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J. Plankton Res. (2022) 44(3): 443–453. First published online April 23, 2022 https://doi.org/10.1093/plankt/fbac019

Comparison of population structure,vertical distribution and growth of
sympatric, carnivorous, mesopelagic
copepods, Paraeuchaeta glacialis andHeterorhabdus norvegicus, in the western
Arctic Ocean
ATSUSHI YAMAGUCHI

1,2, *, CARIN J. ASHJIAN3 AND ROBERT G. CAMPBELL4

1

graduate school of fisheries sciences, hokkaido university, 3-1-1 minato-cho, hakodate, hokkaido 041-8611, japan, 2 arctic research
center, hokkaido university, kita-21 nishi-11 kita-ku, sapporo, hokkaido 001-0021, japan, 3 biology department, woods hole oceanographic
institution, 266 woods hole rd., woods hole, ma 02543, usa and 4 graduate school of oceanography, university of rhode island,narragansett, ri, 02882, usa*corresponding author: a-yama@ﬁsh.hokudai.ac.jp
Received March 7, 2021; editorial decision March 23, 2022; accepted March 23, 2022
Corresponding editor: Marja Koski

In the Arctic Ocean, the life cycles of interzonal omnivorous copepods have been studied, whereas little information
is available on the life cycles of mesopelagic carnivorous species. Here, the life cycles of two mesopelagic carnivorous
copepods (Paraeuchaeta glacialis and Heterorhabdus norvegicus) are described from vertically stratiﬁed samples collected at anannual ice-station (SHEBA) in the western Arctic Ocean during 1996–1997. Reproduction estimated to occur between
January and March for both species. Vertical distributions and population growth varied between the species. Early
copepodite stages and adult males of P. glacialis were distributed in deeper layers, whereas late copepodite stages andadult females were observed in shallower layers. The skewed sex ratio towards females was observed for adults, which
may be related to the cease feeding and short longevity for adult males. In contrast, all the H. norvegicus life stages were
distributed in the mesopelagic layer. Clear peaks of the young stages and their sequence suggest that H. norvegicus may
complete its life cycle within 1 year. A specialized feeding mode (incorporating a venomous injection spine and large

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ORIGINAL ARTICLE

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2022beak) could be a key trait facilitating the achievement of rapid growth in H. norvegicus in the food-limited mesopelagic
layer.
KEYWORDS: Arctic Ocean; Carnivorous copepods; Growth rate; Life cycle

INTRODUCTIONMETHODS
Zooplankton samples were collected during a Surface
Heat Budget of the Arctic Ocean (SHEBA) expedition(e.g. Ashjian et al., 2003), which drifted through theCanada Basin to the Mendeleev Plain between October
1997 and September 1998 (Supplemental material
1 [Fig. S1]). Stratiﬁed vertical hauls (normally 0–
50 m, 50–100 m, 100–200 m, 200–1500 m and 1500–
2800 m, depending on bottom depth) were madeabove the seaﬂoor at 10–14-day intervals (total 30

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In the Arctic Ocean, seasonal changes in daylight lengthand ice cover inﬂuence the population and activity
dynamics of organisms (Steele and Dickinson, 2016
and references therein). In response to the considerable
seasonal and environmental ﬂuctuations, primary productivity exhibits clear seasonality (Bélanger et al., 2013;
Ji et al., 2013). Mesozooplankton, particularly copepods,
are the major secondary producers in the Arctic Ocean(Kosobokova, 1982; Kosobokova and Hirche, 2000).
Most studies on the life cycles of Arctic copepods havefocused on the large interzonal omnivorous copepods:
Calanus hyperboreus, Calanus glacialis and Metridia longa andhave shown that the life events of these species, such as
reproduction and development, are well synchronizedwith phytoplankton bloom (Conover, 1988; Ashjian et al.,
2003; Søreide et al., 2010). In contrast, information on
the life cycles of mesopelagic copepod species with otherfeeding modes (carnivores or detritivores) is limited.
Two mesopelagic carnivorous copepods, Paraeuchaeta
glacialis and Heterorhabdus norvegicus, are abundant throughout the Arctic Ocean (Kosobokova and Hirche, 2000;
Kosobokova and Hopcroft, 2010; Kosobokova et al.,2011). In the Arctic Ocean, P. glacialis accounts for 1–2%
of mesozooplankton and 1–8% of the copepod biomass(Kosobokova, 1982; Kosobokova and Hirche, 2000;
Kosobokova and Hopcroft, 2010). In addition, P. glacialis
accounts for 3% of the food-item biomass of the Arctic
cod (Boreogadus saida) and is the third most important
copepod prey species, after C. hyperboreus and C. glacialis(Majewski et al., 2016). The year-round presence of eggcarrying females of P. glacialis has been reported (Johnson,1963), in addition to a sex ratio skewed towards females(Dvoretsky and Dvoretsky, 2015). Based on the results ofvertically stratiﬁed sampling activities, P. glacialis males
in the early copepodite and adult stages are abundantat depths of 500 m or greater, and the copepodites
ascend to shallower depths during development from
copepodite stages 1–5 (C1–C5) (Yamaguchi et al., 2019).
Such ontogenetic migration behavior combined withincrement in weight at each stage being greater thanthat for the shallow-depth inhabiting stages suggests thatthe upward ontogenetic migration is associated with theirraptorial feeding and food (prey) availability (Yamaguchi
et al., 2019). Although such information would be valuable

for understanding deep-sea biology, seasonal changes in
the population structure and life cycle of P. glacialis in the
Arctic Ocean are relatively unknown.
H. norvegicus is spread over the entire geographical range of the Arctic Ocean (Kosobokova, 1982;
Kosobokova and Hirche, 2000; Kosobokova and Hopcroft,
2010; Smoot and Hopcroft, 2017). In contrast to P.
glacialis, the adult sex ratio of H. norvegicus is reportedly
skewed towards males (Tokuhiro et al., 2019). Heterorhabdus
species have a specialized mouthpart morphology andfeeding modes. They are capable of injecting venom
via a mandibular tooth and labral glands (Nishida and
Ohtsuka, 1996) and use a large beak in the labrum–
paragnath complex as a feeding apparatus (Lewis, 2014).
Furthermore, H. norvegicus has the smallest eggs amongst
the 14 species whose reproductive behavior and egg
production have been studied in the Arctic Ocean(Kosobokova et al., 2007). The specialized H. norvegicus
feeding mode and egg size characteristics are distinct
from P. glacialis. However, a comparison of the ecology ofthese two species is not researched.
In this study, we quantiﬁed populations and measured
the weights of each stage of P. glacialis and H. norvegicus from vertically stratiﬁed samples collected at an icestation (SHEBA, Ashjian et al., 2003) in the western Arctic
Ocean from October 1996 to September 1997. We aimed
to evaluate and compare the ecological characteristics(population structure, vertical distribution and growth) of
the two sympatric mesopelagic carnivorous copepods in
the Arctic Ocean. Through these data, we calculate thegrowth rates of each species and discuss the mechanismof the sympatric carnivorous copepods to maintain their
population in the mesopelagic layer of the Arctic Ocean.

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ECOLOGICAL COMPARISON OF TWO MESOPELAGIC COPEPODS IN THE ARCTIC OCEAN

seasonal abundance and population structure (Supplemental material 4 [Table S1] and 5 [Table S2]).
The core depth distribution (D50% ) was calculated
based on abundance (ind. m−2 ) in each sampling layer(Yamaguchi et al., 2020):
D50% = d1 + (d2 − d1 ) ×

50 − p1p2

where d 1 is the depth (m) of the upper depth of the
50% individual occurrence layer, d 2 is the maximum
depth (m) of the 50% individual occurrence layer, p1 isthe cumulative individual percentage (%) that occurredat depths shallower than the 50% individual occurrence
layer and p2 is the individual percentage (%) at the 50%
individual occurrence layer. The means and standard
deviations of the D50% of each copepodite stage were
calculated during the polar night (mid-November–earlyFebruary) and the midnight sun (late April–August). The
differences were tested using the Mann–Whitney U -test.
Dates with maximum sampling depths shallower than
900 m or collected during transition periods between
the midnight sun and polar night were omitted from thedescriptions of vertical distributions, retaining three dates
during the midnight sun and six dates during the polarnight (Supplemental material 4 [Table S1] and 5 [TableS2]). Ontogenetic changes in vertical distribution during
the midnight sun and polar night were tested using oneway ANOVA based on the D50% of each copepodite
stage.
Prosome length (PL), wet weight (WW), dry weight(DW) and ash-free dry weight (AFDW) were measured
for each stage using formalin-preserved samples. Copepodite stages were selected and photographed using astereomicroscope. PL was measured in images at a 10μm precision using ImageJ (https://imagej.nih.gov/ij/).
WW was determined for pooled specimens (2–21 individuals of each stage) that had been rinsed brieﬂy in
distilled water, blotted dry on a ﬁlter paper and weighedin a preweighed combusted aluminum pan. P. glacialis
weights were also measured for individual egg sacs andnauplius. Samples were dried in an oven at 60◦ C for
5 h and then reweighed to determine DW. Ash content
was determined by reweighing the same samples after
combusting them at 480◦ C for 5 h. AFDW was thendetermined based on the difference. All weights were
determined to a precision of 1 μg using a CAHN (C33) microbalance. To determine the stages when PL andweight growth occurred, the proportions of growth (PG,%) that occurred at Cn-1 /Cn for PL, WW, DW and
AFDW were determined for females and males, treating
the values of adults as 100% (Yamaguchi et al., 2020):

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sampling dates) using a 1-m2 mouth area opening–closing net equipped with 150-μm mesh (Ashjian et al.,2003). The samples were preserved in 4% bufferedformalin-seawater. Vertical temperature proﬁles werecollected using conductivity-temperature-depth (CTD)
sensors.
We sorted and counted all copepodite stages of P.
glacialis and H. norvegicus in each sample. Morphologicaldifferentiation of females and males was possible forstages C4 to adults in P. glacialis. The females lackswimming leg 5, whereas males have leg 5 in C4–C6(Campbell, 1934). Since sex separation was possible forC4–C6 P. glacialis, their stage composition within each sex
was compared and tested by one-way analysis of variance(ANOVA) and post hoc Tukey–Kramer test. In H.
norvegicus, separation of the sexes was only possible at stage
C6 (See Supplemental material 2 [Fig. S2] [P. glacialis] and3 [Fig. S3] [H. norvegicus] for details of each copepodite
stage). All P. glacialis copepodite stages were observed in
the samples. In the case of H. norvegicus, only stages C3
and older occurred in the samples. Based on the prosome
widths (PWs) of the observed stages and the diagonallengths of the net mesh used (212 μm), we assume theabove-mentioned stages were quantitatively collected(PW of P. glacialis C1 was 335 ± 23 μm [mean ± 1sd,
n = 10], PW of H. norvegicus C3 was 250 ± 29 μm [n = 4]).
Specimens with spermatophores attached in the caseof adult females (C6F) for both species (Supplemental
material 2 [Fig. S2] and 3 [Fig. S3]) were counted separately. In P. glacialis (C6F), egg-carrying individuals werealso observed and counted separately. For egg sacs, thesubstantial numbers with detached were observed in thesamples. However, since we did not quantify the detached
egg sacs in the samples species identiﬁcation via egg sacs
was uncertain.
Sympatric sibling species, Paraeuchaeta barbata and Paraheterorhabdus compactus, occurred in the samples for eachspecies. Because the sibling species had relatively fat body
shapes, their PWs were larger than those of P. glacialis andH. norvegicus at the same stages, especially in C1–C3. In
addition, their occurrence at greater depths in the watercolumn conﬁrmed their species identity.
Seaﬂoor depth was in the 352–3850-m range over the
year-long drift (Ashjian et al., 2003). The number of depth
intervals sampled on each date changed from two to eight(Supplemental material 4 [Table S1] and 5 [Table S2])
partially because of the variation in seaﬂoor depth. As
P. glacialis and H. norvegicus are primarily found at depths
greater than 250 m (see below, Fig. 4a), samples collected
at depths shallower than 400 m were not considered,
reducing the number of available sampling dates to 20
from an original 30. The successive dates obtained wereseparated by at most 1 month, permitting analysis of

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Table I: Sex ratio (% of females in total adult)
of Paraeuchaeta glacialis and Heterorhabdus
norvegicus based on year-round (1997–1998)
observations at ice station SHEBA in the western Arctic Ocean
SpeciesStage

59.4 ± 3.9
59.3 ± 3.7
81.9 ± 6.1
44.1 ± 11.3

Values are annual mean ± standard error (SE). Note that sex separation was possible for C4–C6 in P. glacialis but only for C6 in H.
norvegicus.

marked by the symbols of the solid triangles in Figs. 1 and3. The exact dates of applied dates for each copepodite
stage are shown in Supplemental material 4 (Table S1)
and 5 (Table S2).

RESULTS
Population structure
P. glacialis
Fig. 1. Paraeuchaeta glacialis. Seasonal abundance of copepodite stages
in the western Arctic Ocean. Females and males were distinguishable at
C4–C6. Values in the parentheses and horizontal broken lines indicate
the annual mean abundance of each stage. Three arrows in the top
panel indicate timings of water mass changes (cf. Ashjian et al. 2003).
For calculation of growth rate, the abundant periods of C1–C3 (greaterthan means) were marked with solid horizontal lines and indicatedtheir middle dates by solid triangles. For the consecutive C4, their peakabundance date marked with solid triangle was also used for the growthrate calculation.

PG = 100 × (value of Cn –value of Cn-1 )/value of adult(C6).
Based on the individual DW and abundant date ofeach copepodite stage, the weight-speciﬁc growth rate (g,day−1 ) was calculated for each species (Hirst et al., 2003):
g = (ln Wt – ln W0 )/t.
where W0 is DW at time zero, Wt is DW at time t and t is
the time in days. The growth rate calculation was madefor C1–C4 of P. glacialis and for C4–C6 of H. norvegicus,of which stages that consecutive traces of the growth ofthe cohorts were possible. For the reached dates of eachcopepodite stage, the middle dates of the abundant period(C1–C3 of P. glacialis and C6 of H. norvegicus) or the peakof each copepodite stage (C4 of P. glacialis and C4–C5
of H. norvegicus) were applied. The applied dates wereClear seasonal abundance patterns were observed foreach stage (Fig. 1). C1 was abundant from February to
July (peaked from April to June), C2 from February toAugust, C3 from May to September, C4 from August to
February and both C5 and C6 were widespread from
May to August. The sex ratio was skewed slightly towards
females in C4 and C5 (females comprised 59.3–59.4%
in the whole population) (Table I) and clearly towards
females in C6 (females comprised 81.9%). For both
sexes, stage composition in C4–C6 was dominated by
C5 (P < 0.0001; one-way ANOVA, P < 0.05; Tukey–
Kramer) (Fig. 2). The abundant seasons of each stage
were similar for both sexes. C4 was abundant during
October to February, C5 from February to September
and C6 from February to July (Fig. 2). Adult females (C6F)
with spermatophores attached were abundant from Julyto August and comprised up to 22% of the total C6F on
11 July. Egg-carrying C6F was abundant from March toJuly and comprised up to 37% of the females on 14 April.
H. norvegicus

Clear seasonal abundance trends were also detected foreach copepodite stage of H. norvegicus (Fig. 3). Stage C3
was generally absent or in low abundance, excluding abrief peak in August; C4 was abundant from December
to March; C5 from January to April and C6 from January

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P. glacialis
C4
C5
C6
H. norvegicus
C6

Annual mean

A. YAMAGUCHI ET AL.

ECOLOGICAL COMPARISON OF TWO MESOPELAGIC COPEPODS IN THE ARCTIC OCEAN

to July. The occurrence of each copepodite stage wasconcentrated in its abundant season, and extremely few
individuals were present in the other seasons. The sex
ratio could only be determined for C6. Females accounted
for only 44.1 ± 11.3% of all adults, which indicated thatmales were dominant at the adult stage. Adult females(C6F) with spermatophores attached accounted up to
25% (11 July) of the total C6F and were abundant during December to August, which corresponded with theseasons of the highest abundance for C6M.

Vertical distribution
The D50% of each copepodite stage of P. glacialis ranged
between 74 m (C5M during the polar night) and 690 m(C6M of the polar night) (Fig. 4). Ontogenetic changes
in D50% were observed for the midnight sun and polarnight periods (P < 0.0001, one-way ANOVA). Stages C1and C6M were most abundant in the deepest layer (500–
750 m), whereas C5F/M was concentrated at the shallowest depths (74–89 m). Differences in D50% between
the midnight sun and polar night periods were observedfor C3 and C6F (P < 0.01, Mann–Whitney U -test). Bothstages showed shallower distributions (108–156 m) during the polar night than during the midnight sun (293–468 m).
The D50% of each copepodite stage of H. norvegicus
ranged between 350 m (C3 at polar night) and 682 m (C5at polar night) (Fig. 4). For H. norvegicus, no ontogenetic
changes were seen for both midnight sun and polar night
periods (P = 0.327–0.927). No temporal changes (midnight sun vs. polar night) were detected for copepodite
stages.

Fig. 3. Heterorhabdus norvegicus. Seasonal abundance of copepodite
stages in the western Arctic Ocean. Values in the parentheses andhorizontal broken lines indicate the annual mean abundance of eachstage. Three arrows in the top panel indicate timings of water masschanges (cf. Ashjian et al. 2003). For the calculation of growth rate, theabundance peaks of C4 and C5 were applied. For C6, the abundant
period was marked with solid horizontal lines and indicated their middle
date by solid triangles. These dates marked with solid triangles were used
for the growth rate calculation.

Growth in length and weight

PG in P. glacialis varied considerably between females andmales (Fig. 5). For females, the largest PG was observed
at C5/C6 (34.0% for PL and 52.4–61.1% for weights). In
contrast, for males, PG at C5/C6 was minor (6.9–22.2%),
and the largest PG was observed at C4/C5, especiallyfor weights (67.4–81.2%). In the case of H. norvegicus, PG
was similar between females and males. In both sexes, thelargest PG was observed at C5/C6, in the 28.5–30.8%
and 67.9–79.3% ranges for PLs and weights, respectively.
The detailed data on the PL, weights (WW, DW,
AFDW) and length–weight regressions are presented inTables II (P. glacialis) and Table III (H. norvegicus). Weights(Y : WW, DW, AFDW, μg) and PL (X : mm) had highly
signiﬁcant relationships, expressed as power functions(Y = a Xb ) (r2 = 0.961–0.996, P < 0.001), with b ranging
between 2.859 and 3.070 (P. glacialis) or 2.995–3.594 (H.
norvegicus).
Growth rate

Based on DW, the g of P. glacialis was calculated for C1–
C4 stages during April to November as 0.011 (Fig. 6). On
the other hand, the g of H. norvegicus was calculated forC4–C6 during January to April as 0.035, which was muchhigher than that of P. glacialis.

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Fig. 2. Paraeuchaeta glacialis. Seasonal abundance and proportionalchanges in C4, C5 and C6 for females (upper) and males (middle).
Seasonal abundance of egg carrying and spermatophore-attached adultfemales (C6F) (bottom).

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Fig. 5. Paraeuchaeta glacialis (left) and Heterorhabdus norvegicus (right). The proportion of growth (PG) in PL, WW, DW, AFDW as a percentage of theC6 values based on stage.

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Fig. 4. Paraeuchaeta glacialis (left) and Heterorhabdus norvegicus (right). Ontogenetic changes in the mean vertical distribution centres (D50% , symbols)
during the midnight sun (open symbols) and polar night (solid symbols). The mean temperatures during the midnight sun (solid line) and polarnight (dotted line) are shown in the right panel. Asterisks indicate signiﬁcant day–night differences (∗∗ P < 0.01; Mann–Whitney U -test).

A. YAMAGUCHI ET AL.

ECOLOGICAL COMPARISON OF TWO MESOPELAGIC COPEPODS IN THE ARCTIC OCEAN

Table II: Paraeuchaeta glacialis. Summarized data of PL, WW, DW and AFDW
Developmental stage

PL (mm)Egg
Nauplius

Constant (a)Power (b)r2P

DW (μg)

AFDW (μg)

114 ± 10(4)
95.1 ± 5.4(4)
176 ± 16(4)311 ± 23(4)857 ± 34(4)2990 ± 927(6)1935 ± 202(8)10 938 ± 2409
(8)9142 ± 963(8)26 661 ± 2914
(8)
10 710 ± 1817
(8)

44.1 ± 2.0(4)22.7 ± 1.0(4)31.0 ± 1.1(4)
39.6 ± 2.4(4)100 ± 14(4)375 ± 73(6)236 ± 64(8)
1934 ± 445(8)1849 ± 402(8)4965 ± 920(8)2393 ± 391(8)41.6 ± 1.5(4)21.0 ± 1.1(4)28.8 ± 1.2(4)
33.6 ± 2.4(4)80.0 ± 11.8(4)290 ± 46(6)231 ± 72
(8)
1802 ± 201(8)1724 ± 394(8)3784 ± 613(8)2215 ± 365
(8)

WW-PL

DW-PL

AFDW-PL

119.4
2.859
0.990
<0.0001

14.96
3.070
0.969
<0.0001

13.27
3.055
0.961
<0.0001

Values are mean ± standard deviation (SD). The number of replicates is in parenthesis. Body allometry was analysed using a power regression
model Y = aXb , where Y is WW, DW or AFDW (μg) and X is PL (mm).

Table III: Heterorhabdus norvegicus. Summarized data of PL, WW, DW and AFDW
Developmental stage

PL (mm)0.80 ± 0.03
(4)C4
1.28 ± 0.05
(10)C5
1.98 ± 0.07
(12)
C6F
2.87 ± 0.12
(10)
C6M
2.77 ± 0.1(10)Regression statistics for body allometry
C3

Constant (a)Power (b)r2P

WW (μg)DW (μg)

AFDW (μg)

54.0 ± 15.4(3)160 ± 31(4)635 ± 46(5)2375 ± 124(5)1975 ± 141(5)3.63 ± 0.50
(3)
15.4 ± 1.4(4)72.1 ± 8.8(5)340.2 ± 48.9
(5)297.2 ± 33.7
(5)

3.42 ± 0.53
(3)
13.6 ± 1.1(4)
63.3 ± 8.3(5)305.2 ± 51.3
(5)
269.2 ± 34.4
(5)

WW-PL

DW-PL

AFDW-PL

90.57
2.995
0.993
<0.001

7.129
3.594
0.996
<0.0001

6.516
3.567
0.995
<0.001

Values are mean ± standard deviation (SD). The number of replicates is in parenthesis. Body allometry was analysed using a power regression
model Y = aXb , where Y is WW, DW or AFDW (μg) and X is PL (mm).

DISCUSSIONLife cycle of P. glacialis
Three changes in the dominant water masses in theupper layer of the SHEBA station have been reported
for 1–2 February, 8–9 June and 23–24 July 1998 (Ashjian

et al., 2003). However, the water mass changes seem tohave minimal effects on the seasonal abundance of eachcopepodite stage of P. glacialis (Fig. 1) due to the potential
deeper distribution of the species. The most prominent
characteristic in the population structure of P. glacialis was
the clear seasonality in the abundance of early copepodite

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1.08 ± 0.04
(10)C2
1.46 ± 0.09
(9)C3
2.08 ± 0.10
(10)
C4F
2.93 ± 0.14
(10)
C4M
2.94 ± 0.20
(9)C5F
4.49 ± 0.23
(10)
C5M
4.43 ± 0.42
(9)
C6F
6.80 ± 0.38
(10)
C6M
4.86 ± 0.38
(10)Regression statistics for body allometryC1

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stages (Fig. 1). Paraeuchaeta spp. has a reproductive mode,
whereby egg sacs contain a limited number of large-sized
eggs, development of the naupliar stages does not require
food and C1 is the ﬁrst feeding stage (Campbell, 1934;
Ikeda and Hirakawa, 1996).
Egg sacs of P. glacialis contain 46–>50 eggs (=clutchsize) and the sizes of the eggs are in the 430–520-μm
range in the Greenland Sea (Auel, 1999, 2004). In the
Arctic Ocean, egg diameter and clutch size of P. glacialis
have been reported to be 475–600 μm (534 ± 35 μm,
mean ± 1sd) and 54–82 eggs (71.7 ± 7.6), respectively(Kosobokova et al., 2007). No information has beenreported for egg and naupliar development in P. glacialis;consequently, we applied the egg hatching time (39.4 days)
and naupliar development time (48.5 days) reported forthe congener Pareuchaeta elongata, which has a similaregg diameter (500–600 μm) and was incubated under0.5◦ C laboratory conditions to estimate its development(Ikeda and Hirakawa, 1996). Notably, the habitat
temperature of P. glacialis was at −1.3–0.7◦ C (Fig. 4a).
Based on the durations above (87.9 days = 39.4 + 48.5),
the reproduction of P. glacialis was estimated to occur
from January to March, about 90 days before the peakof C1 (April–June) (Fig. 1). Based on the year-roundobservation on the population structure collected by themoored sediment trap, clear seasonal recruitment of C1–
C3 stages of P. glacialis was reported for May–July at St.
NAPt in the western Arctic Ocean (Matsuno et al., 2014,2015). These seasonal changes in early copepodite stages
correspond well with those of this study (April–June,
Fig. 1). These facts suggest the synchronized reproduction
timing (January–March) was present for P. glacialis in thewestern Arctic Ocean.
Although January—March was suggested as the
reproductive period, the egg-carrying females observed

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in the SHEBA samples were not consistent with thattiming and had an abrupt peak in April (Fig. 2). Thismay have been due to the detachment of the egg sacsfrom females and loss during sampling or preservation.
Such detachment from P. glacialis C6F occurred evenunder the stereomicroscopic observation (Yamaguchi,
unpublished data). The year-round occurrence of eggcarrying females of P. glacialis has been reported forthe western Arctic Ocean (Johnson, 1963). Notably inthis study, the abundance of the egg-carrying females(between 1 and 7.5 ind. m−2 ) was not high enough,considering the clutch sizes (46–82 eggs per sac), tomaintain the peak abundance of C1 (200 ind. m−2 ) basedon the early mortality in nauplii. The other phenology
demonstrated by our data was that mating occurred from
July to August, conﬁrmed by the high proportion of C6F
with spermatophores attached (Fig. 2). As spermatophore
was difficult to detach (Yamaguchi, unpublished data), we
consider that the suggested mating period (July to August)would be a solid result.
Ontogenetic vertical migration in Paraeuchaeta spp.
is well documented and is characterized by the deep
occurrence of early copepodite stages and developmental
ascent (Campbell, 1934; Morioka, 1975; Ikeda and
Hirakawa, 1996; Yamaguchi and Ikeda, 2002; Yamaguchi et al., 2019). The deeper distribution of the early
copepodite stages may reduce mortality (Yamaguchi and
Ikeda, 2002; Yamaguchi et al., 2019). The developmental
ascent from 690 m (C1) to 74 m (C5) was demonstrated
here for P. glacialis (Fig. 4). Particularly, the vertical
distribution within the stage was shallower at polar night
than at midnight sun, excluding in the case of C6M(Fig. 4). Since visual predation impact is expected to behigh during the midnight sun, the deeper occurrence atthe period may be related to predation avoidance. Arctic
cod have been reported to be key predators of P. glacialis(Majewski et al., 2016). Notably, the shallowest distributed
stage (C5) was the only stage that revealed no differencesin vertical distribution between midnight sun and polarnight (Fig. 4). It may be attributed to the C5 stage being
the active predator facilitating massive growth, especiallyin weight (Fig. 5). For greater growth, the C5 stage
may stay at the shallower depths (74 m), where food isabundant both at midnight sun and at polar night.

Life cycle of H. norvegicus
Because of the species’ long generation length, seasonality
was relatively obscured at the mid- to late-copepodite
stages of P. glacialis. By contrast, clear seasonality wasevident for all observed copepodite stages (C3–C6) of H.
norvegicus, and the abundance of the other seasons was
extremely low for all the stages (Fig. 3), suggesting that450

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Fig. 6. Scatter plots between individual mass (μg DW ind.−1 ) andseason (Julian day) for C1–C4 of Paraeuchaeta glacialis (open squares) andC4–C6 of Heterorhabdus norvegicus (solid circles). The growth rates (g) were
calculated for daily bases. For details, see text.

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A. YAMAGUCHI ET AL.

ECOLOGICAL COMPARISON OF TWO MESOPELAGIC COPEPODS IN THE ARCTIC OCEAN

2014). The seasonal abundance of early copepodite stages(C1–C2) was consistent with that of later stages observedin this study (C3 occurred in August). The dominanceof C6M in the adult population was also consistent withthis study’s observations. In a later study, using 2 yearsof sediment trap data, the life cycle of H. norvegicus wasrevised to show that C1 was most abundant in April–May,
C5 and C6M were dominant in November–February andAugust–October respectively, and reproduction occurredin February–March (Matsuno et al., 2015). The observed
H. norvegicus reproduction during a limited period may bereﬂected in the sharp C3 peak in August in this study(Fig. 3). Together, the ﬁndings suggest that the life cycleof H. norvegicus has a 1-year generation length with themain period of reproduction being from February to
March. The slight differences in abundant seasons (1 or
2 months) of each copepodite stage between the studies
may be caused by the regional differences in phenology(ice cover, peak of primary productivity, zooplankton
abundance and biomass) which varied greatly within the
Arctic Ocean (Søreide et al., 2010; Bélanger et al., 2013;
Ji et al., 2013; Steele and Dickinson, 2016).

CONCLUSIONS
Based on the time-series of year-round, vertical stratiﬁed net tows of zooplankton samples conducted at the
SHEBA ice-station in the Arctic Ocean, ecological characteristics (population structure, vertical distribution andlength and weight growth) were compared for the twodominant sympatric mesopelagic carnivorous copepods(P. glacialis and H. norvegicus). The reproductive timingsof the two species were similar, occurring from January
to March. Vertical distribution and PG between stages
varied between the species. For P. glacialis, early copepodite stages and C6M occurred in the deepest layers, apparently to reduce mortality due to predation byvisual predators. In contrast, for H. norvegicus, all developmental stages occurred in the same mesopelagic layers,
and they exhibited faster growth that seemed to allow
them to have shorter 1-year generation lengths. Although
their habitat (mesopelagic) is characterized by limited
food resources, H. norvegicus had a faster growth rate andshorter generation length. The specialized feeding mode(armored venom injection teeth and large-beak labrum)of H. norvegicus could be essential for achieving such rapid
growth rates in the mesopelagic zone.

ACKNOWLEDGEMENTS
We thank the crew members of the CCGS Des Groseilliers and the
SHEBA project members, especially Harold “Buster” Welch, for451

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H. norvegicus produced one cohort per year with a 1-year
generation length.
For H. norvegicus, the sexes could only be distinguishedat the adult stage. The sex ratio was nearly 1:1 orskewed towards males (Table I). The dominance ofmales in H. norvegicus adults has also been reported
for the western Arctic Ocean based on year-roundsediment trap observations (annual mean C6F: total
C6 = 39.8%) (Tokuhiro et al., 2019). For a congener
species in the western subarctic Paciﬁc (Heterorhabdus
tanneri), the dominance of males (annual mean C6F: total
C6 = 45.3%) has also been reported following year-roundobservation (Yamaguchi and Ikeda, 2000b). A skewed
sex ratio towards males, which has been documented for
Heterorhabdus species from three regions, is a unique characteristic of the genus. In general, various mesopelagic
copepods with a body size similar to that of Heterorhabdus
spp. (e.g. Euchaetidae, Aetideidae, Scolecitrichidae) havedegeneration of feeding appendages and cease feedingat C6M, which may induce short longevity of C6M
and skewed sex ratio to C6F in adults (Yamaguchi and
Ikeda, 2000a, 2002; Yamaguchi et al., 2020). However,Heterorhabdus have functional feeding appendages even at
C6M (Brodsky, 1950) and have longer longevity, which
likely contributes to the skewed sex ratio towards males.
Such longevity enhances the chances of mating andfertilization.
The specialized raptorial feeding modes of Heterorhabdus species are quite distinct from the sympatricParaeuchaeta species (Lewis, 2014). According to Nishida
and Ohtsuka (1996), a specialized feeding mechanism,
wherein venom or anaesthetic is injected from the labralgland pores into the tubular lumen of the mandibular
ventral-most tooth, has been proposed. The labrum–
paragnath complex of Heterorhabdus spp. is beak-likeand has a much larger mouth than other similar sized
copepod species (Lewis, 2014). The much faster growthrate (g = 0.035) of H. norvegicus than that of the sympatricP. glacialis (g = 0.011) may be related to the specialized
feeding modes of Heterorhabdus species (Fig. 6).
The specialized ecology of Heterorhabdus spp. is also
apparent in their reproduction. H. norvegicus shed 93
and 95 eggs freely, with a diameter of 150–157 μm(Kosobokova et al., 2007). Thus, their reproduction would
be characterized by a large number of small-sized eggs. As
most of the deep-sea copepods produce a small numberof large-sized eggs (cf. Marshall, 1979; Herring, 2002),
the reproduction mode of H. norvegicus is anomalous fora mesopelagic species.
From sediment traps moored at St. NAPt in the western Arctic Ocean, H. norvegicus C1 and C2 occurred in
June–July, C6M outnumbered C6F throughout the year
and reproduction occurred in April–May (Matsuno et al.,

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2022

assistance in collecting samples and CTD data. The constructive
comments by the anonymous reviewers were very helpful andgreatly improved the text.

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Kosobokova, K. N., Hopcroft, R. R. and Hirche, H.-J. (2011) Patternsof zooplankton diversity through the depths of the Arctic’s central
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The collection of the samples was supported in part by grants#OCE9707184 to C.J. Ashjian and #OCE9707182 to R.G. Campbell
from the US National Science Foundation. Y. Abe assisted ﬁgure illustration. This work was partially supported by the Arctic Challenge for Sustainability II (ArCS II), Program Grant Number JPMXD1420318865.
This research was also supported by the Environment Research andTechnology Development Fund (JPMEERF20214002) of the Environmental Restoration and Conservation Agency of Japan. In addition, thiswork was partly supported by a Grant-in-Aid for Challenging Research(Pioneering) JP20K20573, and Scientiﬁc Research JP22H00374 (A),JP20H03054 (B), JP19H03037 (B), JP21H02263 (B) and JP17H01483(A) from the Japanese Society for the Promotion of Science (JSPS).

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