. labradoriensis and O. vanhoeffeni corre­
spond to variations in prey size arising from changes in the phyto­plankton assemblage (Choe and Deibel, 2008). In our study region,seasonal succession of the phytoplankton community and cell-size may
be a factor, but these were not consistently measured on most cruises.
The two species of Oikopleurea are distributed in different regions:O. labradoriensis occurs in the Bering Basin at depths greater than 200 m(Shiga, 1982), O. vanhoeffeni is distributed in the Bering Shelf Water(Shiga, 1993a, 1993b) and throughout the Arctic Ocean. We presume
high abundance of O. labradoriensis in June and July was driven by
inflow of Anadyr Water, and O. vanhoeffeni in August and September by
inflow of Bering Shelf water (Shiga, 1993a, 1993b). Although BSW was
not dominant during August and September, O. vanhoeffeni wasincreased by their active reproduction accompanying the phytoplankton
bloom (Deibel and Lowen, 2012). These results are consistent with theseasonal exchange of water masses as revealed by changes inzooplankton community structure. In other words, it is suggested thatappendicularian species composition may change seasonally because of
inflows of different water masses and active reproduction associated4.3. Seasonal changes in chaetognatha
Two species of chaetognaths, P. elegans and E. hamata, were observed
between 0 and 150 m, especially P. elegans, with a widespread distri­bution (Kotori, 1976). Formerly, the species present were used as anindex for water mass type, but in our study, these two species had similar
distributions with regard to water mass type. Growth rates of chaeto­gnaths differ regionally from 3 to 6 mm month− 1 in the Celtic Sea(Conway and Williams, 1986; Terazaki and Miller, 1986), and withtemperature (Sameoto, 1971). Unfortunately, it was impossible to esti­
mate growth rate in this study, possibly due to water mass exchanges
accompanying different temperatures.
The timing of P. elegans reproduction varies with region. Reproduc­tion is observed during three times (early summer, autumn and winter)in the eastern North Pacific (Terazaki and Miller, 1986), or two times(from spring to autumn) in the Bedford Basin, Celtic Sea and Canadian
Arctic Ocean (Zo, 1973; Conway and Williams, 1986; Grigor et al., 2014,2017). In this study, because smaller individuals occurred in every
month while mature individuals occurred only during August and
September, this species reproduced at least in August/September.

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Deep-Sea Research Part II 181-182 (2020) 104901

Fig. 13. Monthly changes in the total length of Parasagitta elegans in thenorthern Bering Sea during June through September 2017. Numbers in pa­
rentheses show total individual measurements. Smooth curves indicate the re­sults of a cohort analysis.

Fig. 14. Monthly changes in the trunk length of Oikopleura spp. in the northern
Bering Sea during June through September 2017. Numbers in parentheses show
total individual measurements.

with rich food conditions in the northern Bering Sea.

observed due to the dominance of BCWW in the bottom layer during
July and August. In the eastern region, community structure differed
every month due to inflow of different water masses, meroplankton
release, and copepod reproduction associated with the phytoplankton
bloom. For copepod population structures, C. glacialis/marshallae,
E. bungii and M. pacifica showed stage progression during the observa­
tion period, differing between species according to their life cycle. These
results illustrate that the zooplankton community and the population

5. Conclusions
This study examined seasonal changes in the zooplankton commu­
nity and population structure for dominant species in the northern
Bering Sea from June to September of 2017. Community compositiondiffered regionally and seasonally in association with changes in watermass distribution. In the western region seasonal changes were not
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F. Kimura et al.

structure of dominant species changed seasonally due to changes inhydrography (water mass) and primary productivity in the northern
Bering Sea. These large seasonal changes in zooplankton between
months are important to the evaluation of long-term changes in theregion. Evaluating long-term changes including seasonal changes willallow us to more accurately predict changes in marine ecosystems under
rapid changes such as changes in the extent of sea ice.

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Author statement
Fumihiko Kimura: Formal analysis, Investigation, Writing - Original
Draft, Visualization, Yoshiyuki Abe: Investigation, Kohei Matsuno:
Conceptualization, Writing - Review & Editing, Supervision, Project
administration, Russell R. Hopcroft: Investigation, Writing - Review &Editing, Atsushi Yamaguchi: Conceptualization, Investigation, Project
administration
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgements
We thank the captain, officers, crew and researchers on board the T/
S Oshoro-Maru, Hokkaido University, R/V Mirai, JAMSTEC and R/VSikuliaq, University of Alaska for their outstanding efforts during thefield sampling. This work was partially conducted as part of the Arctic
Challenge for Sustainability (ArCS) (Program Grant Number
JPMXD1300000000) and Arctic Challenge for Sustainability II (ArCS II)(Program Grant Number JPMXD1420318865). A portion of the study
was supported through a Grant-in-Aids for Scientific Research
19H03037(B), 18K14506 (Early Career Scientists), and 17H01483 (A)from the Japanese Society for Promotion of Science (JSPS), as well as theNorth Pacific Research Board’s Arctic program A91-99a and A91-00a.
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