Journal of
Plankton Research
plankt.oxfordjournals.org
J. Plankton Res. (2013) 35(5): 1035 – 1045. First published online May 24, 2013 doi:10.1093/plankt/fbt050
Temperature-regulated egg production
rate, and seasonal and interannual
variations in Paracalanus parvus
MIN-CHUL JANG1, KYOUNGSOON SHIN1, BONGGIL HYUN1, TONGSUP LEE2 AND KEUN-HYUNG CHOI1*
1
BALLAST WATER CENTER, KOREA INSTITUTE OF OCEAN SCIENCE AND TECHNOLOGY, GEOJE
OCEANOGRAPHY, PUSAN NATIONAL UNIVERSITY, BUSAN
656-834, REPUBLIC OF KOREA AND 2DEPARTMENT OF
609-735, REPUBLIC OF KOREA
*CORRESPONDING AUTHOR: [email protected]
Received March 7, 2013; accepted April 29, 2013
Corresponding editor: Roger Harris
Weekly to biweekly measurements of the in situ egg production rate (EPR) of a dominant warm-temperature copepod (Paracalanus parvus) were made from August 2009
to July 2010 at a coastal station, together with analysis of environmental and food
conditions. In addition, the results of a 10-year survey of P. parvus abundance and environmental parameters are presented. EPR ranged from ,1 to 24 eggs female – 1
day – 1 with a mean of four eggs female – 1 day – 1. The calculated female growth rate
was highest in August at 0.26 day – 1, coinciding with the highest EPR, but growth
was very low in winter (,0.01 day – 1). The EPR and weight-specific female growth
of P. parvus were both strongly related to water temperature, but weakly associated
with chlorophyll-a (Chl-a) concentration. However, large variability was noticed in
the summer (.208C) values of these relationships, with a negative relationship
between EPR and salinity. This seemed to be related to local input, which may
provide heterotrophic food from terrigenous sources. Observed high abundances
during times of extremely low female growth and low EPR suggest that
the populations might be sustained by supplements from offshore, where their
growth condition could be better (e.g. higher water temperature). Future warming
would contribute to a trend of increasing abundance of this copepod, especially of
non-summer populations.
KEYWORDS: egg production rate; Paracalanus parvus; seasonal patterns; female
growth rate; population
available online at www.plankt.oxfordjournals.org
# The Author 2013. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected]
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I N T RO D U C T I O N
Small marine copepods are important mediators in
marine food webs (Hirst and Bunker, 2003; Turner,
2004). They often show a preference for microzooplankton as food, even when suitably sized phytoplankton are
available (Atkinson, 1996; Castellani et al., 2005). Shortand long-term variations in their abundance can have
important impacts on the dynamics of lower trophic
levels. This is important given that many marine environments have been experiencing warming caused by
climate change in recent decades, as warming can
induce long-term changes in copepod abundance and
community composition (Rebstock and Kang, 2003;
Batten and Welch, 2004; Drinkwater, 2006; Hooff and
Peterson, 2006; Wiafe et al., 2008).
Copepod population dynamics are determined
largely by recruitment, which is measured most frequently as the egg production rate (EPR) and hatching
success, which can be limited by factors such as temperature and food quantity and quality (Corkett and
Mcllaren, 1978; Checkley, 1980; Uye and Shibuno,
1992; Kimmerer et al., 2005). The eggs of copepods
are thus an important parameter determining population growth, which shapes the population dynamics of
marine copepods.
Paracalanus parvus s.l. (hereafter P. parvus) is a neritic,
warm water calanoid copepod that broadcasts its eggs. It
is one of the most important particle grazers in terms of
biomass and production rate in many estuarine and
coastal waters (Morgan et al., 2003; Islama et al., 2006;
Sun et al., 2008; Moon et al., 2010; Lee et al., 2011).
Paracalanus parvus ingests ciliates, dinoflagellates and
nanoflagellates in large quantities, in addition to phytoplankton (Suzuki et al., 1999; Wu et al., 2010), resulting in
increased phytoplankton abundance by selectively
ingesting protozoans (Jang et al., 2010). Feeding on
microzooplankton such as ciliates and heterotrophic
dinoflagellates is an important parameter for the EPR of
P. parvus (Vargas et al., 2007). The copepods also form a
primary prey of larger predators such as Sagitta spp.
(Giesecke and González, 2008) and larval fishes (Nielsen
and Munk, 1998; Sánchez-Velasco, 1998). Therefore,
P. parvus forms an important link in carbon flow from
microplankton to higher trophic levels in many temperate marine ecosystems.
Paracalanus parvus is one of the dominant copepods in
the neritic waters of Korea and the northern East China
Sea (Moon et al., 2010). Given its importance in terms of
numerical abundance and trophic impacts on planktonic
food webs, characterizing long-term fluctuations in the
P. parvus population, as well as its reproductive rate in
relation to environmental conditions, is important.
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In this paper, we present weekly or biweekly measurements over one year of P. parvus EPR and female growth
estimates for an estuarine station with an inventory of the
microplankton available as potential food for the
copepod. We also explore a 10-year data set of observations of the population dynamics of P. parvus constructed
from weekly or biweekly surveys conducted at the same
site to characterize their seasonal and interannual dynamics in an estuarine water body.
METHOD
The study was carried out at a station in Jangmok Bay
(348590 3800 N, 1288400 2900 E) on the northern side of
Geoje Island off the southern coast of Korea. The site
connects to the southern shelf waters of Korea, which
have undergone a significant rise in water temperature
over the past decades (at a rate of 0.0248C per year;
MOMAF, 2010). The sampling station is located off a
pier (Fig. 1), where the water has an average depth
of 8.5 m and a mean tidal range of 2.2 m. No river
flows into the bay, but following rainfall, the bay
receives water and suspended solids directly from nearby
mountains.
Egg production rate
Paracalanus parvus females were collected at 7 – 10-day
intervals from August 2009 to July 2010, with a total of
44 collections made for EPR experiments conducted at
the station. In situ measurements of temperature and salinity were also taken using an Ocean Seven 319 CTD
probe (Idronaut). Surface waters from a depth of 1 m
were collected using a Niskin sampler to measure
chlorophyll-a (Chl-a) concentrations, for which 0.5 L of
seawater was filtered through 47-mm-diameter
Whatmanw GF/F glass fiber filters and stored at
2208C for further analysis in the laboratory. Chl-a concentrations were determined fluorometrically (10AU
Fluorometer, Turner Designs) after extraction with 90%
acetone for 24 h in the dark (Parsons et al., 1984).
Microplankton samples were prepared by adding acid
Lugol’s iodine to 250 mL of seawater (5%, final concentration) and storing samples in the dark until analysis.
Subsamples of 50– 100 mL were concentrated in sedimentation chambers for 48 h, and the concentrate
was examined under an inverted microscope (Zeiss
Axioplan2) at 100 to 200.
Live copepods were collected using a conical net
(mesh size 200 mm, mouth diameter 45 cm). Healthy
females were collected and three to five females were
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EGG PRODUCTION RATE OF PARACALANUS PARVUS
Fig. 1. Jangmok Bay and the sampling site (experimental site) showing bottom depth contours (dotted lines).
added to each of triplicate acrylic funnel style containers
(500 mL), with a 45-mm mesh screen at the top and a
200-mm mesh screen attached at the middle, the latter
being used to separate the eggs from females to minimize
egg cannibalism. Eggs that passed through the 200-mm
mesh screen were collected on a 45-mm mesh screen
attached at the bottom of the containers. Post hoc examination of the 200-mm mesh screen showed no eggs
remaining on the screen. The incubation bottles were
held vertically in a larger transparent acrylic container
into which seawater was pumped from below by a diaphragm pump to provide a constant in situ level of food to
the copepods. The experimental chambers were submerged at 1 m depth at the pier. Eggs were recovered
after about 24 h of incubation and examined under a dissecting microscope (Zeiss Stemi SV11) to determine the
number of eggs produced by females.
Calculation of growth rate
Individual carbon weights (Wc, mgC) were calculated
from prosome lengths (PL, mm) using the equation Wc ¼
PL3.128 1028.451 for P. parvus (Liang and Uye, 1996).
Egg volume was converted to carbon assuming perfect
spheres by the relationship 0.14 10 – 26 mgC mm – 3
(Kiørboe et al., 1985; Huntley and Lopez, 1992). The
female growth rate (gf ) was calculated using the equation
gf ¼ (We/Wf ) (24/t), where We is the weight of eggs
produced (mgC), Wf is the weight of the female (mgC)
and t is the incubation time (1 h), with the contribution of
adult males omitted.
Sampling for interannual variation
Copepod and environmental samples were collected
weekly or biweekly from the same station for EPR experiments from January 2001 to December 2010. All
samples were taken only during flood tides to reduce the
effects of tidal variation on abundance. Copepods were
collected using a conical net (200-mm mesh with a 45-cm
diameter mouth) equipped with a digital flowmeter
(Hydro-Bios 438115). The net was towed vertically from
the sea bottom to the surface at 0.5 – 1.0 m s – 1 in triplicate, yielding a total of 1443 samples for copepod analysis. All samples were preserved in situ in buffered
formaldehyde (final concentration 5%). Subsampling
was carried out using a Folsom (Motoda) plankton
splitter, and the copepods were transferred to a
Bogorov– Rass counting chamber and examined under a
stereomicroscope (Zeiss Stemi SV11). Zooplankton
abundance was standardized with the volume of water
filtered and expressed as the number of individuals per
cubic meter (inds m – 3), and a mean value was obtained
from the triplicate samples for each sampling event.
Statistical analyses
Linear simple and stepwise multiple regression analyses
were performed to examine relationships among
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environmental and biological factors. Model selection
was based on Akaike’s information criterion (AIC;
Akaike, 1974). Nonlinear regression analyses (Venables
and Ripley, 2003) were also conducted to examine the
relationships of EPR and long-term copepod abundance
to water temperature and Chl-a concentration.
A seasonal Mann – Kendall test was performed to
evaluate interannual trends in P. parvus and environmental factors at the site. This is a nonparametric test for
identifying trends in time series data, and therefore, the
data need not conform to any particular distribution.
The test compares the relative magnitudes of sample data
rather than the data values themselves (Gilbert, 1987).
Statistical analyses were all performed using a program
developed in R, an object-oriented open-source programming language (R Development Core Team, 2006).
R E S U LT S
Environmental conditions during EPR
experiments
Seasonal variations in water temperature and salinity
showed opposite patterns, typical of a monsoonal temperate region (Fig. 2a and b). Temperature varied widely
from 5.3 to 26.98C, while salinity varied only from 28.4
to 33.2, suggesting that summer seawater dilution due to
freshwater discharge was limited at the site.
Potential copepod prey distribution
The Chl-a concentration varied from 1.0 to 15. 2 mg L – 1,
with high concentrations observed only in summer
(.208C) and low concentrations (,5 mg L – 1) persisting
during non-summer periods (November 2009–June 2010;
Fig. 2c). Summer blooms of phytoplankton were driven by
net-phytoplankton and nano-phytoplankton (Fig. 2c and
d), with pico-phytoplankton contributing a smaller percentage (,20%) of the total observed Chl-a during
August–October 2009 (Fig. 2d). Pico-phytoplankton,
however, often constituted more than half of the total
Chl-a concentration. Overall, the contributions of each
size class of phytoplankton were similar (Table I).
Summer phytoplankton was characterized by the
increased abundance of diatoms and dinoflagellates
(Fig. 2e and f ). Diatoms were the most abundant phytoplankton group (Table I), present at high density in
summer and low density in the winter, rapidly building in
density starting in May to a level similar to that reached
in the previous summer of 2009 (Fig. 2e). Dinoflagellates
showed a summer maximum, occurred at low density
during winter and showed a smaller increase in the
following late spring (Fig. 2f ). Nanoflagellates,
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cryptomonads and crysophycea showed seasonal patterns of several large increases in abundance (Fig. 2g – i).
Generalizing about the temporal abundance patterns
of any of the ciliates was difficult. Oligotrichs were dominant among the ciliates and increased in abundance
during periods of moderate water temperature (10–
208C; Fig. 2j). Tintinnids also appeared with a similar
temporal pattern to that of oligotrichs, peaking in August
(15 000 cells L – 1). Tintinnid abundance was below the
detection limit in winter and spring, reappearing in the
following late spring at around 5000 cells L – 1 (Fig. 2k).
Mesodinium spp. were irregularly but frequently observed
throughout the period, reaching a peak of 8500 cells L – 1
in May 2010 (Fig. 2l).
Patterns of P. parvus parameters
The maximum abundance of P. parvus was around
3700 inds m – 3 in August, but rapidly decreased as the
water temperature declined in fall (Fig. 3a). Except
during November, at around 2000 inds m – 3, P. parvus
abundance was low (,500 inds m – 3) during the cold
seasons until June (mean 167 inds m – 3). Abundance
increased rapidly starting in July when water temperatures exceeded 208C. Copepod biomass closely followed
the seasonal pattern of abundance (Fig. 3b), ranging from
0.1 to 11.0 mgC m – 3, with a mean of 2.1 mgC m – 3.
Female prosome length apparently showed an increasing trend from August 2009 to May 2010, then declined
from April to June by about 30% from its previous level
before rising again toward summer (Fig. 3c). Multiple
regression analysis showed that prosome length was
weakly but negatively associated with water temperature
(P , 0.001, r 2 ¼ 0.32), but not with Chl-a concentration.
More adult females than adult males were observed
during the whole period of the survey, with females comprising from 66 to 99% of the total adult copepod abundance (Fig. 3d). The percentage of females appeared to
be highest in winter and lowest in April. The ratio of
female abundance to that of both male and female
P. parvus combined was weakly positively associated with
salinity (P ¼ 0.005, r 2 ¼ 0.15), but not with temperature
or total Chl-a concentration.
EPR and female growth
The copepods produced eggs throughout the year,
ranging from ,1 to 24 eggs female – 1 day – 1 with a mean
of 4 eggs female – 1 day – 1. EPR reached a maximum of
24 eggs female – 1 day – 1 in August, which was then followed by a sharp decline. Low EPR (,5 eggs female – 1
day – 1) persisted from September through June and elevated EPR of .5 eggs female – 1 day – 1 was observed
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Fig. 2. Weekly/biweekly variation in environmental conditions and biological parameters during P. parvus egg production experiments from August
2009 to July 2010. (a) Temperature (8C), (b) salinity, (c) Chl-a (mg L – 1), (d) relative cumulative contribution of net- (dark), nano- (gray) and
picophytoplankton (white) to total chlorophyll, (e) diatoms (103 cells L – 1), (f ) dinoflagellates (103 cells L – 1), (g) Chrysophycea (103 cells L – 1),
(h) Cryptophycea (103 cells L – 1), (i) nanoflagellates (103 cells L – 1), ( j) Oligotrichs (103 cells L – 1), (k) Tintinnids (103 cells L – 1), (l)
Mesodinium spp. (103 cells L – 1).
only in July and August (Fig. 3e). An examination of randomly selected samples showed that all of the eggs
hatched into nauplii.
The calculated female growth rate also exhibited
strong seasonality, with the highest growth rate estimated
as 0.26 day – 1 in August (Fig. 3f ), coinciding with the
highest EPR. Little growth was detected in winter, with
virtually no growth in January (Fig. 3f ). EPR was strongly
related to water temperature with a pattern of exponential increase, exhibiting greater variability at high temperatures (Fig. 4a). The EPR was highly variable with
increasing Chl-a concentration, notably at .3 mg L – 1,
but appeared to be little influenced by Chl-a concentration (Fig. 4b), with food limitation apparent only at low
food concentrations (e.g. ,2 mg L – 1 of Chl-a). EPR was
not related either to any protozoan abundance, including
those of ciliates or dinoflagellates or to nanoflagellates
(P . 0.05 for all analyses). Female growth rate also
showed an exponential increase with water temperature
(Fig. 4c).
The large variability in summer (.208C) EPR was
further analyzed using a partial regression (Fig. 5). This
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revealed that the summer EPR (eggs female – 1 day – 1)
was negatively related to salinity, when temperature
effects on EPR were held constant ( partial regression,
P , 0.001, r 2 ¼ 0.76). The summer EPR was not
affected either by the abundance of any protozoan or by
Chl-a (P . 0.05 for all analyses).
Seasonal and interannual variations in
copepod abundance
Interannual variations in seasonal changes revealed a
detailed picture of long-term variation in the copepod
population. Temperature showed little variation during
any season over the years (Fig. 6a), showing no significant
Table I: Means and 95% confidence limits for
the microplankton community at the station in
Jangmok Bay
Parameter
–1
Net chl-a (mg L )
Nano chl-a (mg L – 1)
Pico chl-a (mg L – 1)
Diatoms (cells L – 1)
Dinoflagellates (cells L – 1)
Chrysophycea (cells L – 1)
Chryptophycea (cells L – 1)
Nanoflagellates (cells L – 1)
Oligotrichs (cells L – 1)
Tintinnid spp. (cells L – 1)
Mesodinium spp. (cells L – 1)
Mean
Lower
Higher
1.1
0.8
0.7
127 730
14 768
2233
47 783
60 768
5583
4
3
0.8
0.6
0.6
76 551
6752
808
22 937
19 234
3900
1
1
1.6
1.1
0.8
213 123
32 300
6173
99 544
191 990
7993
17
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increase over the 10 years (seasonal Mann– Kendall test,
t ¼ 0.125, P ¼ 0.27; Fig. 6a). Salinity reflected an
increased influence of summer freshwater discharge
(Fig. 6b), decreasing between 2001 and 2003 and then
rising after 2003 (t ¼ 0.125, P ¼ 0.042; Fig. 6b). Chl-a
was generally elevated in the summer from June to
October, but the peak shifted to fall and winter in later
years (Fig. 6c). An interannual increase in Chl-a concentrations was detected (t ¼ 0.157, P ¼ 0.011), with a
rapid increase since 2007. Paracalanus parvus showed high
numbers between July and mid-November (Fig. 6d). No
increasing interannual trend was detected (t ¼ 0.133,
P ¼ 0.06), but winter abundances appeared to have
increased in later years (e.g. the January abundance in
later years; Fig. 6d). Multiple regression analysis revealed
that the copepod abundance, pooled for the 10 years of
observation, showed a positive relationship with water
temperature (r 2 ¼ 0.234, P , 0.001), but not with Chl-a
concentration.
DISCUSSION
Copepod EPR and growth
The EPR and weight-specific female growth of P. parvus
were both strongly related to water temperature (Fig. 4),
but little related to Chl-a concentration. No apparent
diatom inhibition of reproductive capability was observed
as has been found to reduce hatching success in some
copepods that feed on diatoms (Pohnert et al., 2002).
Fig. 3. Weekly/biweekly variations in P. parvus abundance and reproductive parameters during egg production experiments from August 2009 to
July 2010. (a) Abundance (inds m – 3), (b) biomass (mgC m – 3), (c) female prosome length (mm), (d) sex ratio (dark ¼ female; gray ¼ male), (e) EPR
(eggs female – 1 day – 1), (f ) female growth rate (day – 1). Error bars (c and e) represent the standard deviation.
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Fig. 4. Relationships of copepod EPR (a and b) and female growth rate (c) to water temperature and Chl-a concentration.
Fig. 5. Partial regression of the EPR (eggs female – 1 day – 1) onto
salinity for summer (.208C), in which temperature effects on EPR
were held constant.
Cannibalism would have been of limited influence as
the incubation chambers were designed to minimize the
effects of cannibalism on the EPR. These results suggest
that temperature is fundamental to the seasonal dynamics of P. parvus in Jangmok Bay. Such a strong temperature
dependency may be natural given the generally eutrophic
condition of the study site and the warm water
characteristics of the copepod. Food limitation effects on
copepod EPR have generally been reported at low Chl-a
concentrations (Uye and Shibuno, 1992). Significant food
limitation affecting Paracalanus sp. EPR may occur at
Chl-a concentrations ,3 mg L – 1 (Uye and Shibuno,
1992). Kimmerer et al. (Kimmerer et al., 2005) reported
that Acartia hudsonica EPR in San Francisco Bay, USA,
where Paracalanus spp. also maintain a significant biomass
(Ambler, 1985), was food limited at Chl-a concentrations
lower than ,4 mg L – 1.
The weak relationship of EPR with Chl-a observed in
the present study may also result from feeding selectivity.
Small-sized copepod species often show a preference for
microzooplankton, even when suitably sized phytoplankton are available (Atkinson, 1996; Castellani et al., 2005),
suggesting that Chl-a might be a poor predictor of
copepod EPR. The calanoid copepod community was
found to remove only between 0.1 and 27.7% (average,
3.6 + 15.8%) of phytoplankton biomass daily during
grazing experiments in Jangmok Bay (Jang et al., 2010).
Grazing pressure was high in winter and early spring
(January – March: 15.6 – 27.7%), but negative to low in
summer (June – August: – 33.1 to 0.0%) and autumn
(September– November: –1.4 to 5.1%; Jang et al., 2010),
suggesting that copepods might facilitate increases in
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Fig. 6. Ten-year variation in the monthly distribution of (a) water temperature (8C), (b) salinity, (c) Chl-a (log, mg L – 1) and (d) P. parvus abundance
(log10 inds m – 3).
phytoplankton growth by selectively ingesting protozoans. Wu et al. (Wu et al., 2010) showed that in the northern
East China Sea, where Paracalanus spp. are dominant, ciliates and small heterotrophic dinoflagellates (sHDFs)
provide the majority of ingested mesozooplankton
carbon, even when phytoplankton biomass is greater
than that of both heterotroph groups. Suzuki et al. (1999)
similarly demonstrated that Paracalanus spp. feed on
sHDFs and ciliates, with sHDFs providing more than
twice as much food as ciliates do. The feeding of P. parvus
on microzooplankton such as ciliates and sHDFs is important for the EPR of the copepod (Vargas et al., 2007).
Although EPR was not related to the abundance of any
protozoan in the present study, the highly variable EPR
at high water temperatures (.208C), when Chl-a concentrations are highest, might suggest that the EPR
responds strongly to the input of terrigenous materials
from adjacent areas (Figs 1 and 5), which generally
would fuel heterotrophic plankton.
Such a response to terrigenous input may account in
part for the high EPR of this copepod, which had an estimated maximum EPR of 27 + 3 eggs female – 1 day – 1
(Fig. 4b). The EPR of P. parvus in Jangmok Bay is generally
lower than that reported from other bays with similar
food conditions. The annual mean EPR ranges from 7.6
to 11.4 eggs female – 1 day – 1 with a maximum EPR of
60.8 eggs female – 1 day – 1 in Jiaozhou Bay, China (Sun
et al., 2008), and a mean and range of 18 and 2 – 83 eggs
female – 1 day – 1 has been reported from the waters off
southern California, USA (Checkley, 1980). The female
weight-specific growth rate was also similar, but very low
at ,0.01 day – 1, during seasons other than summer.
Copepod sex ratio
The present study shows that the sex ratio of P. parvus was
highly skewed toward females throughout the year
(Fig. 3d). The sex ratio of males to total adults (0.01–0.34)
in the present study is a bit higher or closer to the reported
range (0.1–0.45, with a mean ratio of 0.2) in adult paracalanids in nature (Kiørboe, 2006). Intersexuality is common
in copepods (Fleminger, 1985), intersexual adults of paracalanids being all morphologically similar to normal
females (Gusmão and McKinnon, 2009). This could have
affected the female skewed sex ratio as all intersexes were
counted as females. Generally, food environment is the
most important factor in determining sex ratio of copepods, with higher percentages of males being obtained
with increased food concentration, as demonstrated for
the sex ratio of adult Calanus (Irigoien, 2000). An exception
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EGG PRODUCTION RATE OF PARACALANUS PARVUS
is the report that more female Eurytemora affinis were produced at higher food densities (Vander Hart, 1976). Under
low food conditions, male copepods switch their sex to
female, and this could have been an adaptive strategy in
nature. In the context of populations, under high food concentrations, copepod populations can rapidly reproduce
by producing more males, which would facilitate mating
with multiple females (Kiørboe, 2006; Choi and
Kimmerer, 2009). The fraction of mated females increases
with the fraction of males in the population (Kiørboe,
2006). Female copepods that can keep sperm probably can
withstand lower male relative to female abundance. In the
present study, the sex ratio was not related to food concentration, and the sex ratio did not change during the
summer when the population rapidly increased via elevated levels of EPR (Fig. 3d and e). Relatively low EPR
than that reported in other regions, with the weak association of the EPR with food concentrations (Fig. 4b) and yet
highly female-biased sex ratio, might suggest a food
quality issue affecting physiological and reproductive
aspects of this species, which needs further studies.
Implications of climate change
The water temperature in the northern East China Sea
region has been increasing steadily since the 1980s at a
rate of 0.0248C year – 1, with the February 188C isopleths
moving northward (MOMAF, 2010). Following this seawater temperature rise, mesozooplankton biomass and
copepod concentrations have increased in all three seas
surrounding the Korean Peninsula (Rebstock and Kang,
2003), although the reason for this remains unresolved.
Estuarine waters generally exhibit greater seasonal fluctuations in temperature than deeper offshore waters due
to their shallow depths and input from land (Jang et al.,
2012), and such local processes may obscure any longterm trends. Increased water temperatures in southern
coastal waters are related to the expansion of warm water
currents (e.g. the Tsushima Warm Current) to the north.
Such expansion of warm water currents could cause the
advection of offshore populations to onshore areas. The
observed extremely low female growth rates and low
EPR (Fig. 3e and f ), yet high abundance, in November
2009, suggests that the copepod populations might be
sustained and supplemented by offshore populations,
where growth conditions could be better (e.g. higher
water temperatures). The Tsushima Warm Current,
which flows northeastward along the Korea Strait
(Fig. 1), is strongest in winter (Guo et al., 2006) and may
carry a greater abundance of copepods into Jangmok
Bay. For example, in February 2009, the abundance of
P. parvus in southern shelf waters exceeded 3500 inds m – 3
(Choi, unpublished data), two orders of magnitude
higher than the numbers found in winter at the Jangmok
station (Fig. 3a). Paracalanus parvus is also a good indicator
of on-shelf waters, suggesting that the northward-flowing
coastal Davidson Current advects warm water subtropical neritic copepods such as P. parvus (Morgan et al., 2003).
During warm periods, subtropical species show higher
abundances and more northerly distributions (Batten
and Welch, 2004). Warm water extension into Jangmok
Bay around the fall – winter period was also reported
from a survey of protozoans (Kim et al., 2012). Warm
water tintinnid species used as biological indicators of the
inflow of warm oceanic waters into Korean coastal
waters were simultaneously detected in Jangmok Bay and
the Korea Strait (Kim et al., 2012). Although difficult to
predict, long-term changes in copepod abundance
suggest that further temperature increases in this region
are likely to increase the population of this species, especially non-summer populations. More importantly,
warming would have implications for the substitution of
cold-water species with warm-water (warm temperature)
ones in the bay, which needs further investigations.
In conclusion, temperature is fundamental to the seasonal dynamics of the EPR of P. parvus in generally eutrophic coastal waters. However, terrigenous materials
associated with lower salinity water that could fuel heterotrophic plankton may be important, possibly facilitating
an increased EPR. Seasonal changes in copepod abundance suggest that warming coastal waters are likely to
result in increased populations of this species, especially
winter populations.
AC K N OW L E D G E M E N T S
We are grateful to Dr H.-K. Kang and two anonymous
reviewers for their comments, which improved an earlier
version of the manuscript. We also thank Ms O.-M.
Hwang for assistance with the field work.
FUNDING
This work was funded by a grant from the Basic Research
Program of KIOST(PE99152) and by the Ministry of
Trade, Industry & Energy of Korea (PN65420).
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