Polar Biol (2011) 34:1349–1360
DOI 10.1007/s00300-011-0988-z

ORIGINAL PAPER

Year-to-year changes of the mesozooplankton community
in the Chukchi Sea during summers of 1991, 1992 and 2007,
2008
Kohei Matsuno • Atsushi Yamaguchi •Toru Hirawake • Ichiro Imai

Received: 6 January 2011 / Revised: 28 February 2011 / Accepted: 28 February 2011 / Published online: 16 March 2011
Ó Springer-Verlag 2011

Abstract A recent drastic decrease in sea ice cover area
was observed in the western Arctic Ocean during summer,
yet little information is available for its effect on zooplankton community. To evaluate the effect of sea ice
reduction on zooplankton, we studied year-to-year changesof zooplankton community structure in the Chukchi Sea
during summers of 1991, 1992 (when sea ice extended),
2007, and 2008 (when sea ice reduced). Zooplankton
abundance ranged from 4,000 to 316,000 ind. m-2 (mean:
70,000) and was greater north of Lisburne Peninsula in2008. Zooplankton biomass ranged from 0.07 to 286 g wet
mass m-2 (mean: 36) and was greater south of Lisburne
Peninsula in 2007. Cluster analysis based on zooplankton
abundance showed a division of the zooplankton community into four groups. Occurrence of each group was separated geographically and interannually, and geographic
distributions of each group in 1991 and 1992 were similar
but those in 2007 and 2008 were shifted northward.
Abundance and biomass in 2007/2008 were higher than in
1991/1992, indicating that further sea ice reduction would
have a positive effect on zooplankton production (e.g.
invasion of large Pacific species and temperature effects on
their growth rate). The northern shift in geographic distribution of the zooplankton community in 2007/2008 indicates that sea ice reduction would have a negative effect on

K. Matsuno (&)  A. Yamaguchi  I. ImaiLaboratory of Marine Biology, Graduate Schoolof Fisheries Science, Hokkaido University,
3-1-1 Minatomachi, Hakodate, Hokkaido 041-8611, Japane-mail: k.matsuno@fish.hokudai.ac.jp
T. Hirawake
Laboratory of Marine Bioresource and Environment Sensing,
Graduate School of Fisheries Science, Hokkaido University,
3-1-1 Minatomachi, Hakodate, Hokkaido 041-8611, Japanthe zooplankton community (loss of characteristic Arctic
species) in part of the Chukchi Sea. These apparently
contradictory effects of sea ice reduction on zooplankton
community emphasize the critical need for continued
monitoring in this area.
Keywords Barnacle larvae  Chukchi Sea  Copepods Interannual variability  Zooplankton community

Introduction
Remarkable reduction of sea ice coverage in the Arctic
Ocean was detected by satellite observation during
1991–2007. The major factor affecting this large reductionof ice coverage is considered to be increased inflow ofwarm Pacific Summer Water (PSW) passed through theBering Strait into the Chukchi Sea, a marginal sea of thewestern Arctic Ocean (Shimada et al. 2006; Woodgate
et al. 2010). The western Arctic Ocean is composed ofshallow (Chukchi Sea and East Siberia Sea) and deep
(Canada Basin and Mendeleyev Ridge) areas, and the sea
ice reduction in these areas is the largest in the Arctic
Ocean (Shimada et al. 2001, 2006). According to Woodgate et al. (2010), in 2007, sea ice coverage was the lowest,
and inflow quantity of PSW and water temperature in the
Bering Strait were the highest observed during the
1991–2007 satellite observation period. The effect of thesedrastic sea ice reductions on marine ecosystem in Arctic
Ocean is of concern (Grebmeier et al. 2006; Hunt andDrinkwater 2007). To evaluate the effect of ice reduction
on marine ecosystem, year-to-year comparative study inthe western Arctic Ocean is essential.
Zooplankton are secondary producers of the marine
ecosystem and comprise a vital link between primary

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Polar Biol (2011) 34:1349–1360

production and fishes or marine mammals in the western
Arctic Ocean (Lowry et al. 2004; Wassmann et al.
2006). In the southern Chukchi Sea, since Pacific waterflows into the sea through the Bering Strait, not only
Arctic copepods (Calanus glacialis Jaschnov) but also
large-sized Pacific copepods (Calanus marshallae Frost,
Neocalanus cristatus (Kröyer), Neocalanus flemingeri
Miller, Neocalanus plumchrus (Marukawa), Eucalanus
bungii Giestbrecht and Metridia pacifica Brodsky) are
dominant taxa (Springer et al. 1989). Zooplankton
community structure in the southern Chukchi Sea varies
geographically and is governed by water masses(Springer et al. 1989; Lane et al. 2008; Hopcroft et al.
2010). While most of the studies of zooplankton in thewestern Arctic Ocean treated a large geographic area,such as the Beaufort Sea (e.g. Thibault et al. 1999;
Ashjian et al. 2005; Darnis et al. 2008), few studies weremade in the Chukchi Sea, especially in the vicinity of
Lisburne Peninsula.
The zooplankton community in the western Arctic
Ocean is expected to be changed after 2007 when the
drastic decrease of sea ice area was observed, but no study
has contrasted zooplankton community structure between
Fig. 1 Location of thesampling stations in the
Chukchi Sea during July–
August of 1991, 1992, 2007,
and 2008. Open and solid
symbols denote stations where
the samplings were conductedin day and night, respectively.
Three digits of station names areshown in the panels; the official
station names combine thesenumbers with a cruise identifier,i.e. OS91, OS92, OS07, orOS08. Details of samplingstations are published elsewhere(Hokkaido University 1992,
1993, 2008, 2009)

72ºN

70ºN

1990s (extended sea ice coverage) and recent years(reduced sea ice coverage). In the present study, we
examined year-to-year changes of the zooplankton community in the western Arctic Ocean in 1991 and 1992
(extended sea ice area) and in 2007 and 2008 (reduced sea
ice area). Based on the whole-year zooplankton abundance
data, zooplankton community clustering and year-to-yearchanges in abundance, biomass, and community structure
are evaluated. Year-to-year changes in stage compositionof large copepods are also revealed. Through these results,
we discuss the effects of sea ice reduction on the zooplankton community in the western Arctic Ocean.

Materials and methods
A total of 120 zooplankton samplings were conducted by
T.S. Oshoro-Maru in the Chukchi Sea (668000 -718110 N,
1628020 -1688580 W) during July 24–31, 1991 (n = 27), July
24–31, 1992 (n = 34), August 5–13, 2007 (n = 31), andJuly 7–13, 2008 (n = 28) (Fig. 1). Zooplankton samples
were collected at day or night by vertical tows with a
NORPAC net (mouth diameter 45 cm, mesh size 335 lm)

1991

Chukchi Sea

170 176 177 178
169 171 175 179
168
173 174165
172
166
183 182180
164 167
184 181163 162

Lisburne Peninsula

68ºN

Alaska159 161
158 160

Chukchi Sea

138139137 140 142
148 143 145
144
146
135
149
136
147
133
134
154 150 151
155
153 152
132
156
Lisburne Peninsula
131
157
130
158
129 159
Alaska
126

125

66ºN

Bering Strait

2007

Chukchi Sea
134 135139
125 123 122
124, 140

66ºN

Lisburne Peninsula
121

119 120117 118
116
115, 141142114
143 113

165ºW

Chukchi Sea

172
171 Lisburne Peninsula

173
174

175

Alaska151

153, 176
152
177

Alaska150

Bering Strait

Bering Strait
170ºW

2008

161
160
162 159 164
165
158 163
157 168 167
166
154, 155156
169 174170

136137138
133 132
131 130
127128
126
129

70ºN

68ºN

128

124

Bering Strait
72ºN

123

1992

160ºW

170ºW

165ºW

160ºW

Polar Biol (2011) 34:1349–1360

from 5 m above the bottom to the surface (depths of moststations were about 50 m). The volume of water filteredthrough the net was estimated using a flow-meter mounted
in the mouth of the net. Zooplankton samples wereimmediately preserved with 5% v/v borax buffered formalin. At zooplankton sampling stations, temperature andsalinity were measured by CTD (Neil Brown, Mark 3B[1991 and 1992] or Sea-Bird Electronics Inc., SBE 911
Plus [2007 and 2008]) casts. These hydrographic data are
published elsewhere (Hokkaido University 1992, 1993,
2008, 2009).
In the land laboratory, zooplankton samples were split
using a Motoda box splitter (Motoda 1959), and half aliquots
were weighed for wet mass (WM) with a precision of 0.01 g
using an electronic balance (Mettler PM4000). Zooplankton
in the remaining aliquots were identified and enumerated
under a dissecting microscope. Calanoid copepods wereidentified to species and copepodid stage level. Identificationof copepods mainly followed Brodsky (1967), but identification of C. marshallae and Pseudocalanus spp. (P. acuspes,
P. major, P. mimus, P. minutus and P. newmani) followed
Frost (1974, 1989). Identification of Pseudocalanus species
late copepodid stages (C5F/M and C6F/M) was at species
level, but early copepodid stages (C1–C4) were treated as
Pseudocalanus spp. because of the difficulty in species-level
identification. Since the coarseness of mesh size (335 lm),
there may be some underestimations of smaller zooplankton
forms (Pseudocalanus spp. C1–C4 and Cyclopoida). Whilethe early copepodid stages of large-sized copepods were
sampled quantitatively (e.g. C. glacialis, E. bungii and
M. pacifica), and their Mean Copepodid Stage (MCS) was
calculated using the following equation:
P6i¼1 i  Ai
MCS ¼ P
6i¼1 Aiwhere i (1–6 indicate C1–C6) is the copepodid stage for a
species, Ai (ind. m-2) is the abundance of a copepodid
stage (cf. Marin 1987).
Zooplankton samplings were conducted during Julyand August (Arctic summer), and daytime samplingaccounted for 91% of total sampling stations (Fig. 1).
Because of this reason, we made no day–night conversion
on abundance and biomass data. Abundance data (X:ind. m-2) for each species were transformed tolog10 (X ? 1) prior to cluster analysis in order to reducethe bias of abundant species. Similarities between samples
were examined by Bray-Curtis index (Bray and Curtis
1957) according to the differences in species composition.
For grouping the samples, the similarity indices were
coupled with hierarchical agglomerative clustering with acomplete linkage method (Unweighted Pair Group
Method using Arithmetic mean: UPGMA) (Field et al.

1351

1982). Nonmetric Multi-Dimensional Scaling (NMDS)
ordination was carried out to delineate the sample groups
on a two-dimensional map. All of these analyses werecarried out using BIOSTAT II software (Sigma Soft).
Multiple-regression analysis was carried out for dependenthydrographic variables (latitude, longitude, depth, integrated mean temperature, and salinity) and two-dimensional NMDS as independent variables. A species
diversity index (H0 ) in each group was calculated using
the equation:
X
H0 ¼ 
n=Ni  ln n=Ni
where n is the abundance (ind. m-2) of ith species andNi is the total zooplankton abundance (ind. m-2) in thegroup (Shannon and Weaver 1949). This calculation wasmade over all zooplankton taxa (not limited to copepods)
because zooplankton taxa other than copepods (e.g.
barnacle larvae) dominated at some stations. Inter-groupdifferences in abundance of each copepod and zooplankton taxon, and MCS of large copepods, were tested
with one-way ANOVA. If the ANOVA identified statistically significant differences (P \ 0.05), an ex post
facto test by Fisher’s Protected Least Significant Difference test (PLSD) was carried out to clarify theinteraction between groups.

Results
Hydrography
Throughout the study area, sea surface and bottom temperatures ranged from -0.9 to 14.0°C and -1.7 to 8.0°C,
respectively (Fig. 2a). In 1991, 1992, and 2008, sea surface
temperatures ranged from -0.9 to 9.6°C, but those in 2007
were 3.9–14.0°C, substantially higher than the other years.
Sea surface and bottom salinities ranged from 25.3 to 32.9
and 30.7 to 33.5, respectively (Fig. 2b). Sea surface
salinities in 1991, 1992, and 2008 ranged from 25.3 to 32.8,
but those in 2007 ranged from 30.0 to 32.9 and were significantly higher than the other years (one-way ANOVA,P \ 0.0001), although bottom salinity did not show interannual variability (Fig. 2b).
Water masses in the Chukchi Sea during summer wereseparated mainly by salinity: Surface Mixed Layer Water(SMLW, salinity \30), Eastern Chukchi Summer Water(ECSW, 31–32 salinity), and Western Chukchi Summer
Water (WCSW, salinity [32) (Shimada et al. 2001). Basedon sea surface temperature and salinity, all stations in 2007
belonged to ECSW, but those in the other years belonged
to SMLW (Fig. 3). The surface salinities in 1991 and 1992

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Polar Biol (2011) 34:1349–1360(a) Temperature(b) Salinity

1991
4

2

29

0

70°N

30

2

6
6

Surface31
32

Bottom

4

2

33

30

29

31

68°N

30

BottomSurface

4
6

32

66°N
26

1992

27
0

4

70°N

29
2

6

32 31.5

30
30

4

68°N

32.5
28
29

28

8

31

6
2

32.5

32

66°N

2007
2

70°N

4

10

68°N

31

6

12

32

32

31

8
8

32.5
6

32

66°N

2008
33

2

70°N

30
0

4

32.5

2

68°N

31

32

2
4

32.5

32

6
2

66°N
170°W

165°W

170°W

165°W

170°W

165°W

170°W

165°W

Fig. 2 Temperature (a) and salinity (b) of the sea surface (left) and bottom (right) of the stations in the Chukchi Sea during July–August of 1991,
1992, 2007, and 2008

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Polar Biol (2011) 34:1349–1360

1991
20

21

22

10

23

24

ECSW

ECSW

15

1992
20
25

26

21

22

23

24

25

27

26

27

WCSW

WCSW

5

0

SMLW

SMLW
15

2007
20

2008

24
21

22

25

23

20

21

22
23

26

10

ECSW

Temperature (ºC)

Fig. 3 T-S diagrams in the
Chukchi Sea during July–
August of 1991, 1992, 2007,
and 2008. Hydrographic data
were collected from 0, 10, 20,
30, 40, and 50 m. Numbers in
the panels indicate water
densities (sigma-T). SMLW
surface mixed layer water(salinity \30), ECSW Eastern
Chukchi Summer Water(salinity = 31–32), WCSW
Western Chukchi summer water(salinity[32) (cf. Shimada et al.
2001)

1353

24

27

25
26
27

SMLW
26

28

30

32

WCSW

0

WCSW

ECSW

5

SMLW

34

26

28

30

32

34

Salinity

were significantly lower than in 2007 and 2008 (one-way
ANOVA, P \ 0.0001).
Zooplankton
Zooplankton abundance ranged from 4,000 to 316,000
ind. m-2 (mean: 70,000) (Fig. 4a). Abundance in 1991,
1992, and 2008 was greater north of Lisburne Peninsula,while in 2007 abundance was greater south of Lisburne
Peninsula (Fig. 4a). Zooplankton biomass ranged from 0.07
to 286 g WM m-2 (mean: 36). The geographic distributionof biomass was not parallel with abundance except for thesouth of Lisburne Peninsula in 2007 (Fig. 4b).
Copepods composed 2–86% (mean: 31) of zooplankton
abundance, and barnacle nauplii and cypris larvae (Balanus
crenatus Brugiere) were also dominant and composed
2–95% (mean: 47) of abundance in the northern area
(Fig. 5). Within the copepods, proportions of C. glacialis
and Pseudocalanus spp. were relatively high, especially in1991 and 1992. In 2007, proportions of Pacific copepods(E. bungii and M. pacifica) were high, while the proportionof barnacle larvae was low (Fig. 5). Barnacle larvae predominated in 2008. Through the 4 years of analysis, 22
species of calanoid copepods belonging to 13 genera wereidentified (Table 1). Within these species, 6 species
belonging to 4 genera: C. marshallae, E. bungii, M.
pacifica, N. cristatus, N. flemingeri, and N. plumchrus were
Pacific copepods (Springer et al. 1989).

Statistical analyses on year-to-year changes in zooplankton abundance showed significant differences for 21
taxa/species (Table 2). Abundance of total copepods was
the highest in 2007, while that of total zooplankton was thehighest in 2008. Significantly abundant taxa/species in eachyear were Appendicularia in 1991, the Arctic copepod
C. glacialis in 1992, and various copepods [Acartia tumida
Willey, Centropages abdominalis Sato, Cyclopoida,
E. bungii, M. pacifica, Microcalanus pygmaeus (Sars), N.
cristatus, P. minutus and Scolecithricella minor (Brady)],
Echinodermata larvae and Polychaeta in 2007, and several
copepods (Eurytemora herdmani Thompson and Scott, N.
plumchrus and Tortanus discaudatus (Thompson and
Scott)), barnacle larva (B. crenatus), Eubrachyura zoea,
and Limacina helicina (Phipps) in 2008. Since Pacificcopepods were dominant in 2007, total copepod abundance
was the greatest in 2007. When barnacle larvae were
dominant in 2008, total zooplankton abundance was thehighest in 2008 (Table 1).
Year-to-year changes in the MCS of large copepods: C.
glacialis, E. bungii, and M. pacifica were tested by one-way
ANOVA. The MCS of C. glacialis and M. pacifica in 2007
was significantly higher (= dominated by late copepodid
stage and faster growth) than in other years (Table 2).
Based on the taxon abundance, zooplankton communities were classified into six groups (A–F) by cluster analysis with 28 and 34% dissimilarities (Fig. 6a). The quantityof stations in each group varied between 3 and 60, and

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Polar Biol (2011) 34:1349–1360(a) Abundance(b) Biomass

70°N

1991
68°N

(37.9)(66,216)

66°N

70°N

1992
68°N

(26.8)(46,439)

66°N

70°N

2007
68°N

(42.8)(71,117)

66°N

70°N

2008
68°N

66°N
170°W

(38.3)

Discussion(103,075)

Abundance(×105 ind. m−2)

Wet mass
×102 g WM m−2)
(×

0 123

01 23

165°W

170°W

165°W

Fig. 4 Geographic distribution of the zooplankton abundance (a) andbiomass (b) in the Chukchi Sea during July–August of 1991, 1992,
2007, and 2008. Values in the parentheses indicate mean values ofeach year123

groups C and F were considered to be outlier groups
because few stations (3–4 stations) belonged to each group(Fig. 6a). Environmental parameters significantly affecting
cluster analysis were latitude, longitude, sea surface temperature, sea surface salinity, and bottom salinity, with
24–37% coefficient of determinations (r2) (Fig. 6b). Meanabundances of groups A, B, and D ranged from 76,800 to
101,030 ind. m-2, but those of groups C, E, and F werelower and ranged from 5,744 to 30,283 ind. m-2 (Fig. 6c).
For groups B, C, and E, barnacle larvae dominated andspecies diversities were low. Groups A, D, and F werecharacterized by few barnacle larvae and dominance ofPacific copepods (groups A, D) or Arctic copepods (groupF) (Fig. 6c). Species diversity of groups A and D was highbecause of the occurrence of both Pacific and Arctic
copepods.
Distribution of each group was well separated both
geographically and interannually (Fig. 7). Group B was
observed offshore north of Lisburne Peninsula, and group
E was observed inshore of the same region (Fig. 7). GroupA was observed south of Lisburne Peninsula in 1991 and
1992, and north of Lisburne Peninsula in 2007 and 2008.
Group D, characterized by the high abundance and dominance of Pacific copepods, was observed only south of
Lisburne Peninsula in 2007.
Concerning interannual variability in the zooplankton
community, geographic distribution was similar for 1991
and 1992 (Fig. 7). In 2007, the whole distribution area wasshifted northward compared to 1991 and 1992, and groupD, characterized by dominance of Pacific copepods, wasobserved south of Lisburne Peninsula. In 2008, geographic
distribution of groups was similar to 1991 and 1992, but
distribution of group A, which was observed south of
Lisburne Peninsula in 1991 and 1992, also penetrated to thenorth of Lisburne Peninsula (Fig. 7). Year-to-year characteristics in hydrographic environment, zooplankton biomass, community structure, species diversity, and growthof large copepods in 1991, 1992, 2007, and 2008 aresummarized in Table 3.

Environmental and zooplankton characteristics
in each year
The years 1991 and 1992 showed similar characteristics:
i.e., presence of fresh and cold ice melt water in the surface, low zooplankton biomass, and low species diversity
due to the dominance of small-sized Arctic copepods andtheir slower development under the low temperature
condition. The zooplankton community in 1991 wasPolar Biol (2011) 34:1349–1360

1355

Fig. 5 Taxonomic composition
in total zooplankton abundanceof the Chukchi Sea during July–
August of 1991, 1992, 2007,
and 2008

100

1991

75
50

100

184

183

182

181

180

179

178

177

176

175

174

173

172

171

170

169

168

167

166

165

164

163

162

161

160

159

0

158

25

1992

75

25
0
100

124
125
126
128
129
130
131
132
133
134
135
136
137
138
139
140
142
143
144
145
146
147
148
149
150
151
152
153
154
155
156
157
158
159

Composition (%)

50

2007

75
50

0
100

113
114
115
116
117
118
119
120
121
122
123
124
125
126
127
128
129
130
131
132
133
134
135
136
137
138
139
140
141
142
143

25

2008

75
50

177

175
176

174

173

171
172

170

169

167
168

166

165

164

163

162

161

160

159

158

157

156

155

154

153

152

151

0

150

25

Station no.
Calanus glacialis
Pseudocalanus spp.
Other zooplankton taxa

characterized by dominance of Appendicularia (mainly
Oikopleura vanhoeffeni), which is known to occur aroundthe ice edge area of the Arctic Ocean (Acuña et al. 1999).
Dominance of Appendicularia in 1991 may be related tothe strong presence of ice melt water in this year.
Water mass formation in 2007 was extremely different
from the other years. During 2007, warm and saline
ECSW, which originated from Pacific, predominatedthroughout the stations. In 2007, zooplankton biomass
was high south of Lisburne Peninsula, which was caused

Eucalanus bungii
Other copepods

Metridia pacifica
Balanus crenatus larvaeby the dominance of large-sized Pacific copepods transported by ECSW. Zooplankton species diversity was alsohigh in 2007, when the zooplankton community wascharacterized by a mixture of the Arctic and Pacificspecies. Warm temperature is the primary cause of fasterdevelopment of copepods (cf. Corkett and McLaren
1978). Development of large copepods (C. glacialis and
M. longa) in 2007 was significantly faster than the otheryears. Since the population structure of E. bungii in 2007
was characterized by the dominance of nauplii and early

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Polar Biol (2011) 34:1349–1360

Table 1 Year-to-yearcomparison of zooplankton
abundances in the Chukchi Sea
during July–August of 1991,
1992, 2007, and 2008

Values are mean abundances ineach year. Differences between
years were tested by one-way
ANOVA and post hoc test by
Fisher’s PLSD. Any years notconnected by the underlines are
significantly different(P \ 0.05). Numbers in theparentheses indicate number ofstations in each year
NS not significant* P \ 0.05, ** P \ 0.01

copepodid stages which may reflect of reproduction, thisspecies had no significant year-to-year differences in
MCS.

123

Zooplankton characteristics in 2008 were similar to
those in 1991/1992, while the hydrography in 2008 wascharacterized by high saline water in the surface layer inPolar Biol (2011) 34:1349–1360

1357

Table 2 Year-to-year comparison on mean copepodid stage of C. glacialis, E. bungii, and M. pacifica in the Chukchi Sea during July–August of
1991, 1992, 2007, and 2008

Differences between years were tested by one-way ANOVA and post hoc test by Fisher’s PLSD. Any years not connected by the underlines are
significantly different (P \ 0.05). Values are mean copepodid stage ± SD. Numbers in the parentheses indicate number of stations in each year
* P \ 0.05, ** P \ 0.01

(a)

(b)
4

A (33)

SST 34%SSS
31%

B (60)

Lon 37%2C (4)BS 24%

Lat 37%D (8)E (12)

A
B
C
D
E
F

0

F (3)
30

40

Stress: 0.198

50−2

Bray-Curtis dissimilarity (%)

(c)

−4

−2

0

1000

3

100

2.5

10

2

1

1.5

0.1

1

Species diversity index (H )20

Abundance (×103 ind. m−2)

Fig. 6 Results of cluster
analysis based on zooplankton
abundance by Bray-Curtis
similarity connected withUPGMA. Six groups(A–F) were identified with thedissimilarity at 28 and 34%,
respectively (dashed lines) (a).
Numbers in the parentheses(a) indicate quantity of stations
included in each group.
Nonmetric multi-dimensional
scaling plots of the six groups,
with arrows and percentages
indicating directions ofenvironmental parameters andcoefficient of determination (r2),respectively (b). BS bottom
salinity, Lat latitude, Lonlongitude, SSS sea surface
salinity, SST sea surface
temperature. Abundance,
species diversity, and taxonomic
composition of each group (c).
Vertical bars in abundanceindicate standard deviations

2

4

Abundance
H

100

Composition (%)

Other zooplankton taxa
Balanus crenatus larvae

75

Other copepods
Pseudocalanus spp.

50

Metridia pacifica
Eucalanus bungii

25

Calanus glacialis
0
A

B

C

D

E

F

Group

contrast to the ice melt water in 1991/1992. In detail,zooplankton biomass in 2008 was low but its abundance
was the highest within the 4 years, which was caused by

the dominance of the small-sized barnacle larvae (B.
crenatus) in 2008 (Table 1; Fig. 5). Because of the predominance of barnacle larvae in 2008, species diversity

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Polar Biol (2011) 34:1349–1360

Fig. 7 Geographic distributionsof the six groups (A–F)
identified from Bray-Curtis
similarity based on zooplankton
abundances (cf. Fig. 6) in the
Chukchi Sea during July–
August of 1991, 1992, 2007,
and 2008

Table 3 Summary of the year-to-year comparisons in hydrography, zooplankton (biomass, community, and diversity), and development of large
copepods in the Chukchi Sea during July–August of 1991, 1992, 2007, and 2008
Year

Hydrography (SSS, SST)

Zooplankton
Biomass(g WM m-2)

Community

Diversity(H0 )Development of large
copepods (cf. Table 2)

1991 Ice melt water (30.0 ± 1.3, 5.2 ± 1.7)

Low (38 ± 26)

ArcticLow (1.61)

Slow

1992 Ice melt water (29.4 ± 1.9, 5.2 ± 2.1)

Low (27 ± 18)

ArcticLow (2.18)

Slow2007 ECSW (31.9 ± 0.7, 9.7 ± 2.6)

High (43 ± 60) Pacific ? Arctic

2008 High saline water (30.9 ± 1.1, 4.3 ± 1.9) Low (38 ± 27)

High (2.56) Fast

Arctic (Balanus larvae dominant) Low (1.13)

Slow

Values in the parentheses indicate mean ± SD for sea surface salinity (SSS), temperature (SST), and biomass, and mean for H0
ECSW Eastern Chukchi summer water

was low. The moderate temperature condition in 2008 may
have induced ordinary developmental rates of large copepods in that year.
Throughout the 4 years studied, 2007 was the mostdistinctive year. According to Woodgate et al. (2010),

123

volume and temperature of inflow PSW in 2007 was thegreatest and warmest of the 1991–2007 period. High volume of PSW in 2007 may have induced high advection oflarge-sized Pacific copepods and led to the high zooplankton biomass and high species diversity observed inPolar Biol (2011) 34:1349–1360

that year. Higher temperature may have led to fasterdevelopment of large copepods in that year, which thisstudy observed for both the Pacific copepod (M. pacifica)
and the Arctic copepod (C. glacialis). Hence, the increaseof inflow of the warm PSW is considered to have a positiveeffect on zooplankton community in terms of biomass anddevelopment of large copepods.
Comparison between 1991/1992 and 2007/2008
Comparison between 1991/1992 (sea ice extent) and2007/2008 (sea ice reduced) showed a remarkable northward shift in geographic distribution of zooplankton communities (Fig. 7). This northward shift in zooplankton
community in 2007/2008 may be related to the differencesin formation of water masses. The greatest differences in
the hydrographic environment between 1991/1992 and2007/2008 was in the presence (1991/1992) or absence(2007/2008) of sea ice melt water and was also evident in
the salinity of the surface layer, which was low for
1991/1992 and high for 2007/2008 (Fig. 3).
Concerning the zooplankton community, the Arctic
copepod C. glacialis was relatively abundant in 1991/1992,
and less so in 2007/2008. The zooplankton community in2007 was characterized by the dominance of Pacificcopepods, and in 2008 was dominated by barnacle larvae(Table 1; Fig. 5). The dominance of barnacle larvae in2008 suggests an earlier release of the larvae from theirbenthic adult form than in 1991/1992.
Concerning the release timing of barnacle larvae frombenthic adults, laboratory rearing studies show that theamount of food concentration (phytoplankton) is a key factor
for release timing (Clare et al. 1984; Clare and Walker 1986).
Field studies also indicate that onset of the phytoplankton
bloom is a key factor stimulating the release of barnacle
larvae (Barnes 1957; Crisp 1962). Because the sea surface
salinity was higher in 2007/2008 than in 1991/1992 (Fig. 3),
the timing of sea ice reduction was considered to be earlier in
2007/2008 (Markus et al. 2009). This earlier sea ice reduction in 2007/2008 may induce that earlier phytoplankton
bloom for these years because of the earlier release from thelight limitation on the photosynthesis. The earlier onset of thephytoplankton bloom in 2008 is considered to be a cause of
the dominance of the barnacle larvae in that year. The earlier
sea ice reduction and onset of phytoplankton bloom was also
the case of 2007. However, the greater inflow of PSW in 2007
forced the barnacle distribution area north (Fig. 7), leading
to a lower abundance of barnacle larvae in 2007 than 2008.
The future prospect
Year-to-year comparisons in this study revealed significant
differences in zooplankton abundance, biomass and1359

community structure (Table 3). Under the global warming
condition, a highly relevant issue in recent years, a large
reduction of ice cover area and increased inflow of the PSW
are expected. Since PSW contains higher nutrient levels than
Arctic water (Springer and McRoy 1993; Cota et al. 1996),
increase of the inflow of the PSW is expected to induce theexpansion of the high primary production area in the
Chukchi Sea. Thus, in terms of primary production, global
warming may have a positive function in this area.
From the viewpoint of zooplankton production, increased
inflow of PSW induced the dominance of the large-sized
Pacific copepods, and thus may have positively affected productivity. However, increased inflow of PSW caused changes
in the marine ecosystem structure in the Chukchi Sea (loss ofcharacteristic Arctic species in part of the region), which isconsidered as a negative effect of global warming.
The zooplankton fauna is completely different between
the Pacific and Arctic Oceans. The PSW contains various
Pacific copepods: i.e. E. bungii, M. pacifica, N. cristatus,
N. flemingeri, and N. plumchrus (Springer et al. 1989). Eucalanus bungii, the most dominant copepod in the PSW, hasa diapause phase during autumn and winter and a flexible
generation length of one to 3 years (Miller et al. 1984; Tsudaet al. 2004; Shoden et al. 2005). Because the family Eucalanidae is a minor component of the North Atlantic andArctic Oceans, the ecological niche that E. bungii occupies in
the PSW is considered to be underutilized in these oceans. If
this assumption is correct, and the Pacific copepods colonize
the Arctic Ocean, they may increase their population by
utilizing this vacant ecological niche. In the future Chukchi
Sea, reduction of ice cover area may accelerate changes inmarine ecosystem structure. Therefore, a critical and continuous monitoring of zooplankton community structure inthis area is needed for future study.
Acknowledgments We thank captains, officers, and crews of the T.S.
Oshoro-Maru for their help in zooplankton sampling and hydrographic
data collection. Dr. Brenda Holladay (University of Alaska Fairbanks)and Dr. Koji Shimada (Tokyo University of Marine Science andTechnology) provided valuable comments on an earlier draft of themanuscript. This study was supported by Grant-in-Aid for Young
Scientists (B) 21780173 by Japan Society for the Promotion of Science.

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