Article

Vertical Distribution, Community and Population Structures of
the Planktonic Chaetognatha in the Western Subarctic Pacific:
Insights on the Eukrohnia Species Group
Yuya Nakamura 1 , Haochen Zhang 1 and Atsushi Yamaguchi 1,2, *1
2*

Citation: Nakamura, Y.; Zhang, H.;
Yamaguchi, A. Vertical Distribution,
Community and Population
Structures of the Planktonic
Chaetognatha in the Western
Subarctic Pacific: Insights on the
Eukrohnia Species Group. Oceans
2023, 4, 253–268. https://doi.org/
10.3390/oceans4030018
Academic Editors: Antonio Bode andSam Dupont
Received: 26 April 2023
Revised: 12 July 2023
Accepted: 20 July 2023

Graduate School of Fisheries Sciences, Hokkaido University, 3-1-1 Minato-cho, Hakodate 041-8611, Japan
Arctic Research Center, Hokkaido University, Kita-21 Nishi-11 Kita-ku, Sapporo 001-0021, Japan
Correspondence: a-yama@fish.hokudai.ac.jp

Abstract: In the oceans, Chaetognatha can contribute significantly to the total zooplankton biomass(up to 10–30%). The genus Eukrohnia, the dominant Chaetognath genus in the western subarctic Pacific,
includes E. hamata and E. bathypelagica. Although it has been pointed out that there is no genetic
difference between the two species, no study has been made that treats them as the same species group.
In this study, we investigated vertical distribution based on the eight vertical stratification samplings
down to 1000 m depths conducted day/night at four seasons covering one year, community structure,and population structure of the three dominant Chaetognath species: Parasagitta elegans, E. hamata,and E. bathypelagica in the western subarctic Pacific. The population densities of each species at
0–1000 m water column were 0.04–0.36 ind. m−3 for P. elegans, 0.14–1.60 ind. m−3 for E. hamata,0.24–1.54 ind. m−3 for E. bathypelagica, and 1.37–2.62 ind. m−3 for Eukrohnia juveniles. The vertical
distributions were consistent both day and night, and no diel changes were observed for all species
throughout the seasons. The vertical distribution of Chaetognaths evaluated by the distribution
center was 61–169 m for P. elegans, 143–206 m for Eukrohnia juveniles, 134–279 m for E. hamata, and
253–612 m for E. bathypelagica. The body length of P. elegans ranged from 4 to 34 mm, and one tothree cohorts were identified at each sampling occasion. While the presence of the eight stages has
been reported for Eukrohnia, only one to five stages occurred, and specimens belonging to six toeight stages were not observed in the samples throughout the year. The body length of the whole
Eukrohnia species ranged from 2 to 14 mm. The body length histograms of the Eukrohnia species
group, including E. hamata and E. bathypelagica, and their juveniles showed the presence of two to fourcohorts at each sampling date. Within the Eukrohnia species group, vertical changes in body length
were present, which were characterized by the smaller specimens occurring at shallower depths,
followed by an increase in body length with increasing depths. From the vertical distribution andpopulation structure of the Eukrohnia species group (Eukrohnia juvenile + E. hamata + E. bathypelagica)in this study, there was no difficulty in treating them as one species. It may suggest that E. hamata
and E. bathypelagica in the western subarctic Pacific could be treated as one species group. To clarify
this point, a detailed genetic analysis of the Eukrohnia species group will be needed for future studies.
Keywords: vertical distribution; population structure; Chaetognatha; Eukrohnia species group

Published: 31 July 2023

1. Introduction
Copyright: © 2023 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms andconditions of the Creative Commons
Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

Chaetognatha is a marine phylum that has a wide distribution from the sea surface tothe bottom of the worldwide oceans. In the oceans, Chaetognatha can contribute significantly to the total zooplankton biomass (up to 10–30%) [1]. Chaetognatha is carnivorousand preys on mainly small-sized copepods [2–4]. On the other hand, Chaetognatha is eaten
by various fish: salmon [5], walleye pollock [6], and mesopelagic myctophids [7]. Thus,
Chaetognatha plays an important role in transporting copepod secondary production tohigher trophic-level organisms [8].

Oceans 2023, 4, 253–268. https://doi.org/10.3390/oceans4030018

https://www.mdpi.com/journal/oceans

Oceans 2023, 4

254

The life history of the pelagic Chaetognatha has been reported from various areas,
including the North Atlantic [9–11], the Arctic Ocean [12,13], and the North Pacific [14–16].
On the other hand, the mtDNA COI analysis of the genus Eukrohnia, which has a worldwide
distribution, shows that there is no genetic difference between E. hamata and E. bathypelagicaof the same region, and E. bathypelagica is suggested to be a post-spawning individualof E. hamata [17]. From this point of view, it has been pointed out that it is necessary to
re-analyze the life history of Chaetognatha, including the existence of cryptic species [18].
In the western subarctic Pacific, St. K2 has been set up as a long-term time-series
observation station, and various biogeochemical studies, including plankton, have been
conducted [19]. At St. K2, Chaetognatha has been reported to dominate in the 50–200 m
depth range, accounting for 14–36% of total zooplankton biomass [20]. The dominanceof Chaetognatha in zooplankton biomass at the mesopelagic layer of St. K2 has also beenreported [21]. Regarding the vertical distribution of Chaetognatha at St. K2, they showedbimodal vertical distribution showing peaks at 0–50 m and 150–300 m, and few individuals
distributed for 50–150 m depth both day and night [22]. Based on the sediment trap mooredat 150 m of St. K2 collected at two-day intervals from June to July, P. elegans was collected
as a zooplankton swimmer, and the body length of P. elegans showed a uni-modal cohort
with peaks at 29.2–31.9 mm, showing the significant growth rate at 0.21 mm day−1 [23].
Although these findings are important, population structure has been observed only at
certain depths and for a limited season. Thus, knowledge of the life cycle of Chaetognatha
at St. K2 is scarce.
An oblique tow of a Bongo net from 0 to 200 m was conducted in the Oyashio region
at 2–5 day intervals from March to April [24]. Data acquired revealed that E. hamata andP. elegans composed 95% of the Chaetognath abundance and showed three peaks in bodylength [24]. The growth rates of E. hamata and P. elegans were 0.039–0.050 mm day−1 and
0.042–0.101 mm day−1 , respectively [24]. For vertical distribution based on the verticalstratification samplings down to 5000 m, the distribution centers of P. elegans, E. hamata, andE. bathypelagica were at 26–187 m, 169–308 m, and 583–728 m, respectively; thus, distribution
depth varied for the species [25]. For the life cycle of Chaetognatha, it has been reported
that the generation time of P. elegans is one or two years based on the time-series samples
collected from 150 m off Kushiro for four years [16]. In addition, based on the time series
sampling by Bongo net from 0 to 1000 m depth in the Oyashio region at 2 to 3 monthintervals, the recruitment of E. hamata juveniles occurs in spring and summer, and their
growth rates show seasonality: fast in summer and autumn, slow in winter and spring, andhaving two-year generation lengths [18]. While these findings are important, as mentioned
above, there is a possibility that E. hamata and E. bathypelagica are the same species within
the Eukrohnia species [17,26]. These facts suggest that an analysis that treats both species as
the same species group is needed, but such a study has not been conducted yet.
This study conducted day/night vertical distribution, seasonal changes in bodylength, and population structure studies of three dominant Chaetognath species (P. elegans, E. hamata, and E. bathypelagica) at St. K2 in the western subarctic Pacific based on
day/night vertical stratification samples down to 1000 m at four seasons covering one
year. For two Eukrohnia species considered to be the same species [17,26], the hypotheticalspecies group “Eukrohnia species group”, including Eukrohnia juvenile, E. hamata, andE. bathypelagica, was set. Then the body length, developmental stage composition, andvertical distribution of the Eukrohnia species group were analyzed. Through such analyses,
the consistency of the treatment of both species as the same species was considered froman ecological perspective.
2. Materials and Methods
2.1. Field Sampling
Day/night vertical stratified oblique tow of Intelligent Operative Net Sampling System(IONESS, SEA, Co. Ltd., Chiba, Japan) equipped 335 µm with 1.5 m2 mouth area wasmade from eight layers (0–50, 50–100, 100–150, 150–200, 200–300, 300–500, 500–750, and2. Materials and Methods
2.1. Field Sampling
Oceans 2023, 4

255
Day/night vertical stratified oblique tow of Intelligent Operative Net Sampling Sys2
tem (IONESS, SEA, Co. Ltd., Chiba, Japan) equipped 335 μm with 1.5 m mouth area wasmade from eight layers (0–50, 50–100, 100–150, 150–200, 200–300, 300–500, 500–750, and
750–1000
750–1000m)m)atatSt.
St.K2
K2(47°(47◦N,
N,160°
160◦E,E,Figure
Figure1,1,Table
Table1)
1)during
duringfour
fouroccasions:occasions:29
29October
October
2010,
26
February,
22–23
April,
and
3–4
July
2011.
The
filteringvolumeofeachsample2010, 26 February, 22–23 April, and 3–4 July 2011. The filtering volume of each sample
was
wasmonitored
a flowmeter.
Samplespreservedby(v/v)
4% (v/v)
borax-bufferedformonitored
by abyflowmeter.
Samples
werewerepreserved
by 4%
borax-bufferedformalin.
malin.
Temperature,salinity,
dissolved
oxygenand fluorescencemeasuredbyTemperature,salinity,
dissolved
oxygen(DO),(DO),and fluorescencewereweremeasuredby CTD
CTD
911plus;Sea-Bird
Scientific)
each samplingoccasion.
the zooplankton(SBE (SBE
911plus;Sea-Bird
Scientific)
at eachatsamplingoccasion.
For the For
zooplankton
samplessamplesin thisdata
study,
on the abundanceand biomassof zooplankton
taxa
have
used in used
this study,
on data
the abundanceand biomassof zooplankton
taxa havealready
already
been
published
[20].
In
this
study,
dataontheabundanceof
copepods,
thepribeen published [20]. In this study, data on the abundance of copepods, the primary preyofmary
prey of Chaetognatha,
Chaetognatha,
were quoted werefrom quoted[20]. from [20].

60°
N

55°
N

ESC
50°
N

K2
SAF

45°
N

OY

40°
N

SAB
KBF

35°
N

KE
30°
N
140°
E

150°
E

160°
E

170°
E

180 °

Figure 1.
1. Location
station(K2)(K2)
in thesubarctic
Pacific gyre.
ArrowsFigureLocation ofofthe
thesampling
sampling
stationinwestern
the western
subarctic
Pacific
gyre. represent
Arrowstheapproximate
positionsanddirectionsofthecurrents.
EKC:
East
Kamchatka
Current,
OY:Current,
Oyashio,
represent the approximate positions and directions of the currents. EKC: East Kamchatka
KE:
Kuroshio
Extension,
TC:
Tsushima
Warm
Current,
SAF:
Subarctic
Front,SAB:
Subarctic
Boundary,OY: Oyashio, KE: Kuroshio Extension, TC: Tsushima Warm Current, SAF: Subarctic Front, SAB:
KBF: Kuroshio
Bifurcation
Front, OSMW:
OkhotskSea OSMW:
Mode Water,
DSW:
Dense
Shelf
Water,
andSubarctic
Boundary,
KBF: Kuroshio
Bifurcation
Front,
Okhotsk
Sea
Mode
Water,
DSW:
Dense
Shelf
Water,SeaandModeOSMW:
Okhotsk Sea Mode Water.
OSMW:
Okhotsk
Water.

Table
Table 1.
1. Sampling
Samplingdata
dataofofthe
thesamples
samplesusedusedininthe
thepresent
presentstudy
studycollectedcollectedatatSt.
St.K2
K2ininthe
thewestern
westernsubarctic
Pacific
gyre
fromOctober
2010
to
July
2021.
All
the
sampleswerecollected
fromsubarctic Pacific gyre from October 2010 to July 2021. All the samples were collected fromeight
eight
discrete depths between 0 and 1000 m by oblique tow of IONESS.
discrete depths between 0 and 1000 m by oblique tow of IONESS.

Sampling Date
Sampling Date
29 Oct. 2010
29 October 2010
29 Oct. 2010
29 October 2010
26February
Feb. 201126
2011
26February
Feb. 201126
2011
22Apr.
April20112011
22
22Apr.
April2011201122
3 July 2011
33–4
July
2011
July
2011
3–4 July 2011

Local Time (Day/Night)
Local Time (Day/Night)
12:09–13:52 (D)
12:09–13:52 (D)22:09–23:38(N)
22:09–23:38 (N)
12:35–14:41
12:35–14:41 (D)(D)
22:01–23:44
22:01–23:44 (N)(N)
21:59–23:56 (N)(N)
21:59–23:56
12:45–14:37(D)
12:45–14:37 (D)
12:05–13:55 (D)
12:05–13:55(D)
22:51–0:55 (N)22:51–0:55 (N)2.2. Abundance, Body Size, and Biomass
In the land laboratory, sorting of Chaetognatha was made on the sub-samples at a division rate of 1/2–1/64, which varied with the number of samples. Under a stereomicroscope,
species identification and enumeration were made. Body length was measured with a precision of 0.1 mm using vernier calipers. For each individual, the developmental condition

Oceans 2023, 4

256

of the gonads was observed. Based on gonad development, P. elegans is classified into threedevelopmental stages: stages 1, 2, and 3 [23]. Stage 1 is an individual without ovaries; stage
2 is an individual with a developing egg but no mature egg; and stage 3 is an individualwith a mature egg [23]. Eukrohnia were classified into stages I to VIII using the criteriaof [27]. The Chaetognatha were sorted by species and placed on a pre-weighed 100 µm
mesh, removed water, and measured wet weight (WW) with a precision of 0.01 mg using
an electronic balance (Mettler Toledo AT261). Calculation of the abundance and biomass
data from per cubic meter (m−3 ) to per square meter (m−2 ) was made by multiplying the
towed depth (m) with the value per cubic meter.
2.3. Vertical Distribution
The vertical distribution of the three dominant species (P. elegans, E. hamata, andE. bathypelagica) and Eukrohnia juvenile was analyzed with day/night for the four seasons.
The vertical distribution core (D50% ), where 50% of the population was distributed, wascalculated based on abundances (ind. m−2 ) in each sampling layer [28]:
D50% = d1 + d2 ×

50 − p1p2

where d1 is the depth (m) of the upper depth of the 50% individual occurrence layer, d2 is the
maximum depth (m) of the 50% individual occurrence layer, p1 is the cumulative individual
percentage (%) that occurred at depths shallower than the 50% individual occurrence layer,
and p2 is the individual percentage (%) at the 50% individual occurrence layer.
2.4. Population Structure (Cohort Analyses)
Population structure analyses were made for the three dominant species: P. elegans,
E. hamata, and E. bathypelagica, and one combined species group: the Eukrohnia species group(E. hamata + E. bathypelagica). Thus, we treated four taxonomic categories in this study.
Based on the total number of the water column (ind. m−2 ) at 0–1000 m, histograms on bodylength were made, and cohort analyses were performed using the aid of the MSExcel solver
function [29]. In addition, depth distribution composition was also calculated for each bodylength at a 1 mm interval. The number of Eukrohnia juveniles was estimated by multiplying
the composition of E. hamata and E. bathypelagica species that occurred in the same sample.
In addition, since E. hamata and E. bathypelagica are genetically identical [17,26], one species
group, the Eukrohnia species group (Eukrohnia juveniles + E. hamata + E. bathypelagica),
was also set, and their body length histogram and distribution depth composition wereanalyzed.
3. Results
3.1. Hydrography
Vertical changes in temperature, salinity, dissolved oxygen, and copepod abundance
during day and night in four seasons are shown in Figure 2. Temperatures ranged from
1.2 to 8.5 ◦ C in October, 1.8 to 3.6 ◦ C in February, 1.4 to 3.7 ◦ C in April, and 1.5 to 6.5 ◦ C in
July. The near-surface layer was warmer in October and July and cooler in February and
April. For all seasons, the temperature decreased to 100 m, had a minimum, then increased
to 200 m with the subsurface small maximum, and decreased below 200 m. Salinity ranged
from 32.6–34.4 in October, 32.9–34.4 in February, 33.0–34.4 in April, and 32.8–34.4 in June.
Salinity was low near the surface, especially in October, then gradually increased withincreasing depth for all seasons. Dissolved oxygen was at 0.3–7.4 mL L−1 in October, 0.3–7.4
mL L−1 in February, 0.3–7.5 mL L−1 in April, and 0.3–7.5 mL L−1 in July. For all seasons,dissolved oxygen showed high values near the surface layer and decreased rapidly withincreasing depth to 200 m, then stabilized around <1.4 mL L−1 below 200 m depths. The
abundance of copepods was 14–732 ind. m−3 in October, 10–145 ind. m−3 in February,
8–174 ind. m−3 in April, and 5–190 ind. m−3 in June. The copepod abundance was high near
the surface layer, especially in October. Common for all seasons, copepod abundance had aOceans 2023, 4

7.4 mL L−1 in February, 0.3–7.5 mL L−1 in April, and 0.3–7.5 mL L−1 in July. For all seasons,dissolved oxygen showed high values near the surface layer and decreased rapidly withincreasing depth to 200 m, then stabilized around <1.4 mL L−1 below 200 m depths. The
abundance of copepods was 14–732 ind. m−3 in October, 10–145 ind. m−3 in February, 8– 257
174 ind. m−3 in April, and 5–190 ind. m−3 in June. The copepod abundance was high near
the surface layer, especially in October. Common for all seasons, copepod abundance hada minimumat 150–200m,m,formeda smallmaximum
below,
thendecreasedwithincreasminimumat 150–200
formeda smallmaximum
below,
thendecreasedwithincreasing
ing depth.
There
were
few
changes
incopepodabundanceandvertical
distribution
bedepth. There were few changes in copepod abundance and vertical distribution between
tween
day
and
night.
day and night.

Figure2. Vertical
distributionof temperature,salinity,
dissolved
oxygenand copepod
Figure2. Vertical
distributionof temperature,salinity,
dissolved
oxygen(DO),(DO),and copepod
abun-abunand night)
at St.K2
the western
subarctic
Pacific
gyre from
October
to2011.
July 2011.
dancedance(day (dayand night)
at St.K2
in theinwestern
subarctic
Pacific
gyre from
October2010 2010
to July
NoteNotethat scalesofcopepodabundance
are
in
log
scales.
that scales of copepod abundance are in log scales.

3.2. Abundance and Biomass of Chaetognaths
In this study, Chaetognatha belonging to two genera and three species were identified (Table 2). Abundances of Chaetognaths at the water column (0–1000 m) were0.04–0.36 ind. m−3 for P. elegans, 0.14–1.60 ind. m−3 for E. hamata, 0.24–1.54 ind. m−3
in E. bathypelagica, and Eukrohnia juveniles were 1.37–2.62 ind. m−3 . Eukrohnia juveniles
accounted for nearly half of the total Chaetognath abundance. The next dominant species
were E. hamata and E. bathypelagica. Both species accounted for about 20% of the total
Chaetognath abundance. The abundance of P. elegans was around 5% of the population.
Table 2. Annual mean abundance and biomass at 0–1000 m water column at St. K2 in the western
subarctic Pacific gyre during October 2010 to July 2021.
Species
Parasagitta elegans
Eukrohnia hamata
Eukrohnia bathypelagica
Eukrohnia juvenile
OthersAbundance(ind. m−3 )0.20 ± 0.03
(0.04–0.36)
0.80 ± 0.17
(0.14–1.60)
0.87 ± 0.13
(0.24–1.54)
1.88 ± 0.15
(1.37–2.62)
0.001 ± 0
(0–0.001)

Biomass
(%)
5.3
21.3
23.2
50.2
0.03

(mg WW m−3 )13.29 ± 2.39
(4.89–26.16)
5.09 ± 1.41
(1.00–10.55)
12.76 ± 2.67
(3.45–25.32)
1.84 ± 0.39
(0.37–3.63)
0.24 ± 0.04
(0.15–0.42)

(%)
40.0
15.3
38.4
5.5
0.7

Oceans 2023, 4

258

Biomasses at 0 to 1000 m water column were 4.89–26.16 mg WW m−3 for P. elegans,
1.00–10.55 mg WW m−3 for E. hamata, juveniles 3.45–25.32 mg WW m−3 for E. bathypelagica,
Oceans 2023, 4, FOR PEER REVIEW and 0.37–3.63 mg WW m−3 for Eukrohnia juveniles (Table 2). Regarding species 7composition,
Eukrohnia juvenile, which had a high composition in abundance, had a low compositionof 5.5% in biomass due to the smaller body size. On the other hand, the numerical minor
P. elegans had the highest composition of biomass, accounting for 40% of total ChaetognathParasagitta elegans
100
104
169
71
62
77
69
biomassdue
to its large
body124size.
Vertical279
Distribution
Three DominantSpecies
Eukrohnia hamata 3.3.250
223 of the 253
172 Chaetognath
222
140

134

The day/night vertical distribution of Chaetognath species (P. elegans, E. hamata,
Eukrohnia bathypelagicaE. 453
612 and427
477
356 is shown
253 in Figure
273 3. The verticalbathypelagica,
Eukrohnia
juvenile) 274
at each season

distribution of Chaetognaths was consistent with day and night for all species, and no
and night
were
for any species
0.05, Kolmogorov–
Eukrohnia juvenile day
199
206 differences
187
196detected175
177 or season
143 (p > 161
Smirnov test) (Table 3).
(a) Parasagitta elegans
5 4 3 2 1 0 1 2 3 4 50Abundance (ind. m-3)
5 4 3 2 1 0 1 2 3 4 5

5 4 3 2 1 0 1 2 3 4 5

5 4 3 2 1 0 1 2 3 4 5

200
400
600
800
1000

(b) Eukrohnia hamata
0

8

12

4

0

4

8

12 12

8

4

0

4

8

12 12

8

4

0

4

8

12 12

8

4

0

4

8

12

200
400

Depth (m)

600
800
1000

(c) Eukrohnia bathypelagica0

8 6 4 2 0 2 4 6 8

8 6 4 2 0 2 4 6 8

8 6 4 2 0 2 4 6 8

8 6 4 2 0 2 4 6 8

200
400
600
800
1000

(d) Eukrohnia juvenile
0

20

10

0

10

20

20

10

0

10

20

20

10

0

10

20

20

10

0

10

20

200
400
600
800
1000

29 Oct. 2010

26 Feb. 201122 Apr. 2011

3–4 July 2011

Figure3. 3.
(open)and (solid)
night vertical(solid)distribution
vertical distributionof the four
dominant
Chaetognaths:
FigureDayDay(open)and nightof the four dominant
Chaetognaths:
Parasagitta
elegans(a), Eukrohnia
hamata (b),Eukrohnia
bathypelagica(c), and Eukrohnia
juvenile(d) atjuvenile
St.
Parasagitta
elegans(a), Eukrohnia
hamata(b), Eukrohnia
bathypelagica(c), andEukrohnia(d) at St.
K2 in the western subarctic Pacific gyre during October 2010 to July 2011. Distribution cores (D50% )were calculated for each sample series and shown with triangles (open: day, solid: night).

Oceans 2023, 4

259

Table 3. Summary of the vertical distribution cores (D50% , m) of each dominant chaetognath species
in the western subarctic Pacific gyre during October 2010 to July 2011. (D): day, (N): night.
Species
Parasagitta elegans
Eukrohnia hamata
Eukrohnia bathypelagica
Eukrohnia juvenile

29 October 2010

26 February 201122 April 2011

3–4 July 2011

(D)

(N)

(D)

(N)

(D)

(N)

(D)

(N)

100
250
453
199

104
279
612
206

169
223
427
187

124
253
477
196

71
172
274
175

62
222
356
177

77
140
253
143

69
134
273
161

The vertical distribution of P. elegans was the shallowest among the species and wasconcentrated at 200 m depth. The vertical distribution of P. elegans was slightly deep in
October and February (D50% : 100–169 m) and shallow in April and July (D50% : 62–77 m).
The vertical distribution of E. hamata was deeper than that of P. elegans, which frequently
occurred at 100–500 m. The vertical distribution of E. hamata was shallower in July (D50% :134–140 m) than in October and February (D50% : 223–279 m). Eukrohnia juvenile wasdistributed at the same depth as E. hamata and abundant at 100–400 m. Like E. hamata,
Eukrohnia juveniles mainly distributed shallower depths in July (D50% : 143–161 m) than in
the other seasons (D50% : 175–206 m). The deepest-distributed species was E. bathypelagica,
which occurred at 200–1000 m. Similar to the other species, the vertical distribution of
E. bathypelagica was relatively deep in October and February (D50% : 253–356 m) and shallow
in April and July (D50% : 253–356 m).
3.4. Population Structure
Body length histograms and depth distributions of the three dominant Chaetognathspecies (P. elegans, E. hamata, and E. bathypelagica) and Eukrohnia species group (E. hamata +E. bathypelagica) are shown in Figures 4–7. The body length of P. elegans ranged from 4 to
34 mm (Figure 4). There were one to three cohorts for the body length of P. elegans at eachsampling date. For example, in July, the large body length, having a mean of 25–26 mm,
was observed as one cohort both day and night. For the vertical distribution at each bodylength, the smaller individuals tended to be distributed at shallower depths, and the larger
individuals were distributed at deeper layers, which was prominent, especially in October.
The body length of E. hamata ranged from 10 to 22 mm (Figure 5). There were two tofour cohorts in body length of E. hamata at each sampling date. Within the eight developmental stages based on the criteria of [27], only stage 1–5 individuals have occurred forE. hamata, and stage 6–8 individuals were not present throughout the samples in this study.
Commonly, for all seasons, the smaller individuals occurred at the shallower depths, andthe larger individuals were distributed at the deeper layer.
The body length of E. bathypelagica ranged from 10 to 22 mm (Figure 6). There were
two to three cohorts in body length of E. bathypelagica at each sampling date. However, it
should be noted that the small body length cohorts of this species were derived from the
combination of Eukrohnia juveniles, as mentioned before. Also, for E. bathypelagica, within
the eight developmental stages of maturation based on the E. hamata criteria [27], only
stage 1–5 individuals have occurred, and stage 6–8 individuals did not occur throughout
the samples. The vertical distribution of E. bathypelagica was shallower in April and Julythan in October and February, but ontogenetic changes in vertical distribution were notclear for this species.
The body length of Eukrohnia juveniles ranged from 2 to 14 mm (Figure 7). For the
Eukrohnia species group (Eukrohnia juvenile + E. hamata + E. bathypelagica), the entire bodylength ranged from 2 to 22 mm. Within the eight developmental stages based on theE. hamata criteria [27], only stage 1–5 individuals occurred, and stage 6–8 individuals were
not present throughout the samples. The Eukrohnia species group showed clear ontogenetic
changes in vertical distribution depth. Seasonally, in April and July, the new adults at
8–12 mm body length were distributed at shallower depths than juveniles at 50–200 m.

Oceans 2023, 4

260

Within adults, vertical distribution became deeper with growth. The largest individuals
9 9were found below 200 m. Seasonal changes in vertical distribution were evidenced
by theshallowest distribution in July.

Oceans 2023,Oceans
4, FORPEER
REVIEW
2023,
4, FOR
PEER REVIEW

Figure 4. Seasonal changes in body length histograms and their distribution depths of Parasagitta

Figure elagans
4. Seasonalin bodylengthhistograms
anddistribution
at St. K2changes
in the western
subarctic
Pacific
gyre during
the their
daytime(upper) and depths
nighttimeof Parasagitta
FigureSeasonalchangesinbody length
histograms
and
their
distribution
depthsParasagitta
occasions(October
2010,
February,
April,
July of2011).
Triangles
elagans4.(lower)
at
St. ofK2theinfourthesampling
westernsubarctic
Pacific
gyreduringtheanddaytime(upper)and nighttime
elagans atdenote
St. K2thethe western
subarctic
Pacific
gyre during the daytime (upper) and nighttime
mean
body lengthsof eachcohort.
(lower) of
the infour
sampling
occasions(October
2010, February, April, and July 2011). Triangles(lower) of the four sampling occasions (October 2010, February, April, and July 2011). Triangles
denotethe
the
mean
body
lengths
ofcohort.
each cohort.
denotemean
bodylengthsof eachFigure 5. Seasonal changes in body length histograms and their distribution depths of Eukrohnia
hamata at St. K2 in the western subarctic Pacific gyre during the daytime (upper) and nighttime(lower) of the four sampling occasions (October 2010, February, April, and July 2011). Triangles
denote the mean body lengths of each cohort. Note that depth distribution data were not shown forthe juveniles and were thus presented only for E. hamata at larger body sizes.

Oceans 2023, 4, FOR PEER REVIEW

Oceans 2023, 4

10

Figure 5. Seasonal changes in body length histograms and their distribution depths of Eukrohnia
hamata at St. K2 in the western subarctic Pacific gyre during the daytime (upper) and nighttime(lower) of the four sampling occasions (October 2010, February, April, and July 2011). Triangles
denote the mean body lengths of each cohort. Note that depth distribution data were not shown forthe juveniles and were thus presented only for E. hamata at larger body sizes.

261

Figurechangesin bodylengthhistogramsand their
distribution
depths ofdepths
Eukrohnia
Figure6.6.Seasonal
Seasonalchangesin bodylengthhistograms
andtheir distributionof Eukrohnia
bathypelagica
at at
St.St.
K2 K2
in thesubarctic
PacificPacificgyre during
the daytime(upper) andnighttimebathypelagica
in western
the western
subarctic
gyre during
the daytime(upper)and nighttime(lower) of the four sampling occasions (October 2010, February, April, and July 2011). Triangles(lower) of the four sampling occasions (October 2010, February, April, and July 2011). Triangles
denote the mean body lengths of each cohort. Note that the data for Eukrohnia juveniles were not
Oceans 2023, 4, FOR PEER REVIEW included
11 were notdenote the
mean
body
lengthspanels.
of each cohort. Note that the data for Eukrohnia juveniles
in thedepth
composition

included in the depth composition panels.

Figure 7. Seasonal changes in body length histograms and their distribution depths of the Eukrohnia
Figure 7. Seasonal changes in body length histograms and their distribution depths of the Eukrohnia
species group (juveniles + E. hamata + E. bathypelagica) at St. K2 in the western subarctic Pacific gyre
speciesthe
group(juveniles
E. hamata+ E.(lower)
bathypelagica)
at St.
K2 in thewesternsubarctic
duringdaytime(upper)+andnighttimeof the four
sampling
occasions(October
2010,Pacific gyreduring thedaytime(upper)and nighttime(lower)thelengths
four samplingoccasions (October 2010,
February,
April,and July2011). Triangles
denote themean ofbody
of each cohort.

February, April, and July 2011). Triangles denote the mean body lengths of each cohort.

The mean body length of each cohort and developmental stage composition of P. elegans, E. hamata, E. bathypelagica, and Eukrohnia species group (Eukrohnia juvenile + E. hamata+ E. bathypelagica) are shown in Figure 8. The body lengths were classified into two toOceans 2023, 4

262

four cohorts at each sampling date. However, it should be noted that the number of cohorts varied between day and night, even at the same sampling date for the E. hamata
FigureSeasonal changes
in bodylengthhistograms Thus,and their
distribution
depths ofwere
the Eukrohnia
and7.Eukrohnia
speciesgroupsin October.
some
discrepancies
present. For
species group (juveniles + E. hamata + E. bathypelagica) at St. K2 in the western subarctic Pacific gyre
P. elegans developmental stage composition, stage II dominated throughout the year, whileduring the daytime (upper) and nighttime (lower) of the four sampling occasions (October 2010,
in Eukrohnia,
stagesII andTriangles
III dominated.
February,
April, andJuly 2011).
denote the mean body lengths of each cohort.

Figure8. Seasonalchangesin meanbodybody
lengths
evaluatedby cohortanalysesfor Prasagitta
elegans elegans
Figure8. Seasonalchangesin meanlengths
evaluatedby cohortanalysesfor Prasagitta(a), Eukrohnia hamata (b), Eukrohnia bathypelagica (c), and Eukrohnia species group (d) at St. K2 in the(a), Eukrohnia hamata (b), Eukrohnia bathypelagica (c), and Eukrohnia species group (d) at St. K2 inwestern subarctic Pacific gyre during the day (D) and night (N) of the four sampling occasions (Octhe2010,
westernsubarctic
Pacific
gyre2011).
duringthe day(N)of therepresent
four samplingoccasionstober
February,
April,and July
Symbolsin(D)the andbodynight
lengthpanelsthe mean(October
April, For
anddetails
July 2011).
Symbols
in seetheFigures
body lengthbodylength 2010,
valuesFebruary,of each cohort.
on eachspecies,
4–7. panels represent the mean
body length values of each cohort. For details on each species, see Figures 4–7.

4. Discussion
4. Discussion
4.1. Abundance and Biomass of Chaetognatha

The dominant Chaetognath species in the western Subarctic Pacific gyre were two
species belonging to the genus Eukrohnia (E. hamata and E. bathypelagica) in abundance andP. elegans in terms of biomass (Table 2). These results well correspond with those in the
Gulf of Alaska in the eastern subarctic Pacific [15]. To add to these species, Pseudosagitta
scrippsae is also listed as the dominant species in the Oyashio region of the western subarctic
Pacific [24]. This might be because the research area of [24] was at a lower latitude than
this study and had a shallower sampling depth (200 m). In fact, the dominant species inthe studies conducted at higher latitudes (basin of the Bering Sea) down to the depth of3000 m corresponded with this study [25].
Within the three dominant species of this study, P. elegans is known to distribute mainlyin the epipelagic zones of the high latitude areas of the Northern Hemisphere, such as
the North Pacific, the North Atlantic, and the Arctic Ocean [1,8,30]. On the other hand,
the two species of Eukrohnia are thought to have a worldwide distribution, distributedin the epipelagic zones of both the Arctic and Southern Oceans and the deep sea of thelower latitudes [3,4,31,32]. However, such a global distribution of Eukrohnia species has
been doubted, and no genetic differences in E. bathypelagica and E. hamata within the same
region, geographically four classifications, and the possibility that E. bathypelagica would
be a post-spawning individual of E. hamata have been proposed by the mtDNA COI region
analyses [17,26]. Furthermore, a genetic study on E. hamata has also been made for thegeographic distribution, and the results of [17] have been confirmed to be correct by [33].
Unfortunately, since the genetic analysis of E. bathypelagica has not been made in [33], theOceans 2023, 4

263

genetic correspondence between E. hamata and E. bathypelagica reported in [17,26] has notbeen tested yet. Thus, this study is the first attempt to treat E. hamata and E. bathypelagica asa single “species group” based on field sampling.
A comparison of the abundance and biomass of the three dominant Chaetognathspecies in this study with those of the other regions is shown in Table 4. Abundances of
P. elegans and E. hamata in this study were similar to or slightly higher than those in theadjacent Oyashio region. The highest abundance of P. elegans (2483–3922 ind. m−2 ) has beenreported in the Celtic Sea and central Long Island Sound in the North Atlantic, where thewater depths are shallow (0–37 or 0–90 m) [34,35]. These facts suggest that the abundanceof the epipelagic species P. elegans is high in the neritic areas, which are characterized byhigh primary productivity.
On the other hand, the vertical distribution of E. hamata has been reported to be
deeper than that of P. elegans in various oceans, including the Arctic Ocean [36,37], thesubarctic Pacific [15,25], and the North Atlantic [38,39]. Since the distribution of E. hamata
extended deeper than that of P. elegans, the abundance in the water column (ind. m−2 )would be higher for the former than the latter [13,18,24,36,37]. The vertical distributionof E. bathypelagica has been reported to be deeper than that of E. hamata [15,25]. Such
restriction of the occurrence depths of E. bathypelagica implies that the abundance of thisspecies remains similar to or slightly lower than that of E. hamata [18,31]. The Eukrohnia is
carnivorous, and their primary diet has been reported to be small copepods [2,4,25,36,37,40].
The abundance of the small copepods was high in the shallower depths and low in the
deep sea (Figure 2). These facts suggest that the competition for the prey animal (small
copepods) would be high in the deep sea, and increasing sizes of head width and hooklength of deep-sea Eukrohnia have been reported and interpreted to capture prey animals in
the resource-limited deeper layers [25]. Considering these facts, E. bathypelagica, distributedin food-scarce environments, is thought to have a limited abundance due to a limited foodsupply, although its vertical distribution is wide.
4.2. Vertical Distribution
The vertical distribution of the same three dominant Chaetognath species in this study
has been reported in the Gulf of Alaska in the eastern subarctic Pacific, and the distribution
depths of P. elegans, E. hamata, and E. bathypelagica are reported to be 0–100 m, 100–500
m, and 250–1000 m, respectively [15]. The same vertical occurrence order of these three
species, P. elegans < E. hamata < E. bathypelagica, has also been reported for the western
subarctic Pacific and its marginal seas [25]. These facts suggest that this pattern is solid andis commonly observed throughout its occurrence areas.
For the whole zooplankton biomass, bimodal vertical distribution has been reported
at St. K2, with peaks at the surface layer and 200–300 m [20,22]. This bimodal vertical
distribution has also been observed even for Chaetognaths [22], and P. elegans formed thesurface maximum, while a deeper maximum was composed by Eukrohnia species (Figure 3).
This study did not detect diel vertical migration (DVM) for any species (Figure 3). On theother hand, the presence of DVM, in which small specimens occur near the surface layer day
and night while large individuals perform nocturnal ascent, has been reported for P. elegans in
the Gulf of Alaska and Dabab Bay in Washington [14,41–43]. The magnitude of this DVM has
been reported to be around 50 m [14]. These facts suggest that the sampling design of thisstudy (minimum depth internal at 25 m) was too large to evaluate such a small DVM.
For the prominent characteristics of the vertical distribution of the Eukrohnia species
group, juveniles occurred at the narrower, shallower depths of 150–300 m. E. hamata
extended to a deeper layer than juveniles, and then E. bathypelagica extended further
deeper than that of E. hamata (Figure 3c). Thus, within Eukrohnia species, their vertical
distribution was seen in the order of Eukrohnia juveniles < E. hamata < E. bathypelagica.
Such a phenomenon as Eukrohnia (developmental descent) has been reported in the North
Pacific [42,44], Arctic Ocean [13,38], and South Ocean [31,40,45]. Thus, such ontogenetic
vertical distribution is considered to be a feature of this genus.

Oceans 2023, 4

264

Table 4. Regional comparison in abundance of the three dominant chaetognath species (Eukrohnia bathypelagica, E. hamata and Parasagitta elegans) from worldwide
oceans.
Abundance (ind. m−2 )RegionOyashio
Celtic Sea
Arctic Ocean
Arctic Ocean
Arctic Ocean
OyashioOyashio
Bering Sea
Okhotsk Sea
western subarctic PacificJapan Sea
Buffin Bay
Long Island Sound
Southern Ocean
K2

SeasonSpringAnnualAnnualAnnualSummerAnnualAnnualSummerSummerSummerSummerSummerAnnualSummer/WinterAnnual

Gear

Bongo
LHPR
Multi-net
Multi-net
Multi-net
NORPAC
Bongo
VMPS
VMPS
VMPS
VMPS
BIONESS
Ring net
Multi-net
IONESS

Mesh
(µm)
335
280
200
200
150
335
335
90
90
90
90
243
202
100
335

Depth
(m)
0–200
0–90
0–520
0–580
0–30000–150
0–10000–50000–50000–50000–50000–500
0–37
0–30000–1000E. bathypelagica

E. hamataP. elegans

Reference

Min

Max

Mean

Min

Max

Mean

Min

Max

Mean

220
27
240

383
82
1540

512
273
360
0
870

113
56
158
804
1738
130
81
140

2543
894
894
1773
3090
444
224
1600

1050
468
1087
2164
970
1475
0
800

52
22
16
16
0
90
127
0
40

380
2483
462
204
16
795
1154
405
3922
360

176
71
3
2359
94
1123
135
200

Abe et al. (2016) [24]Conway and Williams (1986) [34]
Grigor et al. (2017) [36]Grigor et al. (2020) [37]
Kosobokova and Hopcroft (2021) [13]Kotori (1999) [16]Matsumoto and Yamaguchi (2020) [18]Ozawa et al. (2007) [25]Ozawa et al. (2007) [25]Ozawa et al. (2007) [25]Ozawa et al. (2007) [25]Sameoto (1987) [38]Tiselius and Peterson (1986) [35]Kruse et al. (2009) [31]This study

Oceans 2023, 4

265

Ontogenetic vertical distribution changes in Chaetognaths: deeper occurrences oflarge-sized specimens have been reported for P. elegans and E. hamata in the Gulf of
Alaska [42]. In this study, both P. elegans and E. hamata showed this developmental descentontogenetic vertical distribution clearly (Figures 4 and 5). Since Chaetognatha are large inbody size, they are important as food for various fish [46–48]. Therefore, to avoid predation
by visual predators such as fish, large-sized specimens may perform a deeper distribution,
which would induce ontogenetic vertical distribution.
4.3. Population Structure of Chaetognaths
This study observed two to four cohorts for the body length histograms of P. elegans,
E. hamata, and E. bathypelagica (Figure 8). Based on the time-series trace of the bodylength cohort, life histories of Chaetognaths in the subarctic Pacific were conducted for
P. elegans [16,24,49] and E. hamata [18,49] by tracing their cohorts over time. The daily
growth rates in body length have been reported as 14–290 µm day−1 in P. elegans and6–100 µm day−1 in E. hamata (see Table 3 of [31]). Considering these values, maturation of
the specimens is possible within three months. However, since the sampling interval ofthis study is three months (four times in one year), it is difficult to analyze their life cycles
by tracing the body length of each cohort.
The most prominent finding of this study is that both Eukrohnia species (E. hamata
and E. bathypelagica) had no large mature specimens reported for E. hamata in the Arctic
Ocean (Figures 5–7). Thus, in the Arctic Ocean, the maturation stages of E. hamata havebeen classified into eight stages [27]. While only stages belonging to 1 to 5 occurredand no individuals belonging to 6 to 8 stages were observed throughout this study, it isalso mentioned that there is a scarce occurrence of mature individuals of E. hamata andE. bathypelagica in the Southern Ocean [3,31]. As the causes of such a low abundance of
mature specimens, it is suggested that the deeper occurrence of mature individuals and thelong time interval (low time resolution) in sampling design may prevent the appropriate
collection of the mature specimens [31].
These two factors (deeper occurrence of mature specimens and failure to collect mature
specimens due to insufficient time resolution) are also inevitable in this study; however,considering their vertical distributions (Figure 3), it is hard to assume that only mature
E. hamata and E. bathypelagica occur below 1000 m depth. Genetic analyses suggest that
E. hamata and E. bathypelagica belong to the same species group and are geographicallydivided into four species groups [17,26]. The four species groups are reported to occur indifferent geographical regions: the northern North Pacific, the Southern Ocean, the tropical
Pacific, and the Atlantic–Arctic Ocean [17,26]. From these geographical distributions ofgenetic groups of Eukrohnia species, it is suggested that the population in the northern
North Pacific (this study) and that in the Arctic Ocean [27] belong to different cryptic
species. If this hypothesis is correct, the cryptic species group of Eukrohnia in the arctic
ocean (Ham-B in [17]) has eight stages of maturity. In contrast, the species of E. hamata in
the northern North Pacific (Ham-D in [17]) has only five maturation stages.
In terms of the body length of Eukrohnia spp., there are substantial differences between
the Arctic Ocean and the northern North Pacific. Thus, the body length of E. hamata (HamB) in the Arctic Ocean has been reported to be as large as 41 mm [13,27]. On the other
hand, E. hamata (Ham-D) in the northern North Pacific has a maximum body length of
28 mm [15,24] (Figures 5–7). Such a large geographical variation in body length may reflect
the genetic differences seen in the Eukrohnia species group.
As another point to consider, there are no genetic differences between E. hamata andE. bathypelagica, and they should be treated as one species, as pointed out by [17]. The vertical distribution and population structure of the Eukrohnia species group, which combines
Eukrohnia juvenile, E. hamata, and E. bathypelagica, have no difficulty considering or treating
one species group (Figure 7). This may suggest that E. hamata and E. bathypelagica are thesame species in the western subarctic Pacific. To clarify this point, detailed genetic analysis

Oceans 2023, 4

266

of the Eukrohnia species group, including Eukrohnia juveniles, small to large individuals of
E. hamata, and E. bathypelagica, will be required in future studies.
In conclusion, regional genetic segregation would be present considering the great
regional differences in body size and mature stage of Eukrohnia species. Within the same
region (especially in the western subarctic Pacific), Eukrohnia species, including E. hamata
and E. bathypelagica, could be treated as one species group. Further molecular analysis will
be required for the Eukrohnia species group to evaluate these issues.
Author Contributions: Conceptualization, Y.N. and A.Y.; methodology, Y.N. and A.Y.; software, Y.N.;
validation, Y.N. and A.Y.; formal analysis, Y.N.; investigation, Y.N.; resources, A.Y.; data curation,
A.Y.; writing—original draft preparation, H.Z.; writing—review and editing, A.Y.; visualization, H.Z.;
supervision, A.Y.; project administration, A.Y.; funding acquisition, A.Y. All authors have read andagreed to the published version of the manuscript.
Funding: Part of this study was supported by Grant-in-Aid for Challenging Research (Pioneering)
20K20573, Scientific Research 22H00374 (A), 20H03054 (B), 19H03037 (B), and 17H01483 (A) fromthe Japan Society for the Promotion of Science (JSPS). This study was partially supported by the
Arctic Challenge for Sustainability II (ArCS II; JPMXD1420318865) and the Environmental Research
and Technology Development Fund (JPMEERF20214002) of the Environmental Restoration andConservation Agency of Japan.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement: Data will be available upon request to the corresponding author.
Acknowledgments: We thank the captains, officers, crews, and researchers onboard the R/V Mirai,
JAMSTEC, for their great efforts during the field sampling. We thank Minoru Kitamura for allowing
us to use the samples for this study.
Conflicts of Interest: The authors declare no conflict of interest.

References
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.

Kotori, M. The biology of Chaetognatha in the Bering Sea and the northern North Pacific Ocean, with emphasis on Sagitta elegans.
Mem. Fac. Fish. Hokkaido Univ. 1976, 23, 95–183.
Øresland, V. Feeding of the chaetognaths Sagitta elegans and S. setosa at different seasons in Gullmarsfjorden, Sweden. Mar. Ecol.
Prog. Ser. 1987, 39, 69–79. [CrossRef]
Kruse, S.; Hagen, W.; Bathmann, U. Feeding ecology and energetics of the Antarctic chaetognaths Eukrohnia hamata, E. bathypelagica
and E. bathyantarctica. Mar. Biol. 2010, 157, 2289–2302. [CrossRef]
Giesecke, R.; Gonzales, H.E. Distribution and feeding of chaetognaths in the epipelagic zone of the Lazarev Sea (Antarctica)
during austral summer. Polar Biol. 2012, 35, 689–703. [CrossRef]
Zavolokin, A.V. Comparative characteristics of food supply of Pacific salmon (Oncorhynchus spp.) in the Bering Sea from 2002 to
2006. J. Ichthyol. 2011, 51, 227–239. [CrossRef]
Yamamura, O.; Funamoto, T.; Chimura, M.; Honda, S.; Oshima, T. Interannual variation in diets of walleye pollock in the Dotoarea, in relation to climate variation. Mar. Ecol. Prog. Ser. 2013, 491, 221–234. [CrossRef]
Beamish, R.J.; Leask, K.D.; Ivanov, O.A.; Balanov, A.A.; Orlov, A.M.; Sinclair, B. The ecology, distribution, and abundance of
midwater fishes of the Subarctic Pacific gyres. Prog. Oceanogr. 1999, 43, 399–442. [CrossRef]
Terazaki, M. Life history, distribution, seasonal variability and feeding of the pelagic chaetognath Sagitta elegans in the subarctic
Pacific: A review. Plankton Biol. Ecol. 1998, 45, 1–17.
McLaren, I.A. Population and production ecology of zooplankton in Ogac Lake, a landlocked fiord on Baffin Island. J. Fish. Res.
Board Can. 1969, 26, 1485–1559. [CrossRef]
Sameoto, D.D. Annual life cycle and production of the chaetognath Sagitta elegans in Berlford Basin, Nova Scotia. J. Fish. Res.
Board Can. 1973, 30, 333–344. [CrossRef]
Choe, N.; Deibel, D. Seasonal vertical distribution and population dynamics of the chaetognath Parasagitta elegans in the watercolumn and hyperbenthic zone of Conception Bay, Newfoundland. Mar. Biol. 1986, 137, 847–856. [CrossRef]
Grigor, J.J.; Soreide, J.E.; Varpe, O. Seasonal ecology and life-history strategy of the high-latitude predatory zooplankter Parasagitta
elegans. Mar. Ecol. Prog. Ser. 2014, 499, 77–88. [CrossRef]
Kosobokova, K.N.; Hopcroft, R.R. Population structure, vertical distribution and fecundity of Eukrohnia hamata (Chaetognatha) in
the Arctic Ocean during summer. Deep-Sea Res. I 2021, 169, 103454. [CrossRef]

Oceans 2023, 4

14.
15.
16.
17.
18.
19.

20.

21.

22.
23.

24.

25.

26.
27.

28.
29.
30.
31.
32.
33.
34.
35.
36.
37.
38.
39.

267

King, K.R. The life history and vertical distribution of the chaetognath, Sagitta elegans, in Dabob Bay, Washington. J. Plankton Res.
1979, 1, 153–167. [CrossRef]
Terazaki, M.; Miller, C.B. Life history and vertical distribution of pelagic chaetognaths at Ocean Station P in the subarctic Pacific.
Deep-Sea Res. 1986, 33A, 323–337. [CrossRef]
Kotori, M. Life cycle and growth rate of the chaetognath Parasagitta elegans in the northern North Pacific Ocean. Plankton Biol.
Ecol. 1999, 46, 153–158.
Miyamoto, H.; Machida, R.J.; Nishida, S. Global phylogeography of the deep-sea pelagic chaetognath Eukrohnia hamata. Prog.
Oceanogr. 2012, 104, 99–109. [CrossRef]
Matsumoto, Y.T.; Yamaguchi, A. Seasonal changes in the community structure of chaetognaths and the life cycle of the dominantchaetognath Eukrohnia hamata in the Oyashio region, western subarctic Pacific. Plankton Benthos Res. 2020, 15, 146–155. [CrossRef]
Honda, M.C.; Wakita, M.; Matsumoto, K.; Fujiki, T.; Siswanto, E.; Sasaoka, K.; Kawakami, H.; Mino, Y.; Sukigara, C.; Kitamura,M.; et al. Comparison of carbon cycle between the western Pacifc subarctic and subtropical time-series stations: Highlights of theK2S1 project. J. Oceanogr. 2017, 73, 647–667. [CrossRef]
Kitamura, M.; Kobari, T.; Honda, M.C.; Matsumoto, K.; Sasaoka, K.; Nakamura, R.; Tanabe, K. Seasonal changes in themesozooplankton biomass and community structure in subarctic and subtropical time-series stations in the western North Pacific.
J. Oceanogr. 2016, 72, 387–402. [CrossRef]
Kobari, T.; Nakamura, R.; Unno, K.; Kitamura, M.; Tanabe, K.; Nagafuku, H.; Niibo, A.; Kawakami, H.; Matsumoto, K.; Honda,
M.C. Seasonal variability in carbon demand and flux by mesozooplankton communities at subarctic and subtropical sites in thewestern North Pacific Ocean. J. Oceanogr. 2016, 72, 403–418. [CrossRef]
Steinberg, D.K.; Cope, J.S.; Wilson, S.E.; Kobari, T. A comparison of mesopelagic mesozooplankton community structure in thesubtropical and subarctic North Pacific Ocean. Deep-Sea Res. II 2008, 55, 1615–1635. [CrossRef]
Ohashi, R.; Ishii, K.-I.; Fujiki, T.; Kitamura, M.; Matsumoto, K.; Honda, M.C.; Yamaguchi, A. Short-term changes in planktonic
community of the western subarctic Pacific during early summer: Analysis of sediment trap samples. Bull. Plankton Soc. Jpn.
2011, 58, 123–135.
Abe, Y.; Miyamoto, H.; Saito, R.; Matsuno, K.; Yamaguchi, A.; Imai, I. Comparative ecology of three dominant pelagic chaetognaths(Eukrohnia hamata, Parasagitta elegans, Pseudosagitta scrippsae) in the Oyashio region during the spring phytoplankton bloom. Reg.
Stud. Mar. Sci. 2016, 8, 122–132. [CrossRef]
Ozawa, M.; Yamaguchi, A.; Ikeda, T.; Watanabe, Y.; Ishizaka, J. Abundance and community structure of chaetognaths from theepipelagic through abyssopelagic zones in the western North Pacific and its adjacent seas. Plankton Benthos Res. 2007, 2, 184–197.
[CrossRef]
Miyamoto, H.; Machida, R.J.; Nishida, S. Molecular phylogeny of pelagic chaetognaths. Bull. Plankton Soc. Jpn. 2015, 62, 29–32.
Kosobokova, K.N.; Isachenko, A.I. The gonad maturation and size structure of the population of abundant planktonic predator
Eukrohnia hamata (Möbius, 1875) (Chaetognatha) in the Eurasian Basin of the Arctic Ocean in summer. Russ. J. Mar. Biol. 2017, 72,
403–418. [CrossRef]
Pennak, R.W. An effective method of diagramming diurnal movements of zooplankton organisms. Ecology 1943, 24, 405–407.
[CrossRef]
Aizawa, Y.; Takiguchi, N. Consideration of the methods for estimating age-composition from the length frequency data with
MS-Excel. Bull. Jpn. Soc. Fish. Oceanogr. 1999, 63, 205–214.
Pearre, S. Feeding by Chaetognatha: Energy balance and importance of various components of the diet of Sagitta elegans. Mar.
Ecol. Prog. Ser. 1981, 5, 45–54. [CrossRef]
Kruse, S.; Bathmann, U.; Brey, T. Meso- and bathypelagic distribution and abundance of chaetognaths in the Atlantic sector of theSouthern Ocean. Polar Biol. 2009, 32, 1359–1376. [CrossRef]
Bieri, R. The distribution of the planktonic Chaetognatha in the Pacific and their relationship to the water masses. Limnol.
Oceanogr. 1959, 4, 1–28. [CrossRef]
Kulagin, D.N.; Stupnikova, A.N.; Neretina, T.V.; Mugue, N.S. Spatial genetic heterogeneity of the cosmopolitan chaetognath
Eukrohnia hamata revealed by mitochondrial DNA. Hydrobiologia 2014, 721, 197–207. [CrossRef]
Conway, D.V.P.; Williams, R. Seasonal population structure, vertical distribution and migration of the chaetognath Sagitta elegans
in the Celtic Sea. Mar. Biol. 1986, 93, 377–387. [CrossRef]
Tiselius, P.T.; Peterson, W.T. Life history and population dynamics of the chaetognath Sagitta elegans in central Long Island Sound.
J. Plankton Res. 1986, 8, 183–195. [CrossRef]
Grigor, J.J.; Schmid, M.S.; Fortier, L. Growth and reproduction of the chaetognaths Eukrohnia hamata and Parasagitta elegans in the
Canadian Arctic Ocean: Capital breeding versus income breeding. J. Plankton Res. 2017, 39, 910–929. [CrossRef]
Grigor, J.J.; Schmid, M.S.; Caouette, M.; St.-Onge, V.; Brown, T.A.; Barthelemy, R.-M. Non-carnivorous feeding in Arctic
chaetognaths. Prog. Oceanogr. 2020, 186, 102388. [CrossRef]
Sameoto, D.D. Vertical distribution and ecological significance of chaetognaths in the Arctic environment of Baffin Bay. Polar Biol.
1987, 7, 317–328. [CrossRef]
Pierrot-Bults, A.C. A short note on the biogeographic patterns of the Chaetognatha fauna in the North Atlantic. Deep–Sea Res. II
2008, 55, 137–141. [CrossRef]

Oceans 2023, 4

40.
41.
42.
43.
44.
45.
46.
47.

48.
49.

268

Øresland, V. Feeding and predation impact of the chaetognath Eukrohnia hamata in Gerlache Strait, Antarctic Peninsula. Mar. Ecol.
Prog. Ser. 1990, 63, 201–209. [CrossRef]
Brodeur, R.D.; Terazaki, M. Springtime abundance of chaetognaths in the shelf region of the northern Gulf of Alaska, withobservations on the vertical distribution and feeding of Sagitta elegans. Fish. Oceeanogr. 1999, 8, 93–103. [CrossRef]
Sullivan, B.K. In situ feeding behavior of Sagittcl elegans and Eukrohnia hamata (Chaetognatha) in relation to the vertical distribution
and abundance of prey at Ocean Station “P”. Limnol. Oceanogr. 1980, 25, 317–326. [CrossRef]
Matsuda, S.; Taniguchi, A. Diel changes in vertical distribution and feeding conditions of the chaetognath Parasagitta elegans(Verill) in the subarctic Pacific in summer. J. Oceanogr. 2001, 57, 353–360. [CrossRef]
Johnson, T.B.; Terazaki, M. Species composition and depth distribution of chaetognaths in a Kuroshio warm-core ring andOyashio water. J. Plankton Res. 2003, 25, 1279–1289. [CrossRef]Øresland, V. Winter population structure and feeding of the chaetognath Eukrohnia hamata and the copepod Euchaeta antarctica in
Gerlache Strait, Antarctic Peninsula. Mar. Ecol. Prog. Ser. 1995, 119, 77–86. [CrossRef]
Nishiuchi, K. Study on the Life History and Annual Variability of the Carnivorous Planktonic Chaetognaths in the Northern
North Pacific Ocean. Ph.D. Thesis, Hokkaido University, Sapporo, Japan, 1999.
Moku, M.; Kawaguchi, K.; Watanabe, H.; Ohno, A. Feeding habits of three dominant myctophid fishes, Diaphus theta, Stenobrachius
leucopsarus and S. nannochir, in the subarctic and transitional waters of the western North Pacific. Mar. Ecol. Prog. Ser. 2000, 207,
129–140. [CrossRef]
Yamamura, O.; Honda, S.; Shida, O.; Hamatsu, T. Diets of walleye pollock Theragra chalcogramma in the Doto area, northern Japan:
Ontogenetic and seasonal variations. Mar. Ecol. Prog. Ser. 2002, 238, 187–198. [CrossRef]
Terazaki, M.; Miller, C.B. Reproduction of meso- and bathypelagic chaetognaths in the genus Eukrohnia. Mar. Biol. 1982, 71,
193–196. [CrossRef]

Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual
author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury topeople or property resulting from any ideas, methods, instructions or products referred to in the content.