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SHORT COMMUNICATION
Ecological behavior of the dinoflagellate
Ceratium furca in Jangmok harbor of
Jinhae Bay, Korea
SEUNG HO BAEK 1*, HYEON HO SHIN 1, HYUN-WOO CHOI 2, SHINJI SHIMODE 3, OK MYUNG HWANG 1, KYOUNGSOON SHIN 1
AND YOUNG-OK KIM 1
1
656-830, REPUBLIC OF KOREA, 2KOREA OCEAN RESEARCH AND
29, ANSON, REPUBLIC OF KOREA AND 3UNIVERSITY OF TOKYO, ATMOSPHERE AND
KOREA OCEAN RESEARCH AND DEVELOPMENT INSTITUTE, SOUTH SEA INSTITUTE, GEOJE
DEVELOPMENT INSTITUTE, OCEAN DATA MANAGEMENT TEAM, PO BOX
OCEAN RESEARCH INSTITUTE, CHIBA
277-8564,
JAPAN
*CORRESPONDING AUTHOR: [email protected]
Received March 8, 2011; accepted in principle July 19, 2011; accepted for publication July 22, 2011
The rhythmic migration pattern of the dinoflagellate Ceratium furca is a result of
ecological adaptation to avoid high irradiance. The high proportions of dividing
cells at deeper depths are likely to be an ecological response to maintain their
population away from the turbulence in the near-surface layer.
KEYWORDS: dinoflagellate; Ceratum furca; migration pattern; cell division timing
Ceratium is a ubiquitous thecate dinoflagellate genus,
slow growing, characteristically found during all seasons
and contributing substantially to annual primary production in the world’s oceans (Dodge and Marshall,
1994). Ceratium furca is a common bloom-forming species
found in coastal waters and the ecological impact
caused by blooms has intensified in recent years
(Machida et al., 1999). However, there is a paucity of
data on ecological parameters of C. furca blooms in
Asian coastal areas, although ecological and physiological characteristics of Ceratium species have been examined by Baek et al. (Baek et al., 2008a,b,c).
Most dinoflagellates have a constant vertical migration
pattern and cell division timing. Ceratium furca is also
known to perform active diel vertical migration (DVM),
depending on nutrients and water temperature in both
natural (Eppley et al., 1968; Edler and Olsson, 1985) and
laboratory conditions (Heaney and Eppley, 1981; Olsson
and Granéli, 1991). Recently, Baek et al. (Baek et al., 2009)
demonstrated that C. furca isolated from Sagami Bay,
Japan, exhibits a constant DVM rhythm based on cell division timing, suggesting that such ecological behavior can
play an important role in overcoming unfavorable conditions in local environments. According to Edler and
Olsson (Edler and Olsson, 1985), different species of dinoflagellates have different ecological abilities. These abilities
are possibly linked with their ecological responses for surviving under local environmental conditions. However,
the understanding of mechanisms such as DVM pattern
and cell division remains limited. Here we investigated the
ecological behavior of C. furca under environmental conditions in Jangmok harbor of Jinhae Bay, Korea.
doi:10.1093/plankt/fbr075, available online at www.plankt.oxfordjournals.org. Advance Access publication September 8, 2011
# The Author 2011. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected]
S. HO BAEK ET AL.
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ECOLOGICAL BEHAVIOR OF THE DINOFLAGELLATE CERATIUM FURCA
Dinoflagellate blooms usually occur during summer
in the coastal areas of the southern sea of Korea
(Park et al., 2001), whereas dense blooms of C. furca
have not been reported so far. However, in Jangmok
harbor, located in the Semi-enclosed Jinhae Bay on
the northern side of Geoje Island (358000 0000 N,
1288400 0000 E), of the southern sea of Korea, a widespread C. furca red tide was recorded in early summer
2009. The harbor is bounded by natural features,
and a manmade structure, rectangular in shape and
approximately 1 km wide and 1.5 km long with an
opening of 0.5 km. The maximal tidal range in the
harbor is approximately 2.2 m and the harbor water
is frequently disturbed by shipping traffic. The
sampling station was close to the tip of the pier of
the South Sea Institute of the Korea Ocean Research
and Development Institute, and the mean water
depth of the sampling station was about 8.5 m. Field
sampling was carried out at three-hourly intervals
between 29 July 2009 and 1 August 2009 at 0, 2, 4,
6 and 8 m depths, during the C. furca bloom. In
addition, to better understand DVM in relation to
cell division, we collected 12 hourly samples from
03:00 to 06:00 AM, based on the experimental methodology of Baek et al. (Baek et al., 2009). During the
study period, solar irradiance was also measured at
1 h intervals using a radiometer (LI-190 SA,
LI-COR), and irradiance was calculated as mmol
m22 s21.
Water samples were collected with a bucket (only
for the surface layer) and with a 2 L Niskin bottle.
Water temperature, salinity and fluorescence values
were simultaneously measured with an Ocean Seven
319 CTD (Idronaut). Water samples for nutrient
analysis were filtered through GF/F glass fiber filters.
The filtered water was placed in a plastic tube and
frozen. Samples were thawed at room temperature
and kept in the dark for measurements. Nitrate þ
2
nitrite (NO2
3 þ NO2 ), ammonium and orthopho32
sphate (PO4 ) concentrations were determined with
an auto-analyzer (QUAATRO Seal Analyzer, USA)
using standard protocols. Total chlorophyll-a (Chl a)
concentrations were obtained by filtering seawater
samples from all depths. Also, sub-samples from 0, 4
and 8 m were filtered through 20 mm polycarbonate
filters and Whatman GF/F glass fiber filters to
analyze the Chl a concentration in a . 20 mm size
fraction (mainly composed of C. furca). The volume of
filtered water for Chl a analysis was 100 mL. Each
filter was placed in a 20-ml brown vial and was
extracted in 10-mL acetone at 48C for 24 h. Chl a
concentration was determined fluorometrically on a
Turner Design fluorometer (Turner-Designs 10-AU).
The population densities of C. furca were immediately
determined for each layer using a Sedgwick-Rafter
chamber after samples were fixed with 1% Lugol solution. The fixed cells were enumerated separately as
follow: non-dividing cells, cells undergoing nuclear division and recently divided cells (Baek et al., 2009). The
relative proportion of dividing cells was estimated at the
different depths.
The cell division proportion at each depth in the
water column was compared using the Kruskal –Wallis
test. A weighted mean depth (WMD), adapted from
Frost and Bollens (Frost and Bollens, 1992), was used to
Fig. 1. Temporal profiles of water temperature (a: 8C), salinity
(b: psu), nitrate þ nitrite (c: mM), ammonium (d: mM), phosphate
(e: mM) and Chlorophyll a concentration of .20 mm fraction
(f: mg m23) from 29 July to 1 August at St. P during dense bloom
periods of Ceratium furca.
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examine the diel and tidal vertical migration of C. furca.
The WMD was calculated as follows:
P
ni di Þ
WMD ¼ P
ni
ð
where ni is cell density at depth di, taken to be the midpoint of each stratum at each sampling time.
Water temperature in Jangmok harbor ranged from
20.18C at the bottom to 22.88C at the surface (Fig. 1a),
and salinity showed a reverse pattern to the temperature, ranging from 29.5 to 31.1 psu (Fig. 1b). No significant stratification was observed during the field study.
As reported previously, since optimum water temperature for the growth of C. furca ranged from 18 to 288C
and significant effects of salinity on growth were not
observed (Baek et al., 2008a), the environmental conditions in the study area were considered favorable for
the outbreak of blooms of C. furca.
There was a large temporal variation in dissolved
inorganic nutrients (Fig. 1c – e) during the study period.
The highest nitrate þ nitrite concentrations were
recorded in the surface layers at the beginning of the
sampling, varying from 0.02 to 25.2 mM (Fig. 1c). The
ammonium concentrations ranged from 0.7 to 6.0 mM
(Fig. 1d) and the phosphate concentration was much
lower, ranging from the lower limit of detection of 0.01
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to 0.27 mM (Fig. 1e). The relatively high cell densities of
C. furca (. 10 000 cells mL21) in the surface layer were
observed at relatively low nutrient conditions, especially
in relation to nitrate þ nitrite concentrations (Figs 1c
and 2). This agrees with results from Sagami Bay,
where the significant increase in C. furca occurred
during relatively poor nutrient conditions. Ceratium furca
has a competitive advantage by adapting to low nutrient
conditions through its physiological characteristics of
nutrient uptake (Baek et al., 2008b).
Ceratium furca maintained very high densities during
the study period (Fig. 2). The cells accumulated at the
surface and their relative concentrations were characterized by a high time-to-time variability. Other phytoplankton groups in the samples collected were much
lower in abundance, and peaks of C. furca cell density
were significantly correlated with Chl a concentrations;
the high Chl a concentrations (. 98 mg m23) are considered to be attributed to C. furca alone (Fig. 1f and 2).
The maximum cell concentration was 10 640 cells mL21
being observed at 24:00 at the surface on 1 August,
while relatively high cell densities were routinely
recorded at 6:00 at the surface. The cell densities at the
surface seemed to decrease in higher daylight irradiance
periods, especially between 09:00 and 15:00, and
WMDs of C. furca were also deep during these periods
(Fig. 3), whereas the WMDs were not correlated with the
Fig. 2. Temporal variations of tidal condition (upper), light intensity (middle) and Ceratium furca (lower) at St. P from 29 July to 1 August 2003.
Black and white circles indicate the WMDs of Ceratium furca abundance. The population abundances are indicated as cells per mL.
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Fig. 3. Vertical distribution of proportions (%) of Ceratium furca dividing cells collected from 03:00 to 06:00 AM during 3 days at St. P. Black and
white circles indicate the WMDs of Ceratium furca.
tidal cycle (P . 0.05), indicating that vertical migration
is not necessarily related to tidal condition. These results
indicate that C. furca in Jangmok harbor exhibits DVM
to avoid strong sunlight. Similarly, Baek et al. (Baek et al.,
2008c) observed that decreases in densities of C. furca in
Sagami Bay were also observed during higher daily irradiance periods and Hasle (Hasle, 1954) and Whittington
et al. (Whittington et al., 2000) reported that Ceratium
species migrate downwards from the surface to avoid
high-light-induced cell damage. In general, vertical
migration has been suggested to be a competitive strategy for phytoplankton under conditions where light and
nutrients are spatially separated (Granf and Oliver,
1982). Therefore, dinoflagellates can alter their vertical
position in the water column by swimming, which allows
them to maintain an optimal depth in terms of light or
nutrients. Consequently, the actual duration of high irradiance in the coastal bays is considered to regulate the
maintenance of the bloom.
In our previous study (Baek et al., 2009), the vertical
migration of C. furca to avoid strong sunlight occurred at
irradiance levels above 1000 mmol m22 s21. In contrast
to the previous result, we observed downward migration
of C. furca from the surface layer even at lower irradiance below 664 mmol m22 s21 on 31 July. This difference implies (i) a local adaptation of physiological
response to irradiance or (ii) the DVM pattern induced
by a specific endogenous rhythm. Weiler and Karl
(Weiler and Karl, 1979) showed, by using a laterally
illuminated culture, that the pattern of vertical
migration in C. furca was not simply a passive response
to diel changes in illumination and phototaxis, but
rather under the control of a circadian rhythm. Thus,
our result suggests the possibility that the vertical
migration of C. furca is not a simple response to high
light intensity and may be under the control of an
Table I: Statistical results for proportions of
Ceratium furca dividing cell collected from
03:00 to 06:00 AM during 3 days in Jinhae
Bay
Proportions of dividing
cells (%)
Mann –Whitney
U-test
Water layer
N
Mean
SD
U
P-value
Upper (0 m, 2 m)
Lower (4 m, 6 m, 8 m)
18
27
9.30
25.55
10.41
26.37
120.5
0.0047
Significant difference in upper and lower layers values based on Mann –
Whitney U-test.
endogenous rhythm. In other words, the rhythmic
migration pattern of C. furca may be a combination of
the endogenous rhythm and an adaptation of the population to avoid strong sunlight.
Kohata and Watanabe (Kohata and Watanabe,
1986) found that the pattern of vertical migration of
Heterosigma akashiwo is based on the cell division cycle.
However, our result here shows that the cell division
of C. furca occurs in the middle and bottom layers
during the dense surface bloom periods (between
03:00 and 06:00), which is indicated by WMDs of
the proportions of dividing cells (Fig. 3). In addition,
the proportions of dividing cells had a positive correlation with depth (Table I). Consequently, C. furca
divides in the deeper layer, irrespective of the DVM
pattern, whereas the species moves toward the surface
during the dark to light transition after cell division
below the surface. The present result raises a question: why the cell division of C. furca occurs not at
the surface but at deeper depth. Recently, Baek et al.
(Baek et al., 2009) mentioned that the cell size of C.
furca was significantly reduced during the cell division
process, and those divided daughter cells seem to be
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weak. As shown in the pictures in the previous study
(see their Fig. 2i and j in Baek et al., 2009), the dividing cells tended to be damaged by physical forces
and did not show successfully growth to a normal
cell-form under conditions such as shaking incubation
bottles or rough pipetting into the bottles. These
abnormal cells were frequently observed in laboratory
conditions as a result of such physical forces (Baek,
personal communication). Under field conditions,
high turbulences near the surface is considered to
accelerate such cell-damage, which is frequently
caused by wave action and disturbance created by
winds and passing ships. Margalef (Margalef, 1978)
suggested that the different life-forms observed in
phytoplankton are functionally interpreted as adaptations to survival in an unstable and turbulent
environment. We suggest that the cell division of C.
furca in the deeper layer would be able to contribute
to keeping the stability in cell-division processes
because the turbulence energy decreased with depth.
Thus, our result suggests the possibility that C. furca
avoids cell division at the surface, although more field
and laboratory experiments will be required to clarify
the effect of wave disturbances on cell division.
In conjunction with the results of previous studies,
our results have revealed the DVM and daily cell division pattern of C. furca, implying an ecological advantage over other algal species under unfavorable
environmental conditions such as low nutrient availability, high irradiance and wave disturbance. Such ecological abilities can play an effective role in adaptation
to local environmental conditions.
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This research was supported by KORDI’s projects
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