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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 24C, photon irradiance 600 mol m2s 1. The growth rate of C. fusus increased with increasing irradiance from 58 to 216 mol m 2s 1, plateauing between 216 and 796 mol m2s1 under all temperature and salinity treatments (except at a temperature of 12C). Both field and laboratory experiments indicated that C. fusus has the ability to grow under wide ranges of water temperatures (1428 C), salinities (2034), and photon irradiance (50800 mol m2s1); 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.
1. Introduction The dinoflagellate genus, Ceratium, is an important component of marine phytoplankton communities. It has an extraordinary biogeographical range through all of the worlds 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@example.com
CopyrightThe Oceanographic Society of Japan/TERRAPUB/Springer
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 27C 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.
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 m 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 m membranes, and stored at 4C 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 4C 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 m). The filtered water was transferred into plastic tubes and kept in a freezer (20C) 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 (20002003). 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 (350915 N, 1390826 E) and the Odawara office of the Japan Meteorological Business Support Center (351501 N, 1390903 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 22C 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 22C under a photon fluence rate of 180 mol m2s 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 M, P: 0.5 M) 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 ml1 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 m Nitex mesh. Elevated concentrations were needed because densities did not increased above 1500 cells ml1, 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 28C), six salinity (17, 20, 24, 27, 30 and 34) and six photon irradiance regimens (0, 58, 180, 230, 600 and 800 mol m2s 1) were established. Cells were incubated at 20, 24 and 28C under all six salinity conditions. They were also incubated at 12 and 16C at a salinity of 34. Experiments ran four days under a 12L: 12D cycle. The specific growth rate ( ) was estimated from:
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 Pearsons 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 29C 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 M on July 2003 to 20.49 M on August 2003, and the mean values during four sampling years were 3.61 2.86 M (Fig. 4). The highest (20.49 M) 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 M on May 2001 to 1.62 M on July 2001, with a mean value of 0.30 0.23 M 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 m3 on November 2002 to 9.66 mg m3 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 m3) 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 m3) 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
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 (20002003). 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.
Depth Temperature Salinity Chl.a NO2 + NO3 POC. fusus 0.152 0.455* 0.478* 0.249 0.325* 0.276* Temperature 0.492* 0.024 0.567* 0.634* 0.144 Salinity Chl.a NO2 +NO3 PO
0.304 0.137 0.342* 0.160
0.229* 0.316* 0.222*
*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 20002002. 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).
mol photons m2s1. 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).
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. Elbrchter (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 <16C) 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
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 28C were tested at salinity value 34 only (Fig. 7a). At 12C, the specific growth rates of C. fusus decreased gradually with increasing photon irradiance between 53 to 183 mol m 2s1, after which there was no growth up to the highest photon irradiance of 796 mol m 2s 1. Although the growth rates increased with increasing photon irradiance from 58 to 796 mol m2s 1 at all temperatures above 16C, the highest growth occurred at 24 and 28C. Accordingly, in salinity treatments below 34 salinity, we measured growth at the following temperatures: 20, 24 and 28C. The specific growth rates of C. fusus increased gradually with increasing photon irradiance from 58 to 216 mol m2s1 in all salinity treatments (except at 12C and a salinity of 34). Growth rates reached a plateau between 216 and 796 mol m 2s 1. Photoinhibition did not occur, even at 796 mol m2s1, the maximum photon irradiance used in this study. In salinities from 24 to 30, high specific growth rates occurred at >24C and the highest rate was 0.59 d 1 in the following treatment combination: 27, 24C and 600
S. H. Baek et al.
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 M and phosphate 0.1 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 M, 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 M, phosphate-P: <0.1 M) 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 28C), with highest growth rates recorded at 24 and 28C (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 >12C. 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 24C 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 (2430), 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
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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