Journal of Plankton Research Vol.20 no.9 pp.1711-1720, 1998
Growth and grazing of a large heterotrophic dinoflagellate,
Noctiluca scintillans, in laboratory cultures
Yasuo Nakamura
National Institute for Environmental Studies, Tsukuba, Ibaraki 305-0053, Japan
Introduction
Noctiluca scintillans is a large heterotrophic dinoflagellate (300-800 um in diameter) with an extensive vacuole that occupies most of the cell volume. The species
is distributed worldwide in neritic waters and is brightly bioluminescent, except for
cells from the west coast of North America (Sweeney, 1978). Cells of N.scintillans
trap prey items on their tentacle with mucous materials and ingest them through
the cytostome (Nawata and Sibaoka, 1983). A wide variety of prey items of N.scintillans have been reported, including phytoplankton cells, copepod eggs,fisheggs,
protozoans in marine snow and possibly bacteria (Hattori, 1962; Sekiguchi and
Kato, 1976; Kimor, 1979; Kirchner et al., 1996; Shanks and Walters, 1996), but
phytoplankton cells are considered to be the main food items in the field (Kirchner et al., 1996). Since N.scintillans is abundant in many coastal areas and forms
conspicuous red tide streaks, several ecological studies of this species have been
conducted both in the field (e.g. Uhlig and Sahling, 1990; Huang and Qi, 1997) and
the laboratory (e.g. Lee and Hirayama, 1992a,b; Buskey, 1995). However, questions still remain. How fast does N.scintillans consume phytoplankton cells? To
what extent is the ingested prey converted to reproduction? Can feeding of N.scintillans control the biomass of phytoplankton in the field? Is the production of
N.scintillans higher than or comparable to that of herbivorous copepods or microzooplankton? These uncertainties probably stem from the scarcity of data on
feeding and growth of Nscintillans (especially as a function of prey concentration)
in laboratory cultures, and insufficiency of field observations on the changes in
Nscintillans populations together with those of potential prey items.
As part of an effort to clarify carbon (C) fluxes through planktonic food webs
in the Seto Inland Sea, Japan, during summer (cf. Nakamura et al., 1995,1997),
© Oxford University Press
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Abstract. Carbon (C) and nitrogen (N) content and growth/grazing characteristics of the heterotrophic dinoflagellate Noctiluca scintillans were examined in laboratory cultures at 24°C. The C and
N contents of N.scintillans per unit cell volume were 2.3 x 10~3 pg C unr 3 and 4.1 X 10""4 pg N unr 3 ,
respectively. These values are almost two orders of magnitude lower than those reported for other
protozoans such as ciliates and 'typical' heterotrophic dinoflagellates due to an extensive vacuole in
the cell of N.scintillans. Among five autotrophic flagellates used as prey, species with an equivalent
spherical diameter (ESD) of >10 um served as good prey for N.scintillans, but species with an ESD
of <5 um did not support growth. Growth rates of N.scintillans fed Chattonella antiqua (ESD = 27 um;
Raphidophyceae) or Heterosigma akashiwo (ESD = 11 um; Raphidophyceae) increased linearly with
prey C concentration (PC), with lower growth thresholds of -100 ug C I"1. Grazing rates of N.scintillans fed C.antiqua or H.akashiwo increased linearly with PC without an obvious threshold. Carbon
budget calculations for grazing and growth indicated that N.scintillans converts 'excess' C (= total
prey C ingested - C necessary for the maintenance of basic metabolic activities) to body C with efficiencies of 0.31 and 0.17 for C.antiqua and H.akashiwo, respectively.
Y.Nakamura
the growth and grazing of N.scintillans were examined in laboratory cultures.
Combining the results obtained in the present study with those of field observations/experiments in the Seto Inland Sea in the summer of 1997 (Nakamura,
1998), ecological roles of this unique heterotrophic dinoflagellate as a member of
the mesozooplankton will be assessed.
Method
Surface sea water (500 ml) was collected by bucket from the pier of Tsuna fishing
harbor in the Seto Inland Sea on 11 March (water temperature 11°C). In the
laboratory, -100 N.scintillans cells were transferred by a pipette into 100 ml of f/2
medium (salinity = 32%o; Guillard and Ryther, 1962) with Heterosigma akashiwo
(Raphidophyceae; >3 X 104 ml"1) and incubated at 15°C and 40 uE nr 2 s"1 with
a 12:12 h light/dark (L/D) cycle for 3 days. Then the temperature was increased
at a rate of 1°C day 1 to 24°C and some N.scintillans cells were transferred to f/2
medium with Chattonella antiqua (Raphidophyceae; >1000 ml"1). They were
cultured at 24°C and 150 uE nr 2 s"1 with a 12:12 h L/D cycle. The N.scintillans
cultures thus established were maintained by inoculating them into fresh cultures
of C.antiqua at intervals of 1-2 weeks. Maintenance cultures were kept static,
except when they were agitated manually once or twice each day.
Carbon and nitrogen contents
About 2000 cells of exponentially growing N.scintillans fed C.antiqua were
isolated by pipette into GF/C-filtered Kuroshiwo sea water and washed four times
to remove prey items. Then, 750 cells were gently filtered onto pre-combusted
GF/C filters in duplicate, rinsed with 0.5 M ammonium formate, dried at 80°C for
48 h, and used for C and nitrogen (N) analysis with an elemental analyzer (MT3, Yanaco; Kohata and Watanabe, 1988). The remaining N.scintillans cells were
fixed with glutaraldehyde (final concentration = 1%) and their cell diameters
were measured under a compound microscope (n = 100) within a week. Although
the volume of N.scintillans cells preserved in glutaraldehyde solution (1%) at 5°C
decreased to -85% of the original value after 3 months, changes in the volume
were negligible within a week after fixation (Y.Nakamura, unpublished results)
and corrections for cell shrinkage were not made.
Growth experiments
Growth rates were measured by placing 50 N.scintillans cells in a 62 ml dissolved
oxygen (DO) bottle with a known phytoplankton concentration. Cultures were
placed on a plankton wheel for 2 or 3 days, rotating at 0.7 r.p.m. to keep prey
items homogeneously distributed. Preliminary experiments showed no deleterious effect of rotation on growth rates (cf. Buskey, 1995). Conditions of incubation
were 24°C, 40 uE nr 2 s"1 with 12:12 h L/D, except as otherwise indicated. After
the completion of incubation, N.scintillans cells were counted under a dissecting
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Establishment of Noctiluca culture
Growth and grazing ot Noctiluca scintillans
Grazing experiments
Chattonella antiqua and H.akashiwo were used as prey for grazing experiments;
300 N.scintillans cells, which had been washed with GF/C-filtered sea water, were
placed in DO bottles (62 ml) with a known concentration of prey items in duplicate and were incubated in the conditions described above. Two DO bottles
containing prey items without N.scintillans served as controls. Experiments
started 4 h after the onset of the light period in order to suppress the cell division
of the prey (Kohata and Watanabe, 1985; Nakamura et al., 1990) and continued
for 6 h. After incubation, prey concentrations were measured using a compound
microscope; clearance rates (CR) and grazing rates (G) were calculated by:
CR = (V/nT) In (QJQf) and G = <Q>CR, where Qc and Q{ are the prey concentrations at the end of incubation in the control and experimental bottles, respectively, <Q> is the prey concentration in the experimental bottle averaged over the
incubation period, V is the volume of the culture bottle (62 ml), n is the number
of N.scintillans used (300 cells) and T is the incubation period (6 h) (Frost, 1972).
Changes in cell concentrations of N.scintillans during incubations were neglected
for the calculation of CR since the growth rate of N.scintillans was <0.3 day"1 and
the incubation period was 0.25 day.
Results
C and N content of Noctiluca scintillans
Elemental analyses were conducted twice: C and N contents were 0.13 ± 0.01 ug
C cell"1 and 0.024 ± 0.002 ug N cell"1, respectively, when the cell diameter (<}>;
average ± SD) was 475 ± 52 um, and 0.10 ± 0.01 ug C cell"1 and 0.018 ± 0.002 ug
N cell"1, respectively, when <}> was 432 ± 46 um. C and N concentrations per unit
cell volume were constant over the cell size range of 432-475 um with values of
2.3 X 10"3 pg C unr 3 and 4.1 X 10"4 pg N unr 3 , respectively (Figure 1).
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microscope by isolating each cell using a pipette. Assuming exponential growth
during the incubation (cf. Buskey, 1995; Y.Nakamura, unpublished results),
growth rates were calculated as u = [In (n^no)]IT, where n0 and n{ are the numbers
of Nscintillans cells in the bottle at the beginning and end of time interval T in
days.
Prey items used were C.antiqua (strain 89-1), Heterocapsa triquetra (Dinophyceae, strain NIES-7), Heterosigma akashiwo (strain NIES-2), Isochrysis
galbana (Prymnesiophyceae, strain CCMP-1323) and Chlamydomonas parkeae
(strain NIES-440). Carbon contents of the strains of C.antiqua (1.0 ng C cell"1)
and H.akashiwo (0.12 ng C cell"1) used in the present study were reported in
previous papers (Kohata and Watanabe, 1985; Nakamura et al., 1992).
Prey concentrations after the growth experiments were determined by counting under a compound microscope; average prey concentrations during incubations (<Q>) were calculated as: <Q> = (Qf - Qo)l\n (Qf/<2o)> where Qo and Qt are
the prey concentration (cells ml"1) at the start and end of incubations, respectively. Then growth rates of N.scintillans were assessed as a function of <Q>.
YJVakamura
0.15
2
4
6
Cell volume ( x 107Mm3cell-1)
Fig. 1. Carbon (O) and nitrogen (•) contents of N.scintillans as functions of cell volume. Vertical bars
denote the range of duplicate measurements.
Table I. Noctiluca scintillans. Growth using different food sources
Prey item
ESD (urn)
u ± SD (day-1)
Chattonella antiqua
Heterocapsa triquetra
Heterosigma akashiwo
Chlamydomonas parkeae
Isochrysis galbana
27
15
11
4.5
4.2
0.35 ± 0.06
0.34 ± 0.02
0.31 ± 0.05
0.07 ± 0.01
-0.06 ± 0.09
ESD, equivalent spherical diameter, u, growth rate; n, total number of cultures examined.
Growth of Noctiluca scintillans
Effects of different food sources on the growth of N.scintillans were examined
under conditions where prey items were sufficiently present (>2000 ug C I"1 as
participate organic carbon). Among five phytoplankton species, Cantiqua,
H.triquetra and H.akashiwo supported rapid growth of N.scintillans. However,
much smaller species with an equivalent spherical diameter (ESD) of <5 um,
I.galbana and Cparkeae, were unsuitable prey items (Table I).
When the growth rates of N.scintillans fed Cantiqua were examined as a function of prey concentration, there was little change in the prey concentrations
during incubation, suggesting that the growth of the prey nearly balanced grazing
by N.scintillans. A lower growth threshold was observed at around 100 cells ml' 1
(100 pg C I"1; Figure 2A). Above that level, the growth rate increased linearly
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0
Growth and grazing otNoctiluca scintillans
0.3 -
(a)
0.2 -
O 0
0
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0.1 -
/o
ep
-0.1 0
n
200
400
600
800
Chattonella antiqua (cells ml"1; ngC H)
Heterosigma akashiwo (ugC M)
0
500
1000
1500
0.3 -
-0.1
0
5
10
15
Heterosigma akashiwo ( x 1Q3 cells ml"1)
Fig. 2. Growth rate of N.scintillans as a function of prey concentration, (a) Chattonella antiqua as the
prey, (b) Heterosigma akashiwo as the prey. Horizontal bars denote the range of the prey concentration during incubation. Solid lines are hand drawn and the dotted line in (b) indicates the growth
rate predicted with C.antiqua fed as the prey.
1715
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Grazing experiments
Grazing rates of N.scintillans fed Cantiqua increased linearly with prey concentration and reached 100 prey cells Noctilucar1 day 1 at a prey level of 500 cells
ml"1 (Figure 3A). No threshold for grazing was apparent. Clearance rates were
constant throughout the prey concentrations examined, at -0.2 ml Noctilucar1
day 1 . When fed H.akashiwo, the grazing rates also increased linearly with prey
concentration and no threshold was observed (Figure 3B), but the clearance
rates (-0.13 ml Noctiluccr1 day 1 ) were lower than in the case of Cantiqua as
prey.
Discussion
As a result of the extensive vacuole that occupies most of the cell volume, the C
and N contents per unit cell volume of N.scintillans were nearly two orders of
magnitude lower than those reported for other protozoans such as ciliates and
'typical' heterotrophic dinoflagellates (Putt and Stoecker, 1989; Lessard, 1991).
However, these values are comparable with those obtained from field populations
of N.scintillans (Tada et al., 1997) and thus can be used as conversion factors to
estimate the biomass of this species in natural populations.
Kirchner et al. (1996) suggested that N.scintillans could use planktonic bacteria
as a food source, based on the observation that Nscintillans ingested bacteriasized fluorescent latex beads. However, Buskey (1995) pointed out that the
growth of N.scintillans was very poor when fed I.galbana (ESDF = 4.2 um).
Results in the present study also indicate that I.galbana and Cparkeae (ESD =
4.5 um) did not support rapid growth of N.scintillans (Table I). I suspect that
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with prey concentration in the range of 100-400 cells ml"1 (100-400 ug C I"1) and
reached 0.20 day 1 at 400 cells ml"1.
Two series of experiments were conducted with H.akashiwo as prey. For the
first series, the prey concentration increased significantly due to its rapid growth
under the light conditions described above (see Method). Thus, in the second
series, light intensity was reduced to 20 uE m~2 s"1 to suppress the growth of
H.akashiwo. The results obtained in the two series were combined and are shown
in Figure 2B. A lower growth threshold was observed at around 0.8 x 103 cells
ml"1, which was comparable to that for Cantiqua in terms of the prey carbon
concentration (PC; 100 ug C I"1). Above the threshold, the growth rate increased
linearly with prey concentration in the range of (0.8-8.0) X 103 cells ml"1.
However, the slope of the growth rate against PC was much lower for H.akashiwo
than for Cantiqua.
Throughout the growth experiments, changes in cell size of N.scintillans during
incubations were not apparent from microscopic observations, although cell sizes
were not measured. Gametocyte mother cells (Zingmark, 1970) were occasionally found during the growth experiments, but the ratio of gametocyte mother
cells to vegetative cells was low (<4%) and gametocyte formation did not affect
growth rate calculations significantly.
Growth and grazing of Noctiluca scintillans
120 •
I
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I
I
CD
2
40 "
CD
0
200
400
600
Chattonella antiqua (cells m l 1 ; |igC H)
Heterosigma akashiwo (|jgC I"1)
0
500
1000
5
10
1500
1000-
1
500-
I
(3
0
Heterosigma akashiwo (X1CP rails ml"')
Fig. 3. Grazing rates of N.scintillans on (a) Cantiqua and (b) H.akashiwo as a function of prey concentration.
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although N.scintillans can ingest bacteria-sized particles, prey items with sizes
<5 um are not good food items.
When C.antiqua or H.akashiwo were fed as prey to N.scintillans, lower growth
thresholds were found at around 100 ug C I"1 (Figure 2A and B). Assuming the
C/chlorophyll a conversion factor to be 40, the threshold is at -2.5 ug I"1 in terms
of chlorophyll a, indicating that N.scintillans can develop their populations only
in eutrophic environments such as the Seto Inland Sea.
The abundance of N.scintillans averaged over the water column in the Seto
Inland Sea during the warm season is of the order of 100 cells I"1 (Tada et al.,
1997). Under these conditions, and assuming a clearance rate of 0.2 ml Noctiluccr1
day 1 , the population of N.scintillans clears 20 ml I"1 day 1 , suggesting that its
feeding impact on phytoplankton populations there is minimal. However, the
biomass of N.scintillans reaches a level comparable to that of copepods (10 ug
C I"1; Uye et al., 1987) when the abundance is 100 cells I"1 (assuming a C content
of 0.1 ug C cell"1). Furthermore, where N.scintillans grows actively (~0.3 day 1 ;
Figure 2) in the field, its production would be 3 ug C I"1 day 1 , comparable to that
of copepods (Uye et al., 1987). Thus, although the feeding impact on phytoplankton is limited, N.scintillans has the potential to play an important role as a
member of the mesozooplankton in the Seto Inland Sea.
Assuming a cell volume of 5 X 107 um3 (cf. Figure 1), the volume-specific clearance rate (CRV) of N.scintillans fed Cantiqua was calculated to be 1.7 X 102 h"1.
This was nearly three orders of magnitude lower than that for other protozoans
including heterotrophic dinoflagellates, and 1-2 orders of magnitude lower than
that for copepods and cladocerans (Hansen et al., 1997). The low value of CRy
for N.scintillans is partly attributable to the low C/volume ratio, which is almost
two orders of magnitude lower than that for other protozoans and copepods (see
above; cf. Hansen et al., 1997). When compared in terms of C-specific clearance
rates (CRQ), CRC for N.scintillans is still one order of magnitude lower than those
for other protozoans, but close to those for copepods and cladocerans whose
volume is comparable to N.scintillans. These considerations indicate that N.scintillans is not an 'energetic' protozooplankton.
Grazing rates of N.scintillans (G) increased linearly with prey carbon concentration (PC): G = k • PC, where k is a constant (Figure 3), and the growth rate
(u) was approximated by: u = A • (PC - PC0), (PC > PC0 and PC0 is the threshold level of prey concentration for growth; A = constant; Figure 2). If we assume
that of the prey carbon ingested per unit time (G), k • PC0 (grazing rate at the
growth threshold) is used for the maintenance of basic metabolic activities (such
as respiration) and 'excess' prey carbon ingested (G - k • PC0) is converted to
production with an efficiency of d, a simple relationship, A = k • d, is obtained.
Applying this equation to Nscintillans fed C.antiqua and H.akashiwo, d values of
0.31 and 0.17 are obtained, respectively. Since the gross growth efficiency
(GGE = u/G) approximates the 9 value if PC » PCQ, GGE of N.scintillans in the
presence of sufficient prey is in the range reported for other heterotrophic dinoflagellates (Hansen, 1992; Nakamura et al., 1992).
In conclusion, N.scintillans is adapted to eutrophic environments and supports
positive growth when the prey concentration is >100 ug C l~l. Although their
Growth and grazing of Noctiluca scintillans
feeding impact on phytoplankton populations in the field is moderate, the
biomass of N.scintillans can reach a level comparable to or exceeding that of
copepods, and thus can potentially play an important role as herbivorous mesozooplankton.
Acknowledgement
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The author expresses his thanks to R.Weisbird for his constructive comments and
linguistic corrections.
YJVakamura
Received on February 14,1998; accepted on April 27,1998
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