ORIGINAL RESEARCH
published: 22 July 2020
doi: 10.3389/fmars.2020.00612

Mass Occurrence of Pacific
Copepods in the Southern Chukchi
Sea During Summer: Implications of
the High-Temperature Bering
Summer Water
Jee-Hoon Kim 1 , Kyoung-Ho Cho 1 , Hyoung Sul La 1 , Eun Jung Choy 1 , Kohei Matsuno 2,3 ,Sung-Ho Kang 1 , Won Kim 4 and Eun Jin Yang 1*
1

Korea Polar Research Institute, Incheon, South Korea, 2 Graduate School of Fisheries Science, Hokkaido University,
Sapporo, Japan, 3 Arctic Research Centre, Hokkaido University, Sapporo, Japan, 4 School of Biological Sciences, Seoul
National University, Seoul, South Korea

Edited by:
Tilmann Harder,
University of Bremen, Germany
Reviewed by:Hans Uwe Dahms,
Kaohsiung Medical University, Taiwan
David Kimmel,
National Marine Fisheries Service(NOAA), United States*Correspondence:
Eun Jin Yangejyang@kopri.re.kr
Specialty section:
This article was submitted toMarine Ecosystem Ecology,
a section of the journal
Frontiers in Marine Science
Received: 27 April 2020
Accepted: 03 July 2020
Published: 22 July 2020
Citation:
Kim J-H, Cho K-H, La HS,
Choy EJ, Matsuno K, Kang S-H,
Kim W and Yang EJ (2020) Mass
Occurrence of Pacific Copepods
in the Southern Chukchi Sea During
Summer: Implications of theHigh-Temperature Bering Summer
Water. Front. Mar. Sci. 7:612.
doi: 10.3389/fmars.2020.00612

The Bering Strait is the only gateway to the Chukchi Sea from the Pacific Ocean and isa major route of Pacific water inflow. We recently investigated the occurrence of Pacificcopepod species along with the warming of the Chukchi Sea and sought to identify thecause of the mass occurrence these copepods through an analysis of the water masses
flowing through the Bering Strait. Zooplankton and Conductivity-Temperature-Depth(CTD) data collection was conducted in the Chukchi Sea and Bering Strait from 2014 to2016. In addition, mooring systems installed in the Bering Strait were analyzed to obtainwater temperature and salinity data during summer to understand the properties of thewater masses. In 2015, a high abundance of Pacific copepod species (Eucalanus bungii,
Metridia pacifica, and Neocalanus spp.) was observed in Bering Summer Water (BSW),
which was relatively warm compared to measurements obtained from 2014 to 2016.
As further confirmation, our results were consistent with 2007, 2009, and 2012 data,
which showed that the abundance of Pacific copepod species was proportional to thetemperature of the BSW entering the Chukchi Sea. In conclusion, we reconfirmed that
Pacific copepod species are entering the Chukchi Sea along with BSW, and we newly
discovered that their high abundance coincided with the relatively warm BSW, insteadof other water masses. These findings suggest that the inflow of the high-temperature
BSW (>3◦ C) plays an important role in the mass occurrence of Pacific copepod species
in the southern Chukchi Sea.
Keywords: Pacific copepod, Arctic, Chukchi Sea, Bering Summer Water, mass occurrence

INTRODUCTION
Large amounts of Pacific heat, nutrients, freshwater, and biota pass through the shallow Bering
Strait and into the Chukchi Sea, entering the Arctic (Pickart et al., 2010; Corlett and Pickart, 2017;
Danielson et al., 2017). Since the 2000s, relatively warm Pacific waters passing through the Bering
Strait into the Chukchi Sea during summer have played a significant role on changes in the marine

Frontiers in Marine Science | www.frontiersin.org

1

July 2020 | Volume 7 | Article 612

Kim et al.

Pacific Copepods Occurrence in SCS

Chukchi Sea or whether the Pacific copepod species increased
only in tandem with the rise of BSW water temperature. The
mass occurrence of Pacific copepod species largely correlatedwith long-term observation data using a mooring system rather
than with the “in situ” water mass examined in CTD surveys.

environment (e.g., rising water temperatures and melting ice)of the Chukchi Sea (Shimada et al., 2006; Brugler et al., 2014;
Wood et al., 2015; Pickart et al., 2016). Zooplankton communities
are more vulnerable to environmental change in polar oceans
because they are affected by various rapid hydrographicalchanges, such as the formation/melting of sea ice, surface cooling,
and convection (Matsuno et al., 2011, 2016; Spear et al., 2019).
The increasing water temperature and Pacific water inflow arealso causing changes in the zooplankton community across the
Arctic boundary (Nelson et al., 2009). Among these changes isthe appearance, reported in previous studies, of a large number
of Pacific copepod species (Eucalanus bungii, Metridia pacifica,
and Neocalanus spp.) in the Chukchi Sea since the late 2000s(Matsuno et al., 2011; Ershova et al., 2015a,b).
The occurrence and community structure of Pacific copepod
species in the Chukchi Sea are influenced by the compositionof water masses flowing from the Bering Sea (Hopcroft et al.,2010; Eisner et al., 2013; Questel et al., 2013; Ershova et al.,2015b; Pinchuk and Eisner, 2017; Xu et al., 2018; Spear et al.,2019). In the southern Chukchi Sea, the northward shift of Pacificzooplankton species is largely correlated with the inflow of Bering
Summer Water (BSW) through the Bering Strait (Matsuno et al.,2011; Ershova et al., 2015b). Additionally, an increase in Pacificcopepod species in the Chukchi Sea is associated with a “warmstate” of sea surface temperature (Pinchuk and Eisner, 2017;
Spear et al., 2019). However, it is difficult to predict the changes
in species abundance and community structure because of theeffects of seasonal and interannual variations on the influx ofPacific waters (Brugler et al., 2014; Corlett and Pickart, 2017).
In particular, the drivers of the interannual variation in theoccurrence and community structure of Pacific copepod species
in the Chukchi Sea are not fully understood. Therefore, to verify
the response of marine organisms and their communities tochanges in the marine environment, it is necessary to observe
oceanographic environmental factors over the long term.
In one sense, it is thought that the reasons for the mass
occurrence of the Pacific copepod species in the Chukchi Sea
were difficult to define because research addressing the impact
on environmental factors offered only a snapshot and included
too few cases. In addition, understanding the impact on thewater mass, which is known to have the greatest influence on
zooplankton communities, was further complicated by analyses
of water systems using different water mass classification criteria(e.g., Matsuno et al., 2011; Questel et al., 2013; Ershova et al.,2015b; Corlett and Pickart, 2017; Pinchuk and Eisner, 2017;
Xu et al., 2018; Spear et al., 2019). The characteristics of water
masses flowing northward through the Bering Strait and directly
affecting the occurrence of Pacific copepod species need to beclarified if we are to understand the interannual variations in
Pacific zooplankton abundances in the Chukchi Sea.
In this study, we discovered the mass occurrence of Pacificcopepod species in the southern Chukchi Sea in August 2015. We
measured hydrographic properties using mooring systems andconductivity/temperature/depth (CTD) surveys and correlated
these with the mass occurrence of Pacific copepods. This study
examined whether an increase in water temperature resulted
in the occurrence of Pacific copepod species in the southern

Frontiers in Marine Science | www.frontiersin.org

MATERIALS AND METHODS
Zooplankton Sample Collection andProcessing
Zooplankton samples were collected in the Bering Strait andChukchi Sea during 5–12 August in 2014, 2015, and 2016
(Figure 1). In all cases, a bongo net was towed at a speed of
60 m min−1 for several minutes to sample the entire watercolumn from the bottom to the surface from the IBRV Araon.
The bongo net had a 330-µm mesh and a mouth diameterof 60 cm; there were 18 net hauls at 11 stations (Figure 1).
Samples from the bongo net were immediately preserved with
5% neutralized formaldehyde for quantitative analyses and wereidentified to the lowest taxonomic level using a microscope.
Abundances [individuals (indiv.) m−3 ] were calculated via therevolution counts from a one-way flowmeter mounted in themouth of the net.
The type of zooplankton sampling gear used influences theabundance, biomass, and composition of the catch as a result of
extrusion or avoidance (Skjoldal et al., 2013). When comparing
zooplankton datasets, differences in sampling gear must be
considered, especially the sizes of the mesh and net mouth.
Traditionally, ring (or bongo, 500 µm, 0.5–1 m mouth diameter),
Nansen (333 µm, 0.7 m mouth diameter), or Juday (∼ 170 µm,
0.37 m mouth diameter) nets are used (Ershova et al., 2015b).
Recently, 150 µm nets have been used to survey small species
in Arctic research (Pinchuk and Eisner, 2017; Spear et al., 2019).
Coarse mesh nets (e.g., 500 µm nets) can undersample small
species, which commonly make up >90% of the total abundancein this area, while fine mesh nets (<170 µm) may underrepresent the larger, faster, and rarer species (Questel et al., 2013).
Therefore, we used a 330 µm net (0.6 m mouth diameter),and directly compared the Pacific copepods, which are common
enough to be well represented when collected with fine-mesh
nets, but large enough to be captured by most coarse nets. The
species abundances were generally converted into individuals(indiv.) m−3 in previous studies.
For comparison with current and historical data, the sampling
grid was subdivided into two domains: Southern Chukchi (SC)south of 68◦ N and Central Chukchi (CC) north of 68◦ N. The
stations at 68◦ N were included in CC. The following wellknown indicator species were chosen and combined as Pacificspecies (Figure 2): E. bungii, M. pacifica, Neocalanus spp.
(Neocalanus cristatus, Neocalanus plumchrus, and Neocalanus
flemingeri). Although some of these taxa are present outside thePacific region, this copepod group has long been recognized
as dominant in waters of the Pacific Bering Sea (Hopcroft
et al., 2010; Matsuno et al., 2011; Ershova et al., 2015b).
MANOVA and one-way ANOVA analyses of zooplankton
abundances and environmental data were performed with IBM

2July 2020 | Volume 7 | Article 612

Kim et al.

Pacific Copepods Occurrence in SCS

FIGURE 1 | Map of the study area with zooplankton collecting locations represented by circles (2016), squares (2015), and dots (2014). The blue asterisk is the A2
mooring location, and the red asterisk is the A3 mooring location.

SPSS v23.0. Canonical correlation analysis was used to evaluate
relationships between the abundance of Pacific copepod species
and environmental data using paleontological statistics (PAST)
software (Hammer et al., 2001). Independent t-tests were used
to re-evaluate relationships between the abundance of Pacificcopepod species and specific water masses based on watertemperature and salinity.

is located slightly north of the strait (Figure 1). In general,
the Anadyr Water via the western channel and warmer/fresher
waters via the eastern channel combine at Site A3. We used atime series of temperature and salinity data available at A2 andA3 during the period of July to September in 2007, 2009, 2012,2014, 2015, and 2016. For more details of the mooring data, pleaserefer to Woodgate et al. (2005).

CTD Casting and Mooring Data

Water Mass Identification

An intensive oceanographic survey was conducted at theentrance of Bering Strait and continued northward to 72.5◦ N
latitude for the 3 years of the study. Along the stations, verticalprofiles of temperature and salinity were obtained from thehydro-casts of a SBE32 carousel water sampler equipped with an
SBE 9plus Conductivity-Temperature-Depth (CTD) profiler. Fora more accurate classification of water masses inflowing throughthe Bering Strait, we used the water temperature and salinity
data obtained from the Bering Strait Mooring Data Archive1 .
The water temperatures and salinities were measured by Sea-Bird
CTD profilers (SBE 16plus and SBE 37) installed at the top andbottom of the mooring system at mooring sites A2 (65◦ 46.90 N,
168◦ 34.10 W) and A3 (66◦ 19.60 N 168◦ 57.50 W, Figure 1). Site A2
is located in the eastern channel of the strait, whereas Site A3

The Chukchi Sea and Bering Strait waters are classified into twoor three main water masses: Alaskan Coastal Water (ACW) and
BSW (or, Bering Shelf Water and Anadyr Water) (Coachman
et al., 1975; Woodgate et al., 2005; Stabeno et al., 2018). Until
recently, various trends in the properties of these water masses
have been reported in the Chukchi Sea (Ershova et al., 2015b;
Corlett and Pickart, 2017; Danielson et al., 2017; Pickart et al.,2019). In particular, excellent analyses of water masses in thisarea have been performed by Pickart and colleagues (Pickart
and Stossmeister, 2008; Pickart et al., 2010, 2016, 2019; Brugler
et al., 2014; Gong and Pickart, 2015, 2016; Pisareva et al.,2015; Corlett and Pickart, 2017; Linders et al., 2017; Lin et al.,2019); many previous studies have cited or applied Pickart’s
classifications when identifying water masses (e.g., Ershova et al.,2015a; Weingartner et al., 2017; Yamashita et al., 2019). Dueto the purpose and region of this study, the water masses

1

http://psc.apl.washington.edu/BeringStrait.html

Frontiers in Marine Science | www.frontiersin.org

3

July 2020 | Volume 7 | Article 612

Kim et al.

Pacific Copepods Occurrence in SCS

FIGURE 2 | (A) Composition of zooplankton and total abundance in summer for the Southern Chukchi Sea 2014–2016; (B) Proportional abundance plots (indiv.
m−3 ) of Pacific copepods in the Chukchi Sea (Eucalanus bungii, Metridia pacifica, and Neocalanus spp. combined); (C) Composition of Pacific copepods in summer
for the Southern Chukchi Sea 2014–2016.

30–32 (Table 1). The AW water mass had high salinity (>33.6,
Table 1). BSW was comprised by combining Anadyr water andBering shelf water in the Bering Strait (Coachman et al., 1975).
The BSW water mass had a salinity range of 30.5–33.6 andtemperature of 0–10◦ C (Corlett and Pickart, 2017; Pickart et al.,2019). One year, we observed warm BSW flowing in during thesummer, which required a separate designation. Therefore, basedon Pickart’s water mass classification of the Chukchi Sea, BSW
with a temperature >3◦ C was referred to as high-temperature
BSW (BSWhighT ) for the purposes of this study (Table 1). By
contrast, BSW with a temperature ≤3◦ C is referred to here as
low-temperature BSW (BSWlowT , Table 1).

were identified with reference to the recent and well-organizedmethods of classification in Corlett and Pickart (2017) andPickart et al. (2019).
Using deep downcast data from each CTD station and datafrom two mooring stations, we plotted the temperature–salinity(T-S) diagram for water mass identification (Supplementary
Figure S1 and Figure 3). The T-S diagram showed that the
study area was occupied by several distinct water masses: ACW,
Atlantic Water (AW), and BSW. However, the CTD data andthe data obtained from mooring systems consisted mainly of
ACW and BSW. ACW was a relatively warm and fresh watermass with high temperatures (3–10◦ C) and a salinity range ofFrontiers in Marine Science | www.frontiersin.org

4

July 2020 | Volume 7 | Article 612

Kim et al.

Pacific Copepods Occurrence in SCS

transported into the Bering Strait in 2014 and 2016 (Figure 4A).
Particularly in 2014, a large amount of ACW, which has hightemperatures (3.5–6.5◦ C), was transported, but Pacific copepod
species rarely appeared (Figure 4). The mean water temperaturesin Figure 4A show that the BSW, which was warmer than 3◦ C,
was transported into the southern Chukchi Sea in 2015 when the
Pacific copepod species were abundant. On the other hand, theBSW waters cooler than 3◦ C were transported in 2014 and 2016
when the Pacific copepod species were almost absent.

TABLE 1 | Summary of southern Chukchi Sea water mass characteristics.
Temperature (◦ C)

Water mass
Alaskan Coastal Water (ACW)
Atlantic Water (AW)Salinity

>3

30–32

> −1.26>33.6>030–33.6

BSWhighT>3

32–33.6

BSWlowT

0–3

30–33.6

Bering Summer Water (BSW)RESULTSDISCUSSION

Zooplankton Abundance

Like the Arctic Ocean, the Chukchi Sea exhibits a predominanceof copepods in terms of zooplankton abundance and biomass(Kosobokova and Hopcroft, 2010; Ershova et al., 2015b; Smootand Hopcroft, 2017; Carstensen et al., 2019; Kasyan, 2020),
although larvaceans and meroplankton also contribute to theabundance and biomass of the zooplankton community during
summer (Lane et al., 2008; Matsuno et al., 2016). Among the
copepods, the zooplankton surveys conducted in 2015 showeda notable increase in Pacific copepod species in the southern
Chukchi Sea. We focused on the relationship between theoccurrence of Pacific copepod species and water masses to
elucidate the cause. Several previous studies have shown that
BSW is one of the most common water masses during summer
in the Bering Strait and in the Chukchi Sea (Ershova et al., 2015b;
Corlett and Pickart, 2017; Danielson et al., 2017; Stabeno et al.,2018). The large Pacific copepods M. pacifica, Neocalanus spp.,
and E. bungii are the dominant species in BSW (Ershova et al.,2015b; Pinchuk and Eisner, 2017).
During 2014–2016, a large amount of BSW inflow occurred
every year (Figure 3), but the Pacific copepod species appearedin high abundance only in 2015. This means that the occurrenceof Pacific copepod species in the southern Chukchi Sea cannot
be explained simply by the inflow of BSW. The mass occurrenceof Pacific copepod species could be the result of an immediatewater mass change, but it could also be the result of the longterm inflow of the water mass. Thus, we analyzed long-termwater temperature and salinity data from the mooring systems.
The results showed that Pacific copepod species appeared in
the Bering Strait and the southern Chukchi Sea when relatively
warm (>3◦ C) BSW was transported (Figure 4). The ACW isrelatively dense and flows surface, whereas the high-density BSW
flows bottom; therefore, the difference is more apparent when
considering the bottom portions of mooring data (Figure 3B).
In 2014 and 2016, when there were few Pacific copepod species,
BSWhighT was rarely encountered (Figures 3, 4A). There havealso been few reports of BSWhighT in many studies of the watermass in the Chukchi Sea (Corlett and Pickart, 2017; Pickart et al.,2019). Specifically, in 2014, a large influx of warm ACW (3.5–
6.5◦ C, Figures 3A, 4A) did not cause the occurrence of Pacific
Copepod species. The abundance of E. bungii, in particular, wasstrongly positively correlated with high temperature and highsalinity (canonical correlation: r = 0.74; p < 0.001). It was alsosignificantly related (p < 0.001) with BSWhighT , with a hightemperature (>3◦ C) and high salinity (32–33.6). In addition,

Zooplankton abundance ranged from 99 to 3,168 indiv. m−3(mean: 799 indiv. m−3 ), with the abundance in the southern
Chukchi Sea being higher than that in the north, especially in2015 (Figure 2A). Copepods comprised 16–93% (mean: 65%)of zooplankton abundance, and plankton larvae comprised 0–
55% (mean: 23%) of abundance. The most dominant species
was Calanus glacialis, which ranged from 4 to 1,732 indiv.
m−3 (mean: 178 indiv. m−3 , Figure 2A). The highest total
zooplankton abundance (3,168 indiv. m−3 ) was recorded in thesouthern Chukchi (SC) Sea in 2015 (mean: 2447 indiv. m−3 ,Table 2). Pacific copepod species accounted for a maximum of
40% of the total zooplankton abundance in the southern Chukchi
Sea (Figure 2A). Particularly, at St. 2 (Figure 1) in 2015, morethan 1,000 indiv. m−3 of Pacific copepod species appeared (meanin SC: 874 indiv. m−3 , Table 2), with a range of 0–1,210 indiv.
m−3 (Figures 2B,C), and E. bungii contributed significantly to
the Pacific copepod species abundance (mean in SC: 843 indiv.
m−3 , p < 0.001, Figure 2C and Table 2). And, the majority ofthese pacific copepod species were late-stage copepodites of C4
and C5 (Figure 2C).

Water Masses and Pacific Copepod
SpeciesIn situ CTD data showed that in 2015, when Pacific copepod
species were collected in abundance, showed an inflow ofBSWhighT (Supplementary Figure S1). However, due to thehigh variability of water temperature and salinity, there wasno statistically significant correlation between the CTD and thebiological data (p > 0.05). We obtained additional long-term
physical data from the mooring systems (A2, A3) in the Bering
Strait (Figure 1). In these mooring systems, long-term watertemperature and salinity data were obtained for approximately
20 days, including observations at the times of zooplankton
collections in 2014–2016. The T-S diagram from the mooringdata (Figure 3) shows that the properties of the water masses inthis region were based on the Pacific summer waters, ACW, and
BSW. In particular, the data from the A3 mooring, located near St.
2 (Figure 1), where Pacific copepod species occurred, consisted
mainly of BSW throughout the study period. In 2015, when
the Pacific copepod species appeared in abundance, the watertemperatures and salinities were relatively high (p < 0.001); of
particular note, the temperature of BSW was >3◦ C (Figure 4A).
On the other hand, relatively cold BSW waters (<3◦ C) were

Frontiers in Marine Science | www.frontiersin.org

5

July 2020 | Volume 7 | Article 612

Kim et al.

Frontiers in Marine Science | www.frontiersin.org

TABLE 2 | Summary of mean abundance (indiv. m−3 ) ± SD for dominant taxa in southern Chukchi Sea (SC) and central Chukchi Sea (CC).
Abundance (indiv. m−3 ) ± SD
Taxon

2014
SC

Pacific copepods

Other copepods

SC

CC

SC

CC

Eucalanus bungii

3.00 ± 1.41

6.33 ± 4.50

843.33 ± 327.97**

5.00 ± 5.10

2.91 ± 2.70−−

4.00 ± 5.66

28.33 ± 28.89

4.67 ± 6.60

6.76 ± 4.89−

Neocalanus spp.

0.33 ± 0.47−

2.33 ± 3.30−

0.74 ± 1.05−

Calanus glacialis

87.33 ± 83.81

198.67 ± 34.24

1060.33 ± 650.50*

101.00 ± 54.52

332.89 ± 260.90

325.41 ± 101.17
105.65 ± 63.32

Pseudocalanus spp.

31.67 ± 28.57

29.33 ± 21.75

258.00 ± 177.20

47.00 ± 9.63

36.50 ± 5.64

Oithona similis

7.67 ± 4.64

3.33 ± 4.71

8.67 ± 12.26

3.33 ± 4.71

3.65 ± 2.72−

Acartia longiremis

6.33 ± 8.26

11.00 ± 5.72

28.67 ± 30.65

15.67 ± 12.12

5.17 ± 3.77

1.63 ± 2.31−−

2.33 ± 3.30

−

−

−

2.00 ± 2.16

1.33 ± 0.94−

1.00 ± 1.41−−

Metridia longa

−

−

−

−

−

2.15 ± 3.04
147.00 ± 100.00

6

Centropages abdominalis

Other zooplankton

CC

2016

Metridia pacifica

Calanus hyperboreus

Planktonic larvae

2015

Cirriped larvae

134.67 ± 153.21

130.00 ± 103.83

14.33 ± 10.78

119.33 ± 92.34

36.31 ± 35.74

Decapoda larvae

−

−

−

−

2.02 ± 0.28**−

Gastropoda larvae−

3.00 ± 2.16**

−

−

−

−

Ophiopluteus larvae

1.67 ± 2.36

2.33 ± 1.70−

28.67 ± 36.38−

2.38 ± 1.71

Polychaeta larvae

1.33 ± 0.94

8.33 ± 9.74

6.67 ± 9.43

11.67 ± 14.43

13.85 ± 8.67

17.80 ± 15.95

Unidentified Cnidaria

1.33 ± 0.94−

4.00 ± 5.66

3.33 ± 2.87

4.04 ± 3.66

8.59 ± 4.71

Sagitta spp.

4.00 ± 4.97

2.33 ± 3.30

28.33 ± 19.26

10.00 ± 4.97

24.12 ± 17.63

10.22 ± 6.89
112.71 ± 106.12

13.00 ± 7.12

9.33 ± 9.88

38.67 ± 50.50

24.00 ± 20.02

29.50 ± 16.48

0.67 ± 0.47

0.33 ± 0.47

9.67 ± 13.67

−

−

−

Unidentified Euphausiacea

4.67 ± 1.89

9.00 ± 10.03

115.67 ± 82.64*

2.00 ± 1.41

9.75 ± 5.67

−

Total

299.67 ± 278.15

421.00 ± 135.97

2447.00 ± 981.71*

376.67 ± 180.61

508.20 ± 220.75

733.55 ± 124.01

Carbon content (mg/m−3 )19.65 ± 9.15

22.39 ± 7.76

308.82 ± 169.99*

23.44 ± 13.77

61.27 ± 25.92

40.09 ± 21.80

July 2020 | Volume 7 | Article 612

Asterisk (*) indicates significant difference (*p < 0.05; **p < 0.001).

Pacific Copepods Occurrence in SCS

Oikopleura spp.
Unidentified Amphipoda

Kim et al.

Pacific Copepods Occurrence in SCS

FIGURE 3 | A2 and A3 mooring T-S Diagram for 20 July–10. August 2014–2016 (A) Surface (B) Bottom. The shapes filled with color are BSW, and the shapes withno color are ACW (Green circles: 2014; Blue squares: 2015; Red triangles: 2016).

Pacific copepods (Ershova et al., 2015b). Notably, planktonic
larvae increased in 2014 when the temperature of the ACW
was high (Figure 2A). This is consistent with previous studies
showing that ACW is dominated by meroplankton (Ershova
et al., 2015b). Thus, the effect of rising water temperatures
exhibits an extremely high variability, but the result might be anincrease in the preponderance of certain species and ultimately,
decreased species diversity in the Chukchi Sea.
In the surface mooring data of the T-S diagram (Figure 3A),
it is difficult to distinguish pure BSW, due to the mixing of
the relatively low-density ACW and relatively high-density BSW.
In some studies, the two water masses (ACW and BSW) andtheir mixed water mass have been defined separately for thisreason (Ershova et al., 2015b; Pinchuk and Eisner, 2017). By
these standards, the occurrence of Pacific copepod species was
related not only to the temperature of the BSW but also to thatof the mixed water mass containing BSW. However, even if we
define mixed water masses (e.g., ACW/BSW) to eliminate theboundary ambiguity caused by the mixing of these water masses,
the boundaries will become blurred again, resulting in further
ambiguity. Therefore, it is considered more important to use awater mass classification system with clear boundaries that arecommonly used and defined by experts in the study area.

long-term mooring data (for 3 weeks) showed that the BSWhighT ,which is more pronounced than in the CTD data, continued tomainly flow in 2015 (Figure 3).
The subarctic Pacific Ocean and the Arctic Ocean have very
different zooplankton compositions (Pomerleau et al., 2014;
Matsuno et al., 2016). E. bungii, M. pacifica, and Neocalanus
spp. are the dominant plankton copepods in the Bering Sea areaof the subarctic Pacific Ocean (Springer et al., 1989; Ershova
et al., 2015b). In recent years, zooplankton communities in the
Chukchi Sea have become increasingly influenced by Bering–
Pacific fauna (Ershova et al., 2015b). In 2015 of the present
study, however, the mass occurrence of Pacific copepods in thesouthern Chukchi Sea was exceptional (Supplementary Table S1and Supplementary Figure S2). In particular, previous studies
have not observed massive occurrences of the large copepod
E. bungii at more than 1000 indiv. m−3 (Shoden et al., 2005;
Ershova et al., 2015a,b). Here, we discovered that E. bungii
occurred in this region as the temperature of the BSW rose. Since
there were relatively high levels of copepodites (Figure 2C), they
were likely introduced with the BSWhighT . Since E. bungii mainly
inhabits the warm North Pacific region, it is well suited to warm
environments. In previous reports, the abundance of E. bungii
also had a higher correlation with water temperature among

Frontiers in Marine Science | www.frontiersin.org

7

July 2020 | Volume 7 | Article 612

Kim et al.

Pacific Copepods Occurrence in SCS

FIGURE 4 | (A) A2 and A3 mooring mean temperature for 20 July – 10. August 2014–2016. Asterisk (*) indicates significant difference (*p < 0.05; **p < 0.001);(B) A2 and A3 mooring mean salinity for 20 July – 10. August 2014–2016 (Red circles: BSW surface; Blue circles: BSW bottom; mauve triangles: ACW surface; cyan
triangles: ACW bottom); (C) St. 1 and St. 2 abundance of Pacific copepods (indiv. m−3 ).

Frontiers in Marine Science | www.frontiersin.org

8

July 2020 | Volume 7 | Article 612

Kim et al.

Pacific Copepods Occurrence in SCS

FIGURE 5 | A2 mooring T-S Diagram for September 2007, 2009, and 2012. The green bars are relative abundance of Pacific copepods.

Previous data showed that the success of the Pacific copepod
species was largely correlated with water temperature, so
increases in the abundance of these species with future warming
are expected (Ershova et al., 2015b). However, in the present
data, only an increase in the temperature of BSW led to anincrease in Pacific species, while an increase in the temperatureof the ACW had no effect. These findings suggest that if
oceanographic changes such as warming and increased BSW
inflows continue in the Chukchi Sea, the mesozooplankton
community could become more volatile and less diverse, withan increased population of Pacific copepod species. However, if
other water masses flow in, in addition to the rise in temperature,
an increase in meroplankton may be likely. In previous studies
and the present one, the summer zooplankton communitiesof the southern Chukchi Sea have been primarily pacific incharacter; warming is more likely to produce greater seasonaland interannual variability than simply accelerating the Pacificcharacter. Despite this high variability, future warming willlead to increased zooplankton biomass via the influx of large
copepods and large-scale occurrence of meroplankton in thesouthern Chukchi Sea, which may lead to increasing numberof predators, such as foraging fish (Pinchuk and Eisner, 2017;
Eisner et al., 2018). As each temperature rise in the water massis important, future studies need to observe long-term data
and analyze changes in the incoming water mass separately, tounderstand the zooplankton communities in the Chukchi Sea
better. These results will provide a baseline for assessing theeffects of future water mass changes on the pelagic ecosystem of
the changing Arctic Ocean.

We also looked at previous data in addition to our 3-year
dataset to further validate our results. A previous study ofzooplankton in the Bering Strait and the Chukchi Sea overthe past 30 years revealed abundant Pacific copepod species
in August and September of 2007 (Matsuno et al., 2011). In
addition, recent studies have found few Pacific copepod species
in September of 2009 and 2012 (Ershova et al., 2015a). Therefore,
we analyzed the water masses from these 3 years using themooring data. These data (Figure 5) showed that BSWhighT
was transported in September 2007, when the Pacific copepod
species appeared in abundance (408 indiv. m−3 ; approximately
15% of the total zooplankton composition), and the BSW
temperature was low (<3◦ C) in September 2009 and 2012,
when Pacific copepod species were rarely found (Supplementary
Table S1). In these reports, E. bungii and M. pacifica also
showed high correlations with BSWhighT (p < 0.05). Thus,
the past and present data indicated that the mass occurrenceof Pacific copepod species was related to the inflow of
the BSWhighT .
In 2015, when Pacific copepod species occurred massively,
there was primarily inflow of BSWhighT for 3 weeks (Figure 3).
In comparison, the water temperature was higher in 2007 thanin 2015, but the BSWhighT was not continuously present for
3 weeks (Figure 5). This shows that the mass occurrence ofPacific copepod species can occur in the southern Chukchi
Sea when the BSWhighT continuously and exclusively flows in.
Although the relationship between the BSWhighT and the Pacificcopepod species was significant in our study period, the water
masses flowing through the Bering Strait showed high seasonalvariability (Woodgate, 2018). The distributions of zooplankton
also depend on season and time and are even affected by thevertical distribution of water masses (La et al., 2018). Our resultscannot be generalized to all of these environments; however,our data reconfirmed the relationship between the occurrence ofPacific copepod species and the BSW in the southern Chukchi Sea(Ershova et al., 2015b). Furthermore, we found that the influx of
BSWhighT could lead to the mass occurrence of Pacific copepod
species, which we revalidated using data from previous studies(Figure 5 and Supplementary Table S1). Recently, planktonic
communities of the Chukchi Sea have experienced climaterelated changes through both shifts in the transport rate andpenetration of Pacific copepod species into the Arctic Ocean(Hopcroft et al., 2010; Ershova et al., 2015b).

Frontiers in Marine Science | www.frontiersin.org

DATA AVAILABILITY STATEMENT
The raw data supporting the conclusions of this article will bemade available by the authors, without undue reservation.

AUTHOR CONTRIBUTIONS
EY conceived the study. J-HK collected the zooplankton samples.
J-HK and K-HC analyzed the physical data. HL, EC, KM, S-HK,
and WK contributed to the study design and data discussion.
J-HK, K-HC, and EY wrote the manuscript. All authors read andapproved the final manuscript.

9

July 2020 | Volume 7 | Article 612

Kim et al.

Pacific Copepods Occurrence in SCS

FUNDINGSUPPLEMENTARY MATERIAL

This research was a part of the project titled “Korea-Arctic
Ocean Observing System (K-AOOS, KOPRI, 20160245)” fundedby the MOF, Korea.

The Supplementary Material for this article can be foundonline at: https://www.frontiersin.org/articles/10.3389/fmars.
2020.00612/full#supplementary-material
FIGURE S1 | T-S Diagram of CTD (Bottom to Top) for the Southern
Chukchi Sea 2014–2016.

ACKNOWLEDGMENTS

FIGURE S2 | Pacific copepod species abundance in the Chukchi Sea after 1946.
Each white symbol represents previous cruise, the red one represents the present
study in 2015. The dashed line shows a fitted linear trend over averaged data.

The authors thank the captain and crew of the IBRV ARAON
who were most helpful in all shipboard operations.

REFERENCES

La, H. S., Shimada, K., Yang, E. J., Cho, K.-H., Ha, S.-Y., Jung, J., et al. (2018).
Further evidence of diel vertical migration of copepods under Arctic sea ice
during summer. Mar. Ecol. Prog. Ser. 592, 283–289. doi: 10.3354/meps12484
Lane, P. V., Llinás, L., Smith, S. L., and Pilz, D. (2008). Zooplankton distribution
in the western Arctic during summer 2002: hydrographic habitats andimplications for food chain dynamics. J. Mar. Syst. 70, 97–133. doi: 10.1016/
j.jmarsys.2007.04.001
Lin, P., Pickart, R. S., McRaven, L. T., Arrigo, K. R., Bahr, F., Lowry, K. E., et al.
(2019). Water mass evolution and circulation of the northeastern Chukchi Sea
in summer: implications for nutrient distributions. J. Geophys. Res. Oceans 124,
4416–4432. doi: 10.1029/2019jc015185
Linders, J., Pickart, R. S., Björk, G., and Moore, G. (2017). On the nature and origin
of water masses in Herald Canyon, Chukchi Sea: synoptic surveys in summer
2004, 2008, and 2009. Prog. Oceanogr. 159, 99–114. doi: 10.1016/j.pocean.2017.
09.005
Matsuno, K., Sanchez, J. M. L., Yamaguchi, A., Hirawake, T., and Kikuchi, T.
(2016). Spatial and geographical changes in the mesozooplankton community
in the Bering and Chukchi Seas during the summers of 2007 and 2008. Polar
Sci. 10, 335–345. doi: 10.1016/j.polar.2016.04.006
Matsuno, K., Yamaguchi, A., Hirawake, T., and Imai, I. (2011). Year-to-yearchanges of the mesozooplankton community in the Chukchi Sea during
summers of 1991, 1992 and 2007, 2008. Polar Biol. 34, 1349–1360. doi: 10.1007/
s00300-011-0988-z
Nelson, R., Carmack, E., McLaughlin, F., and Cooper, G. (2009). Penetration ofPacific zooplankton into the western Arctic Ocean tracked with molecular
population genetics. Mar. Ecol. Prog. Ser. 381, 129–138. doi: 10.3354/
meps07940
Pickart, R. S., Moore, G., Mao, C., Bahr, F., Nobre, C., and Weingartner, T. J. (2016).
Circulation of winter water on the Chukchi shelf in early Summer. Deep Sea Res.
Part II Top. Stud. Oceanogr. 130, 56–75. doi: 10.1016/j.dsr2.2016.05.001
Pickart, R. S., Nobre, C., Lin, P., Arrigo, K. R., Ashjian, C. J., Berchok, C., et al.
(2019). Seasonal to mesoscale variability of water masses and atmosphericconditions in Barrow Canyon, Chukchi Sea. Deep Sea Res. Part II Top. Stud.
Oceanogr. 162, 32–49. doi: 10.1016/j.dsr2.2019.02.003
Pickart, R. S., Pratt, L. J., Torres, D. J., Whitledge, T. E., Proshutinsky, A. Y.,
Aagaard, K., et al. (2010). Evolution and dynamics of the flow through herald
canyon in the western Chukchi Sea. Deep Sea Res. Part II Top. Stud. Oceanogr.
57, 5–26. doi: 10.1016/j.dsr2.2009.08.002
Pickart, R. S., and Stossmeister, G. (2008). Outflow of pacific water from the
Chukchi Sea to the Arctic Ocean. Chin. J. Polar Oceanogr. 19, 135–148.
Pinchuk, A. I., and Eisner, L. B. (2017). Spatial heterogeneity in zooplankton
summer distribution in the eastern Chukchi Sea in 2012-2013 as a resultof large-scale interactions of water masses. Deep Sea Res. Part II Top. Stud.
Oceanogr. 135, 27–39. doi: 10.1016/j.dsr2.2016.11.003
Pisareva, M. N., Pickart, R. S., Spall, M., Nobre, C., Torres, D., Moore, G., et al.
(2015). Flow of Pacific water in the western Chukchi sea: results from the 2009
RUSALCA expedition. Deep Sea Res. Part I Oceanogr. Res. Pap. 105, 53–73.
doi: 10.1016/j.dsr.2015.08.011
Pomerleau, C., Nelson, R. J., Hunt, B. P., Sastri, A. R., and Williams, W. J. (2014).
Spatial patterns in zooplankton communities and stable isotope ratios (δ13Cand δ15N) in relation to oceanographic conditions in the sub-Arctic Pacific andwestern Arctic regions during the summer of 2008. J. Plankt. Res. 36, 757–775.
doi: 10.1093/plankt/fbt129

Brugler, E. T., Pickart, R. S., Moore, G., Roberts, S., Weingartner, T. J., andStatscewich, H. (2014). Seasonal to interannual variability of the Pacific waterboundary current in the Beaufort Sea. Prog. Oceanogr. 127, 1–20. doi: 10.1016/
j.pocean.2014.05.002
Carstensen, J., Olszewska, A., and Kwasniewski, S. (2019). Summer
mesozooplankton biomass distribution in the West Spitsbergen current(2001-2014). Front. Mar. Sci. 6:202. doi: 10.3389/fmars.2019.00202
Coachman, L. K., Coachman, L. K., Aagaard, K., and Tripp, R. (1975). Bering
Strait: the Regional Physical Oceanography. Washington, DC: University ofWashington Press.
Corlett, W. B., and Pickart, R. S. (2017). The Chukchi slope current. Prog. Oceanogr.
153, 50–65. doi: 10.1016/j.pocean.2017.04.005
Danielson, S. L., Eisner, L., Ladd, C., Mordy, C., Sousa, L., and Weingartner,
T. J. (2017). A comparison between late summer 2012 and 2013 water masses,
macronutrients, and phytoplankton standing crops in the northern Bering and
Chukchi Seas. Deep Sea Res. Part II Top. Stud. Oceanogr. 135, 7–26. doi:
10.1016/j.dsr2.2016.05.024
Eisner, L., Hillgruber, N., Martinson, E., and Maselko, J. (2013). Pelagic fish andzooplankton species assemblages in relation to water mass characteristics inthe northern Bering and southeast Chukchi seas. Polar Biol. 36, 87–113. doi:
10.1007/s00300-012-1241-0
Eisner, L. B., Pinchuk, A. I., Kimmel, D. G., Mier, K. L., Harpold, C. E., andSiddon, E. C. (2018). Seasonal, interannual, and spatial patterns of community
composition over the eastern Bering Sea shelf in cold years. Part I Zooplank.
ICES J. Mar. Sci. 75, 72–86. doi: 10.1093/icesjms/fsx156
Ershova, E. A., Hopcroft, R. R., and Kosobokova, K. N. (2015a). Interannual variability of summer mesozooplankton communities of the western
Chukchi Sea: 2004-2012. Polar Biol. 38, 1461–1481. doi: 10.1007/s00300-0151709-9
Ershova, E. A., Hopcroft, R. R., Kosobokova, K. N., Matsuno, K., Nelson, R. J.,
Yamaguchi, A., et al. (2015b). Long-term changes in summer zooplankton
communities of the western Chukchi Sea, 1945-2012. Oceanography 28, 100–
115. doi: 10.5670/oceanog.2015.60
Gong, D., and Pickart, R. S. (2015). Summertime circulation in the eastern Chukchi
Sea. Deep Sea Res. Part II Top. Stud. Oceanogr. 118, 18–31. doi: 10.1016/j.dsr2.
2015.02.006
Gong, D., and Pickart, R. S. (2016). Early summer water mass transformation in
the eastern Chukchi Sea. Deep Sea Res. Part II Top. Stud. Oceanogr. 130, 43–55.
doi: 10.1016/j.dsr2.2016.04.015
Hammer, Ø, Harper, D. A., and Ryan, P. D. (2001). PAST: paleontological statistics
software package for education and data analysis. Palaeontol. Electron. 4:9.
Hopcroft, R. R., Kosobokova, K. N., and Pinchuk, A. I. (2010). Zooplankton
community patterns in the Chukchi Sea during summer 2004. Deep Sea
Res. Part II Top. Stud. Oceanogr. 57, 27–39. doi: 10.1016/j.dsr2.2009.
08.003Kasyan, V. V. (2020). Variability and spatial distribution of zooplankton
communities in the western Chukchi Sea during early fall. Polar Sci. 24:100508.
doi: 10.1016/j.polar.2020.100508
Kosobokova, K. N., and Hopcroft, R. R. (2010). Diversity and vertical distributionof mesozooplankton in the Arctic’s Canada Basin. Deep Sea Res. Part II Top.
Stud. Oceanogr. 57, 96–110. doi: 10.1016/j.dsr2.2009.08.009

Frontiers in Marine Science | www.frontiersin.org

10

July 2020 | Volume 7 | Article 612

Kim et al.

Pacific Copepods Occurrence in SCS

Questel, J. M., Clarke, C., and Hopcroft, R. R. (2013). Seasonal and interannual
variation in the planktonic communities of the northeastern Chukchi Sea
during the summer and early fall. Continent. Shelf Res. 67, 23–41. doi: 10.1016/
j.csr.2012.11.003
Shimada, K., Kamoshida, T., Itoh, M., Nishino, S., Carmack, E., McLaughlin, F.,et al. (2006). Pacific Ocean inflow: influence on catastrophic reduction of sea
ice cover in the Arctic ocean. Geophys. Res. Lett. 33:624.
Shoden, S., Ikeda, T., and Yamaguchi, A. (2005). Vertical distribution, population
structure and lifecycle of Eucalanus bungii (Copepoda: Calanoida) in the
Oyashio region, with notes on its regional variations. Mar. Biol. 146, 497–511.
doi: 10.1007/s00227-004-1450-3
Skjoldal, H. R., Wiebe, P. H., Postel, L., Knutsen, T., Kaartvedt, S., and Sameoto,
D. D. (2013). Intercomparison of zooplankton (net) sampling systems: resultsfrom the ICES/GLOBEC sea-going workshop. Prog. Oceanogr. 108, 1–42. doi:
10.1016/j.pocean.2012.10.006
Smoot, C. A., and Hopcroft, R. R. (2017). Depth-stratified community structure of
Beaufort Sea slope zooplankton and its relations to water masses. J. Plankt. Res.
39, 79–91. doi: 10.1093/plankt/fbw087
Spear, A., Duffy-Anderson, J., Kimmel, D., Napp, J., Randall, J., and Stabeno,
P. (2019). Physical and biological drivers of zooplankton communities in the
Chukchi Sea. Polar Biol. 42, 1107–1124. doi: 10.1007/s00300-019-02498-0
Springer, A. M., McRoY, C. P., and Turco, K. R. (1989). The paradox of pelagic foodwebs in the northern Bering Sea—II. Zooplankton communities. Continent.
Shelf Res. 9, 359–386. doi: 10.1016/0278-4343(89)90039-3
Stabeno, P., Kachel, N., Ladd, C., and Woodgate, R. (2018). Flow patterns in
the eastern Chukchi Sea: 2010-2015. J. Geophys. Res. Oceans 123, 1177–1195.
doi: 10.1002/2017jc013135
Weingartner, T., Fang, Y.-C., Winsor, P., Dobbins, E., Potter, R., Statscewich, H.,
et al. (2017). The summer hydrographic structure of the Hanna shoal region on
the northeastern Chukchi Sea shelf: 2011-2013. Deep Sea Res. Part II Top. Stud.
Oceanogr. 144, 6–20. doi: 10.1016/j.dsr2.2017.08.006

Frontiers in Marine Science | www.frontiersin.org

Wood, K. R., Bond, N. A., Danielson, S. L., Overland, J. E., Salo, S. A., Stabeno, P. J.,
et al. (2015). A decade of environmental change in the Pacific Arctic region.
Prog. Oceanogr. 136, 12–31. doi: 10.1016/j.pocean.2015.05.005
Woodgate, R. A. (2018). Increases in the Pacific inflow to the Arctic from 1990
to 2015, and insights into seasonal trends and driving mechanisms from yearround Bering Strait mooring data. Prog. Oceanogr. 160, 124–154. doi: 10.1016/
j.pocean.2017.12.007
Woodgate, R. A., Aagaard, K., and Weingartner, T. J. (2005). A year in the physicaloceanography of the Chukchi Sea: moored measurements from autumn 19901991. Deep Sea Res. Part II Top. Stud. Oceanogr. 52, 3116–3149. doi: 10.1016/j.
dsr2.2005.10.016
Xu, Z., Zhang, G., and Sun, S. (2018). Inter-annual variation of the summer
zooplankton community in the Chukchi Sea: spatial heterogeneity during adecade of rapid ice decline. Polar Biol. 41, 1827–1843. doi: 10.1007/s00300018-2324-3
Yamashita, Y., Yagi, Y., Ueno, H., Ooki, A., and Hirawake, T. (2019).
Characterization of the water masses in the shelf region of the Bering and
Chukchi Seas with fluorescent organic matter. J. Geophys. Res. Oceans 124,
7545–7556. doi: 10.1029/2019jc015476
Conflict of Interest: The authors declare that the research was conducted in theabsence of any commercial or financial relationships that could be construed as apotential conflict of interest.
Copyright © 2020 Kim, Cho, La, Choy, Matsuno, Kang, Kim and Yang. This is an
open-access article distributed under the terms of the Creative Commons Attribution
License (CC BY). The use, distribution or reproduction in other forums is permitted,
provided the original author(s) and the copyright owner(s) are credited and that theoriginal publication in this journal is cited, in accordance with accepted academic
practice. No use, distribution or reproduction is permitted which does not comply
with these terms.

11

July 2020 | Volume 7 | Article 612