TYPE Original Research
PUBLISHED 19 August 2022
DOI 10.3389/fmars.2022.943100

OPEN ACCESSEDITED BY

Daniel J. Mayor,
National Oceanography Centre,
United Kingdom
REVIEWED BY

Kathryn Barbara Cook,
University of Southampton,
United Kingdom
Marianne Wootton,
Marine Biological Association,
United Kingdom*CORRESPONDENCE

Inter-species comparison of the
copepodite stage morphology,
vertical distribution, andseasonal population structureof ﬁve sympatric mesopelagic
aetideid copepods in thewestern Arctic Ocean

Yunosuke Koguchi
makaroni1009@eis.hokudai.ac.jp
SPECIALTY SECTION

This article was submitted toMarine Ecosystem Ecology,
a section of the journal
Frontiers in Marine Science
RECEIVED 13 May 2022
ACCEPTED 28 July 2022

Yunosuke Koguchi 1*, Koki Tokuhiro 1, Carin J. Ashjian 2,
Robert G. Campbell 3 and Atsushi Yamaguchi 1,4
Faculty/Graduate School of Fisheries Sciences, Hokkaido University, Hakodate, Japan,
Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA, United States,
3
Graduate School of Oceanography, University of Rhode Island, Narragansett, RI, United States,
4
Arctic Research Center, Hokkaido University, Sapporo, Japan
1

2

PUBLISHED 19 August 2022
CITATION

Koguchi Y, Tokuhiro K, Ashjian CJ,
Campbell RG and Yamaguchi A (2022)
Inter-species comparison of the
copepodite stage morphology, vertical
distribution, and seasonal population
structure of ﬁve sympatricmesopelagic aetideid copepods in thewestern Arctic Ocean.
Front. Mar. Sci. 9:943100.
doi: 10.3389/fmars.2022.943100
COPYRIGHT© 2022 Koguchi, Tokuhiro, Ashjian,Campbell and Yamaguchi. This is an
open-access article distributed under
the terms of the Creative Commons
Attribution License (CC BY). The use,
distribution or reproduction in otherforums is permitted, provided theoriginal author(s) and the copyrightowner(s) are credited and that theoriginal publication in this journal iscited, in accordance with accepted
academic practice. No use,
distribution or reproduction ispermitted which does not comply withthese terms.

Frontiers in Marine Science

Aetideidae is a calanoid copepod family dominant in the mesopelagic layer ofthe Arctic Ocean for which little ecological information is available because
species identiﬁcation, especially of early copepodite stages, is difﬁcult. In thisstudy, we developed a species identiﬁcation ﬂow for the whole copepodite
stages of ﬁve sympatric aetideid copepods (Chiridius obtusifrons, Gaetanus
tenuispinus, G. brevispinus, Aetideopsis multiserrata, and A. rostrata). Vertical
distributions and seasonal population structures of these species were
evaluated using a year-round sample time-series collected at the drifting ice
station (SHEBA) in the western Arctic Ocean. Combinations of morphologicalcharacteristics (prosome length, cephalosome, and prosome widths) wereused to identify the early copepodite stages to species. Aetideopsis rostrata
was distributed in deep waters (1,032–1,065 m) throughout the year. The otherspecies all were found at 600–700 m during the midnight sun. However,during the polar night, the vertical distributions of each species were distinct,
resulting from ascent, descent, or depth maintenance, indicating seasonalvertical migration which may function to reduce inter-speciﬁc competition
during the polar night when food resources are scarce. Reproduction timing
varied among four aetideid copepods: C.obtusifrons and G. tenuispinus
showed polar night ascent and reproduction at the end of the polar night,
whereas G. brevispinus and A. multiserrata showed descent or depth
maintenance during the polar night and reproduction at the beginning of thepolar night. There was not sufﬁcient data to examine reproduction timing of A.
rostrata. Common for all aetideid species, d15N values of the adult females
indicate more carnivorous feeding modes during the polar night than those in

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the midnight sun. Such vertical distribution and timing of reproduction variation
among these ﬁve aetideid copepods may function to reduce species
competition in the mesopelagic layer of the Arctic Ocean.
KEYWORDS

Aetideidae, sympatric mesopelagic copepods, vertical distribution, population
structure, reproduction, the Arctic Ocean

1 Introduction

condition of the deep Arctic Ocean is homogenous (cold andfresh), coexistence of Aetideidae species is thought to occur byvertical and food segregation (Laakmann et al., 2009a;
Laakmann et al., 2009b; Laakmann and Auel, 2010). Stable
isotopes especially d15N are a useful guide for food preference(Laakmann et al., 2009a; Laakmann et al., 2009b; Laakmann and
Auel, 2010). Mesopelagic copepods are reported to have asubstantial effect on vertical material ﬂux to the deep sea by
feeding on sinking particles and excretion in the form of faecal
pellets (Dilling et al., 1998; Wilson et al., 2010), and aetideid
copepods in the Greenland Sea are reported to consume 40% of
the particulate organic carbon ﬂux that reaches at their habitat
depth (Auel, 1999). These facts suggest that Aetideidae is an
important copepod taxon in the Arctic Ocean, both from species
diversity and vertical material ﬂux perspectives.
A key challenge to conducting an ecological study of
Aetideidae is the difﬁculty of species identiﬁcation, especiallyfor the early copepodite stages (C1–C3). In part, this is because
morphological identiﬁcation keys for each sympatric species
have not yet been created, and the early copepodite stages of
the Aetideidae have been treated as aetideid copepods C1–C3 inprevious studies conducted in the Arctic Ocean (e.g.,
Kosobokova and Hirche, 2000; Auel and Hagen, 2002).
Consequently, little is known about the life history, seasonal
population structure, and timing of reproduction of the aetideid
copepods in the Arctic Ocean. To improve our knowledge of theecology of aetideid copepods, it is necessary to create species
identiﬁcation criteria based on morphological characteristics ofall the copepodite stages.
In this study, we examined a year-round time series ofzooplankton samples collected from the drifting Surface Heat
Budget of the Arctic Ocean (SHEBA) ice station in the western
Arctic Ocean. We conducted morphological identiﬁcation of all
the copepodite stages of ﬁve dominant sympatric aetideid
copepods. We also determined the seasonal changes in thevertical distribution and population structure of these ﬁve
species. We measured d15N of adult females of all aetideid
copepods with midnight sun and polar night for evaluation of
their food preference. We compared the seasonal dynamics of
the ﬁve sympatric aetideid copepods and considered theIn the Arctic Ocean marine ecosystem, the zooplankton
community is an important secondary producer and plays a rolein energy transfer to higher trophic level organisms as well as
mediating vertical material transportation (Lowry et al., 2004;
Wassmann et al., 2006). Copepods are the dominant taxon of thezooplankton community in the Arctic Ocean (Thibault et al.,
1999; Ashjian et al., 2003). Because of seasonal ice coverage,
most information about Arctic Ocean copepod ecology has beenobtained during the summer (under midnight sun conditions)(cf. Laakmann et al., 2009a), and few studies have been
conducted to investigate copepod ecology during the winter(under polar night conditions) (Zhang et al., 2010).
Consequently, ecological and standing stock information about
the Arctic copepods during the winter and their seasonalchanges is scarce. To ﬁll this knowledge gap, we consideredthat zooplankton sampling conducted from the drifting ice
station in the Arctic could facilitate the year-roundobservation of standing stocks, population structure, andvertical distribution of Arctic copepods (Ashjian et al., 2003).
Most of the existing ecological information on Arctic
planktonic copepods is available for surface-dwelling,
numerically dominant copepod species (e.g., Pseudocalanusspp.) and interzonal, particle-feeding copepods that have a
diapause phase at deeper depths (e.g., Calanus spp.). However,the species diversity of copepods is known to be high in the deepsea, especially in the mesopelagic zone (Lee, 2000; Norris, 2000;
Goetze, 2003). The Aetideidae is a family of copepods that
dominates the copepod community in the mesopelagic zone,
and is characterized by a high species diversity (Richter, 1995;
Markhaseva, 1996; Auel, 1999). Members of the Aetideidae are
known to be omnivores or detritivores and are described asopportunistic feeders (Richter, 1995; Auel, 1999; Sano et al.,2013; Sano et al., 2015). The occurrence of species-speciﬁc foodpreferences (Laakmann et al., 2009a; Laakmann et al., 2009b;
Sano et al., 2013; Sano et al., 2015) and species-speciﬁc verticalsegregation within the family (Kosobokova and Hirche, 2000;
Auel and Hagen, 2002; Laakmann et al., 2009a; Smoot andHopcroft, 2017) is well documented. Although the hydrographic

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consequently, the zooplankton collection depth and the numberof layers sampled ranged from 0–100 m to 0–3,500 m and from 2
to 7 layers, respectively. The details of the sampling layer at eachsampling date are available in Ashjian and Campbell (2007). The
zooplankton samples were preserved using 4% bufferedformaldehyde seawater. On each sampling day, watertemperature, salinity, and chlorophyll a (Chl. a) ﬂuorescencevalues were measured for the upper water column (maximum
depth: 300 or 700 m) with a SeaBird SB11 Seacat CTD (SeaBird
Scientiﬁc, Bellevue, WA, USA), equipped with a calibrated
ﬂuorometer. Daylight hours for each sampling day were
calculated based on the latitude of the sampling site (cf.
Brock, 1981).

mechanism of coexistence of these copepod species in themesopelagic layer of the Arctic Ocean.

2 Materials and methods
2.1. Field sampling
Zooplankton sampling was conducted from the drifting
SHEBA ice station from 27 October 1997 to 29 September
1998. Vertical stratiﬁcation samples were collected from 2–7
depth layers over a depth range of 0–3,500 m depth using aclosing net with a 1 m2 mouth area and 150 μm or 53 μm mesh.
The small mesh (53 μm) was used for the shallow samples(<200 m) of the restricted period (February-August 1998).
Samples were collected at 10–14 day intervals (Figure 1). The
SHEBA ice station drifted from the Canadian Basin to theMendeleyev Basin during the one-year sampling period(Ashjian et al., 2003). Because of this drift, the water depth
varied from 352 m to 3,800 m during the sampling period,

2.2. Microscope observations
Using a stereomicroscope, each copepodite stage of the ﬁve
dominant aetideid copepods (Chiridius obtusifrons, Gaetanus
tenuispinus, G. brevispinus, Aetideopsis multiserrata, and A.

FIGURE 1

Location of the zooplankton sampling sites (black circles) along the drift track of the Surface Heat Budget of the Arctic Ocean (SHEBA) ice
station through the Canada Basin to the Mendeleev Plain from 27 October 1997 to 29 September 1998 (cf. Ashjian et al., 2003).

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rostrata) was identiﬁed and enumerated. Based on the presence(male) or absence (female) of a ﬁfth swimming leg, males andfemales were distinguishable for specimens of the C4–C6 stages(hereafter referred to as C4F–C6F and C4M–C6M). We provide
a ﬂow diagram showing species identiﬁcation of the whole
copepodite stages of the aetideid copepods in Table 1.
For species identiﬁcation of stages C4–C6, we used the shape ofthe spine at the end of the thoracic segment (Brodskii, 1950). Since
the shape of the spine was similar for C. obtusifrons and Aetideopsis
spp., we used the number of thoracic segments (three for C.
obtusifrons and four for Aetideopsis) which was identiﬁable fromthe dorsal view as an identiﬁcation guide (Figure 2). For thecongener species, body sizes determined as prosome length (PL)varied: for Gaetanus spp., G. brevispinus was larger than G.
tenuispinus, and for Aetideopsis spp., A. rostrata was larger thanA. multiserrata. Because the spine at the end of the thoracic segment
was not developed in stages C1–C3, we used the cephalosome widtharound the antenna (CWA2) and cephalosome width around the
mandible (CWMd) (Figure 2) as alternative species-identiﬁcation
characteristics for C1–C3. The cephalosome outer margin of
Gaetanus was smooth, whereas the outer margins of Chiridius
and Aetideopsis were expanded around the antenna. Based on thesemorphological features, the C1–C3 copepodite stages wereidentiﬁed to the genus level based on the CWA2: CWMd ratio,

thus, a specimen with a large CWA2: CWMd ratio was identiﬁed as
Chiridius and Aetideopsis, and specimens with a small CWA2:CWMd ratio as Gaetanus. Identiﬁcation of species within a genus
was based on PL. Because the C1–C3 stages of C. obtusifrons and A.
multiserrata were similar in PL and morphology of the outercephalosome margin, we observed the prosome width at the
middle of the prosome (PW) and identiﬁed large PW specimens
as C. obtusifrons and small PW specimens as A. multiserrata. To
deﬁne the size ranges used to discriminate species (Figure 4), the PL,
CWA2, and CWMd were measured for 5–10 individuals of eachcopepodite stage of each species sorted from the most abundantsamples under a stereomicroscope using an eyepiece micrometrewith a precision of 10 μm. For the C1–C3 stages of C. obtusifrons
and A. multiserrata, PW was also measured. For means, standard
deviations, and ranges of each parameter (PL, PW, CWA2, CWMd,
and CWA2: CWMd) at each stage, we provide the data in
Supplementary Tables 1–9.
It should be noted that the identiﬁcation for the juvenile
copepodite stages of this study is not conﬁrmed by molecular
identiﬁcation. Thus, the identiﬁcation should be termed theopen nomenclature term incerta (Horton et al., 2021) toindicate uncertain identiﬁcation (e.g. C. obtusifrons sp. inc., G.
tenuispinus sp. inc., G. brevispinus sp. inc., A. multiserrata sp.
inc., and A. rostrata sp. inc.).

TABLE 1 Flow diagram for species identiﬁcation on juvenile copepodite stages of ﬁve sympatric Aetideidae copepods (Chiridius obtusifrons,
Gaetanus tenuispinus, Gaetanus brevispinus, Aetideopsis multiserrata, and Aetoideopsis rostrata) in the western Arctic Ocean.

StagesObservation point

Figure references

C4–C5•The shape of the spine at end of the thoracic segment (Brodskii, 1950)

2•Number of the thoracic segments in dorsal view2

Three ! C. obutusifrons
Four ! Aetideopsis spp.
•Within the genera, PL was varied with species.

4A

Gaetanus spp.
Large PL ! G. brevispinus
Small PL ! G. tenuispinus
Aetideopsis spp.
Large PL ! A. rostrata
Small PL ! A. multiserrata
C1–C3•Cephalosome outer margin in dorsal view (CWA2: CWMd)

4A

Expanded around the antenna (large CWA2: CWMd)! C. obutusifrons and Aetideopsis spp.
Smooth (small CWA2: CWMd)! Gaetanus spp.
•Within Gaetanus, PL was varied with species.

4A

Large PL ! G. brevispinus
Small PL ! G. tenuispinus•PW was varied with species.

4B

Large PW ! C. obtusifrons
Small PW ! A. multiserrata
Prosome length: PL, cephalosome width around the antenna: CWA2, cephalosome width around the mandible: CWMd, prosome width: PW. For means, standard deviations, and ranges ofeach parameter (PL, PW, CWA2, CWMd, and CWA2:CWMd) in each stage, we provided the data in Supplementary Tables 1–9.

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FIGURE 2

Diagrams showing body size measurements: cephalosome width at antenna (CWA2), cephalosome width at mandible (CWMd), prosome width at
middle of the prosome (PW), and prosome length (PL) for Chiridius obtusifrons (left), Gaetanus tenuispinus (centre) and Aetideopsis multiserrata(right). Scale bar represents 1 mm.

MCS = oi =6162.3. Population structureoi = 1 Ai

The depth topography below the ice station varied
temporally as a consequence of drift, and this determined the
maximum sampling depth on any one sampling day. Because
Aetideidae species are distributed in the mesopelagic layer(Kosobokova and Hopcroft, 2010; Kosobokova et al., 2011),
shallower sampling depths on some sampling days may haveresulted in failure to collect representative samples of the
Aetideidae populations at every sampling site. The likelihoodof this is evidenced by the low abundance of Aetideidae species
at the shallower sampling depths (see Supplementary Tables 10–13). Therefore, we used population structure data of the four
species: C. obtusifrons, G. tenuispinus, G. brevispinus, and A.
multiserrata only from sampling sites where the maximum
sampling depths were greater than 500 m and omitted thedata for the shallower sampling depths (<500 m maximum
sampling depth) (Supplementary Tables 10–13). This resulted
in a reduction in the number of sampling days from 30 to 19;
however, the reduced data set comprised approximately onemonth intervals, except for July 1998. The impact of maximum
sampling depth was most severe for the deepest dwelling species,
A. rostrata, and population structure data collected at depths
shallower than 900 m were omitted for this species(Supplementary Table 14). As a result, time-series data for A.
rostrata were not available from April to July 1998. To reduce
the abrupt changes in the population structure data related tohydrographic and geographical changes, we standardized theabundance data for each copepodite stage by calculating themoving average of three consecutive sampling dates. For eachsampling date, the mean copepodite stage (MCS) was calculatedusing the following formula (Marin, 1987):

Frontiers in Marine Sciencei Aiwhere i is the number of copepodite stages (1 for C1, 6 for C6)
and Ai is the number of individuals at copepodite stage i (ind. m−2).

2.4. Vertical distribution
The vertical distribution core (D50%) where 50% of the
population was distributed, was calculated based onabundances (ind. m−2) in each sampling layer (Pennak, 1943):
D50% ¼ d1 +ðd2 − d1 Þ 

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 p 2 is theindividual percentage (%) at the 50% individual occurrence
layer. The difference in D50% between the polar night andmidnight sun for all copepodite stages of each species wastested using the Mann-Whitney U-test. Differences in D50%
among copepodite stages within a species during the same
period (i.e., during the polar night and during the midnightsun) were tested by one-way ANOVA. In addition, differencesin D50% among species during the same period were tested by
one-way ANOVA and a post hoc test (Tukey-Kramer test). For
the evaluation of D50%, we excluded the sampling dates whenthe maximum depth of collection was shallower than 900 m forall species because Aetideidae species are distributed in the05

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remaining deep waters contained Arctic Intermediate Water andPolar Intermediate Water throughout the year (Ashjian
et al., 2003).

mesopelagic layer. Excluding data based on this criterion, we
analysed six sampling dates for the polar night and threesampling dates for the midnight sun for comparison of thevertical distribution of Aetideidae ( Supplementary
Tables 10–14).

3.2. Morphological characteristics
2.5. d15N value

Scatter plots showing the relationship between the CWA2:CWMd ratio and PL for each copepodite stage of the ﬁve aetideid
copepods are shown in Figure 4A. For all copepodite stages
except C6M, CWA2: CWMd was low (approximately 0.9–1) for
Gaetanus spp., whereas this ratio was high (approximately 1–1.1) for Chiridius and Aetideopsis species. This ﬁnding reﬂected
the morphological difference of the cephalosome outer marginwhich was fused around the antenna in Chiridius and
Aetideopsis species, but smooth in Gaetanus spp. Note thatsome variability was present for CWA2: CWMd ratio, especiallyfor early copepodite stages (C1 and C3). Within the congener
species, PL varied with species, where, for Gaetanus spp., the PL
of G. brevispinus was larger than that of G. tenuispinus, and for
the Aetideopsis spp. the PL of A. rostrata was larger than that of
A. multiserrata. It should be noted that CWA2: CWMd was
similar for C. obtusifrons and A. multiserrata, while someoverlap was present, the PL of C. obtusifrons was larger thanthat of A. multiserrata. For identiﬁcation of C. obtusifrons and A.
multiserrata, the number of thoracic segments was used forstages older than C4. For identiﬁcation of earlier stages (C1–C3)of these species, PW was used, where a large PW distinguished
C. obtusifrons, and a small PW distinguished A. multiserrata(Figure 4B). For means, standard deviations, and ranges of eachparameter (PL, PW, CWA2, CWMd, and CWA2: CWMd) in eachstage, we provide the data in Supplementary Tables 1–9.

For evaluation of food preference, d 15 N value wasmeasured for C6F of each species with polar night andmidnight sun. From the most abundant samples at eachperiod, the batches of C6F specimens (since 5 mg DW was
required for each measurement, 9–18 individuals which variedwith species were set for each batch) were sorted, rinsed with
distilled water then dried in a 60°C oven for ﬁve hours. Dried
samples were ground into a ﬁne powder with a ceramic mortar
and pestle and used for measurement of 15N and 14N by using
an elemental analyzer/isotope-ratio mass spectrometer (FlashEA1112-Delta V Plus He-Flow System, Thermo Fisher
Scientiﬁc, Germany). The measurements were made in
triplicate (three batches). d 15 N was calculated from thefollowing equation:
d

15

N=





15Nsample =14Nsample )=ð15Nstandard =14Nstandard Þ − 1  1000

where 15Nsample and 14Nsample are the values of the samples,and 15Nstandard and 14Nstandard are the values of the standard.
Species differences in d15N values were tested by one-way
ANOVA and Tukey-Kramer test. Temporal changes (polarnight vs midnight sun) within the species were tested byMann-Whitney U-test.

3 Results

3.3. Vertical distribution

3.1 Hydrography

The vertical distribution core (D50%) of each copepodite
stage of the ﬁve studied Aetideidae species during the polar night
and the midnight sun is shown in Figure 5. Within the samestages, signiﬁcant differences in vertical distribution between thepolar night and midnight sun were observed only for C.
obtusifrons C6F (p<0.05, Mann-Whitney U-test). Within thesame season, signiﬁcant differences in vertical distribution
between the copepodite stages of the same species wereobserved only for A. rostrata during the polar night (p<0.05,
one-way ANOVA). Comparisons between species and temporalchanges within species based on the mean D50% of all the
copepodite stages during the polar night and midnight sun are
shown in Table 2. During the polar night, C. obtusifrons and G.
tenuispinus distributed at the shallowest depths (298–381 m),
whereas G. brevispinus and A. multiserrata occurred 300–400 m
deeper (628–791 m), and A. rostrata showed the deepest
distribution (1,065 m). In contrast, during the midnight sun,

Seasonal variations in the daily daylight length, watertemperature, salinity, and Chl a ﬂuorescence determined at the
SHEBA ice station are shown in Figure 3. Based on the daylight
length at the SHEBA ice station, the polar night was demarcatedto have occurred from early November 1997 to early February
1998, and the midnight sun from late April to late August 1998.
The remaining periods were deﬁned as transition periods. The
water temperatures ranged between −1.76 and 0.91°C, and werelower in the shallower water and higher at depth. The salinity
range was 26.60−34.91, being lower near the surface, and thehalocline was observed at a depth range of approximately 100–
200 m throughout the year. The Chl. a ﬂuorescence ranged from0.002 to 4.259 and was high above a depth of 30 m from June toAugust. During the course of the drifting ice station, three water
masses were present for the shallower depths (< 100 m), but the

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FIGURE 3

Seasonal changes in daylength, temperature, salinity, and chlorophyll a ﬂuorescence recorded at the Surface Heat Budget of the Arctic Ocean(SHEBA) ice station as it drifted through the Canada Basin to the Mendeleev Plain from 27 October 1997 to 29 September 1998.

during the midnight sun (p<0.001, Mann-Whitney U-test),
whereas G. brevispinus showed a deeper distribution during
the polar night compared to that during the midnight sun(p<0.01). The deepest dwelling species, the two Aetideopsis
spp., showed no differences in their D50% between the polarnight and the midnight sun (p>0.05).

four of the species: C. obtusifrons, the two Gaetanus spp., and A.
multiserrata distributed at similar depths (within a 100 m
range), and only A. rostrata showed a signiﬁcantly different
distribution (p<0.01), at a depth approximately 300 m deeper
than that of the other species. C. obtusifrons and G. tenuispinus
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A

B

FIGURE 4(A) Scatter plots of the ratio of the cephalosome width at the antenna (CWA2): cephalosome width at the mandible (CWMd) and the prosome
length (PL) for each copepodite stage of the ﬁve Aetideidae copepods dominant in the western Arctic Ocean. The species are: Chiridius
obtusifrons, Gaetanus tenuispinus, G. brevispinus, Aetideopsis multiserrata, and A. rostrata. (B) Scatter plots of prosome width (PW) and prosome
length (PL) for the early copepodite stages of C. obtusifrons and A. multiserrata. F, female; M, male. Dashed lines represent approximate
separation for each species at each copepodite stage. Because the scatter plots for C. obtusifrons and A. multiserrata in (A) were similar,
additional plots were created for these two species in (B).

were lowest when the recruitment of the early copepodite stages
occurred. The lowest MCS value was observed in April–May forC. obtusifrons and G. tenuispinus, whereas it was recorded for G.
brevispinus from January to March, and from February to March
for A. multiserrata. The seasonal timing of early stage copepodite
recruitment corresponded with the peak abundance seasons ofeach species. A common feature of all ﬁve species was a much
lower proportion of C6 individuals in the male populationcompared to that in the female population. The proportion of

3.4. Population structure
Seasonal changes in abundance, copepodite stage
composition, MCS, and the proportion of C4–C6 in the female
and male populations of the ﬁve aetideid copepods studied areshown in Figure 6. The season of peak abundance varied withspecies. The abundance of C. obtusifrons and G. tenuispinus washighest in May, whereas the abundance of G. brevispinus and A.
multiserrata peaked in March. In all species, the MCS values

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FIGURE 5

Ontogenetic changes in vertical distribution of the copepodite stages of the ﬁve Aetideidae copepods dominant in the western Arctic Ocean
during the polar night and midnight sun. Symbols and bars represent means of the distribution centres (D50%) and their standard deviations,
respectively. F, female; M, male. The species are: Chiridius obtusifrons, Gaetanus tenuispinus, G. brevispinus, Aetideopsis multiserrata, and A.
rostrata. Alphabet letters for A. rostrata during the polar night indicate signiﬁcant differences between stages.

3.5. d15N value

females (%) in each copepodite stage (C4–C6) is shown in
Table 3. For all species, females were dominant (56.6%–66.7%)
in the C4–C6 populations, whereas males dominated the C4 andC5 populations. In all species, the C6 population was
predominantly female (76.3%–97.3%), which may account for
the higher overall proportion of females in the C4–C6 populations.

d15N values of adult females of the aetideid copepods during
the polar night and midnight sun are summarized in Table 4.
During the polar night, d15N values were 14.1–16.4, with thelower values for Gaetanus spp. and higher values for C.
obtusifrons and Aetideopsis spp. During the midnight sun,

TABLE 2 Summary of vertical distribution (vertical distribution core: D50%, mean ± SE) of ﬁve Aetideidae copepods in the western Arctic Ocean
during the polar night and midnight sun.

D50% (mean ± SE)
Polar night

Midnight sun

U-testC. obtusifrons

298 ± 52a609 ± 31a***

G. tenuispinusa

381 ± 49a

662 ± 26***

G. brevispinus

791 ± 22b

695 ± 34a**

A. multiserrata

628 ± 60b

709 ± 43ans

A. rostrata

1065 ± 68c

1032 ± 182b

ns

***

***

Species

one-way ANOVA

Within the species, temporal changes (polar night vs. midnight sun) were tested by the Mann-Whitney U-test. For inter-species comparison, one-way ANOVA and Tukey-Kramer test were
performed for the data within the same period (polar night or midnight sun). Results of Tukey-Kramer tests are shown by the differences in the superscript alphabets. **p < 0.01, ***p <0.001, ns: not signiﬁcant.

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FIGURE 6

Seasonal changes in total abundance, stage composition, and population structure (for C4–C6) of females and males of the ﬁve dominant
Aetideidae copepods in the western Arctic Ocean from 27 October 1997 to 29 September 1998. Mean copepodite stage (white circles) was
calculated for each species for each sampling date. Populations of Aetideopsis rostrata, the deepest dwelling species, were not quantiﬁed
between March and August 1998 because zooplankton collection was restricted to the shallower depths related to drifting of the ice station.
The shallower dwelling species are Chiridius obtusifrons, Gaetanus tenuispinus, G. brevispinus, and Aetideopsis multiserrata.

d15N values were 13.4–15.4 somewhat lower than the polar nightvalues within the species, although there was no signiﬁcantdifference between the polar night and the midnight sun. The
species order in d15N values of the aetideid copepods was thesame for the polar night and midnight sun.

information is available for the vertical distribution of A.
multiserrata, this species is treated as a meso- to bathypelagic
species and was reported to distribute at depths of approximately
500–1,500 m (Richter, 1994; Richter, 1995). Thus, the vertical
distribution ranges of the ﬁve aetideid copepods recorded in thisstudy correspond with the reported vertical distribution depths inprevious Arctic Ocean studies (Figure 5).
Information about the vertical distribution of aetideid copepods
during the polar night is scarce. Moreover, limited information isavailable about the seasonal dynamics of their vertical distribution.
As a notable exception, Richter (1994); Richter (1995) reported that
there are no seasonal changes in the vertical distribution of
Aetideidae in the Greenland Sea. In contrast to this Greenland
Sea ﬁnding, results of the present study indicate that the fourshallower-dwelling aedtideid copepods (C. obtusifrons, G.
tenuispinus, G. brevispinus, and A. multiserrata) showed clear
vertical depth separation during the polar night and exhibitedseasonal vertical migration (Table 2). The coexistencemechanisms of the sympatric sibling copepods in the deep-sea of
the Arctic Ocean are reported to include separation in vertical
distribution and different food preferences (Laakmann et al., 2009a;
Laakmann et al., 2009b; Laakmann and Auel, 2010). In terms of
their feeding modes, the aetideid copepods are considered to beomnivores or detritivores and are reported to perform opportunistic
feeding, utilising passive, sinking, particulate organic matter as theirprimary food sources (Richter, 1995; Auel, 1999; Sano et al., 2013;
Sano et al., 2015). In the western Arctic Ocean, the amount ofpassive, sinking particle organic carbon ﬂux is reported to be highfor the midnight sun during spring to autumn, and low for the polar

4 Discussion
4.1. Vertical distribution
A schematic diagram of the seasonal vertical distributions andreproductive periods of the ﬁve aetideid copepods in the western
Arctic Ocean is shown in Figure 7. During the midnight sun, thefour species with the shallower distributions: C. obtusifrons, G.
tenuispinus, G. brevispinus, and A. multiserrata were distributed atsimilar depths. However, during the polar night, C. obtusifrons andthe two Gaetanus species changed their habitat depths (C.
obtusifrons and G. tenuispinus ascended, whereas G. brevispinus
descended), and their habitat depths were clearly separated during
this period (Table 2). In contrast, the A. rostrata populations were
distributed in deep waters throughout the year. Most of ourknowledge about the vertical distribution of the aetideid copepods
in the Arctic Ocean is derived from the summer season, particularly
August–September; the end of the midnight sun. At this time, C.
obtusifrons was reported to be distributed mainly at depths of 0–
2,500 m, G. tenuispinus at 0–1,000 m, G. brevispinus at 100–2,000
m, and A. rostrata at 200–2,000 m (Kosobokova and Hirche, 2000;
Laakmann et al., 2009a; Smoot and Hopcroft, 2017). Although little

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TABLE 3 Sex ratio (% of females in total population) of the ﬁve
Aetideidae copepods abundant in the western Arctic Ocean during
October 1996 to September 1997.

SpeciesStage

The low MCS values indicated that population recruitment
occurred for each species, and, common to all species, theseasonal timing of the low MCS values corresponded closelywith the seasonal timing of the abundance peak of each species(Figure 6). By combining the timing of recruitment of early
copepodite stages and the time taken for development of the eggs
and nauplii, the seasonal reproduction period of each species canbe estimated (Yamaguchi et al., 2020). Regarding aetideid
copepod reproduction, egg diameters have been reported as
315 ± 10 mm (mean ± 1sd) for G. tenuispinus, 440 ± 66 mm
for G. brevispinus, 290 ± 12 μm for C. obtusifrons, and 270–300
μm (range) for A. rostrata (Kosobokova et al., 2007), and it has
been observed that the development time of early copepod stages
is affected by temperature, food availability, and body size (eggdiameter) (Mauchline, 1998). Because the egg diameters of the
deep-sea aetideid copepods are much larger compared to thoseof the surface-dwelling copepods, their naupliar stages aresuggested to be able to develop without feeding (Kosobokova
et al., 2007). These facts indicate that the development times of
eggs and nauplii could be estimated by two factors: habitat
temperature and body size (egg diameter).
The relationships between temperature and the development
time of early mesopelagic copepod stages with non-feeding
naupliar stages have been reported for Gaetanus variabilis (=Gaidius variabilis) and Paraeuchaeta elongata, which have egg
diameters of 325 ± 11 mm (G. variabilis) and 460 ± 30 mm (P.
elongata) (Ozaki and Ikeda, 1997; Yamaguchi and Ikeda, 2000).
These egg sizes are comparable to those of the aetideid copepods
researched in this study (270–440 μm). Applying publishedBělehrá dek equations for G. variabilis and P. elongata (Ozaki
and Ikeda, 1997; Yamaguchi and Ikeda, 2000) and habitat
temperature of the aetideid copepods in this study: 0.57°C(mean temperature below 300 m; range: −0.23 to 1.07°C,
Figure 3), the development times for eggs and nauplii to reachC1 are estimated to be 67.6–83.1 days. From ﬁeld data, therecruitment of early copepodite stages was observed to be April–
May for C. obtusifrons and G. tenuispinus, January–March for G.
brevispinus, and February–March for A. multiserrata (Figure 6).
Considering the estimated development time of eggs and nauplii(67.6–83.1 days), the reproductive period of each species was
back-calculated as: February–March for C. obtusifrons and G.
tenuispinus, November–January for G. brevispinus, andDecember–January for A. multiserrata (Figure 7). These
reproductive periods corresponded with the timing of thepolar night or occurred during the sunlight recovery season in
the ﬁeld.
Of the factors that determine the timing of copepod
reproduction, food availability is known to be the mostimportant (cf. Mauchline, 1998). At the SHEBA ice station,
increases in phytoplankton and microplankton were reported tooccur from late May to June (Sherr and Sherr, 2003; Sherr et al.,2003). This period corresponds with the growth season of theearly copepodite stages of the aetideid species observed in thisFemales in total (%)(mean ± SD)

Chiridius obtusifrons
C4

48.4 ± 12.8

C5

43.6 ± 13.1

C6

92.9 ± 4.7

Total (C4–C6)

61.6 ± 10.2

Gaetanus tenuispinus
C4

54.3 ± 11.9

C5

42.9 ± 11.3

C6

76.3 ± 15.6

Total (C4–C6)

57.8 ± 13.0

Gaetanus brevispinus
C4

45.6 ± 9.0

C543.4 ± 9.8

C680.7 ± 13.5

Total (C4–C6)

56.6 ± 10.7

Aetideopsis multiserrata
C4

57.6 ± 11.1

C5

46.7 ± 18.2

C6

95.8 ± 4.9

Total (C4–C6)

66.7 ± 11.4

Aetideopsis rostrata
C4

47.7 ± 26.8

C5

35.7 ± 10.6

C6

97.3 ± 3.7

Total (C4–C6)

60.3 ± 13.7

Values are mean ± SD.

night during winter (O’Brien et al., 2006; Honjo et al., 2010). Theseseasonal changes in the amount of sinking particle ﬂux may explain
the seasonal vertical distribution of the sympatric aetideid copepods.
It may be that during the midnight sun, a sufﬁciently highavailability of sinking particles may provide sufﬁcient foodresources to support all four of the aetideid copepods, thus
enabling their distribution and coexistence at similar depths.
However, during the polar night, because of the low amount ofsinking particles available across the depth range, the four copepod
species may separate their habitat depths to reduce competition forfood resources, a dynamic that may function as niche separation.
Vertical separation in habitat depths and preference for carnivory
are reported for the aetideid copepods (Laakmann et al., 2009a;
Laakmann et al., 2009b; Laakmann and Auel, 2010).

4.2. Population structure
In this study, seasonal changes in population structure wereobserved for four of the aetideid copepods, except A. rostrata.

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by G. brevispinus and A. multiserrata. Both these species remained
in deeper waters, even during the polar night, and began
reproducing at the beginning of the polar night (Figure 7),
which was comparatively earlier than for the two shallowerdwelling species. The timing of reproduction of these two
deeper-dwelling species corresponded with the timing in
reproduction of the large-sized copepod Calanus hyperboreus,
which dominates the zooplankton biomass in part of the Arctic
Ocean (Conover and Huntley, 1991; Hirche and Niehoff, 1996;
Ashjian et al., 2003). During the winter to spring period, C.
hyperboreus descends to the mesopelagic layer and sheds
ﬂoating eggs (Conover and Huntley, 1991; Hirche and Niehoff,
1996; Ashjian et al., 2003). To perform raptorial feeding on theeggs and nauplii of C. hyperboreus, the two deeper-dwelling
aetideid copepods, G. brevispinus and A. multiserrata, may
remain at the deeper depths during the polar night in order to
use the abundance of C. hyperboreus eggs and nauplii as theirmain energy source for reproduction. These seasonal trends infeeding modes were evidenced by the d15N values of the aetideid
adult specimens (Table 4). The differences in vertical distribution
and timing of reproduction among the ﬁve sympatric aetideid
copepods observed in this study may function to reduce
interspeciﬁc competition within the resource-limited
mesopelagic layers and could be a key mechanism maintaining
high biodiversity at these depths in the Arctic Ocean.

study (Figure 6). Thus, as an energy source for the initiation of
the reproduction of the aetideid copepods, other food resources
may be important. Although Aetideidae species are known to beomnivorous, the importance of carnivorous feeding has beenreported, especially for the adult stages, and their food isreported to comprise the energy-rich eggs and nauplii of thelarge-sized Calanus copepods, and adults of small-sized
copepods such as Microcalanus and Pseudocalanus species(Richter, 1995; Auel, 1999; Sano et al., 2013; Sano et al., 2015).
These carnivorous feeding modes of the aetideid copepods havebeen conﬁrmed by fatty acid analysis (Laakmann et al., 2009a;
Laakmann et al., 2009b; Laakmann and Auel, 2010). These facts
suggest that the link between food resource availability and theinitiation of reproduction of four of the aetideid copepods
investigated in this study may be related to carnivorous
feeding on small-sized copepods. Since d15N values of adultfemales were higher for C. obtusifrons and Aetideopsis spp. thanthose of Gaetanus spp., the carnivorous feeding modes would be
more pronounced for the former species. And common for all
aetideid copepods, carnivorous feeding modes were morecommon during the polar night than those in the midnightsun (Table 4).
In the present study, the reproduction of the four shallowerdwelling aetideid copepods could be classiﬁed into two types
based on vertical distribution and seasonality (Figure 7). In theﬁrst type of reproduction, exhibited by C. obtusifrons and G.
tenuispinus, both species ascended to shallower depths during thepolar night, and their reproductive period occurred from the endof the polar night into the sunlight recovery period (Figure 7). The
timing of reproduction of these species corresponded with theseasonal population increase of the small-sized and abundant
copepod: Microcalanus pygmaeus (Ashjian et al., 2003). Since M.
pygmaeus is distributed mainly in the upper mesopelagic layer(Auel and Hagen, 2002; Ashjian et al., 2003), the upwardmigration of C. obtusifrons and G. tenuispinus during the polarnight may be an adaptive strategy for prey capture at shallower
depths, which may provide an important energy source to support
their reproduction. The other type of reproduction was exhibited

5 Conclusions
In this study, we developed a set of metrics to aid species
identiﬁcation of early copepodite stages of ﬁve sympatricaetideid copepods (Chiridius obtusifrons, Gaetanus tenuispinus,
G. brevispinus, Aetideopsis multiserrata, and A. rostrata), andevaluated vertical distribution and seasonal population structureof these species using a year-round sample time-series collected at
the drifting ice station (SHEBA) in the western Arctic Ocean.
Combinations of morphological characteristics (prosome length,
cephalosome, and prosome widths) were used to identify the early

TABLE 4 Summary of d15N value (‰, mean ± SE) of ﬁve Aetideidae copepods in the western Arctic Ocean during the polar night andmidnight sun.

d15N (‰, mean ± SE)
Polar night

Midnight sun

U-testC. obtusifrons

15.4 ± 0.1c

14.4 ± 0.1c

ns

G. tenuispinus

14.1 ± 0.1

aa13.4 ± 0.1

ns

G. brevispinus

14.6 ± 0.1b13.8 ± 0.1bns

A. multiserrata

16.4 ± 0.1d

15.4 ± 0.1dns

A. rostrata

15.4 ± 0.0c

14.8c

–

***

***

one-way ANOVA

Within the species, temporal changes (polar night vs. midnight sun) were tested by the Mann-Whitney U-test. For inter-species comparison, one-way ANOVA and Tukey-Kramer test were
performed for the data within the same period (polar night or midnight sun). Results of Tukey-Kramer tests are shown by the differences in the superscript alphabets. ***: p<0.001, ns:
not signiﬁcant.

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FIGURE 7

Schematic diagram showing seasonal changes in vertical distribution and timing of reproduction of four of the dominant Aetideidae copepods inthe western Arctic Ocean. The open, solid, and grey triangles indicate the sampling dates during the midnight sun, polar night, and theirtransition periods, respectively. The shallower-dwelling species are Chiridius obtusifrons, Gaetanus tenuispinus, G. brevispinus, and Aetideopsis
multiserrata.

copepodite stages to species. Aetideopsis rostrata was distributed indeep waters throughout the year. The other species distributed atsimilar depths during the midnight sun, whereas their vertical
distribution varied with species during the polar night.
Reproduction timing also varied among these four aetideid
copepods and occurred at the start or at the end of the polarnight, possibly related to food availability. Seasonal distribution
dynamics and different reproductive periods may reduce interspeciﬁc competition among aetideid copepods in the Arctic Ocean.

Funding
Collection of the samples was supported in part by grants#OCE9707184 to CA and #OCE9707182 to RC from the US
National Science Foundation. This work was partially supportedby the Arctic Challenge for Sustainability II (ArCS II), Program
Grant Number JPMXD1420318865. This research was also
supported by the Environment Research and Technology
Development Fund (JPMEERF20214002) of theEnvironmental Restoration and Conservation Agency of Japan.
In addition, this work was partly supported by a Grant-in-Aid
for Challenging Research (Pioneering) JP20K20573, andScientiﬁc Research JP20H03054 (B), JP19H03037 (B),
JP21H02263 (B), and JP17H01483 (A) from the JapaneseSociety for the Promotion of Science (JSPS).

Data availability statement
The original contributions presented in the study areincluded in the article/Supplementary Material. Further
inquiries can be directed to the corresponding author.

Author contributions

Acknowledgments

YK, KT, CA, RC, and AY designed the study; CA and RC
collected the samples; YK and KT analysed the samples; YK and AY
analysed the data; YK and AY wrote the paper with contributions
from all authors. All authors read and approved the ﬁnal manuscript.

We thank the crew members of the CCGS Des Groseilliers
and the SHEBA project members, most especially Harold“Buster” Welch, for assistance in collecting the samples and
CTD data.

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organizations, or those of the publisher, the editors and thereviewers. Any product that may be evaluated in this article, or
claim that may be made by its manufacturer, is not guaranteedor endorsed by the publisher.

Conﬂict of interest
The authors declare that the research was conducted in theabsence of any commercial or ﬁnancial relationships that could
be construed as a potential conﬂict of interest.

Supplementary material
Publisher’s note
The Supplementary Material for this article can be foundonline at: https://www.frontiersin.org/articles/10.3389/
fmars.2022.943100/full#supplementary-material

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