Title

Seasonal, regional, and diel changes in the abundance of five large, dominant copepods in the western subarctic Pacific: Insights from Continuous Plankton Recorder surveys

Author(s)Fukai, Yutaka; Chiba, Sanae; Batten, Sonia; Sasaki, Yuka; Matsuno, Kohei; Richardson, Anthony J.; Yamaguchi,
AtsushiCitation

北海道大学水産科学研究彙報, 72(1), 17-26

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2022-08-22

10.14943/bull.fish.72.1.17

http://hdl.handle.net/2115/86613

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bull.fish.72.1.17.pdf

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Hokkaido University Collection of Scholarly and Academic Papers : HUSCAPBull. Fish. Sci. Hokkaido Univ.
72(1), 17-26, 2022.
DOI 10.14943/bull.fish.72.1.17

FUKAI et al. : Large copepods in the Paciﬁc CPR

Seasonal, regional, and diel changes in the abundance of five large,
dominant copepods in the western subarctic Pacific :Insights from Continuous Plankton Recorder surveys
Yutaka Fukai1),2), Sanae Chiba3), Sonia Batten3), Yuka Sasaki4), Kohei Matsuno5),6),Anthony J. Richardson7) and Atsushi Yamaguchi5),6)(Received 21 April 2022, Accepted 10 May 2022)
Abstract   In the marine ecosystem, mesozooplankton, especially large copepods, have an important role both in the mediation of primary production to higher trophic levels and in the transportation of organic materials from the surface to the deep ocean, termed
the biological pump. Continuous Plankton Recorder (CPR) surveys have been used as a long-term monitoring method formesozooplankton over wide geographical areas, including the North Pacific, where a CPR survey began in 2000. In this study,
we used CPR samples collected in the western subarctic Pacific during 2001-2015 to investigate the abundance and population
structure of five large, dominant copepods (Neocalanus cristatus, N. flemingeri, N. plumchrus, Eucalanus bungii and Metridia
pacifica) and evaluate the differences in season, region, and diel scales between species. Significant seasonal changes in abundance and population structure were detected, and these changes were considered to reflect the life history of each species. Regional differences were detected for the three Necalanus species and were considered to be related to sea surface
temperature and food availability. Diel changes in abundance were observed for N. cristatus and M. pacifica, with both species
more abundant near the surface at night suggesting diel vertical migration.
Key words : Continuous Plankton Recorder, Copepods, Eucalanus bungii, Metridia pacifica, Neocalanus spp., Western Subarctic PacificIntroduction
In the marine ecosystem, mesozooplankton, especiallylarge copepods, have an important role both in the mediationof primary production to higher trophic levels and in thetransportation of organic materials from the surface to thedeep ocean, termed the biological pump (Kobari et al.,2003 ; Jónasdóttir et al., 2015). Continuous Plankton
Recorder (CPR) instruments, which are towed by commercial
vessels, have been used in the North Atlantic since 1931 as along term monitoring method for large copepods covering-

wide geographical areas (Batten et al., 2003a ; Richardson etal., 2006). Currently, CPRs are towed in more than sevenareas in the world’s oceans, and these surveys are helping
clarify the effect of climate change on the zooplankton community (Beaugrand et al., 2002 ; Beaugrand and Kirby,2010).
Because CPRs are towed continually, diel changes in abundance of the dominant copepods have been reported in the
North Atlantic, where the majority of CPR samples have beencollected (Hays, 1995a, 1995b ; Hays et al., 1995). Suchdiel changes in abundance have been attributed to diel vertical

1)

Laboratory of Marine Biology, Graduate School of Fisheries Sciences, Hokkaido University(北海道大学大学院水産科学院海洋生物学分野)
2)
Present address : Kushiro Fisheries Research Institute, Hokkaido Research Organization(現所属：北海道立総合研究機構釧路水産試験場)
3)
The North Pacific Marine Science Organization (PICES), Canada(北太平洋海洋科学機関 (PICES), カナダ)
4)
Suidosha Co. Ltd.
(株式会社 水土舎)
5)Laboratory of Marine Biology, Faculty of Fisheries Sciences, Hokkaido University(北海道大学大学院水産科学研究院海洋生物学分野)
6)
Arctic Research Center, Hokkaido University(北海道大学北極域研究センター)
7)
University of Queensland, Australia(クイーンズランド大学 , オーストラリア)
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Bull. Fish. Sci. Hokkaido Univ. 72(1), 2022

migration (DVM) behaviour (Hays et al., 1995). In the
North Pacific, similar CPR surveys began in 2000 (Lindleyand Batten, 2008). Various studies have been conductedusing the Pacific CPR survey data, focusing primarily on thedominant copepods (Batten et al., 2003b ; Batten and Walne,2011 ; Yoshiki et al., 2013 ; Chiba et al., 2015). However,there are no reports on diel changes in abundance based on
the Pacific CPR samples.
The large, dominant copepods in the subarctic Pacific are
Neocalanus cristatus, N. flemingeri, N. plumchrus, Eucalanus
bungii and Metridia pacifica, and they account for more than
77% of the mesozooplankton biomass in this area (Miller etal., 1984 ; Ikeda et al., 2008). Regional differences in life
cycles (e.g., generation length and resting stage) have beenreported for N. flemingeri, E. bungii and M. pacifica between
the western and eastern subarctic Pacific (Kobari and Ikeda,
2001b ; Padmavati et al., 2004 ; Shoden et al., 2005). Sucheast west differences in life cycles are attributed to regional
differences in thermal and food conditions (Shoden et al.,2005). Since the dominant copepods have a wide distribution range throughout the subarctic Pacific, horizontal changes
in the timing of their life histories have been estimated fromphysical oceanographic models (Tatebe et al., 2010), but there
have not been any direct observations on these changes.
CPR tows, which can collect zooplankton samples frequently
and continuously at the sea surface, are a useful tool for evaluating the horizontal differences in the life cycles of these
copepods.
In this study, we investigated the abundance and population
structure of the five large, dominant copepods and evaluatedthe differences in (1) season, (2) region and (3) diel scales
using CPR samples collected in the western subarctic Pacificbetween 2001 and 2015. We evaluated changes in abundance due to the three factors using Generalized Additive
Models (GAMs).

Fig. 1.

-

Sampling locations of the CPR surveys in the western
North Pacific during three seasons (spring [April-May],
summer [June-July], and autumn [September-October])for 2001-2015. Sampling points were separated into
two sectors based on longitude (155°E) : the Oyashio
region and the Western Subarctic Gyre.

et al., 2003a ; Richardson et al., 2006). The local time ofeach sample collection was recorded as field collection data,with a binary response for day and night based on sunrise andsunset times. Following collection, each continuous tow
was divided into discrete samples, each representing 18.5 km(10 nautical miles) of tow. The sampling points in Fig. 1
indicate the mid points of the discrete samples. The fivedominant copepods (N. cristatus, N. flemingeri, N. plumchrus,
E. bungii and M. pacifica) in each sample were identified andcounted to species level and copepodite stage using a microscope. Abundance was represented by the number of individuals per sample (ind. sample 1).
--

Environmental data and statistical analyses
We used satellite derived sea surface temperature (SST)data for 2000 2011 from Chiba et al. (2015) and chlorophylla (chl a) concentration data for 2000 2009 from Chiba et al.
(2012) to represent environmental data for each region andseason. SST was summarized by season and region, and chl
a was classified into month and region. Regional differences in SST and chl a between each season or month were
evaluated using the Mann Whitney U test.
Using GAMs, we evaluated the effects of season, region
and local time on the abundance of the five large dominant
copepods. Within the analysis, the abundance of the fivecopepods was used as a response variable, and seasons(spring, summer and autumn), regions (OY and WSG), andcollection time (local time) were included as explanatory variables. A smoothing spline approximation based on local
time was performed. Because the abundance data contained
many zeros, the scale was converted to log10(X+1), where X isabundance (ind. sample 1) to reduce bias, and used as a-Materials and methods--

Sample collection and enumeration
Zooplankton samples were collected during 2001 2015 by
CPR tows along transects three times annually : spring(April May), summer (June July) and autumn (September
October). The CPR was towed by a merchant ship between
Vancouver and northern Japan. In this study, we analyzed
samples collected in the western subarctic Pacific (40° 54°N,
143°E 174°E) (Fig. 1). For regional classification, we
divided the sampling area into the Oyashio region (OY) westof 155°E and the Western Subarctic Gyre (WSG) east of
155°E (Yoshiki et al., 2013).
The CPR was towed horizontally at a depth of approximately 7 m and collected samples through a 1.27 cm2 square
mouth opening with 270 µm mesh. Collected samples were
fixed in a formalin preservative tank inside the CPR (Batten
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---FUKAI et al. : Large copepods in the Paciﬁc CPR

response variable. All statistical analyses were carried out inR software with the package “mgcv” (version 3.6.2, R Development Core Team, 2017).
Results

spring. In contrast, SST was higher in the OY than in the
WSG during summer and autumn. Chl a ranged from 0.04
to 64.6, and peaked in May for both regions. Chl a was 1.4
2.4 times higher in the OY than in the WSG from February to
April. However, chl a was higher in the WSG in May andhad a pulse like peak.
--Hydrography
Seasonal changes in SST and chl a in the OY and WSG
based on satellite data are shown in Fig. 2. There were significant regional differences in SST between each season andin chl a between each month (p<0.001, Mann Whitney
U test). SST ranged from 0.5 to 16.9°C and continuously
increased from spring to autumn in both the OY and
WSG. SST was lower in the OY than the WSG in--

Abundance and population structure
The mean seasonal abundance of each copepodid stage(C1 C6) of the five dominant copepods at each local time
during 2001 2015 was calculated for the OY (Fig. 3) andWSG (Fig. 4). N. cristatus was abundant in both regions
during spring and summer, and its population structure wasdominated by C5. In every season, the abundance washigher in the WSG than in the OY. N. flemingeri was abundant in both regions during spring, declined in summer, andrarely appeared in autumn. The population structure inspring was mainly composed of C2, with abundance higher in
the WSG than in the OY. N. plumchrus was abundant inboth regions during summer, and its population structure wasdominated by C2. E. bungii was abundant in both regions
during summer and comprised mainly early copepodid stages
such as C1. M. pacifica was abundant in both regions during summer and autumn, and all copepodid stages were present evenly. It should be noted that N. plumchrus, E. bungiiand M. pacifica occurred in the OY in spring but were rare in
the WSG (Figs. 3, 4).
--

GAM analysis

Fig. 2.

Seasonal changes in sea surface temperature (upper) and
chlorophyll a (lower) in the Oyashio region and Western
Subarctic Gyre of the western North Pacific Ocean.
Temperature and chlorophyll a data were derived fromsatellite data (cf. Chiba et al., 2012, 2015). Symbols
and bars represent means and standard errors, respectively. *** : p<0.001, Mann-Whitney U-test.

The results of the GAM analysis that evaluated seasonal
and regional differences in the abundance of the five large
dominant copepods are shown in Table 1. N. cristatus, N.
flemingeri and E. bungii had large seasonal differences, andthey were more abundant in spring and summer than inautumn. N. plumchrus showed no difference between spring
and autumn and was most abundant in summer. M. pacifica
was the only species that was least abundant in spring. Significant regional differences were observed for the three Neocalanus species (Table 1). N. cristatus and N. flemingeri
were more abundant in the WSG, while N. plumchrus wasmore abundant in the OY. The results of the smoothing
spline regression on the relationship between the abundanceof the five large dominant copepods and local time are shownin Fig. 5. Abundances of N. cristatus and M. pacifica hadsignificant relationships with local time, with both species
more abundant at night. N. cristatus, N. flemingeri, N. plumchrus and M. pacifica had seasonal differences in dielchange. Additionally, regional differences were observed
for the diel changes of N. flemingeri, E. bungii and M. pacifica (Fig. 5).

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Bull. Fish. Sci. Hokkaido Univ. 72(1), 2022

Fig. 3.

Mean seasonal abundance of each copepodid stage of Neocalanus cristatus, N. flemingeri, N. plumchrus, Eucalanus bungii,
and Metridia pacifica along with local time in the Oyashio region during 2001-2015. Panels are separated by season. Daylight and dark hours are indicated in top row.
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FUKAI et al. : Large copepods in the Paciﬁc CPR

Fig. 4.

Mean seasonal abundance of each copepodid stage of Neocalanus cristatus, N. flemingeri, N. plumchrus, Eucalanus bungii,
and Metridia pacifica along with local time in the Western Subarctic Gyre during 2001-2015. Panels are separated by season. Daylight and dark hours are indicated in top row.
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Bull. Fish. Sci. Hokkaido Univ. 72(1), 2022
Table 1. Results of the GAMs based on the total abundanceof Neocalanus cristatus, N. flemingeri, N. plumchrus, Eucalanus bungii, and Metridia pacifica
within the season and region. + : positive, − :negative, +/− : p<0.05, ++/−− : p<0.01, +++/−−− : p<0.001, ns : not significant. The estimated smooths for each level of factor are shown in
Fig. 5.
SpeciesN. cristatus
N. flemingeri
N. plumchrus
E. bungii
M. pacifica

SeasonRegion(spring)(summer)(spring)(summer)(summer)(spring)(summer)−− (spring)+++ (WSG)

+++
+++
+++
+++
+++
+++
+++

constantly higher in the OY than in the WSG (Fig. 2). However, since these species in the WSG are in a diapause phaseat depth during spring, they may be less abundant in the WSG
than in the OY (Fig. 4).
Seasonally, abundances of the three Neocalanus species
and E. bungii were high in spring summer (Table 1). All ofthese species undergo diapause in the deep ocean (Miller etal., 1984). In autumn, since the main populations descend to
the deep ocean, abundances of these species were extremely
low (Figs. 3, 4). In contrast, M. pacifica was abundant insummer and autumn (Table 1). M. pacifica has beenreported to have three generations in a year in the Gulf of
Alaska, reproducing in late winter, summer, and autumn(Batchelder, 1985), and two generations per year in the Oyashio region, reproducing in April May and June July (Padmavati et al., 2004). The results of the present study indicatethat M. pacifica occupies the surface layer after the Neocalanus species, then has a diapause phase, and finally descends
to the deep ocean.
-+++ (WSG)−− (WSG)ns-

ns

Discussion-

Seasonality of abundance and population structure

Regional differences in abundance

Seasonal changes in abundance and population structure of
the five large dominant species could be interpreted as areflection of the life cycle of each species. It is well known
that Neocalanus species reproduce in the deep sea, and only
stages C1 C5 appear at the surface (Miller et al., 1984 ;Miller and Clemons, 1988). The growth of N. cristatus andN. flemingeri at shallow depths occurs from winter to spring(Kobari and Ikeda, 1999, 2001b). In contrast, the growth ofN. plumchrus at the epipelagic layer occurs later than that ofN. flemingeri (Tsuda et al., 1999 ; Kobari and Ikeda,
2001a). The results of the present study agree with thesefindings for the three Neocalanus species. Thus, C6 did notoccur in the Neocalanus species, and N. cristatus and N. flemingeri were abundant in spring, while N. plumchrus was morecommon in summer (Figs. 3, 4). Unlike the Neocalanus
species, E. bungii and M. pacifica are known to reproduce atthe surface layer (Miller et al., 1984 ; Batchelder, 1985). In
this study, adults (C6) of E. bungii and M. pacifica were common at the surface layer (Figs. 3, 4).
Three species, including N. plumchrus, E. bungii and M.
pacifica, which were more abundant in summer than inspring, occurred in the OY during spring, and the adults (C6)of E. bungii and M. pacifica were dominant, especially inspring (Figs. 3, 4). In the western subarctic Pacific, it is wellknown that E. bungii and M. pacifica undergo diapause, withdiapause ending and reproduction occurring during phytoplankton blooms in the spring (Padmavati et al., 2004 ;Shoden et al., 2005). Since the magnitude of the spring
bloom is larger in the OY than in the WSG (Okamoto et al.,2010 ; Fujiki et al., 2014), the C6s of both species awakened
from diapause are considered to occur at the surface layer inspring (Fig. 3). Actually, chl a from February to April was

Regional differences were detected for the three Neocalanus species ; N. cristatus and N. flemingeri were more abundant in the WSG, while N. plumchrus was more common in
the OY (Table 1). Notably, the species showing regional
differences in abundance were all Neocalanus spp. In thesubarctic Pacific, Neocalanus copepods are preyed upon bypelagic fishes such as salmon and sardines (Odate, 1994), andare the primary prey for the Pacific saury (Cololabis saira),
which performs a large scale feeding migration to the subarctic region during summer (Taka et al., 1982). Within the
Neocalanus species, N. flemingeri, the abundant species inspring, showed high abundance in the WSG (Fig. 4). Thismight be because the other competitive species (N. plumchrus, E. bungii and M. pacifica) occurred less frequently in
the WSG during spring (Fig. 4).
Meanwhile, the abundance of N. cristatus in the WSG washigh, especially during summer (Fig. 4). This might be areflection of the fact that N. cristatus can feed effectively on
sporadic phytoplankton blooms that occurred in the WSG
during May (Fig. 2). Since the chl a values of these sporadic
phytoplankton bloom were the highest throughout the regionand season (Fig. 2), and large sized chain forming diatoms
are considered to be major taxonomic components (Tsuda etal., 2005a ; Suzuki et al., 2011). N. cristatus is the largest
copepod in the epipelagic zone of the subarctic Pacific andprimarily feeds on large (>20 µm) particles (Liu et al.,2005). These facts suggest that N. cristatus can respondquickly and feed on the pulse like phytoplankton blooms
observed in the WSG (Fig. 2). As a result of effective grazing on these blooms, the growth and survival rates of N. cristatus may be higher, and their abundance in the WSG has thepotential to become much higher than in the OY (Figs. 3,-

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----FUKAI et al. : Large copepods in the Paciﬁc CPR

Fig. 5.

GAM smooths for the effects on the abundance of local time in each season (left) and region (right) for five dominant copepods (Neocalanus cristatus, N. flemingeri, N. plumchrus, Eucalanus bungii, and Metridia pacifica) in the western subarctic
Pacific. Asterisks represent significant seasonal and regional differences in the abundance of each species changing withlocal time. The shaded area marks the 95% CL around the mean prediction. WSG : Western Subarctic Gyre,
OY : Oyashio.
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Bull. Fish. Sci. Hokkaido Univ. 72(1), 2022

4). It has also been reported that the vertical distribution of
N. cristatus changes quickly in response to artificial phytoplankton blooms induced by in situ iron enrichment experiments (Tsuda et al., 2006).
Among the three Neocalanus species, N. plumchrus occurs
at the surface layer later than the other two species and adapts
to higher temperatures during summer (Tsuda et al.,1999 ; Kobari et al., 2001a). The seasonal increase in SST
in the OY was more remarkable than in the WSG (Fig.
2). To avoid higher temperatures, the two other Neocalanus
species are expected to descend to the deep layer much earlier
in the OY. In fact, the abundances of the two other Neocalanus species in the OY were low in summer (Fig. 3). Becauseof the lower abundance of congener species that compete forfeeding, N. plumchrus may have a higher abundance in the
OY during summer. N. plumchrus composes >90% of theprey biomass of the Pacific saury, which performs a feeding
migration around the Kuril Islands during summer (Taka etal., 1982). Thus, the regional differences in the abundanceof the three Neocalanus species can be interpreted as reflections of the thermal and feeding environments of each region.
Diel changes in abundanceDiel changes in abundance were observed for N. cristatus
and M. pacifica (Fig. 5). Both species were commonly moreabundant at night (Fig. 5). These facts suggest that DVM isa major factor in their diel changes in abundance. The
occurrence of DVM is well reported for M. pacifica (Batchelder, 1985 ; Padmavati et al., 2004 ; Takahashi et al.,2009 ; Sato et al., 2011). In contrast, DVM has not beenreported for N. cristatus (Miller et al., 1984 ; Kobari and
Ikeda, 1999 ; Sato et al., 2011). However, several studies
have reported that N. cristatus performs small scale DVM
within the 0 40 m depth range (Tsuda et al., 1993) and small
DVM during iron fertilization experiments (Tsuda et al.,2005b). Since N. cristatus is the largest copepod that occurs
at the surface layer in the subarctic Pacific (Brodsky, 1950), itis thought that large N. cristatus perform DVM to avoid predation by visual predators (e.g., pelagic fishes). However,
because the magnitude of DVM behaviour is expected to besmall, it might be difficult to evaluate this behaviour using
ordinary plankton net samplings, which usually sample
through wide depth ranges. Thus, the small scale DVM
behaviour of N. cristatus could be detected by diel scale continuous samplings from the sea surface (5 7 m depth), such as
pump up sampling (from 5 m depth, Tsuda et al., 1993) or the
CPR tows used in this study.
Among the two species with diel changes in abundance, N.
cristatus showed seasonal differences characterized by alarge scale diel change in spring and summer (Fig. 5). Theseseasonal differences may be because N. cristatus occurs at thesurface in spring and summer and descends to undergo diapause in autumn (Miller et al., 1984). Since N. cristatus

migrates to the deep ocean, there would be no diel differencesin abundance in autumn. For M. pacifica, diel changes inabundance were observed in autumn and in the OY and WSG
regions. These facts suggest that M. pacifica performs amore prominent DVM in autumn when the other large sized
dominant copepods descend to the deep ocean, and its DVM
behaviour is common in both regions.
-

Summary
In this study, we used CPR samples collected in the western subarctic Pacific to evaluate the differences in abundance
and population structure at seasonal, regional and dielscales. Large species specific, seasonal changes in abundance and population structure were detected for the dominant copepods, and these changes were considered to bereflections of the life history of each species. Regional differences were detected for the three Neocalanus species andwere considered to be related to SST and food availability. Diel changes in abundance were observed for N. cristatus and M. pacifica. Since their abundances was commonly
higher at night, these changes were thought to be due to
DVM. DVM has been well reported in M. pacifica, but is
not well known in N. cristatus. Several studies havereported that N. cristatus performs small scale DVM, whichmakes it difficult to evaluate using ordinary net sampling. Since the magnitude of the DVM behaviour of N.
cristatus is small (within 0 40 m), its DVM would be detectable based on continuous samplings from the sea surface (5 7m), such as by pump up collection or CPR samplings.
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Acknowledgements

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We acknowledge the captains and crews of the volunteer
ships, M/V Skaubryn and M/V Qindao, which towed the
CPR, and the analysts who conducted the microscopic observations on zooplankton. This study was supported by a consortium for the North Pacific CPR survey coordinated by theNorth Pacific Marine Science Organization (PICES) and
funded by the North Pacific Research Board (NPRB), Canadian Department of Fisheries and Oceans and the CPR Survey at the Marine Biological Association (formerly Sir Alister
Hardy Foundation for Ocean Science (SAHFOS)). Dr. John
R. Bower (Hokkaido University) kindly provided English
editing which improved the manuscript significantly. 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 and Technology 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 Research̶ 24 ̶

--FUKAI et al. : Large copepods in the Paciﬁc CPR

JP22H00374 (A), JP21H02263 (B), JP20H03054 (B), andJP19H03037 (B) from the Japan Society for the Promotion of
Science (JSPS).
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