Deep-Sea Research II 94 (2013) 44–56

Contents lists available at ScienceDirect

Deep-Sea Research II
journal homepage: www.elsevier.com/locate/dsr2

Interannual changes in the zooplankton community structure on thesoutheastern Bering Sea shelf during summers of 1994–2009
Rie Ohashi a, Atsushi Yamaguchi a,n, Kohei Matsuno a, Rui Saito a, Nao Yamada b,
Anai Iijima c, Naonobu Shiga d, Ichiro Imai aaGraduate School of Fisheries Sciences, Hokkaido University, 3-1-1 Minato, Hakodate, Hokkaido 041-8611, Japan
Hokkaido Hakodate Fisheries High School, 2-15-3 Nanaehama, Hokuto, Hokkaido 049-0111, Japanc
Donan Research Branch, Salmon and Freshwater Fisheries Research Institute, Hokkaido Research Organization, 189-43 Kumaishi Ayukawacho, Yakumocho,
Futami, Hokkaido 043-0402, Japand
Hakodate Junior College, 52-1 Takaokacho, Hakodate, Hokkaido 042-0955, Japanb

art ic l e i nf o

a b s t r a c t

Available online 15 March 2013

On the southeastern Bering Sea shelf, mesozooplankton plays an important role in material transfer
between primary producers and ﬁsheries resources. The biomass of mesozooplankton in this region is
known to vary annually, but little is known about annual changes in community structure and species
composition. In the present study, regional and long-term changes in abundance, biomass andcommunity structure of copepods and chaetognaths on the shelf were evaluated based on NORPAC
net samples collected during summers of 1994–2009. During the study period, regime shifts occurredfrom high interannual variability regime (1994–1999) to low interannual variability regime with hightemperature (2000–2005), then to a low interannual variability regime with low temperature (2007–2009). A total of 24 calanoid copepod species belonging to 21 genera were identiﬁed from samples.
Copepod abundance ranged from 150 to 834,486 inds. m−2, was greatest on the Middle shelf, and washigher in cold years, than in warm years. Copepod biomass ranged from 0.013 to 150 g DM m-2, and was
also higher in cold years than in warm years. Based on the results of cluster analysis, the copepod
community was divided into six groups (A–F). The regional and interannual distributions of each groupwere distinct. Interannual changes in abundance of the dominant copepod on the Outer shelf and Middle
shelf were highly signiﬁcant (po 0.0001), and their abundances were negatively correlated withtemperature and salinity. Interannual changes in copepod community that occurred between cold andwarm years are thought to have been caused by differences in the magnitude and timing of the spring
phytoplankton bloom between the two regimes. Abundance and biomass of the chaetognath Parasagitta
elegans ranged from 30 to 15,180 inds. m-2 and from 11 to 1559 mg DM m−2, respectively. Chaetognathabundance was signiﬁcantly correlated with the abundance of the dominant copepods (po 0.0001).
Differences in cold and warm years may also affect recruitment of walleye pollock. We conclude that on
the southeastern Bering Sea shelf, the magnitude and timing of primary production, which is related toclimate change, may signiﬁcantly affect how it is transferred through the food web.
& 2013 Elsevier Ltd. All rights reserved.

Keywords:
Annual variations
Abundance
Biomass
Zooplankton
Community composition
Species diversity

1. Introduction
The southeastern Bering Sea shelf is characterized by highbiological productivity, has large amounts of phytoplankton,
zooplankton, benthos, ﬁshes, seabirds and marine mammals, andis an important ﬁshing ground of walleye pollock (Theragra
chalcogramma) (Springer, 1992; Springer et al., 1996). Recently,
this region has undergone large biological/environmental changes(Jin et al., 2009; Stabeno et al., 2010). In 1997, a coccolithophore(Emiliania huxleyi) bloom was observed (Napp and Hunt, 2001;nCorresponding author. Tel.: þ81 138 40 5543; fax: þ 81 138 40 5542.
E-mail address: a-yama@ﬁsh.hokudai.ac.jp (A. Yamaguchi).

0967-0645/$ - see front matter & 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.dsr2.2013.03.018

Stockwell et al., 2001; Sukhanova and Flint, 1998), and massmortality of short-tailed shearwaters (Pufﬁnus tenuirostris)
occurred near the Pribilof Islands (Baduini et al., 2001). In 1998,
a climate regime shift was reported (McFarlane et al., 2000), andthe biomass of the jellyﬁsh Chrysaora melanaster was observed topeak (Brodeur et al., 2008). To describe the effect of climate regime
shifts on lower to higher trophic levels, Hunt et al. (2002)
proposed the Oscillation Control Hypothesis (OCH). In 2006, a
climate regime shift from a warm period to cold period wasreported, and the OCH was revised based on observations during
this period (Hunt et al., 2011).
In the Bering Sea ecosystem, mesozooplankton are importantbecause they connect primary production to higher trophic levelproduction. In the mesozooplankton fauna of this region, theR. Ohashi et al. / Deep-Sea Research II 94 (2013) 44–56

dominant taxon is Copepoda, and various studies have been conducted on their biology and ecology. They include studies of seasonalvariations of community structure during spring and summer (Smith
and Vidal, 1986), interannual variations in their total wet-weightbiomass (Hunt et al., 2008; Napp et al., 2002; Sugimoto and
Tadokoro, 1997, 1998), seasonal and spatial variations in community
structure (Kang et al., 2006), and the effects of El Niño and La Niña onbiomass and production (Coyle and Pinchuk, 2002). However, moststudies of long-term variations in mesozooplankton have treated
only wet-weight biomass data without examining the species caught
or separating sub-regions or domains. In studies of species andzooplankton community structure, the study areas have been narrow, and the study periods have been short. Consequently, information on long-term changes in mesozooplankton community and their
species composition is extremely scarce.
The second most abundant taxonomic group in the Bering Sea
mesozooplankton biomass is chaetognaths (Coyle and Pinchuk,2002). They are carnivores, prey upon small zooplankton and ﬁshlarvae, contribute to vertical ﬂuxes to deep water (Brodeur andTerazaki, 1999), and sometimes account for nearly 50% of the preyof walleye pollock larvae (Brodeur and Wilson, 1996). Thus,
chaetognaths are important because of their role linking lower
to higher trophic levels. However, little is known about their longterm variation in the Bering Sea.
In the present study, regional and long-term changes inabundance, biomass and community structure of copepods andchaetognaths are evaluated based on samples collected over thesoutheastern Bering Sea shelf during the summers of 1994–2009.
Long-term data on copepods and chaetognaths are compared withhydrographic data, and we discuss possible mechanisms controlling interannual variations in mesozooplankton community structures and species composition.

Table 1
Calanoid copepod species collected in the southeastern Bering Sea during summersof 1994–2009. Major region of occurrence is also shown for each species. ●: Largeoceanic copepods that have a diapause phase in deep layer (Miller et al., 1984).
Region abbreviations are: I: Inner shelf, M: Middle shelf, O: Outer shelf, S: Slope
and B: Basin.*: Rare species (occurred onlyo 2% of the whole stations) omitted
from data for cluster analysis (cf. Fig. 4).
Species

Major region of occurrence

Acartia longiremis (Lilljeborg, 1853)
A. tumida Willey, 1920
*Aetideopsis rostrata Sars, 1903
*Aetideus paciﬁcus Brodsky, 1950
Calanus spp.
Candacia columbiae Campbell, 1929
Centropages abdominalis Sato, 1913
Epilabidocera amphitrites (McMurrich, 1916)●
Eucalanus bungii Giesbrecht, 1892
Eurytemora herdmani Thompson and Scott, 1897
Gaetanus intermedius Wolfenden, 1905
G. simplex Brodsky, 1950
Heterorhabdus tanneri (Giesbrecht, 1895)
Metridia paciﬁca Brodsky, 1950
Microcalanus pygmaeus (Sars, 1900)●
Neocalanus cristatus (Kröyer, 1848)●
N. ﬂemingeri Miller, 1988●
N. plumchrus (Marukawa, 1921)
Paraeuchaeta elongata (Esterly, 1913)
Pleuromamma scutullata Brodsky, 1950
Pseudocalanus spp.
*Racovitzanus antarcticus Giesbrecht, 1902
Scolecithricella minor (Brady, 1883)*S. ovata (Farran, 1905)
Tortanus discaudatus (Thompson and Scott, 1897)
Undinopsis paciﬁcus Brodsky, 1950

I, M, O
M, O
B
B
M, O, S, B
S, B
I, M
I
O,S,B
I
S,B
S,B
S,B
O,S,B
M,O
O,S,B
O, S, B
O,S,B
B
S,B
I, M, O, S, B
B
O, S, B
B
I
O,S

45

2. Material and methods
2.1. Field sampling
Sampling was conducted over the southeastern Bering Sea shelfduring 1994–2009 between 24 June and 8 August on board the T/SOshoro-Maru of the Faculty of Fisheries, Hokkaido University. For eachyear, samples were collected within a two week period. Zooplankton
samples were collected by vertical hauls of ﬂowmeter-equipped
NORPAC nets (45 cm mouth diameter, 0.335 mm mesh; Motoda,
1957) from 150 m depth or near the bottom (where the depth wasshallower than 150 m) to the surface. Zooplankton samples wereimmediately preserved with 5% formaldehyde-seawater buffered withsodium tetraborate. In addition, temperature and salinity were measured with a CTD (Neil Brown, Mark IIIB during 1994–2001 andSeabird SBE-911plus during 2002–2009). Water samples from the CTD
rosette were ﬁltered through GF/F ﬁlters, extracted with acetone orDMF and chlorophyll a concentration was measured using a ﬂuorometer (Turner Designs, Inc.).
The number of sampling stations in any one year was 9–49
(total¼96), and the total number of samples was 428 (Fig. 1).
Based on the bottom depth, the southeastern Bering Sea shelf wasdivided into three regions: Inner shelf (o50 m), Middle shelf(50–100 m) and Outer shelf (100–200 m) (Coachman and Charnell,
1979; Coachman, 1986). Areas with depth of 200–1000 m and
41000 m were classiﬁed as Slope and Basin, respectively. Six
stations on the Outer shelf and six on the Middle shelf were
sampled every year of the study (Fig. 1), so only the data fromthese twelve stations were used to analyze long-term changes.

2.2. Sample analysis
Based on the biomass of the samples, subsamples were createdwith a Motoda plankton splitter (Motoda, 1959), and the subsamples were examined under a stereomicroscope.
Copepods were staged and identiﬁed to the lowest possible
taxonomic level. For copepods, the most important genus in thisregion (Calanus) is reported to be mixture of Calanus glacialis andCalanus marshallae (Nelson et al., 2009). We could not distinguish

62°N
50
100

200

50

Outer
shelf
Inner
shelf

200
1000

58°N

50

Pribilof
Islands

Middle
shelf

Slope
200

54°N

Basin

176°W

100

1000

168°W

160°W

Fig. 1. Location of the sampling stations in the southeastern Bering Sea during thesummers of 1994–2009 (circles). Solid symbols denote stations where sampling
was conducted in all years from 1994–2009, providing the data used for annualcomparisons. Line indicates 1661W transect where the hydrographic data wereanalyzed (cf. Fig. 2).

46

R. Ohashi et al. / Deep-Sea Research II 94 (2013) 44–56

0
40
80
120
0
40

Depth (m)

80
120
0
40
80
120
0
40
80
120
0
40
80
120
0
40

Depth (m)

80
120
0
40
80
120
0
40
80
120
56

57

58

56

57

58
56
Latitude (ºN)

57

58

56

57

58

Fig. 2. (A) Temperature and (B) chlorophyll a stations along 1661W during summers of 1994–2009.

the two species and treated them as “Calanus spp.”. For biomass
estimation, copepods were separated into four groups: Calanus
spp., Neocalanus spp., Eucalanus bungii and other copepods. One
hundred individuals in each group were chosen randomly formeasurement of total lengths (TL, mm) by ocular micrometer. Dry
mass (DM, mg) was estimated using the following equations
derived for organisms from the Oyashio region (Imao, 2005):
Calanus and Neocalanus spp. (less lipids)log 10 DM ¼ 2:48 log 10 TL−6:00(1)

Calanus and Neocalanus spp. (more lipids)log 10 DM ¼ 3:00 log 10 TL−7:70(2)

log 10 DM ¼ 3:16 log 10 TL−9:16(3)

E. bungii

Other copepods

log 10 DM ¼ 2:62 log 10 TL−6:40(4)

For Calanus spp. and Neocalanus spp., lipid accumulation was
separated into two: less lipids ( o20% of prosome volume) andmore lipids (≥20% of prosome volume). Then Eqs. (1) and (2) wereapplied for less and more lipid specimens, respectively. The total

R. Ohashi et al. / Deep-Sea Research II 94 (2013) 44–56

47

62
58

Latitude (ºN)

54
62
58
54
62
58
54
62
58

Latitude (ºN)

54
62
58
54
62
58
54
172

164

172

164

172

164
172
164
Longitude (ºW)

172

164

172

164

Fig. 3. Regional variations in (A) copepod abundance and (B) biomass in the southeastern Bering Sea during summers of 1994–2009.

biomass of copepods (mg DM m−2) was estimated by multiplying
the average individual mass (mg DM inds.−1) by the abundance(inds. m−2).
Chaetognaths were identiﬁed to species based on the samples
collected during 1996–2009. The total length (TL, mm) of thedominant chaetognath, P. elegans, was measured using a ruler forlarge individuals (TL≥10 mm) and an ocular micrometer for small
specimens (TL o10 mm). Specimens were classiﬁed according to
McLaren (1969), Sameoto (1973) and Zo (1973): Stage I (juveniles),Stage II (immature) and Stage III (mature). To estimate DM, ashfree dry mass (AFDM, mg) was estimated from the TL using thefollowing equation (Mumm, 1991):
AFDM ¼ 0:0002TL 2:6924

ð5Þ

Dry mass was estimated as DM¼ AFDM/0.9 (Båmstedt, 1986).
2.3. Data analysis
Zooplankton samples were collected day and night. Since thedepths of most sampling stations were o150 m and the sampling
was conducted throughout the water column, day–night differences in abundance and biomass were expected to be small. There

were no signiﬁcant differences between day and night abundanceor biomass of copepods and chaetognaths for all years (p ¼0.06–
0.93, U-test). Thus, no day-night conversions were done forabundance or biomass.
To examine community structure, we conducted cluster analysis and nonmetric multidimensional scaling (NMDS) ordination.
Abundance data (X: inds. m−2) of each species were transformed
to log10(X þ1) prior to analysis to reduce the bias of abundantspecies. Rare species which occurred only o2% of the wholestations were eliminated from the data for analysis (cf. Table 1).
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 a complete linkage method. The NMDS ordination was carried out todelineate the sample groups on the two-dimensional map. All ofthese analyses were carried out using BIOSTAT II software(Sigma Soft).
To evaluate environmental factors that may have inﬂuenced
sample groups determined by cluster analysis, nonmetric multidimensional scaling (NMDS) ordination was carried out to delineate the sample groups in two-dimensional space. We then

48

R. Ohashi et al. / Deep-Sea Research II 94 (2013) 44–56

3

A (127)

A
D

B
E

C
F

2

B (92)C (24)1

D (93)0

E (68)-1

F (24)Lon SSS SST 9%
Depth 77%
14% 20%-2

BS 18%

30

40

Lat 70%-3-3Dissimilarity index (%)

-2

-1

2

12
Abundance( x104inds. m-2)

0

8
1
4
0

0
100

Stress = 0.12

1Species diversity (H')

20

2

3

Abundance
H'

Other copepods
80
Composition (%)

Pseudocalanus spp.
Neocalanus spp.

60

Metridia pacifica
Eucalanus bungii

40

Calanus spp.
20

Acartia spp.

0
A

B

C

D

E

F

Group
Fig. 4. Copepod assemblages: (A) dendrograms from the cluster analysis based on copepod abundance. Six groups (A–F) were identiﬁed with dissimilarity at 20% (dashedline). Numbers in the parentheses indicate quantity of stations included in each group. (B) Nonmetric multidimensional scaling plots of the six groups, with arrows andpercentages indicating directions of environmental parameters and coefﬁcient of determinations (r2), respectively. Lat: latitude, Lon: longitude, SSS: sea surface salinity, SST:
sea surface temperature, BS: bottom salinity. (C) Mean abundance with standard deviations and species diversity (H′) (upper) and taxonomic composition of each group(lower).

conducted multiple-regression analysis (Y¼ aX1 þbX2 þc) with thehydrographic data (Y: latitude, longitude, depth, sea surface andbottom temperature and sea surface and bottom salinity) are thedependent variables and two-dimensional NMDS as independent
variables (thus, axis 1 as X1 and axis 2 as X2) (a, b, c are ﬁtted
constants). Shannon's diversity index (H′) in each group was
calculated using the equation:
H′ ¼ −∑ni =N  lnni =Nð6Þwhere ni is the abundance (inds. m−2) of the ith species, and N is
the total copepod abundance (inds. m−2) in the group (Shannon
and Weaver, 1949).
To evaluate factors affecting the variability of copepod abundance,
two-way ANOVA with year and station as independent variables wasused. To determine which factors controlled annual changes incopepod abundance, correlation analysis was done between theabundance of dominant copepods and three factors: watertemperature (throughout whole water column, in upper layer andin lower layer), salinity and chlorophyll a (whole water column).
For P. elegans, cohort analysis was done based on the TL
histogram data from the Middle shelf using Microsoft Excel Solver(Aizawa and Takiguchi, 1999).
To evaluate what factors controlled the interannual changes inchaetognath abundance, we tested for correlations between the
chaetognath abundance for the Outer shelf and Middle shelf andfour factors: water temperature (whole water column, upper andlower layer), salinity (whole water column), chlorophyll a (wholewater column) and abundance of the dominant copepods.
3. Results
3.1. Hydrography
In all years, a thermocline was present 20–30 m, and the bottom
temperature of Middle shelf ranged between 0 and 4 1C, but was

R. Ohashi et al. / Deep-Sea Research II 94 (2013) 44–56

3.2. Copepods

higher for the Inner and Outer shelves (Fig. 2A). The Middle shelf,bottom temperature was about 41C during 2001–2005, and lower(0–3 1C) during 2007–2009. Owing to Stabeno et al. (2012), there
were three regimes in depth-averaged ocean temperature: cold;
1995, 1997, 1999, 2007–2009, average; 1996, 2000, 2006, and warm;
1998, 2001–2005. Our results conﬁrmed this pattern (Fig. 2A).
The peak of summer chlorophyll a at each station varied between
0.5 and 25.4 mg m−3, and chlorophyll a was high above the thermocline and on the Inner shelf (Fig. 2B). The peak of chlorophyll a waslow (ca. 1 mg m−3) during the warm regime (2001–2005).

60

Regional and interannual changes in total copepod abundanceand biomass were observed (Fig. 3). Copepod abundance ranged
from 150 to 834,486 inds. m−2, and was greatest on the Middle
shelf (Fig. 3A). Copepod abundance was high during cold years(1995, 1997, 1999 and 2007–2009), and low in warm years (2001–
2005) (Fig. 3A). Copepod biomass ranged from 0.013 to
150 g DM m−2, and was highest on the Outer and Middle shelves(Fig. 3B). The biomass peak occurred in more oceanic waters than

1995

1996

1997

1998

1999

2000

2001

2002

2003

2004

2005

2006

2007

2008

2009

1994

58
100

Middle
shelf
Outer
shelf

56
54
60

49

58

Latitude (ºN)

56
54
60
58
56
54
60
58
56
54
166

170

166
170
Longitude (ºW)

170

166

170

166

100
80

Composition (%)

60

A: Outer-cold40

B: Outer-warm

20
0

C: Outer-Basin

100

D: Middle-cold

80

E: Middle-warm

60
F: Inner

40

C

C W C

Warm

2009

2008

2007

2006

2005

2004

2003

2001

2002

2000

1999

1998

1996

1997

1995

0

1994

20

Cold

Year
Fig. 5. (A) Spatial and temporal distribution of six copepod communities identiﬁed from Bray–Curtis dissimilarity analysis. Annual distribution of groups on the (B) Outer
shelf and (C) Middle shelf.

50

R. Ohashi et al. / Deep-Sea Research II 94 (2013) 44–56

the abundance peak due to the dominance of large-sized oceanic
copepods. Copepod biomass and abundance were both high incold years and low in warm years.
Throughout the study period, 24 calanoid copepod species
from 21 genera were identiﬁed (Table 1). Pseudocalanus spp. was
the most numerous, and Calanus spp. was dominated the copepod
biomass. Large-sized oceanic copepods that diapause at depth (i.e.,
E. bungii, Metridia paciﬁca, Neocalanus cristatus, Neocalanus ﬂemingeri and Neocalanus plumchrus) were collected on the Outer shelf,
on the Slope and in the Basin (Table 1).
Based on abundance of each species, cluster analysis divided
the copepod community into six groups (A–F). The groups contained 24–127 stations (Fig. 4A). From multiple-regression analysis, environmental factors that were signiﬁcantly related with thegroup separation were latitude, longitude, depth, sea surface
temperature, sea surface salinity and bottom salinity. The mostimportant factors were latitude and depth; they determined
70–77% of the variability of the copepod community (Fig. 4B). Mean
copepod abundance was highest in group D and lowest in group E(Fig. 4C). Species diversity was higher in groups A and C (H′¼ 1.6)
than in groups B, D, E and F (H′¼ 1.0–1.1). These group-speciﬁc
differences in species diversity were caused by their species
composition. For groups A–C, Pseudocalanus spp. and large, oceanic
Table 2
Variance analysis (two-way ANOVA) on year-to-year and station-to-station differences in abundance (inds. m−2) of dominant copepod taxa on Outer and Middle
shelf of the southeastern Bering Sea during summers of 1994–2009.
DomainSpecies

F-value df1, df2
Year15,30

Station2,30

Acartia spp.
Calanus spp.
Eucalanus bungii
Metridia paciﬁca
Neocalanus spp.
Pseudocalanus spp.

2.136*
1.259ns
1.402ns
2.060*
5.228***
1.190ns

1.215ns
3.027ns2.610ns
1.464ns
1.956ns0.194ns

Acartia spp.
Calanus spp.
Pseudocalanus spp.

6.574****
6.026****
5.791****

2.798ns3.745*
0.195ns

copepods (M. paciﬁca, E. bungii, Neocalanus spp.) were abundant(Fig. 4C). For groups D and E, species diversity was lower, and thespecies compositions were similar; they were comprised of Pseudocalanus spp. (55–58%), Acartia spp. (24%) and Calanus spp. (18–19%). In group F, the proportion of Calanus spp. decreased, and themain species were Pseudocalanus spp. (69%), and Acartia spp. (18%).
Endemic species, such as Epilabidocera amphitrites, Eurytemora
herdmani and Tortanus discaudatus, were also observed (Fig. 4C,
Table 1).
The regional and interannual distributions of each group wereclearly separated (Fig. 5A). Composition of group A was greater incold years (1995, 1997, 1999 and 2007–2009) on the Outer shelf,
and that of group B was greater in warm years (1998, 2001–2005)
on the Outer shelf, and group C was seen mainly on the Outer shelfand in the Basin, but also on the Middle shelf in 2006–2008(Fig. 5B). Group D was mainly observed in cold years on the Middle
shelf, group E was seen in warm years on the Middle shelf, andgroup F was centered on the Inner shelf (Fig. 5A).
Two-way analysis of variance (ANOVA) on annual and geographical differences in abundance of the dominant copepods showedsigniﬁcant interannual changes for Acartia spp., M. paciﬁca and
Neocalanus spp. on the Outer shelf (Table 2). Signiﬁcant station-tostation differences were detected only for Calanus spp. on the
Middle shelf. All dominant copepods on the Middle shelf (Acartia
spp., Calanus spp. and Pseudocalanus spp.) showed highly signiﬁcant interannual changes in abundance (p o0.0001, Table 2).
Correlation analysis was used to evaluate which environmental
parameters were related to the interannual changes in copepod
abundance. Abundances of the three dominant copepods on the
Middle shelf, which all showed high interannual variability, werestrongly negatively correlated with temperature and salinity (Table 3).

Outer shelf3.3. Chaetognaths
Two chaetognath species (P. elegans and Eukrohnia hamata) werecollected. P. elegans dominated the chaetognath fauna, composing
84% of the total chaetognath abundance and 89% of the chaetognathabundance on the Middle shelf. For this reason, E. hamata was notincluded in the subsequent analysis of chaetognaths.
P. elegans abundance ranged from 30 to 15,180 inds. m−2, andwas highest on the Middle shelf (Fig. 6A). Abundance was low
during 2000–2004 and high during 1996–1999 and 2005–2009. P.
elegans biomass varied from 11 to 1559 mg DM m−2 (Fig. 6B).
Biomass was low during 2002–2004 and high during 1996–1999
and 2005–2009. Differences in the timing of the abundance andMiddle shelfns: not signiﬁcant.
n

po 0.05.
p o 0.001.
nnnn
p o 0.0001.

nnn

Table 3
Correlation coefﬁcients (r) between abundance of dominant copepods and various environmental parameters in the southeastern Bering Sea during summers of 1994–2009.
DomainSpecies

Temperature (n¼91)

Salinity (n ¼91)

Chlorophyll a (n¼ 45)
Whole water column

Whole water column

Upper layer

Lower layer

Whole water column

Acartia spp.
Calanus spp.
Eucalanus bungii
Metridia paciﬁca
Neocalanus spp.
Pseudocalanus spp.

0.207n−0.423nnnn
0.138−0.231n−0.285nn−0.1590.149−0.101−0.143−0.258n−0.404nnn−0.1420.186−0.406nnn
0.307nn−0.105−0.108−0.044−0.140−0.294nn
0.517nnnn
0.076
0.252n−0.028

0.067
0.192
0.071
0.370n0.369n0.341nAcartia spp.
Calanus spp.
Pseudocalanus spp.

−0.410nnn−0.448nnnn−0.567nnnn−0.146−0.340nn−0.292nn−0.431nnnn−0.457nnnn−0.539nnnn−0.506nnnn−0.407nnn−0.484nnnn−0.111−0.126−0.037

Outer shelf

Middle shelfnp o 0.05.
p o0.01.
nnn
po 0.001.
nnnn
p o 0.0001.
nnR. Ohashi et al. / Deep-Sea Research II 94 (2013) 44–56

51

Fig. 6. Regional variations in Parasagitta elegans: (A) abundance and (B) biomass during summers of 1996–2009.

biomass peaks might have been caused by interannual changes in
P. elegans body-size composition.
In every year, P. elegans TL composition on the Middle shelf had
two or three cohorts (Fig. 7). The small-sized cohort was dominated by Stage I (juveniles), the middle-sized cohort by Stage II(immature), and the large-sized cohort by Stage III (mature)individuals. Stage III was not observed in 2003 or 2004 (Fig. 7).
The average TL of the small-sized cohort (Stage I) was signiﬁcantly
larger (3.5–8.5 mm) during 1996–2005 than those (2.5–5.5 mm)
during 2006–2009 (Fig. 7) (p o0.05, U-test).
P. elegans abundance on the Outer shelf was positively correlated with dominant copepod abundance (Acartia spp., Calanus

52

R. Ohashi et al. / Deep-Sea Research II 94 (2013) 44–56

20

20
1997

1996
15

n=8010

15

10

10

5

5

0
12

0
12

Stage II
Stage III

15

1998

Composition (%)

8

n=2310Stage I

n=6813

2000

1999
n=5111

8

10

4

4

5

0
12

0
25

0
15

2001
8

n=1658

n=800

15
10

4

2003

2002

20

n=932

10

n=560

5

5
0
20

0
40

0
20
2004

15

2006

2005
30

15
n=1776n=166

n=2444

10

10

20

5

5

10

0
12

0
30

0
20

2007
8

n=528

2008
20

2009
15
n=347

n=404
10

4

0

10

5
0

0
Total length (mm)Fig. 7. Annual patterns of Parasagitta elegans length frequency on Middle shelf during summers of 1996–2009. n: number of measured specimens.

spp. and Pseudocalanus spp.), but not with environmental factors(Table 4). On the Middle shelf, P. elegans had a highly signiﬁcant
positive correlation with dominant copepod abundance(p o0.0001) and signiﬁcant negative correlations with temperature and salinity. Thus on the Middle shelf, P. elegans abundance
was high when temperature and salinity were low, and low whentemperature and salinity were high, which is similar to the patternobserved in copepod abundance (Table 4).

4. Discussion
The copepod community on the Bering Sea shelf showed large
interannual differences across the shelf (Fig. 5A). The major
environmental factors that were related to the copepod

community were latitude and depth (Fig. 4B), and species diversity
was highest on the Outer shelf because of the occurrence of theoceanic copepods in addition to the shelf copepods (Fig. 4C). Theseﬁndings correspond well with the horizontal distribution of
copepod community structure reported by Cooney and Coyle(1982). These cross-shelf differences in copepod species may berelated to the occurrence of frontal structures (Coachman andCharnell, 1979; Coachman, 1986). The large number of oceanic
species on the Middle shelf in 1998 (Fig. 5C) may be caused by thetransportation of oceanic copepods by strong cross-shelf advection(Stabeno et al., 2001) (Fig. 1). Stabeno et al. (2012) also reported
the transport of oceanic species during warm years.
Long-term changes in zooplankton on the southeastern Bering
Sea shelf based upon wet-weight biomass have been reported(Sugimoto and Tadokoro, 1997, 1998; Napp et al., 2002). Recently,

R. Ohashi et al. / Deep-Sea Research II 94 (2013) 44–56

Table 4
Correlation coefﬁcients (r) between abundance of chaetognath Parasagitta elegans
and various parameters (water temperature, salinity and copepod abundance) on
the Outer shelf and Middle shelf in the southeastern Bering Sea during summers of
1996–2009.
Parameters
Temperature
Whole water column
Upper layer
Lower layer
Salinity
Whole water column
Copepods
Acartia spp.
Calanus spp.
Eucalanus bungii
Metridia paciﬁca
Neocalanus spp.
Pseudocalanus spp.

Outer shelf

Middle shelf−0.137−0.057−0.057−0.519nnnn−0.301nn−0.547nnnn−0.172−0.513nnnn

0.343nn
0.431nnnn
0.129
0.195
0.093
0.291nn

0.563nnnn
0.503nnnn–––
0.566nnnn–: not applicable.
nn

p o 0.01.
p o0.0001.

nnnn

Hunt et al. (2008) also reported that the zooplankton wet mass was
lower in the early 2000s than in the late 1990s. This corresponds with
the interannual changes in copepod abundance and biomass observedin the present study (Fig. 3). In the present study, the copepod
community greatly varied between cold years (1995, 1997, 1999
and 2007–2009) and warm years (1998, 2001–2005) on both theOuter and Middle shelves. In warm years, oceanic species decreasedon the Outer shelf, but showed no change on the Middle shelf, andthe abundance of all copepod species drastically decreased on both
the Outer and Middle shelf (Fig. 5). Thus, these ﬁndings clearly
indicate that both the wet mass and copepod community structure
showed interannual changes on the southeastern Bering Sea shelf(Fig. 8).
Physical and biological changes have occurred in the southeastern Bering Sea shelf over the last two decades (Fig. 8). During
the 1997 El Niño/Southern Oscillation (ENSO) event, there wereanomalous atmospheric conditions over the southeastern Bering
Sea shelf (Overland et al., 2001), a warm surface layer, a bloom of
the coccolithophorid E. huxleyi (Sukhanova and Flint, 1998) andmass mortality of short-tailed shearwaters (P. tenuirostris) (Baduini
et al., 2001). Short-tailed shearwaters prey on large zooplankton,
especially adult euphausiids (Hunt et al., 1996), and the starvationof shearwaters that occurred during the summer of 1997 may havebeen due to low densities of adult euphausiids (Stockwell et al.,2001) or difﬁculty in ﬁnding prey patches due to low watertransparency caused by the coccolithophore blooms (Lovvorn
et al., 2001). Thus, the mass mortality of short-tailed shearwaters
may not have been related with the pattern of mesozooplankton
abundance and biomass described in this study.
Coccolithophore (E. huxleyi) blooms in recent times were ﬁrst
observed in this region in September 1997 (Vance et al., 1998).
Large-scale coccolithophore blooms were also observed in June
1998 and 2000 (Sukhanova and Flint, 1998; Iida et al., 2002, 2008,2012). As an ecological consequence of coccolithophores, negative
effect for short-tailed shearwaters and their nutritional values for
copepods should be considered. Information in the literature
regarding ingestion of coccolithophores by copepods is contradictory. For example, Huskin et al. (2000) state that E. huxleyi is
difﬁcult to digest and has low nutritional value, it is not a preferredfood item for Calanus species. However, Nejstgaard et al. (1997)
reported that about 75% of the carbon consumed by Calanus
ﬁnmarchicus during an E. huxleyi bloom came from E. huxleyi(4 30  106 cells L−1), and high abundance of Calanus spp. was53

observed on the Inner shelf during a coccolithophore bloom (Coyleand Pinchuk, 2002). The latter observations suggest that coccolithophore production may have little effect on Calanus spp. In fact,
years of coccolithophore blooms (1997, 1998 and 2000) did notcorrespond with years of low copepod abundance or biomass(Fig. 8B). This discrepancy between coccolithophore blooms andcopepod abundance could be explained if coccolithophorids areingested by Calanus species (Nejstgaard et al., 1997) and havesome nutritional value. As the other possible cause, turbid watersof coccolithophore bloom may provide copepods refuge fromvisual predators (Lovvorn et al., 2001).
During the study period, there were cold (1995, 1997, 1999,
2007–2010), average (1996, 2000, 2006) and warm years (1998,
2001–2005) (Fig. 2A). During cold and warm years, the timing andmagnitude of the spring bloom differ (Stabeno et al., 2001; Huntet al., 2002, 2011). During cold years, the sea ice remains during
the severe winter storms, and ice-edge blooms occur. In warm
years, the sea ice melts before the spring storms, and strong wind
mixing delays the start of the bloom until stratiﬁcation occurs
when the thermocline develops. From long-term (1960–2005)
simulation modeling, Jin et al. (2009) reported that in cold years(PDOo −1), phytoplankton blooms start early, last long and arelarge, while in warm years (PDO 41), they occur later with shortpulses and are small. These differences in bloom timing between
cold and warm years have also been recorded in mooring observations in this region (Hunt et al., 2011).
Copepod abundance and biomass on both the Outer shelf andMiddle shelf were high during cold years (1995, 1997, 1999 and
2007–2009) and low during warm years except 1998 (2001–2005)(Fig. 3, Table 3). The dominant copepod, Calanus spp., has anextended spawning period; it starts well before the spring phytoplankton bloom (February) and ends in May; however the survival
rate of early developmental stages depends on whether theyencounter a phytoplankton bloom or not, and recruitment ofcopepodid stages increases if they encounter early ice associatedblooms, which are highly productive (Baier and Napp, 2003). Low
temperatures in cold years may also lead to greater abundance ofthe small copepods Pseudocalanus spp. and Acartia spp. especiallyin the Middle shelf (Table 3). Cold temperature may provide thelonger growing season and high primary productivity of ice-edge
blooms, sufﬁcient food condition for copepods, resulting inincreased abundance of both large and small copepods.
In this study, copepod abundance on both the Outer andMiddle shelf was negatively correlated with temperature(Table 3). In contrast, on the Inner shelf, positive correlations werereported between spring temperatures and the abundance of
three copepods (Calanus spp., Pseudocalanus spp. and Acartiaspp.), and between summer temperatures and two copepods(Pseudocalanus spp. and Acartia spp.) (Coyle and Pinchuk, 2002).
This suggests that the response of copepods to temperature mayvary between the Outer-Middle shelf (negative, this study), andthe Inner shelf (positive, Coyle and Pinchuk, 2002). In this study,
differences between cold and warm years on the Middle shelfwere observed in copepod abundance, but not in species composition (groups D and E in Fig. 4C). This is partly because both large
and small copepods were abundant in cold years and lessabundant in warm years (Table 3). Coyle et al. (2008) compared
the summer zooplankton community on the Middle shelf between
a cold (1999) and warm year (2004), and reported that thedominant species shifted from large species in the cold year tosmall species in the warm year. However, this phenomenon was
not observed during the 16 years of the present study. Our results
showed that both large- and small-sized copepods showed a clear
negative correlation with habitat temperature (Table 3).
Similar to copepods, the biomass of the jellyﬁsh C. melanaster ishigh in cold years and low in warm years (Brodeur et al., 2008).

54

R. Ohashi et al. / Deep-Sea Research II 94 (2013) 44–56

Reference
Large
bloom

Coccolithophores

1

Mass mortality of seabirds(short-tailed shearwaters)

2

Climate regime shift
Cold

3

Warm

High jellyfish biomass

Low jellyfish biomass

Peak

4

Warm temperature

Cold

5

4

80

60

2

40

1

20

0
10

0
1.6

Biomass (g DM m-2)

Biomass
3

8

6
0.8
4

No data

0.4
2

Biomass (g DM m-2)

1.2

No dataAbundance (x103 inds. m-2)

Abundance (x105 inds.m-2)

Abundance

0
2009

2008

2007

2006

2005

2004

2003

2002

2001

2000

1999

1998

1997

1996

1995

1994

0

Year
Fig. 8. (A) Annual changes in biological/environmental conditions, (B) copepod abundance and biomass and (C) chaetognath (Parasagitta elegans) abundance and biomass on
Middle shelf of the southeastern Bering Sea during summers of 1994–2009. Values are means and error bars indicate standard deviations. For references in (A), 1: Sukhanova
and Flint (1998), Iida et al. (2002,2008), 2: Baduini et al. (2001), 3: McFarlane et al. (2000), 4: Brodeur et al. (2008), Hunt et al. (2010), 5: Stabeno et al. (2012).

The increase in cold years may be due to improved feeding
conditions for polyps (mass sinking of phytoplankton after iceedge bloom), and subsequent abundant food (copepods) for
pelagic medusae may improve survival and growth (Brodeur
et al., 2008). In contrast, oceanic blooms in warm years are lessproductive and provide less food (sinking phytoplankton) for
polyps, as well as less food (copepods) for planktonic medusae,
resulting in low growth and survival of polyps and medusae.
Interannual changes in chaetognath abundance and biomass
were somewhat similar to the changes in copepods (Fig. 8).
This may be an example of bottom-up control on predatory

chaetognath abundance by prey (copepods) abundance. Chaetognaths in this region change their food items and size at maturity
between cold and warm years; in cold years, they prey on large
Calanus spp. and mature at large size, while in warm years, they
feed on small Pseudocalanus spp. and mature at small size (Baierand Terazaki, 2005). The TL of most mature (Stage III) individuals
in the present study was 4 20 mm in cold years (1997, 1999 and
2007–2009), and o 20 mm in warm years (1998, 2001, 2002 and2005), and no mature individuals were observed in the warm
years 2003 and 2004 (Fig. 7). These facts support the ﬁnding ofBaier and Terazaki (2005), who reported that sufﬁcient foodR. Ohashi et al. / Deep-Sea Research II 94 (2013) 44–56

conditions in cold years result in a large size at maturity, while
food limitation in warm years induces small size at maturity.
For the early life history stages of walleye pollock, an importantﬁsheries resource in this region, food conditions differ between cold
and warm years (Napp et al., 2000; Hunt et al., 2011). In cold years,
there may be a mismatch between the production of pollock larvae
and their prey (Napp et al., 2000), but an early start of the ice-edge
bloom and high abundance of lipid-rich prey for age-0 ﬁsh(copepods and euphausiids) results in high survival rates and low
cannibalism (Hunt et al., 2011). In warm years, the late start of the
open-water bloom results in a low abundance of lipid-rich prey forthe age-0 pollock and chaetognaths. Under this food-limited condition, growth and survival of walleye pollock juveniles decrease,and the proportion of cannibalism may increase. This results in adecrease in recruitment (Hunt et al., 2011, Heintz et al., 2013). Thus,
the timing and magnitude of primary production related withclimate change affects production through the entire food web
structure on the southeastern Bering Sea shelf.

Acknowledgments
We thank Dr. J.R. Bower of Hokkaido University for his comments on the manuscript. All samples and hydrographic data usedin this study were collected by the T/S Oshoro-Maru. We are gratefulto the captain and crew for their help. Some of the chaetognath data
were collected by Mr. N. Hagimoto. This study was supported by
Grant-in-Aid for Scientiﬁc Research (A) 24248032 and Grant-in-Aid
for Scientiﬁc Research on Innovative Areas 24110005 from the Japan
Society for the Promotion of Science (JSPS).
References
Aizawa, Y., Takiguchi, N., 1999. Consideration of the methods for estimating theage-composition from the length frequency data with MS-Excel. Bull. Jpn. Soc.
Fish. Oceanogr. 63, 205–214, in Japanese.
Baduini, C.L., Hyrenbach, K.D., Coyle, K.O., Pinchuk, A., Mendenhall, V., Hunt Jr., G.L.,
2001. Mass mortality of short-tailed shearwaters in the south-eastern Bering
Sea during summer 1997. Fish. Oceanogr. 10, 117–130.
Baier, C.T., Napp, J.M., 2003. Climate-induced variability in Calanus marshallae
populations. J. Plankton Res. 25, 771–782.
Baier, C.T., Terazaki, M., 2005. Interannual variability in a predator-prey interaction:
climate, chaetognaths and copepods in the southeastern Bering Sea. J. Plankton
Res. 27, 1113–1125.
Båmstedt, U., 1986. Chemical composition and energy content. In: Corner, E.D.S.,
O’Hara, S.C.M. (Eds.), The Biological Chemistry of Marine Copepods. Clarendon
Press, Oxford, pp. 1–58.
Bray, J.R., Curtis, J.T., 1957. An ordination of the upland forest communities ofsouthern Wisconsin. Ecol. Monogr. 27, 325–349.
Brodeur, R.D., Decker, M.B., Ciannelli, L., Purcell, J.E., Bond, N.A., Stabeno, P.J., Acuna,E., Hunt Jr., G.L., 2008. Rise and fall of jellyﬁsh in the eastern Bering Sea in
relation to climate regime shifts. Prog. Oceanogr. 77, 103–111.
Brodeur, R.D., Terazaki, M., 1999. Springtime abundance of chaetognaths in the
shelf region of the northern Gulf of Alaska, with observations on the vertical
distribution and feeding of Sagitta elegans. Fish. Oceanogr. 8, 93–103.
Brodeur, R.D., Wilson, M.T., 1996. A review of the distribution, ecology andpopulation dynamics of age-0 walleye pollock in the Gulf of Alaska. Fish.
Oceanogr. 5, 148–166.
Coachman, L.K., 1986. Circulation, water masses, and ﬂuxes on the southeastern
Bering Sea shelf. Cont. Shelf Res. 5, 23–108.
Coachman, L.K., Charnell, R.L., 1979. On lateral water mass interaction—a case study,
Bristol Bay, Alaska. J. Phys. Oceanogr. 6, 278–297.
Cooney, R.T., Coyle, K.O., 1982. Trophic implications of cross-shelf copepod
distributions in the southeastern Bering Sea. Mar. Biol. 70, 187–196.
Coyle, K.O., Pinchuk, A.I., 2002. Climate-related differences in zooplankton density
and growth on the inner shelf of the southeastern Bering Sea. Prog. Oceanogr.
55, 177–194.
Coyle, K.O., Pinchuk, A.I., Eisner, L.B., Napp, J.M., 2008. Zooplankton species
composition, abundance and biomass on the eastern Bering Sea shelf during
summer: the potential role of water-column stability and nutrients in structuring the zooplankton community. Deep-Sea Res. II 55, 1775–1791.
Hunt Jr., G.L., Allen, B.M., Angliss, R.P., Baker, T., Bond, N., Buck, G., Byrd, G.V., Coyle,
K.O., Devol, A., Eggers, D.M., Eisner, L., Feely, R., Fitzgerald, S., Fritz, L.W., Gritsay,
E.V., Ladd, C., Lewis, W., Mathis, J., Mordy, C.W., Mueter, F., Napp, J., Sherr, E.,
Shull, D., Stabeno, P., Stepanenko, M.A., Strom, S., Whitledge, T.E., 2010.
Status and trends of the Bering Sea region, 2003–2008. In: McKinnell, S.M.,

55

Dagg, M.J. (Eds.), Marine Ecosystems of the North Paciﬁc Ocean, 2003–2008, 4.
PICES Special Publication, pp. 196–267.
Hunt Jr., G.L., Coyle, K.O., Eisner, L.B., Farley, E.V., Heintz, R.A., Mueter, F., Napp, J.F.,
Overland, J.E., Ressler, P.H., Salo, S., Stabeno, P.J., 2011. Climate impacts oneastern Bering Sea food webs: a synthesis of new data and an assessment of theOscillating Control Hypothesis. ICES J. Mar. Sci. 68, 1230–1243.
Hunt Jr., G.L., Coyle, K.O., Hoffman, S., Decker, M.B., Flint, E.N., 1996. Foraging
ecology of short-tailed shearwaters near the Pribilof Islands, Bering Sea. Mar.
Ecol. Prog. Ser. 141, 1–11.
Hunt Jr., G.L., Stabeno, P.J., Strom, S., Napp, J.M., 2008. Patterns of spatial andtemporal variation in the marine ecosystem of the southeastern Bering Sea,
with special reference to the Pribilof Domain. Deep-Sea Res. II 55, 1919–1944.
Hunt Jr., G.L., Stabeno, P., Walters, G., Sinclair, E., Brodeur, R.D., Napp, J.M., Bond, N.
A., 2002. Climate changes and control of the southeastern Bering Sea pelagic
ecosystem. Deep-Sea Res. II 49, 5821–5853.
Huskin, I., Anadón, R., Álvarez-Marqués, F., Harris, R.P., 2000. Ingestion, fecal pellet
and egg production rates of Calanus helgolandicus feeding coccolithophorid
versus non-coccolithophorid diets. J. Exp. Mar. Biol. Ecol. 248, 239–254.
Iida, T., Mizobata, K., Saitoh, S.I., 2008. Temporal and spatial variability ofphytoplankton in the Bering Sea—from diatom bloom in spring to coccolithophore bloom in summer and fall. Kaiyo Mon. Extra 50, 127–137. (in Japanese).
Iida, T., Mizobata, K., Saitoh, S.-I., 2012. Interannual variability of coccolithophore
Emiliania huxleyi blooms in response to changes in water column stability inthe eastern Bering Sea. Cont. Shelf Res. 34, 7–17.
Iida, T., Saitoh, S.-I., Miyamura, T., Toratani, M., Fukushima, H., Shiga, N., 2002.
Temporal and spatial variability of coccolithophore blooms in the eastern
Bering Sea, 1998–2001. Prog. Oceanogr. 55, 165–177.
Imao, F., 2005. Zooplankton Community Structure and Their Functional Role in
Carbon Cycle in the Oyashio Region, Western Subarctic Paciﬁc. Master Thesis,
Hokkaido University, 42 pp.
Jin, M., Deal, C., Wang, J., McRoy, C.P., 2009. Response of lower trophic levelproduction to long-term climate change in the southeastern Bering Sea. J.
Geophys. Res. 114, C04010, http://dx.doi.org/10.1029/2008JC005105.
Kang, Y., Kim, S., Lee, W., 2006. Seasonal and spatial variations of zooplankton in thecentral and southeastern Bering Sea during the mid-1990s. Deep-Sea Res. I 53,
795–803.
Lovvorn, J.R., Baduini, C.L., Hunt Jr., G.L., 2001. Modeling underwater visual andﬁlter feeding by planktivorous shearwaters in unusual sea conditions. Ecology
82, 2342–2356.
McFarlane, G.A., King, J.R., Beamish, R.J., 2000. Have there been recent changes inclimate? Ask the ﬁsh. Prog. Oceanogr. 47, 147–169.
McLaren, I.A., 1969. Population and production ecology of zooplankton in Ogac
Lake, a landlocked Fjord on Bafﬁn Island. J. Fish. Res. Bd. Canada 26, 1485–1559.
Miller, C.B., Frost, B.W., Batchelder, H.P., Clemons, M.J., Conway, R.E., 1984. Life
histories of large, grazing copepods in a Subarctic Ocean Gyre: Neocalanus
plumchrus, Neocalanus cristatus, and Eucalanus bungii in the Northeast Paciﬁc.
Prog. Oceanogr. 13, 201–243.
Motoda, S., 1957. North Paciﬁc standard plankton net. Inf. Bull. Planktol. Jpn. 4,
13–15.
Motoda, S., 1959. Devices of simple plankton apparatus. Mem. Fac. Fish. Hokkaido
Univ. 7, 73–94.
Mumm, N., 1991. On the summer distribution of mesozooplankton in the Nansen
Basin, Arctic Ocean. Rep. Polar Res. 92, 1–146.
Napp, J.M., Baier, C.T., Brodeur, R.D., Coyle, K.O., Shiga, N., Mier, K., 2002.
Interannual and decadal variability in zooplankton communities of the southeast Bering Sea shelf. Deep-Sea Res. II 49, 5991–6008.
Napp, J.M., Hunt, G.L., 2001. Anomalous conditions in the south-eastern Bering Sea 1997:
linkage among climate, weather, ocean, and biology. Fish. Oceanogr. 10, 61–68.
Napp, J.M., Kendall Jr., A.W., Schumacher, J.D., 2000. A synthesis of biological andphysical processes affecting the feeding environment of larval walleye pollock(Theragra chalcogramma) in the eastern Bering Sea. Fish. Oceanogr. 9, 147–162.
Nejstgaard, J.C., Gismervik, I., Solberg, P.T., 1997. Feeding and reproduction by Calanus
ﬁnmarchicus, and microzooplankton grazing during mesocosm blooms of diatoms
and the coccolithophore Emiliania huxleyi. Mar. Ecol. Prog. Ser. 147, 197–217.
Nelson, R.J., Carmack, E.C., McLaughlin, F.A., Cooper, G.A., 2009. Penetration of
Paciﬁc zooplankton into the western Arctic Ocean tracked with molecular
population genetics. Mar. Ecol. Prog. Ser. 381, 129–138.
Overland, J.E., Bond, N.A., Adams, J.M., 2001. North Paciﬁc atmospheric and SST
anomalies in 1997: links to ENSO? Fish. Oceanogr. 10, 69–80.
Sameoto, D.D., 1973. Annual life cycle and production of the chaetognath Sagitta
elegans in Bedford Basin, Nova Scotia. J. Fish. Res. Bd. Canada 30, 333–344.
Shannon, C.E., Weaver, W., 1949. The Mathematical Theory of Communication. The
University of Illinois Press, Urbana.
Smith, S.L., Vidal, J., 1986. Variations in the distribution, abundance, and development of copepods in the southeastern Bering Sea in 1980 and 1981. Cont. Shelf
Res. 5, 215–239.
Springer, A.M., 1992. A review: Walleye pollock in the North Paciﬁc—how muchdifference do they really make? Fish. Oceanogr. 1, 80–96.
Springer, A.M., McRoy, C.P., Flint, M.V., 1996. The Bering Sea Green Belt: shelf-edge
processes and ecosystem production. Fish. Oceanogr. 5, 205–223.
Stabeno, P.J., Bond, N.A., Kachel, N.B., Salo, S.A., Schumacher, J.D., 2001. On thetemporal variability of the physical environment over the south-eastern Bering
Sea. Fish. Oceanogr. 10, 81–98.
Stabeno, P.J., Napp, J., Mordy, C., Whitledge, T., 2010. Factors inﬂuencing physicalstructure and lower trophic levels of the eastern Bering Sea shelf in 2005: ice,tides and winds. Prog. Oceanogr. 85, 180–196.

56

R. Ohashi et al. / Deep-Sea Research II 94 (2013) 44–56

Stabeno, P.J., Kachel, N.B., Moore, S.E., Napp, J.M., Sigler, M., Yamaguchi, A., Zerbini,
A.N., 2012. Comparison of warm and cold years on the southeastern Bering Sea
shelf and some implications for the ecosystem. Deep-Sea Res. II 65-70, 31–45.
Stockwell, D.A., Whitledge, T.E., Zeeman, S.I., Coyle, K.O., Napp, J.M., Brodeur, R.D.,
Pinchuk, A.I., Hunt Jr., G.L., 2001. Anomalous conditions in the south-eastern
Bering Sea, 1997: nutrients, phytoplankton and zooplankton. Fish. Oceanogr. 10,
99–116.
Sugimoto, T., Tadokoro, K., 1997. Interannual–interdecadal variations in zooplankton biomass, chlorophyll concentration and physical environment in thesubarctic Paciﬁc and Bering Sea. Fish. Oceanogr. 6, 74–93.

Sugimoto, T., Tadokoro, K., 1998. Interdecadal variations of plankton biomass andphysical environment in the North Paciﬁc. Fish. Oceanogr. 7, 289–299.
Sukhanova, I.N., Flint, M.V., 1998. Anomalous blooming of coccolithophorids overthe eastern Bering Sea self. Oceanology 38, 502–505.
Vance, T.C., Schumacher, J.D., Stabeno, P.J., Baier, C.T., Wyllie-Echeverria, T., Tynan,
C.T., Brodeur, R.D., Napp, J.M., Coyle, K.O., Decker, M.B., Hunt Jr., G.L., Stockwell,D., Whitledge, T.E., Jump, M., Zeeman, S., 1998. Aquamarine waters recorded forﬁrst time in Eastern Bering Sea. Eos Trans. Am. Geophys. Union 79, 121–126.
Zo, Z., 1973. Breeding and growth of the chaetognath Sagitta elegans in Bedford
Basin. Limnol. Oceanogr. 18, 750–756.