Article

Seasonal Changes in Vertical Distribution and Population
Structure of the Dominant Hydrozoan Aglantha digitale in theWestern Subarctic Pacific
Mari Aizawa 1 , Tian Gao 1 and Atsushi Yamaguchi 1,2, *1

2*

Citation: Gao, T.; Aizawa, M.;
Yamaguchi, A. Seasonal Changes in
Vertical Distribution and Population
Structure of the DominantHydrozoan Aglantha digitale in the

Graduate School of Fisheries Sciences, Hokkaido University, 3–1–1 Minato-cho,
Hakodate 041-8611, Hokkaido, Japan; o1417marimari@gmail.com (M.A.); gaotianbio@yeah.net (T.G.)
Arctic Research Center, Hokkaido University, Kita-21 Nishi-11 Kita-ku, Sapporo 001-0021, Hokkaido, Japan
Correspondence: a-yama@fish.hokudai.ac.jp

Abstract: Hydrozoans are numerically dominant taxa in gelatinous zooplankton communities of theworldwide oceans and play an energy transfer role connecting primary producers and higher trophic
level organisms. In the western subarctic Pacific, St. K2 has been established as a long-term timeseries monitoring station. Various studies on zooplankton have been conducted, while hydrozoans
have not been treated. This study presents the abundance, vertical distribution, and population
structure of the dominant hydrozoan species (Aglantha digitale) at St. K2. Samples collected by verticalstratification samplings from eight layers of 0–1000 m both day and night during four seasons in one
year. Hydrozoans occur throughout the year. The annual mean abundance of A. digitale was 198.4 ind.
m−2 and composed of 91.9% of hydrozoans. The vertical distribution of A. digitale was concentrated
for the epipelagic layer (0–200 m), both day and night of the most season. The bell height (BH) of
A. digitale ranged between 2.4–18.9 mm. Most of the mature individuals, with gonad length larger
than 10% of BH, occurred only in July. The BH of mature individuals ranged from 4.7 to 17.6 mm, with
the BH of most mature individuals were larger than >10 mm. Through observation on BH at eachsampling layer, small individuals with BH < 6 mm were distributed below 300 m depths throughout
the seasons, expanding their vertical distribution to the deeper layers. Inter-region comparison ofabundance, maturation body size, and generation length of A. digitale revealed that these parameters
are varied with the region and depend on the marine ecosystem structures.
Keywords: hydrozoa; Aglantha digitale; abundance; population structure; life cycle

Western Subarctic Pacific. Oceans
2023, 4, 242–252. https://doi.org/10.3390/oceans4030017

1. Introduction
Academic Editors: Antonio Bode andSam Dupont
Received: 26 April 2023
Revised: 7 June 2023
Accepted: 20 July 2023
Published: 31 July 2023

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/).

From worldwide oceans, hydrozoans are numerically dominant taxa in gelatinous
zooplankton communities, feed on small zooplankton and serve as food for fishes, andact as mediators transporting energy between primary producers and higher trophic level
organisms [1]. Recent climate changes (North Atlantic Oscillation, North Pacific Decadal
Oscillation, El Nino, etc.) have had a significant impact on standing stocks of jellyfish
in worldwide oceans, and may increase the duration of occurrence of hydrozoans in thetemperate to subarctic regions [2]. This increase in hydrozoans is predicted to alter the balance of prey-predator relationships in marine ecosystems, with significant effects on lowerand higher trophic-level organisms [3,4]. On the other hand, the chemical compositions ofhydrozoans are characterized by low carbon but high nitrogen and phosphorus contents,
and their outbreak affects the nutrient balance (C:N:P ratio) of the marine ecosystem, andthe decomposition of their carcasses by bacteria has a significant impact on the marine
mineral cycles [5,6].
In the Northern Hemisphere, Aglantha digitale is the most abundant hydrozoan inboth abundance and biomass at high latitudes [1]. A. digitale has been reported as themost dominant hydrozoan species in the western subarctic Pacific [7,8], eastern subarctic

Oceans 2023, 4, 242–252. https://doi.org/10.3390/oceans4030017

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

Oceans 2023, 4

dominant hydrozoan species in the western subarctic Pacific [7,8], eastern subarct[9], northern North Pacific [10], western Arctic Ocean [11], Toyama Bay in the sJapan Sea [12], Norwegian fjords and Svalbard Islands [13–15], eastern
243 North[16,17], Irish Sea [18], and White Sea [19,20]. As the ecology of A. digitale, feeding
nisms [21,22], feeding impact [13,20,23], and swimming behavior [24] have been r
Pacific[9],histories,
northern North[10], western[11],
Toyamaincluding
Bay in thethe Oya
For life
there Pacifichave beenreportsArctic
from Ocean
variousoceans,southern
Japan
Sea
[12],
NorwegianfjordsandSvalbard
Islands[13–15],eastern
North Northgion [7,8], the eastern subarctic Pacific [9], Toyama Bay [12], the western
Atlantic [16,17], Irish Sea [18], and White Sea [19,20]. As the ecology of A. digitale, feeding[16], the Norwegian fjords [14], and the White Sea [19].
mechanisms [21,22], feeding impact [13,20,23], and swimming behavior [24] have been
In thesubarctic
Pacific,
K2 hassetoceans,as a long-term
reported.
For western
life histories,
there havebeen St.
reports
frombeenvarious
including time-serie
theto monitor
parameters[25].BayAs[12],
thetheinformation
on hydro
Oyashioregionvarious[7,8], thebiogeochemical
eastern subarctic Pacific[9], Toyama
western North
Atlantic[16], the Norwegian
fjords [14], andwith
the White
St. K2 bimodal
vertical distribution
peaksSea
at[19].
0–50 m and 200–300 m, with a m
In the western subarctic Pacific, St. K2 has been set as a long-term time-series station
at 150–200 m, and no day/night diﬀerences in abundance have been reported [2to monitor various biogeochemical parameters [25]. As the information on hydrozoans at
K2,
arevertical
severalstudies withon zooplankton
but m,
nowithspecificstudies on hSt.
K2therebimodaldistribution
peaks at 0–50 m[27–31],
and 200–300
a minimumans
are available.
Despite theirimportanceon thelower
and higherleveat
150–200
m, and no day/nightdifferencesin abundance
havebeen reported[26]. trophic
At St.
K2,
there
arematerial
several studies
on zooplankton[27–31],no specific studies
on areahydrozoans
isms
andtransport,
information
onbuthydrozoans
in thisare currently
are available.
Despitetheir importanceon the lowerand higher
trophic level
This study
conducted
abundance,
vertical
distribution,
andorganisms
population stru
and material transport, information on hydrozoans in this area are currently scarce.
the Thisdominanthydrozoans (A. digitale) at St. K2 in the western subarctic Pacific u
study conducted abundance, vertical distribution, and population structure of themalin-preserved
collected
from
day andnight Pacificverticallydominanthydrozoanssamples(A. digitale)at St. K2 inthe western
subarctic
usingstratified
formalin- samp
tween 0–1000
mcollected
covering
fourseasonsof verticallyone year.stratified
As newsamplings
scientificbetween
information,
preserved
samplesfromday
and night
0–1000m
covering
fourseasons
of
one
year.
As
new
scientificinformation,seasonal
and at ea
and day-night changes in bell height (BH, Figure 1) and gonad maturation
day-night changes in bell height (BH, Figure 1) and gonad maturation at each sampling
pling depth down to 1000 m have been evaluated. The results were compareddepth down to 1000 m have been evaluated. The results were compared with the same
same
in thevariousregions ofwaters
high-latitude
watersof the Northern Hemi
species species
in the various
regionsof high-latitudeof the Northern
Hemisphere.

Figure1. 1.
Pictureon specimensof Aglantha
digitale (left)
and theirmeasuredbodyparts: bell bodyheight parts: b
FigurePictureon specimensof Aglantha
digitale(left)and theirmeasured(BH)
gonad
length(GL) (right).
(BH)andandgonadlength(GL) (right).

2. Materials and Methods
2. Materials
and Methods
2.1.
Field Samplingnight vertically stratified zooplankton samplings were made by oblique
2.1.Day
FieldandSampling
tow of Intelligent Operative Net Sampling System (IONESS, SEA Co., Ltd., Bristol, UK)
Day and night vertically stratified zooplankton samplings were made by obli
equipped 335 µm mesh and 1.5 m2 mouth area, from eight layers (0–50, 50–100, 100–150,◦ N, 160◦ E,
of Intelligent
Net 750–1000
Sampling
System(IONESS,
SEA
Ltd., Bris
150–200,
200–300, Operative
300–500, 500–750,m) at
St. K2 (475230 Co.,m depth,equipped
335 µmand 1.5
m2 mouthfromeight2010,
layers(0–50, 50–100,
Figure2), locatedin meshthe western
subarctic
Pacificarea,
on 29
October
26 February,
22–23
April,200–300,
and 3–4 July
2011 (Table
1). After
collection,
zooplankton
sampleswere
150–200,
300–500,
500–750,
750–1000m) at
St. K2 (47°N, 160°E, 5230 m
immediately preserved with 4% buffered formalin seawater. At each sampling occasion,

Figure 2), located in the western subarctic Pacific on 29 October 2010, 26 Februar
April, and 3–4 July 2011 (Table 1). After collection, zooplankton samples were
ately preserved with 4% buﬀered formalin seawater. At each sampling occasion,
mental data such as water temperature, salinity, dissolved oxygen (DO), and chla (Chl. a) fluorescence were measured by fluorometer and DO-sensor mounted C

Oceans 2023, 4244

Oceans 2023, 4, FOR PEER REVIEW

environmental data such as water temperature, salinity, dissolved oxygen (DO), and chlorophylla (Chl.
a) fluorescence
wereInc.,
measuredby fluorometer
911 plus;
Sea-Bird
Electronics
Bellevue,
WA, USA).and
TheDO-sensor
details ofmounted
the environme
CTD
(SBE
911
plus;
Sea-Bird
Electronics
Inc.,
Bellevue,
WA,
USA).
The
detailsof thedata and zooplankton biomass have been published elsewhere [27].
environmental data and zooplankton biomass have been published elsewhere [27].

◦◦Figuresampling
stationK2 (47in thewesternsubarcticsubarctic
Pacific. The
Figure2.2.Location
Locationofof
sampling
stationK2 N,(47°160
N, E)
160°
E) in
the western
Pacific. Th
approximate
positionsofthecurrentsaresuperimposed[32].
proximate positions of the currents are superimposed [32].

Table 1. Zooplankton samplings (eight vertical stratification samplings between 0–1000 m) at St. K2
Table 1. Zooplankton samplings (eight vertical stratification samplings between 0–1000 m) at S
in the western subarctic Pacific gyre. D: day, N: night.

in the western subarctic Pacific gyre. D: day, N: night.
SeasonSeasonSampling Date

Local Time (Day/Night)

Sampling Date
Local Time (Day/Nigh29 October 2010
12:09–13:52 (D)Autumn29 October
2010(D)
29 October2010
22:09–23:3812:09–13:52(N)
Autumn26 February
2011
12:35–14:4122:09–23:38(D)
29 October
2010(N)
Winter
26 February 2011
22:01–23:56 (N)26 February 201112:35–14:41 (D)22 April 2011
21:59–23:56 (N)WinterSpring26 February
2011(N)
23 April2011
12:45–14:3722:01–23:56(D)
3 July2011
12:05–13:55(D)
22 April 2011
21:59–23:56 (N)Summer
3–4 July 2011
22:51–0:55 (N)Spring
23 April 2011
12:45–14:37 (D)3 July 201112:05–13:55 (D)2.2. Sample Analysis
Summer
3–4sorted
July 2011
In the land laboratory, hydrozoans werefrom the sub-samples22:51–0:55
divided at (N)1/2–1/64 according to the amount of samples. Bell height (BH) and gonad length (GL)ofA.Sample
digitale,Analysis
the numerically and biomass-dominated hydrozoans, were measured at a
2.2.
precision of 0.05 mm by using an eyepiece micrometer under a stereomicroscope (Figure 1).
In the land laboratory, hydrozoans were sorted from the sub-samples divided at
Individuals with more than 10% GL in BH were treated as mature individuals [7,12,16].
1/64Asaccordingtheamountof samples.
Bell ofheight(BH) andgonad
an index oftothe
vertical
distribution,
the depth
the population
center
(D50%length) was (GL) odigitale, thenumericallyandbiomass-dominatedhydrozoans, were measured at a p
calculated
using
the following
formula[30,33].

sion of 0.05 mm by using an eyepiece micrometer under a stereomicroscope (Figur
50 − p1
d1 in+ dBH
Individuals with more thanD10%
GL
2 × were treated as mature individuals [7,12,1
50% =p2
As an index of the vertical distribution, the depth of the population center (D50%)
calculated using the following formula [30,33].
𝐷

%

𝑑

𝑑

50

𝑝
𝑝

where d1 is the depth (m) of the upper depth of the 50% individual occurrence layer,Oceans 2023, 4245

Oceans 2023, 4, FOR PEER REVIEW

4

where d1 is the depth (m) of the upper depth of the 50% individual occurrence layer, d2 isthe sampling depth interval (m) of the 50% individual occurrence layer, p1 is the cumulative
layer. Day-night
diﬀerencesinoccurred
vertical distributions
on eachthancollection
datewere tested
individual
percentage(%) thatat depths shallower
the 50%
individual
by the Kolmogorov-Smirnov
test.
occurrence
layer, and p2 is the individual
percentage (%) at the 50% individual occurrenceof A. digitale
was inexpressedby histograms
basedon the date
integrated
abundance
layer.BH
Day-night
differences
vertical distributions
on eachcollection
were tested
by
−2
the
Kolmogorov-Smirnov
test.
(ind. m ) at 0–1000 m water column for the day and night of each sampling date. The
BH
of A. digitaleofwas
by histogramson the integrated abundance
depth
composition
eachexpressed
BH interval(1 mm) wasbased
also calculated.
(ind. m−2 ) at 0–1000 m water column for the day and night of each sampling date. The
depth
composition of each BH interval (1 mm) was also calculated.
3. Results

3.1.
Hydrography
3.
Results
Vertical distributions of temperature, salinity, dissolved oxygen, and fluorescence at
3.1. Hydrography
eachVerticalsampling
date are shownin Figure 3.
Throughout
the oxygen,season, thedistributionsof temperature,salinity,
dissolved
and temperature
fluorescence wasat each0.7–8.5°C,salinityfor
32.5–34.5,
DOrangedbetween
0.6
and
10.4
mg
L−1, and fluoressampling date are shown in Figure 3. Throughout the season, the temperature◦cence
0.02–2.32.
Seasonal
thermocline
aroundm10.4
in Julywas
at was
0.7–8.5
C, salinity
for 32.5–34.5,
DO developed
ranged between
0.6 50andmg andL−1 , October,andfluorescence
was 0.02–2.32.
Seasonal
thermocline
around50 m inandand temperatures
were almost
constantfor 100 mdevelopedin Februaryand April.
ForJuly
all seasons,
October,and showedtemperatures
were almost
for 100 m in
February
andApril.
For
temperature
a minimumof 1–2constant°C approximately
at 100m, thenhad
a maximum◦ C approximately at 100 m, then hadallseasons,temperature
showedaminimumof
1–2
of about 3.5 °C around 200 m, and finally decreased with increasing depth. Salinity inacreased
maximum
aboutfor3.5all◦ C
aroundSalinity
200 m, andincreasing
withofdepth
seasons.
wasfinallysimilardecreased
for depthswith
below
100 m indepth.
February
Salinity
increased
with
depth
for
all
seasons.
Salinitywassimilarfor
depthsbelow
100m
and April, while was below 33 at <50 m, forming surface halocline in July and October.
in February and April, while was below 33 at <50 m, forming surface halocline in Julyand−1
DO decreased with increasing depth and was extremely low, less than 2 mg L below 200
October. DO decreased with increasing depth and was extremely low, less than 2 mg L−1
m depth. Fluorescence was high at the surface layer above the thermocline (<50 m) in July
below 200 m depth. Fluorescence was high at the surface layer above the thermocline
and October and at 0–100 m in February and April.
(<50 m) in July and October and at 0–100 m in February and April.
Fluorescence

6

10 12

0

2

2.0

0.0

0.5 1.0

0

2

4

8

0.0

0.5

1.0 1.5

0

2

4

6

32.5
10

33.0

33.5

34.0

4

6

8

10 12

1.5

2.0 2.5

0

2

4

6

8

1.0

1.5

2

4

6

33.0

33.5

10 12

0

2

2.0

0.0

0.5

1.0

0

2

4

33.0

33.5

4

6

8

10 12

DO(mg L-1)

2.5

0.0

0.5

2.5

1.5

2.0

2.5

Temperature (℃)

8

0

2

4

6

8

0

8

6

8

Salinity

Depth (m)29 Oct. 201034.5 32.5

33.0

33.5

34.0 34.5

26 Feb. 2011

32.5

34.0

22 Apr. 201134.5 32.5

34.0

34.5

3 July 2011

100

1000

Figuresalinity,
dissolved
oxygen,andandfluorescenceat St.at
K2St. K2
Figure 3.
3. Vertical
Verticaldistribution
distributionofoftemperature,temperature,salinity,
dissolved
oxygen,fluorescencein theoccasionsfrom
October2010
to July
2011.
NoteNotethat thatthe vertical
the subarctic
subarcticPacificPacificgyre
gyreononfour
four
occasionsfrom
October2010
to July2011.
the verticalscale
scale (depth)(depth)isisininthe
thelogscale.
logscale.

3.2. Aglantha digitale

3.2. Aglantha digitale

Hydrozoans occurred in the western subarctic Pacific throughout the year. A. digitale
Hydrozoans occurred in the western subarctic Pacific throughout the year. A. digitale
was the most abundant species, with an annual mean abundance of 198.4 ind. m−2 at−2
was themmost
species, withan annual
mean abundanceof 198.4
0–1000waterabundant
column, composedof 91.9%of hydrozoan
abundance (Table2). ind. m at 0–1000 m water column, composed of 91.9% of hydrozoan abundance (Table 2).
The day-night vertical distribution and D50% of A. digitale at each sampling date areshown in Figure 4. The vertical distribution of A. digitale was concentrated at 0–200 m bothday and night for most seasons. While in October, the certain population density was seen
to extend below 300 m both day and night. The highest population density of A. digitale
was 1.36 ind. m−3 at 100–150 m depth during a night in February. D50% of A. digitale was atOceans 2023, 4

3–5 mm and 8–17 mm were observed for both day and night in April. In July, the majority
of individuals was at the BH in 8–17 mm both day and night. Most of the mature specimens, GL composed >10% of the BH, occurred only in July. The BH of the mature individuals ranged from 4.7 to 17.6 mm, with most of them was at >10 mm.
Concerning the vertical distribution composition of each BH of A. digitale, the 246
distribution below 300 m was seen in October for all BH sizes, indicating that the extension ofvertical distribution down to the deeper layer was a typical feature of all BH ranges (Figure5).2.In
February,
the modal
BHofindividuals
at 8–16mm BH
were column
distributed
near
Table
Annualmean standing
stockscnidarian species
for 0–1000
m waterat St. K2
in thesurface
both
day
and
night,
while
othersmallerandlargerindividuals
weredistributed
the western subarctic Pacific from October 2010 to July 2011. Values are mean ± SD.
at deeper layers. In April, small individuals with BH < 6 mm were distributed below 300
Standing Stockm, whileFamily
most the individuals
with a BH > 12 mm were distributed
below 100 m. In July,
Species−2(ind. m at
) >200 m, but at(%)
individuals with BH smaller than 6 mm were distributednight, the main
Aglantha
digitale
individuals with BH between
8 and
16 mm were concentrated for the surface layer at 0–
198.4 ± 107.8
91.9
Rhopalonematidae
Muller, 1776
50 m.
Other Cnidaria (including fragments difficult
to make species identification)

17.4 ± 10.1
8.1
Table 2. Annual mean standing stocks of cnidarian species for 0–1000 m water column at St. K2 inthe western subarctic Pacific from October 2010 to July 2011. Values are mean ± SD.

The day-night vertical distribution and D50% of A. digitale at each sampling date areStanding Stockshown
in Figure 4. The vertical Species
distribution of A. digitale was concentrated
at 0–200 m both
Family−2)(ind.
m
day and night for most seasons. While in October, the certain population density(%)
was seen
to extend below 300 mAglantha
both daydigitaleand night.
The highest population density of A. digitale
Muller,Rhopalonematidae
198.4 ± 107.8
91.9
was 1.36 ind. m−3 at 100–150 m depth
1776 during a night in February. D50% of A. digitale was at
26–129 mdifficult
depth throughand nightof all seasons.17.4
Diel±change
Other Cnidaria (including fragments
to makeday
species
identification)
10.1 in vertical distribution
8.1
was observed in July, with significantly shallower depths at night (p < 0.05).

Figure(solid)vertical
distributionof ofAglathadigitaleat St.
K2 in
Figure 4.
4. DayDay(open)(open)and
andnight
night(solid)vertical
distribution
Aglathadigitaleat St.
K2thein westernthesubarctic
Pacific
gyreduringfour
sampling
occasions(October
2010,
February,
April,
andJuly
2011).
western subarctic Pacific gyre during four sampling occasions (October 2010, February, April, andDistribution
cores(D50%) are shown by the triangles. Diel changes were tested by the KolmogorovJuly 2011). Distribution cores (D50% ) are shown by the triangles. Diel changes were tested by the
Smirnov
test (*: p < 0.05).
Kolmogorov-Smirnov
test (*: p < 0.05).

Histograms on BH of A. digitale and their vertical distribution composition both day
and night at each sampling date are shown in Figure 5. The BH of A. digitale ranged
between 2.4 and 18.9 mm. In October and February, the most numerous individuals wereseen for the BH at 8–16 mm both day and night. On the other hand, two modes of BH at
3–5 mm and 8–17 mm were observed for both day and night in April. In July, the majority
of individuals was at the BH in 8–17 mm both day and night. Most of the mature specimens,
GL composed >10% of the BH, occurred only in July. The BH of the mature individuals
ranged from 4.7 to 17.6 mm, with most of them was at >10 mm.

Oceans2023,
4, FOR
Oceans2023,
4 PEER REVIEW

247 6

FigureHistograms
bellheightsofofAglantha
Aglanthadigitale
digitaleintegrated
integratedover
over0–1000
0–1000 m
m waterwater column
column at
Figure5. 5.
Histograms
onon
bell
heights
St.inK2thein thewesternsubarctic
Pacific
gyreduringthe
thedayday (upper)(upper) andfour
St.atK2
westernsubarctic
Pacific
gyreduringand nightnight(lower)(lower)ofofthethefoursampling
occasions(October(October2010,2010,February,
February, April,
April, andcompositions
sampling
occasionsand JuneJune2011).
2011).Depth
Depthdistribution
distribution
compositions
withintheeight
columnisisalso
alsoshownshownforforeacheachpanel.
withintheeightdepth
depthstrata
strataof
of0–1000
0–1000 m
m water column
panel.

Concerning the vertical distribution composition of each BH of A. digitale, the distri4. Discussion

bution below 300 m was seen in October for all BH sizes, indicating that the extensionof vertical distribution down to the deeper layer was a typical feature of all BH ranges
At St.5).
K2,
digitale was
the predominanthydrozoan,
accounting
more than
90%(FigureIn A.
February,
the modal
BH individuals
at 8–16 mm
BH werefor
distributed
nearof thethesurfacehydrozoan
abundance(Table2).otherA. digitalea cosmopolitan
species
widelydistribboth day
and night,
while
smallerisandlarger individuals
weredistributedat deeper
In areas
April, insmallwith BH < 6[2,4,13].
mm weredistributedon
below
uted
at highlayers.
latitude
the individuals
Northern Hemisphere
Information
abun300 m,
while
the individuals
BH > 12 mm
werebelow 100m. In
dance,
BH,
BH mostof mature
specimens,withandageneration
timeof distributed
A. digitale reported
from
varJuly,
individuals
with BH smaller
than 3.
6 mm
weredistributed>200m, but atof
night,
theious
locations
are summarizedin TableIn thepresent
study,atthe
abundance
A. digitale
main individuals
with
BH391.1
betweenand
16 mmwere concentrated
for the surface
layer wellat
−2 forrangedbetween 58.5
andind.8m
the 0–1000
m water column.
This value
0–50m.
corresponds with the values reported in the subarctic Pacific (368 ind. m−2) [10] and the4.1. Abundance of A. digitale

northeastern
North Pacific (38–221 ind. m−2) [11]. As for the marginal areas of the western
4. Discussion
subarctic
Pacific,ofvalues
in the Oyashio region during spring (16–316 ind. m−2) [8] and val4.1. Abundance
A. digitaleues based on the annual sampling in the Oyashio region (55–896 ind. m−2) [7] are also
At St. K2, A. digitale was the predominant hydrozoan, accounting for more than 90% ofcomparable.
For the areas with similar values of A. digitale abundance in this study (<100the hydrozoan abundance (Table 2). A. digitale is a cosmopolitan species widely distributed−2), the Norwegian fjords (Korsfjord and Fanafjord) [14] and the Arctic Ocean [15]ind.
mat high latitude areas in the Northern Hemisphere [2,4,13]. Information on abundance, BH,
areBH
available.
the otherandhand,high abundancesof A. reported
digitale overind.locations
m−2 haveof matureOn
specimens,
generation
time of A. digitalefrom1000
variousbeenreported forinToyama
inpresent
the southernJapan
Sea (maximum:4427
ind.betweenm−2) [12],are summarized
Table 3. Bay
In thestudy, theabundanceof A. digitale
ranged−2) [18] and the White Sea (5000 ind. m−2)
−2 forAtlantic
the58.5
Irish
them
North
(5350
ind. mandcoast
391.1inind.
the 0–1000
m watercolumn.
This value well corresponds with
−2 ) [10] and theembayment[19]
A characteristicof these
regions
themsemi-enclosed
the(Table
values3).
reportedin the subarctic
Pacific(368 isind.
northeasternhavingNorth aPacificwater(38–221ind. m−2with) [11].
Asouter
for themarginal
areas
ofsuggest
the western
Pacific,
limiting
exchangetheregion.
These
factsthat subarctic
the semi-enclosed
valuesthe Oyashio
region(16–316m−2 ) [8]withoutand values
based on thebyarea
mayinhavemaintained
a during
higher spring
population
ofind.
A. digitaletransportation−2 ) [7] are also comparable. For
annualsampling
intheOyashioregion(55–896ind.
mflushing discharge caused by the ocean currents. In summary, the abundance of A. digitaleof A.
digitaleopenabundancein thisthestudy(<100transportind. m−2 ),wouldthe−2 for theis thelessareas
thanwith
1000similar
ind. mvalues
oceanic
area where
current
Norwegianfjords(Korsfjord
andFanafjord)
[14]
and
the
Arctic
Ocean
[15]
are
available.
prevent to accumulation of high density/abundance. While in the−semi-enclosed
embay2 have been reported
On
the
other
hand,
high
abundancesofA.
digitale
over
1000
ind.
m
−2
ment condition, A. digitale can maintain high density/abundance−(>5000
ind. m ) underfor Toyama Bay in the southern Japan Sea (maximum: 4427 ind. m 2 ) [12], the Irish coast
low flushing and transport to the otherregion.
−2−2
in the North Atlantic (5350 ind. m ) [18] and the White Sea (5000 ind. m ) [19] (Table 3).
A characteristic of these regions is the semi-enclosed embayment having a limiting waterexchange with the outer region. These facts suggest that the semi-enclosed area may haveOceans 2023, 4

248

maintained a higher population of A. digitale without transportation by flushing discharge
caused by the ocean currents. In summary, the abundance of A. digitale is less than 1000 ind.
m−2 for the oceanic open area where the current transport would prevent to accumulationof high density/abundance. While in the semi-enclosed embayment condition, A. digitale
can maintain high density/abundance (>5000 ind. m−2 ) under low flushing and transport
to the other region.
Table 3. Regional comparison on abundance, bell height, and generation length of Aglantha digitalefrom worldwide ocean.
RegionToyama Bay,
southern Japan Sea
Eastern/Western
subarctic PacificOyashio region
Oyashio region
northeastern North
Pacific
Northern PacificSouthern Irish
coastal waterNortheast Atlantic
Ocean
Korsfjord andFanafjord
White Sea
High-Arctic coastal
Western Subarctic
Pacific (K2)

Sampling

Bell Height (mm)SeasonDepth (m)Abundance(ind. m−2 )Range

MatureGeneration
Length (year−1 )Reference

Annual0–500

73–4427

1–17

6–17

2

[12]

Summer

0–150

0–368

–

8.5–15.2–[10]AnnualSpring0–2000<200

55–89616–316

1–23
4–18

11–23
–

1
1

[7]
[8]

Summer0–150

38–221

0.6–17

1.1–16–[11]

Summer

<200

–

5–20

15<

1

[9]

Summer

0–25

<5350

–

–

–

[18]

Autumn/winter

0–100

–

1–18

–

–

[17]

Annual

0–640

156–358

–

–

2

[14]

AnnualAnnual

0–100
0–180

5–5000
<720

–
–

8–12
–

1
–

[19]
[15]

Annual0–100058.5–391.1

2.4–18.9

4.7–17.6

1This study

4.2. Vertical Distribution of A. digitale
Vertical distribution of A. digitale was concentrated at <200 m for most seasons. Seasonally, diel changes in vertical distribution were seen in July when the thermocline developed,
and deeper distribution (>300 m) was observed in October (Figure 5). In July, it should be
noted that the day-night differences in abundance were substantially low at night and nosize fraction less than 8 mm at night-histogram. It can be concluded that there is a spatial
horizontal heterogeneity in the distribution of medusae. While diel changes in vertical
distribution were denied in this study, nocturnal ascent diel vertical migration of A. digitale
has also been reported from the Saanich Inlet off Vancouver [9]. The deepening vertical
distribution of A. digitale has also been reported in the fjords of Svalbard from August to
October [15]. These findings correspond with the results of this study.
As a new finding of this study, the depth distribution at each BH was determinedwith season and day/night. Small individuals (<6 mm BH) were distributed for the
deep layers or extremely shallower depths in all seasons (Figure 5). These facts suggestthat small individuals with less swimming ability could be easily transported verticallyfrom the vertical mixing and diffusion of water masses. Swimming behaviors of six
hydrozoan species, including A. digitale, are highly varied with species, and A. digitale
is considered to be a jet-swimming species [24,34]. Within the three hydrozoan species
applying jet-swimming, A. digitale is the smallest body size and has the longest jet intervalin time [24]. These facts indicate that A. digitale is most affected by vertical and horizontal
water diffusion, especially for their small-sized specimen, which has less swimming ability.
These low swimming abilities of the small individuals of A. digitale would be difficult tostay in a stable layer because of the vulnerability of the diffusion of the water masses. It
induces an extremely shallower or deeper distribution of them.

Oceans 2023, 4

249

The main prey item of A. digitale is reported to be small copepods such as Pseudocalanus [20,22,24]. For Pseudocalanus in the western subarctic Pacific, two species: P. minutus
and P. newmani are present [35]. Within them, P. minutus accumulates lipids in their bodyand is known to have a resting (diapausing) stage at the deep layer during its life history,
and their descent to deep-sea achieved summer to autumn [35,36]. Since the diapausing
P. minutus at the deep layer contains much lipids, their nutrition values would be high,and the swimming behavior of dormant copepods is reduced to maintain a low metabolic
rate [37,38]. These characteristics of the deep-sea dormant P. minutus (small body size, highnutritional value, and low swimming behavior) suggest that they are a sufficient prey item
for A. digitale. Thus, the extension of the vertical distribution of A. digitale to the deep layer
during October can be explained from viewpoint of their food availability (e.g., to capture
nutrient-rich P. minutus distributing deep layer during these seasons).
4.3. Population Structure and Body Size of A. digitale
The BH range of A. digitale observed in this study (2.4–18.9 mm) well corresponds
to those reported in Toyama Bay in the southern Japan Sea [12], in the spring Oyashio
region [8], in the northeastern North Pacific [11], and in the northeastern North Atlantic [17](Table 3). It should be noted that most of the listed studies applied similar mesh sizes tothis study (200–335 µm); thus, differences in the applied mesh size would be negligible.
Concerning BH, large BH (up to 20 mm) have been reported from the Saanich Inlet off
Vancouver and annual observations in the Oyashio region [7,9]. For such a subarctic coastal
area, the abundance of small copepods, the primary prey of A. digitale, has been reported
to be high [39]. These facts suggest that favorable food conditions would be an importantfactor in achieving large body sizes of A. digitale.
The minimum maturation size of A. digitale: 6 mm BH has been reported in Toyama
Bay, southern Japan Sea [12]. Such a small mature specimen of A. digitale (8–12 mm BH)
has also been reported in the White Sea [19]. Common characteristics of these areas withsmall maturation sizes of A. digitale are that these areas are semi-enclosed seas having highabundances of them (>1000 ind. m−2 ) (Table 3). The feeding mode of A. digitale is basicallycarnivorous [13,20,23,24]. The energy transfer for such a higher trophic level organism isconsidered to be higher in the areas where the marine ecosystems are composed of simply
limited species [40,41]. The regions where high abundance and small maturation bodysize of A. digitale Toyama Bay and the White Sea are characterized by semi-enclosed seas,
having such high energy transfer efficiency food web and marine ecosystem structures
composed by the limited species [12,19]. Thus, in the areas where the marine ecosystem iscomposed of the simple species structure and high energy transfer efficiency to the higher
trophic level organisms, abundance of A. digitale would be high, and they may mature atsmaller body-sizes. In this study, the observed minimum maturation size of A. digitale wassmall as 4.7 mm, while most of the mature specimens were at BH over 10 mm (Figure 5).
These facts suggest that the few small body-sized mature individuals are considered to betransported to the oceanic St. K2 from the marginal areas, such as the Aleutian Islands or
the Okhotsk Sea.
In this study, one or two cohorts were identified for BH of A. digitale on each sampling
date (Figure 5). while because of the scarce sampling occasions (four times per year), it
was difficult to trace the growth of each cohort. For the developmental stages, mature
specimens only occurred in July (Figure 5). These facts suggest that the life history of
A. digitale is a one-year generation length having reproduction in summer for the western
subarctic Pacific. Concerning the life span of A. digitale, one or two generations per year
have been reported in the Oyashio region [7,8], Toyama Bay in the southern Japan Sea [12],Saanich Inlet off Vancouver [9], Norwegian fjords [14], and the White Sea [19] (Table 3).
Thus, the generation time in this study, one year, is an ordinary generation length for
A. digitale in the open oceanic region.
On the other hand, two generations per year of A. digitale have been reported forToyama Bay in the southern Japan Sea and Norwegian fjords (Table 3). These regions areOceans 2023, 4

250

semi-enclosed seas where the energy transfer efficiency to the higher trophic level organisms
is expected to be high. Thus, the abundance, maturation body size, and generation lengthof A. digitale would be related and determined by the component organisms in the marine
ecosystem in each region. In semi-enclosed seas composed of the simple species group,
because of the high energy transfer to hydrozoans A. digitale, they may have high abundanceand small maturation sizes, which implies a shorter generation time. Thus, two generations
per year of A. digitale have seen such areas [12,24]. The major reproductive period summer
observed in this study is also consistent with the life history of this species in the adjacentOyashio region [7]. In these regions, summer is the season when copepods, the main preyof A. digitale, reaches annual peak abundance at the surface layer [35,39]. It is interpreted
that A. digitale may mature and have reproduction under sufficient food conditions during
the summer season.
Author Contributions: Conceptualization, M.A. and A.Y.; methodology, M.A. and A.Y.; software,
M.A.; validation, M.A. and A.Y.; formal analysis, M.A.; investigation, M.A.; resources, M.A.; data
curation, A.Y.; writing—original draft preparation, T.G.; writing—review and editing, A.Y.; visualization, T.G.; supervision, A.Y.; project administration, A.Y.; funding acquisition, A.Y. All authors haveread and agreed 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 from 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.
Conflicts of Interest: The authors declare no conflict of interest.

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

Arai, M.N. Pelagic coelenterates and eutrophication: A review. Hydrobiologia 2001, 451, 69–87. [CrossRef]
Purcell, J.E. Climate effects on formation of jellyfish and ctenophore blooms: A review. J. Mar. Biol. Assoc. U. K. 2005, 85, 461–476.
[CrossRef]
Purcell, J.E. Extension of methods for jellyfish and ctenophore trophic ecology to large-scale research. Hydrobiologia 2009, 616,
23–50. [CrossRef]
Wright, R.M.; Quéré, C.L.; Buitenhuis, E.; Pitois, S.; Gibbons, M.J. Role of jellyfish in the plankton ecosystem revealed using a
global ocean biogeochemical model. Biogeosciences 2021, 18, 1291–1320. [CrossRef]
Pitt, K.A.; Welsh, D.T.; Condon, R.H. Influence of jellyfish blooms on carbon, nitrogen and phosphorus cycling and plankton
production. Hydrobiologia 2009, 616, 133–149. [CrossRef]
Sweetman, A.K.; Chapman, A. First assessment of flux rates of jellyfish carcasses (jelly-falls) to the benthos reveals the importanceof gelatinous material for biological C-cycling in jellyfish-dominated ecosystems. Front. Mar. Sci. 2015, 2, 47. [CrossRef]
Takahashi, D.; Ikeda, T. Abundance, vertical distribution and life cycle patterns of the hydromedusa Aglantha digitale in the
Oyashio region, western subarctic Pacific. Plankton Benthos Res. 2006, 1, 91–96. [CrossRef]
Abe, Y.; Yamaguchi, A.; Matsuno, K.; Kono, T.; Imai, I. Short-term changes in the population structure of hydromedusa Aglantha
digitale during the spring phytoplankton bloom in the Oyashio region. Bull. Fish. Sci. Hokkaido Univ. 2014, 64, 71–81.
Arai, M.N.; Fulton, J. Diel migration and breeding cycle of Aglantha digitale from two locations in the northeastern Pacific. J. Fish.
Res. Board Can. 1973, 30, 551–553. [CrossRef]
Saito, R.; Yamaguchi, A.; Saitoh, S.; Kuma, K.; Imai, I. Abundance, biomass and body size of the hydromedusa Aglantha digitale in
the western and eastern subarctic Pacific during the summers of 2003–2006. Plankton Benthos. Res. 2012, 7, 96–99. [CrossRef]
Shiota, T.; Yamaguchi, A.; Saito, R.; Imai, I. Geographical variations in abundance and body size of the hydromedusa Aglantha
digitale in the northern North Pacific and its adjacent seas. Bull. Fish. Sci. Hokkaido Univ. 2012, 62, 63–69.
Ikeda, T.; Imamura, A. Abundance, vertical distribution and life cycle of a hydromedusa Aglantha digitale in Toyama Bay, southern
Japan Sea. Bull. Plankton Soc. Jpn. 1996, 43, 31–43.

Oceans 2023, 4

13.
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.

251

Pagés, F.; González, H.E.; González, S.R. Diet of the gelatinous zooplankton in Hardangerfjord (Norway) and potential predatory
impact by Aglantha digitale (Tranchymedusae). Mar. Ecol. Prog. Ser. 1996, 139, 69–77. [CrossRef]
Hosia, A.; Båmstedt, U. Seasonal changes in the gelatinous zooplankton community and hydromedusa abundances in Korsfjord
and Fanafjord, western Norway. Mar. Ecol. Prog. Ser. 2007, 351, 113–127. [CrossRef]
Bandara, K.; Varpe, Ø.; Søreide, J.E.; Wallenschus, J.; Berge, J.; Eiane, K. Seasonal vertical strategies in a high-Arctic coastal
zooplankton community. Mar. Ecol. Prog. Ser. 2016, 555, 49–64. [CrossRef]
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]
Williams, R.; Conway, D.V.P. Vertical distribution and seasonal abundance of Aglantha digitale (O.F. Müller) (Coelenterata:
Trachymedusae) and other planktonic coelenterates in the northeast Atlantic Ocean. J. Plankton Res. 1981, 3, 633–643. [CrossRef]
Baxter, E.J.; McAllen, R.; Allcock, A.L.; Doyle, T.K. Abundance, distribution and community composition of small gelatinous
zooplankton in southern Irish coastal waters. Biol. Environ. 2012, 112B, 91–103. [CrossRef]
Pertsova, N.M.; Kosobokova, K.N.; Prudkovsky, A.A. Population size structure, spatial distribution, and life cycle of thehydromedusa Aglantha digitale (O.F. Müller, 1766) in the White Sea. Oceanology 2006, 46, 228–237. [CrossRef]
Prudkovsky, A.A. Trophic role of ambush-foraging hydromedusae in the White Sea. Mar. Ecol. 2013, 34, 153–164. [CrossRef]
Costello, J.H.; Colin, S.P. Prey resource use by coexistent hydromedusae from Friday Harbor, Washington. Limnol. Oceanogr. 2002,
47, 934–942. [CrossRef]
Corrales-Ugalde, M.; Colin, S.P.; Sutherland, K.R. Nematocyst distribution corresponds to prey capture location in hydromedusae
with different predation modes. Mar. Ecol. Prog. Ser. 2017, 568, 101–110. [CrossRef]
Matsakis, S.; Conover, R.J. Abundance and feeding of medusae and their potential impact predators on other zooplankton in
Bedford Basin (Nova Scotia, Canada) during spring. Can. J. Fish. Aquat. Sci. 1991, 48, 1419–1430. [CrossRef]
Colin, S.P.; Costello, J.H. Morphology, swimming performance and propulsive mode of six co-occurring hydromedusae. J. Exp.
Biol. 2002, 205, 427–437. [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 Pacific subarctic and subtropical time-series stations: Highlights of theK2S1 project. J. Oceanogr. 2017, 73, 647–667. [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]
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]
Yokoi, N.; Abe, Y.; Kitamura, M.; Honda, M.C.; Yamaguchi, A. Comparisons between POC and zooplankton swimmer flux fromsediment traps in the subarctic and subtropical North Pacific. Deep-Sea Res. I 2018, 133, 19–26. [CrossRef]
Amei, K.; Jimi, N.; Kitamura, M.; Yokoi, N.; Yamaguchi, A. Community structure and seasonal changes in population structure ofpelagic polychaetes collected by sediment traps moored in the subarctic and subtropical western North Pacific Ocean. Zoosymposia
2020, 19, 41–50. [CrossRef]
Amei, K.; Dobashi, R.; Jimi, N.; Kitamura, M.; Yamaguchi, A. Vertical changes in abundance, biomass and community structure ofpelagic polychaetes down to 1000 m depths at Station K2 in the western subarctic Pacific Ocean covering the four seasons andday-night. J. Plankton Res. 2021, 43, 442–457. [CrossRef]
Yasuda, I. Hydrographic structure and variability in the Kuroshio-Oyashio transition area. J. Oceanogr. 2003, 59, 389–402.
[CrossRef]
Pennak, R.W. An effective method of diagramming diurnal movements of zooplankton organisms. Ecology 1943, 24, 405–407.
[CrossRef]
Colin, S.P.; Costello, J.H.; Klos, E. In situ swimming and feeding behavior of eight co-occurring hydromedusae. Mar. Ecol. Prog.
Ser. 2003, 253, 305–309. [CrossRef]
Yamaguchi, A.; Shiga, N. Vertical distribution and life history of Pseudocalanus minutus and P. newmani (Copepoda; Calanoida) off
cape Esan, southwestern Hokkaido. Bull. Plankton Soc. Jpn. 1997, 44, 11–20.
Yamaguchi, A.; Ikeda, T.; Shiga, N. Population structure and life cycle of Pseudocalanus minutus and Pseudocalanus newmani(Copepoda: Calanoida) in Toyama Bay, southern Japan Sea. Plankton Biol. Ecol. 1998, 45, 183–193.
Ikeda, T.; Hirakawa, K.; Kajihara, N. Some characterristics of a coldwater copepod Calanus cristatus from regions of the Japan Sea
covered by the Tsushima warm current. Bull. Jpn. Sea Natl. Res. Inst. 1990, 40, 51–65.
Ikeda, T.; Sano, F.; Yamaguchi, A. Metabolism and body composition of a copepod (Neocalanus cristatus: Crustacea) from thebathypelagic zone of the Oyashio region, western subarctic Pacific. Mar. Biol. 2004, 145, 1181–1190. [CrossRef]
Ikeda, T.; Shiga, N.; Yamaguchi, A. Structure, biomass distribution and trophodynamics of the pelagic ecosystem in the Oyashio
region, western subarctic Pacific. J. Oceanogr. 2008, 64, 339–354. [CrossRef]

Oceans 2023, 4

40.
41.

252

Lalli, C.M.; Parsons, T.R. Biological Oceanography: An Introduction, 2nd ed.; Butterworth-Heinemann: Burlington, MA, USA, 1997;
p. 326.
Miller, C.B.; Wheeler, P.A. Biological Oceanography, 2nd ed.; John Wiley and Sons: Oxford, UK, 2012; p. 512.

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.