Journal of Oceanography, Vol. 63, pp. 35 to 45, 2007
Reproductive Ecology of the Dominant Dinoflagellate,
Ceratium fusus, in Coastal Area of Sagami Bay, Japan
S EUNG H O BAEK*, SHINJI SHIMODE and TOMOHIKO KIKUCHI
Graduate School of Environmental and Information Sciences, Yokohama National University,
Tokiwadai, Hodogaya-ku, Yokohama 240-8501, Japan
(Received 12 March 2006; in revised form 1 September 2006; accepted 1 September 2006)
The seasonal abundance of the dominant dinoflagellate, Ceratium fusus, was investigated from January 2000 to December 2003 in a coastal region of Sagami Bay, Japan.
The growth of this species was also examined under laboratory conditions. In Sagami
Bay, C. fusus increased significantly from April to September, and decreased from
November to February, though it was found at all times through out the observation
period. C. fusus increased markedly in September 2001 and August 2003 after heavy
rainfalls that produced pycnoclines. Rapid growth was observed over a salinity range
of 24 to 30, with the highest specific rate of 0.59 d –1 measured under the following
conditions: salinity 27, temperature 24°C, photon irradiance 600 µ mol m–2s –1. The
growth rate of C. fusus increased with increasing irradiance from 58 to 216
µ mol m –2s –1, plateauing between 216 and 796 µ mol m–2s–1 under all temperature and
salinity treatments (except at a temperature of 12°C). Both field and laboratory experiments indicated that C. fusus has the ability to grow under wide ranges of water
temperatures (14–28 °C), salinities (20–34), and photon irradiance (50–800
µ mol m–2s–1); it is also able to grow at low nutrient concentrations. This physiological
flexibility ensures that populations persist when bloom conditions come to an end.
Keywords:
⋅ Dinoflagellate
Ceratium fusus,
⋅ reproductive
strategy,
⋅ bloom,
⋅ growth rates,
⋅ Sagami Bay, Japan.
2003). In addition, red tides occurred from March to July
in 1997 along the Pacific coast of central Japan from
Wakayama to Ibaraki Prefecture (Machida et al., 1999).
Furthermore, C. fusus has a seasonality similar to that of
C. furca. The cell density of C. fusus at the peak of proliferation exceeds an average value for red tides (Mulford,
1963; Dodge and Marshall, 1994). There have been field
and laboratory studies of factors that control seasonal
changes in C. furca, and optimal environmental conditions for bloom outbreaks have been determined (Baek et
al., 2006). There is no similar information for C. fusus,
though a few authors have reported on cell tolerance to
changes in temperature and salinity. For example, C. fusus
is able to survive at temperatures ranging from 1.7 to 27°C
and salinities between 14.4 and 34.8 in water from Virginia, USA (Mulford, 1963).
Due to difficulties in isolating C. fusus from natural
seawater and subsequent laboratory cultivation, there have
been few ecological or physiological studies of the species, and there is a shortage of information obtained under controlled laboratory experiments on the life cycle
(including cyst populations), and on nutrient requirements, light intensities, salinities and water temperatures
for optimal growth.
1. Introduction
The dinoflagellate genus, Ceratium, is an important
component of marine phytoplankton communities. It has
an extraordinary biogeographical range through all of the
world’s oceans, from the warmest waters of the tropics to
the cold polar seas (Graham, 1941). Within the North
Atlantic Ocean and adjacent seas, distribution depends
significantly on water temperature (Dodge and Marshall,
1994). Some species of the genus Ceratium frequently
dominate coastal phytoplankton communities, where they
contribute substantially to annual primary production
(Nielsen, 1991; Dodge and Marshall, 1994).
Ceratium fusus and Ceratium furca have recently
been recognized as dominant red tide species in eastern
Asian areas, such as Chinese coastal water, Hong Kong,
the Philippine Sea and the Gulf of Thailand etc (Lu, 2003;
Yin, 2003; Lirdwitayaprasit, 2003). Although both species are frequently observed in coastal areas of Korea and
Japan, red tides of C. furca have been especially frequent
on the southern coast of Korea since 1995 (Suh et al.,
* Corresponding author. E-mail: [email protected]
Copyright©The Oceanographic Society of Japan/TERRAPUB/Springer
35
Fig. 1. The sampling stations.
Ceratium fusus is a dominant red tide species in
Sagami Bay; high cell numbers are observed frequently
from April to September, after the spring diatom bloom.
The species sometimes occurs as a red tide under relatively low nutrient conditions. Population densities in the
water column decrease from November to February. This
seasonal pattern of occurrence has not been as rigorously
assessed as those of other dinoflagellates. In this study,
the natural population of C. fusus was monitored to provide information on the relationship between cell abundance and environmental factors (water temperature, salinity, nutrients) in the coastal waters of Sagami Bay.
Laboratory cultures were used to examine optimum physiological requirements for growth. The experimental results were compared to observations of the natural population to better understand the reproductive ecology of
the species in Sagami Bay.
2. Materials and Methods
2.1 Field investigation
Sampling was conducted monthly from 2000 to 2003
at two coastal stations, designated St. 40 and 70 (ca. 40
m and 70 m depth, respectively) in the north-western part
of Sagami Bay, Central Japan (Fig. 1). Sagami Bay faces
the Pacific Ocean and its hydrography is related primarily to fluctuations of the Kuroshio Current axis. It is also
influenced by the fresh water discharged from the Sagami
and Sakawa Rivers as well as the water from Tokyo Bay
(Hogetsu and Taga, 1977). Interaction between the current and river discharges results in stratified waters in
Sagami Bay. The surface layer consists of a mixture of
waters from the Kuroshio Current and fresh waters (Iwata,
1985).
Water samples were collected with a bucket (surface
36
S. H. Baek et al.
layers only) and with 6 L Niskin bottles. The sampling
depths at the two stations were 0 m, 5 m, 20 m and 35 m
at St. 40, and 0 m, 5 m, 20 m, 40 m and 65 m at St. 70.
Debris and large-sized plankters in the collected waters
were removed by filtering through 330 µm mesh on board
ship immediately after measurement of water temperature with a mercury thermometer. Each filtered water sample was kept in a dark bottle and taken to the laboratory
for determination of salinity, inorganic nutrients, chlorophyll a (Chl.a) concentrations, and phytoplankton assemblages. Salinity was measured using an inductive salinometer (Model 601 MK-IV, Watanabe Keiki MFG. Co. Ltd.).
Subsamples for the estimation of phytoplankton abundances were fixed immediately with 2.5% (final concentration) glutal aldehyde solution after filtration through
TTTP type 2.0 µm membranes, and stored at 4°C in the
dark until cells were counted (using a Sedgwick-Rafter
chamber).
Duplicate subsamples of >100 ml were filtered onto
Whatman GF/F glass fiber filters for analysis of Chl.a.
Each filter was extracted in the dark at 4°C for 24 h in a
10 ml brown vial containing 10 ml N,NDimethylformamide (DMF) (Suzuki and Ishimaru, 1990).
Chl.a concentration was determined fluorometrically on
a Turner Design fluorometer according to the method of
Holm-Hansen et al. (1965). Water samples for determination of dissolved inorganic nutrients were filtered
through Millipore Milex filters (pore size: 0.45 µm). The
filtered water was transferred into plastic tubes and kept
in a freezer (–20°C) for later measurement of nutrients.
The water samples were thawed to room temperature, and
nitrite + nitrate-N (NO 2 – + NO 3 – ), and phosphate-P
(PO 43–) concentrations were analyzed using an autoanalyzer (Bran Luebbe, AACS-II), following analytical
methods based on Parsons et al. (1984).
Fig. 2. Seasonal changes in vertical profiles of water temperature and salinity at St. 70, Sagami Bay, Japan (2000–2003). Black
dots indicate sampling depths.
Rainfall was measured every day during the sampling period with rain gauges located on the roof of the
Manazuru City Hall (35°09′15″ N, 139°08′26″ E) and the
Odawara office of the Japan Meteorological Business
Support Center (35°15′01″ N, 139°09′03″ E).
2.2 Isolation and culture of Ceratium fusus
Individual cells of C. fusus were isolated from natural assemblages in waters of Sagami Bay during July 2003,
when water temperature and salinity were approximately
22°C and 32.5, respectively. Each of the isolated C. fusus
cells was washed by serial transfer through three droplets of T1 medium containing H2SeO3 (Ogata et al., 1987;
Baek et al., 2006), and then pipetted into one 5 ml well
of a 12-well tissue culture plate. For acclimation to laboratory conditions, the cells were cultured for a period of
one month at 22°C under a photon fluence rate of 180
µmol m–2s –1 with a 12 L: 12 D cycle (using cool white
fluorescent lamps). Enriched seawater (modified T5 medium, i.e., T1 medium concentrated five-fold) with soil
extract was used in the acclimation period. Preliminary
experiments showed that T5 medium (N: 5 µM, P: 0.5
µM) promoted better cell population growth than T1 medium. The following experiments were conducted after
T5 medium-acclimation.
2.3 Specific growth rate experiments
We tested the effects of varying light, temperature
and salinity on the growth rate of C. fusus populations
maintained in 100 ml flasks in T5 medium with soil extract. Stock cultures containing 3000 cells ml–1 of C. fusus
were concentrated by gentle reverse filtration through a
Reproductive Ecology of Ceratium fusus
37
Fig. 3. Variation in rainfall in the north-western part of Sagami Bay, Japan. White and black bars indicate average rainfall in
month and total rainfall over five days preceding sampling date, respectively.
20 µm Nitex mesh. Elevated concentrations were needed
because densities did not increased above 1500 cells
ml–1, even under optimal conditions. One ml of the cell
concentrate was transferred into each 100 ml conical flask.
Thus, the initial cell density was 30 ml –1. The densities
were determined as means of three replicate cell counts
using a 1 ml cell counts using a 1 ml Sedgwick-Rafter
counting chamber under a microscope. The experiments
were run three times.
Five temperature (12, 16, 20, 24 and 28°C), six salinity (17, 20, 24, 27, 30 and 34) and six photon irradiance regimens (0, 58, 180, 230, 600 and 800
µmol m–2s –1) were established. Cells were incubated at
20, 24 and 28°C under all six salinity conditions. They
were also incubated at 12 and 16°C at a salinity of 34.
Experiments ran four days under a 12L: 12D cycle. The
specific growth rate ( µ) was estimated from:
µ = ln(Nt/N0)/t,
where N0 and Nt represent the initial and final cell densities and t represents incubation time (day).
2.4 Data analysis
We examined relationships among cell densities and
environmental parameters (Temperature, Salinity, Chl.a,
NO 2– + NO 3– and PO 43–) in the field using Pearson’s
correlation analysis. A significance level of P < 0.05 was
used in all statistical analyses.
3. Results
3.1 Abiotic factors
Seasonal changes in environmental factors were almost identical at the two stations. Therefore, we show
only the results obtained at St. 70.
Water temperature varied from 12 to 29°C during the
sampling period (Fig. 2). In each sampling year, the highest temperature was recorded in August or September and
38
S. H. Baek et al.
the lowest in March. The water column was well mixed
vertically from November to March, and gradually stratified thereafter. Salinity varied from 23.0 to 34.7 during
the sampling period, and low salinities were frequently
recorded in summer due to rainfall (Figs. 2 and 3). In
particular, salinity decreased drastically from 34.5 to 24.5
in September 2001, and from 34.5 to 23 in August 2003,
probably due to heavy rain two to four days prior to sampling in both months. In contrast, we did not find salinities
of less than 30 after relatively high rainfall (>100 mm) in
June of 2000 and 2002. Large rainfall events were recorded from May to October during all 4 years (Fig. 3).
The largest annual rainfall during the study period occurred in 2003. Average rainfalls five days prior to each
sampling day were in excess of 100 mm on four occasions during summer (June to September) in each sampling year.
Concentrations of nitrate + nitrite-N ranged from
>0.02 µM on July 2003 to 20.49 µM on August 2003,
and the mean values during four sampling years were
3.61 ± 2.86 µM (Fig. 4). The highest (20.49 µM) nitrate
+ nitrite-N value was recorded in surface water on August 2003 after heavy rainfall. The second highest concentration was observed on July 2001, although there was
no rain in the day (July 7 to 13) preceding the sampling
date. Phosphate-P concentrations ranged from >0.02 µM
on May 2001 to 1.62 µM on July 2001, with a mean value
of 0.30 ± 0.23 µM over the four sampling years (Fig. 3).
3.2 Chl.a concentrations and phytoplankton assemblages
Chl.a concentrations at 5 m depth in the two station
are shown in Fig. 5. The Chl.a concentrations ranged from
0.02 mg m–3 on November 2002 to 9.66 mg m–3 on March
2001 at St. 40. The concentrations remained at low values through September to January in each of four years,
and tended to increase from February to July. Eight peaks
(>5 mg m–3) of Chl.a concentration were observed at both
stations. Seasonal changes in Chl.a concentrations were
almost identical at the two stations. Spring blooms, rec-
Fig. 4. Seasonal changes of vertical profiles of nutrients (NO2– + NO3–-N and PO 43–-P) at St. 70, Sagami Bay, Japan (2000–
2003). Black dots indicate sampling depths.
ognizable by high Chl.a concentrations (>5 mg m–3) following mixing of the water column in winter, were mostly
dominated by diatoms such as Eucampia spp.,
Rhizosolenia spp., and Chaetoceros spp. The
phytoplankton assemblages during the summer periods
consisted mainly of dinoflagellates, such as Ceratium
furca and C. fusus. When the two species bloomed at both
stations in September 2001 and May 2002, C. fusus made
up >90% of total phytoplankton cell density. In addition
to Ceratium species, other dinoflagellates, such as
Prorocentrum spp. and smaller diatoms, such as Nitzschia
spp., increased in abundance after heavy rainfall during
summer.
3.3 Temporal variation of C. fusus abundance
Population densities of C. fusus were measured at
Fig. 5. Variation in Chl.a concentrations at 5 m depth during
the study period. White and black bars indicate St. 40 and
St. 70, respectively. Arrows indicate point in time when C.
fusus accounted for more than ca. 80% of total
phytoplankton abundance.
Reproductive Ecology of Ceratium fusus
39
Fig. 6. Seasonal changes in cell density (cells l –1) of Ceratium fusus by depth at St. 40 (a) and St. 70 (b) in Sagami Bay, Japan
(2000–2003). Black dots indicate sampling depths.
Table 1. Pearson correlation coefficients (r) indicating relationships between environmental factors and cell density of Ceratium
fusus between 2000 and 2003.
Temperature
Salinity
Chl.a
NO2 – + NO3 –
PO4 3 –
C. fusus
Depth
Temperature
Salinity
Chl.a
NO2 – +NO3 –
PO4 3 –
–0.152
0.455*
–0.478*
0.249
0.325*
–0.276*
–0.492*
–0.024
–0.567*
–0.634*
0.144
–0.304
0.137
0.342*
–0.160
–0.229*
–0.316*
0.222*
0.776*
–0.299*
–0.244
*Significant correlations (P < 0.01).
both stations in each sampling year (Fig. 6). Total abundances at St. 70 were slightly lower than those at St. 40.
Populations remained at low densities through October
to January, and increased from April to September.
40
S. H. Baek et al.
Marked seasonal blooms of the species were observed
during the periods from April to August in 2000–2002. In
2003, abundance was exceptionally high in both summer
and winter in comparison with the previous three years.
Fig. 7. Changes in growth rates of Ceratium fusus with increasing photon irradiance at different salinity (a: 34, b: 30, c: 27, d: 24,
e: 20, f: 17) and temperature conditions. Error bars are SD.
During the study period, individual blooms persisted for
no more than one month at both stations.
Maximum densities of C. fusus occurred between the
surface and 20 m depth. Subsurface maxima were frequently observed at 5 m depth, with sharply decreasing
abundances with increasing depth at each station during
the summer period. In contrast, during winter periods of
2002 and 2003 at both stations, cells were observed
throughout the water column (as a result of vertical mixing). The annual average density calculated from 0 to 5
m depth was always higher at St. 40 than at St. 70, except
in 2000 when the average value was higher at St. 70.
The relationship between environmental factors and
abundances of C. fusus during the 4 years are shown in
Table 1. The abundance of the species was not significantly correlated with water temperature and salinity. In
contrast, the abundance was significantly negatively correlated with water depth (r = –0.276, p < 0.01), nitrate +
nitrite-N concentrations (r = –0.299, p < 0.01), and phosphate concentration (r = –0.244, p < 0.01).
Reproductive Ecology of Ceratium fusus
41
µmol photons m–2s–1. However, growth rates at salinities
of 34, 20 and 17 were lower than those in the range from
24 to 30. At a salinity of 17, morphologically abnormal
cells without apical horns were observed during incubation. At salinity <14 (data not shown), we also observed
cells damaged by phenomena such as cytolysis (Fig. 8).
Fig. 8. Cell morphology of Ceratium fusus. (a) Normal vegetative cell; arrow points to flagella. (b) and (c) show abnormal forms; white arrow indicates cytolysis in yellowbrown chloroplasts of and the nucleus.
3.4 Specific growth rate
Laboratory experiments were conducted to investigate effects of temperature, salinity and irradiance on the
specific growth rate of C. fusus (Fig. 7). Five temperatures between 12 and 28°C were tested at salinity value
34 only (Fig. 7a). At 12°C, the specific growth rates of C.
fusus decreased gradually with increasing photon irradiance between 53 to 183 µmol m –2s–1, after which there
was no growth up to the highest photon irradiance of 796
µmol m –2s –1. Although the growth rates increased with
increasing photon irradiance from 58 to 796 µmol m–2s –1
at all temperatures above 16°C, the highest growth occurred at 24 and 28°C. Accordingly, in salinity treatments
below 34 salinity, we measured growth at the following
temperatures: 20, 24 and 28°C. The specific growth rates
of C. fusus increased gradually with increasing photon
irradiance from 58 to 216 µmol m–2s–1 in all salinity treatments (except at 12°C and a salinity of 34). Growth rates
reached a plateau between 216 and 796 µ mol m –2s –1 .
Photoinhibition did not occur, even at 796 µmol m–2s–1,
the maximum photon irradiance used in this study.
In salinities from 24 to 30, high specific growth rates
occurred at >24°C and the highest rate was 0.59 d –1 in
the following treatment combination: 27, 24°C and 600
42
S. H. Baek et al.
4. Discussion
Donaghay and Osborn (1997) stated that, ecologically, bloom dynamics seem to be dominated by interactions between biological and physical processes that occur over a broad range of temporal and spatial scales.
Morse (1947) reported that Ceratium furca reached an
especially high density in warm water above the
pycnocline in Patuxent River, Maryland, USA. Dense
populations of C. fusus have been observed mostly near
pycnoclines in stratified water columns, in accordance
with the general observation that the pycnocline is a necessary precondition for the development of dinoflagellate
populations (Donaghay and Osborn, 1997). Pycnoclines
also play an important role in the occurrence of subsurface populations and their occurrence has often been interpreted as an underlying factor in phytoplankton patchiness (Rasmussen and Richardson, 1989; Horner et al.,
1997). At our sampling sites, stratification of the water
column developed gradually from spring to summer. Red
tides of C. fusus broke out 5 days after heavy rainfall on
20 August 2003 (Kinoshita, personal communication).
Three days later (8 days after the rain), high abundances
of C. fusus were observed when surface water was at relatively low salinity (24), and strong pycnocline layers appeared, especially near the surface. The results suggest
that the development of the dinoflagellate populations
probably requires a stabilized water column under the
pycnocline, subsequent to nutrient addition by natural
rainfall inputs during the rainy season from late spring to
summer.
Cell densities of C. fusus decreased gradually from
the late summer to autumn. Factors that may be related to
the decline are: (1) breakdown of summer stratification
with decreasing temperature, and (2) continuous high salinity condition of more than 34 during the period of reduced rainfall after October. Elbrächter (1973) reported
that water temperature clearly influenced generation time
for Ceratium species. Our results from the field survey
and laboratory experiments indicate that the growth rates
of C. fusus in the field are probably limited by a gradual
water temperature decline (to <16°C) and continuous high
salinity (>34) during the fall (though the doubling time
of C. fusus in the field is likely shorter in the laboratory).
Our results suggest that, in addition to the low growth
rate caused by falling temperatures in autumn, the reduction of the field populations results from vertical and horizontal diffusion induced by vertical water mixing after
breakdown of stratification in the latter part of year.
Nutrient concentrations are often regarded as important in determining bloom scale and period. Relatively
high abundances of Ceratium in oligotrophic conditions
are closely related to the occurrence of phagotrophy,
which compensates for low nutrient levels (Norris, 1969;
Weiler, 1980). In this study, high abundances of C. fusus
were usually observed during months when nutrient concentrations were low. In addition, there were significant
negative correlations between the densities of the species and nutrient concentrations (nitrate + nitrite-N and
phosphate-P; Table 1). We successfully isolated the species from natural assemblages with T1 medium, which
has a fairly low nutrient level (nitrate ≤1.0 µM and phosphate ≤0.1 µ M). The medium concentration was similar
to the seawater level during the bloom period of the species. According to Dortch and Whitedge (1992) and Justic
et al. (1995), growth of phytoplankton species may be
considered limited when concentrations of dissolved inorganic nitrogen (DIN; nitrate, nitrite and ammonium) and
phosphate are <1.0 and 0.2 µM, respectively. However,
because Ceratium species are motile, their relatively high
division rates might also reflect an ability to change vertical positions to find an optimal depth for nutrient availability; this would be an advantage over non-motile forms.
Downward nocturnal migration to nutrient-rich water layers allows uptake of nitrogen (Cullen and Horrigan, 1981)
and phosphorus (Watanabe et al., 1988), giving an advantage to photosynthetic cells that subsequently migrate
upward to the surface layer during the day (Eppley et al.,
1968; Heaney and Eppley, 1981). We found that nutrient
concentrations in the deeper water layers in the field were
comparatively high, even when values at the surface were
low (nitrate + nitrite-N: <0.5 µM, phosphate-P: <0.1 µM)
in early summer.
Because of difficulties in isolation and culture from
natural seawater, there is limited information on the
growth rate of C. fusus. Our laboratory experiments promote a better understanding of the physiology and life
strategies of the species. The results of growth measurements at various temperature and irradiance combinations
indicate an ability to tolerate a wide range of temperature
(16 to 28°C), with highest growth rates recorded at 24
and 28°C (Fig. 7). There is clearly growth stimulation at
the temperatures encountered in temperate or tropical
ocean water, and vegetative cells have an obvious ability
to overwinter when water temperature is >12°C.
C. fusus in culture was able to tolerate a wide range
of salinity (17 to 34), with higher growth rates at 24, 27
and 30 (Figs. 7b to d). Nordli (1953) reported rapid growth
of this species in the field at temperatures over 24°C and
salinities from 20 to 25. In contrast, Smalley and Coats
(2002) reported that C. furca appeared to be restricted to
low salinities of >10, and was most abundant at ca. 14 in
the Chesapeake Bay, USA. However, we found that specific growth rates of C. fusus decreased at salinity 17. In
addition, cells of both C. furca and C. fusus were irreversibly damaged at salinity below 14. Baek et al. (2006)
found that growth rates of C. furca in culture were similar and relatively high at salinities between 17 to 34. Although there are some variations between the studies, the
results indicate that high growth rates of C. fusus are
stimulated by relatively low salinities (24–30), as commonly encountered in coastal waters.
Most dinoflagellates dominating coastal waters produce two different types of non-motile cells, i.e., a temporary cyst and/or a resting cyst, in their life cycle. The
resting cysts in particular have an important ecological
role as a seed for recurrent blooms. However, there are
no reports of resting cyst formations by C. fusus. The
mechanism by which vegetative cells recruit from the
initial stage before the bloom has not been well understood. We found that C. fusus cells adapt to a wide-range
of variations in water temperature, salinity, irradiance and
reduced nutrient concentrations. Observations on seasonal
variations in abundance suggest that C. fusus is able to
sustain a population in the water column throughout the
year. Small numbers of cells in the water column, particularly during the winter, may play an important survival role, allowing the population to sustain adequate
levels (without cyst formation) to initiate the next bloom.
Ceratium species (C. furca, C. fusus and C. tripos)
have been considered primarily photosynthetic, but, food
vacuoles were observed by Bockstahler and Coats (1993)
and Li et al. (1996). Smalley and Coats (2002), and
Mouritsen and Richardson (2003) noted that distributions
of these potentially mixotrophic Ceratium species (C.
furca, C. fusus and C. tripos) are strongly influenced by
the vertical and horizontal distribution of ciliate prey in a
stratified estuary. Smalley et al. (2003) also found that
the feeding of C. furca in the culture occurred when cells
had been growing under N- or P-depleted conditions,
while nutrient-replete cells did not ingest prey. There is a
need for research into the detail of mixotrophy in C. fusus.
In conclusion, C. fusus can survive through
unfavorable environment changes and small surviving
populations may play an important role in seeding the
next bloom (C. fusus does not have cyst stages). Our results also indicate that the species probably requires stratification in the water column for remarkable population
growth subsequent to nutrient addition by natural rainfall inputs during the rainy season from late spring to summer.
Acknowledgements
We are grateful to Profs. S. Taguchi and T. Toda, and
Dr. A. Shibata of Soka University for their invaluable
discussion on this study and permission to use instruments
Reproductive Ecology of Ceratium fusus
43
for the field sampling and laboratory experiments. Drs.
V. S. Kuwahara, T. Fujiki and A. Kuwata are thanked for
reviewing an earlier version of this manuscript. Mr. Y.
Asakura of the Manazuru Marine Station and colleagues
from the Yokohama National University and Soka University are thanked for their assistance in the present study.
We also thank Manazuru City Hall and Odawara office
the Japan Meteorological Business Support Center for
supplying data on rainfall. We are grateful to The 21st
Century COE Program “Environmental Risk Management
for Bio/Eco-Systems” of the Ministry of Education, Culture, Sports, Science and Technology of Japan for financial support. We also appreciate the editor and anonymous
reviewer for their thoughtful comments for improving this
article.
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