Mesodinium rubrum
is a cosmopolitan ciliate that often causes red tides. Predation by heterotrophic protists is a critical factor that affects the population dynamics of red tide species. However, there have been few studies on protistan predators feeding on
M. rubrum.
To investigate heterotrophic protists grazing on
M. rubrum
, we tested whether the hererotrophic dinoflagellates
Gyrodiniellum shiwhaense, Gyrodinium dominans, Gyrodinium spirale, Luciella masanensis, Oblea rotunda, Oxyrrhis marina, Pfiesteria piscicida, Polykrikos kofoidii, Protoperidinium bipes
, and
Stoeckeria algicida
, and the ciliate
Strombidium
sp. preyed on
M. rubrum. G. dominans, L. masanensis, O. rotunda, P. kofoidii
, and
Strombidium
sp. preyed on
M. rubrum
. However, only
G. dominans
had a positive growth feeding on
M. rubrum
. The growth and ingestion rates of
G. dominans
on
M. rubrum
increased rapidly with increasing mean prey concentration <321 ng C mL
-1
, but became saturated or slowly at higher concentrations. The maximum growth rate of
G. dominans
on
M. rubrum
was 0.48 d
-1
, while the maximum ingestion rate was 0.55 ng C predator
-1
d
-1
. The grazing coefficients by
G. dominans
on populations of
M. rubrum
were up to 0.236 h
-1
. Thus,
G. dominans
may sometimes have a considerable grazing impact on populations of
M. rubrum
.
INTRODUCTION
Mesodinium rubrum
is a globally distributed ciliate (
Lindholm 1985
,
Crawford 1989
,
Williams 1996
,
Gibson et al. 1997
) that sometimes causes red tides in coastal waters (
Johnson et al. 2004
,
Yih et al. 2004
,
Hansen and Fenchel 2006
,
Hansen et al. 2013
,
Johnson et al. 2013
,
Kang et al. 2013
).
M. rubrum
is capable of both photosynthesis and prey ingestion (
Gustafson et al. 2000
,
Yih et al. 2004
,
2013
). In addition, this species is an important prey for some dinoflagellate predators (i.e.,
Amylax triacantha, Alexandrium pseudogonyaulax, Dinophysis
spp.,
Neoceratium furca,
and
Oxyphysis oxytoxoides
) and an effective grazer of cryptophytes (
Yih et al. 2004
,
Park et al. 2006
,
2011
,
2013
,
Blossom et al. 2012
,
Hansen et al. 2013
,
Johnson et al. 2013
).
The predation of
M. rubrum
by heterotrophic protists is one of the critical factors that affect the population dynamics of red tide species. Heterotrophic protists play an important role in marine food webs, as they connect phototrophic plankton to higher trophic levels (
Stoecker and Capuzzo 1990
,
Sherr and Sherr 2002
,
Myung et al. 2011
,
Garzio and Steinberg 2013
). However, there have been few studies on the feeding patterns of common heterotrophic protists that frequently co-occur with
M. rubrum
.
O. oxytoxoides
is the only heterotrophic dinoflagellate that is known to feed on
M. rubrum
(
Park et al. 2011
). However, the growth and ingestion rates and / or the impact of heterotrophic protist grazing on
M. rubrum
have not been reported.
Gyrodiniellum shiwhaense, Gyrodinium dominans, Gyrodinium spirale, Luciella masanensis, Oblea rotunda, Oxyrrhis marina, Pfiesteria piscicida, Polykrikos kofoidii, Protoperidinium bipes
, and
Stoeckeria algicida
, and naked ciliates having sizes of 30-50 μm have been reported to be present in many waters (
Strom and Buskey 1993
,
Jeong et al. 2004
,
2005
,
2006
,
2007
,
2011
,
2011
,
Kim and Jeong 2004
,
Yoo et al. 2010
,
2013
,
Seuthe et al. 2011
,
Kang et al. 2013
). Furthermore, they often co-occur with
M. rubrum
(
Hansen et al. 1995
,
Bouley and Kimmerer 2006
,
Kang et al. 2013
). Thus it is worthwhile to explore interactions between
M. rubrum
and these heterotrophic protists.
The results of the present study would provide a basis for understanding the interactions between
M. rubrum
and heterotrophic protists.
MATERIALS AND METHODS
- Preparation of experimental organisms
M. rubrum
(MR-MAL01) was isolated from water samples collected from Gomso Bay, Korea (35˚40′ N, 126˚40′ E) in May 2001 at a water temperature and salinity of 18℃ and 31.5, respectively. A clonal culture of
M. rubrum
was established as in
Yih et al. (2004)
. The culture was maintained with
Teleaulax
sp. (previously described as a cryptophyte) in 500-mL bottles on a shelf at 20℃ under an illumination of 20 µE m
-2
s
-1
of cool white fluorescent light on a 14 h : 10 h light-dark cycle (
Yih et al. 2004
).
For the isolation and culture of the heterotrophic dinoflagellates
G. shiwhaense, G. dominans, G. spirale, L. masanensis, O. rotunda, O. marina, P. piscicida, P. kofoidii, P. bipes, S. algicida
, and the naked ciliate
Strombidium
sp. plankton samples were collected from the waters of coastal area in Korea in 2001-2013, and a clonal culture of each species was established by two serial single-cell isolations (
Table 1
).
The carbon contents for
M. rubrum
(0.43 ng C cell
-1
, n= 40), the heterotrophic dinoflagellates, and the ciliates were estimated from cell volume according to
Menden-Deuer and Lessard (2000)
. The cell volume of the preserved predators after each feeding experiment was conducted was estimated using the methods of
Kim and Jeong (2004)
for
G. dominans
and
G. spirale
, the protocol of
Jeong et al. (2008)
for
O. marina
, and the methods of
Jeong et al. (2001)
for
P. kofoidii
. The cell volume of
O. rotunda
was calculated with an assumption that its geometry is an ellipsoid.
Conditions for the isolation and maintenance of the experimental organisms, and feeding occurrence by diverse heterotrophic protistan predators
FM, feeding mechanism; HTD, heterotrophic dinoflagellate; PD, peduncle feeder; N, the predator observed not to feed on a living M. rubrum cell; EG, engulfment feeder; Y, the predator observed to feed on a living M. rubrum cell; PA, pallium feeder; NC, naked ciliate; FF, filter feeder; MNC, Mixotrophic naked ciliate.
- Feeding occurrence
Experiment 1 was designed to test whether
G. shiwhaense, G. dominans, G. spirale, L. masanensis, O. rotunda, O. marina, P. piscicida, P. kofoidii, P. bipes
, and
S. algicida
, and the naked ciliate
Strombidium
sp. were able to feed on
M. rubrum
(
Table 1
).
Approximately 10,000
M. rubrum
cells were added to each of the two 42-mL polycarbonate (PC) bottles containing each of the heterotrophic dinoflagellates (2,000-10,000 cells) and the ciliates (10-80 cells) (final
M. rubrum
prey concentration = ca. 1,000-5,000 cells mL
-1
). One control bottle (without prey) was set up for each experiment. The bottles were placed on a plankton wheel rotating at 0.9 rpm and incubated at 20℃ under an illumination of 20 μE m
-2
s
-1
on a 14 h : 10 h light-dark cycle.
Five milliliter aliquots were removed from each bottle after 1, 2, 6, and 24 h incubation and then transferred into 6-well plate. Approximately 200 cells in the plate chamber were observed under a dissecting microscope at a magnification of 10-63× (SZX10; Olympus, Tokyo, Japan) to determine whether the predators were able to feed on
M. rubrum.
Predator cells containing prey cells were transferred onto glass slides and then their photographs were taken at a magnification of 400-1,000× with a camera mounted on an inverted microscope (Zeiss-Axiovert 200M; Carl Zeiss Ltd., Gottingen, Germany).
- Prey concentration effects on growth and ingestion rates
Experiment 2 was designed to measure the growth and ingestion rates of
G. dominans
as a function of
M. rubrum
concentration.
Dense cultures of
G. dominans
growing on the algal prey listed in
Table 1
were transferred to 500-mL PC bottles containing filtered seawater. The bottles were filled to capacity with freshly filtered seawater, capped, and placed on plankton wheels rotating at 0.9 rpm and incubated at 20℃ under an illumination of 20 μE m
-2
s
-1
on a 14 h : 10 h light-dark cycle. To monitor the conditions and interaction between the predator and prey species, the cultures were periodically removed from the rotating wheels, examined through the surface of the capped bottles using a dissecting microscope, and then returned to the rotating wheels. At timepoints at which prey cells were no longer present in ambient water, they were still observed inside the protoplasm of the predators. We therefore decided to starve the predators for 1 day in order to minimize possible residual growth resulting from the ingestion of prey during batch culture. After this incubation period, cell concentrations of
G. dominans
were determined in three 1-mL aliquots from each bottle using a light microscope, and the cultures were then used to conduct experiments.
For each experiment, the initial concentrations of
G. dominans
and
M. rubrum
were established using an autopipette to deliver predetermined volumes of known cell concentrations to the bottles. Triplicate 42-mL PC experiment bottles (mixtures of predator and prey) and triplicate control bottles (prey only) were set up at each predator-prey combination. Triplicate control bottles containing only
G. dominans
were also established at one predator concentration. To obtain similar water conditions, the water of predator cultures was filtered through a 0.7-μm GF/F filter and then added to the prey control bottles in the same amount as the predator culture for each predator-prey combination. All bottles were then filled to capacity with freshly filtered seawater and capped. To determine the actual predator and prey densities at the beginning of the experiment, a 5-mL aliquot was removed from each bottle, fixed with 5% Lugol’s solution, and examined using a light microscope to enumerate the cells in three 1-mL Sedgwick-Rafter chambers (SRCs). The bottles were refilled to capacity with freshly filtered seawater, capped, and placed on rotating wheels under the conditions described above. Dilution of the cultures associated with refilling the bottles was considered when calculating growth and ingestion rates. A 10-mL aliquot was taken from each bottle after 48-h incubation and fixed with 5% Lugol’s solution, and the abundance of
G. dominans
and prey were determined by counting all or >300 cells in three 1-mL SRCs. Before taking the subsamples, the conditions of
G. dominans
and their prey were assessed using a dissecting microscope as described above.
The specific growth rate of G. dominans, μ (d
-1
), was calculated as:
, where P
0
and P
t
= the concentration of
G. dominans
at 0 d and 2 d, respectively.
Data for
G. dominans
growth rates were fitted to a Michaelis-Menten equation:
, where μ
max
= the maximum growth rate (d
-1
); x = prey concentration (cells mL
-1
or ng C mL
-1
), x’ = threshold prey concentration (the prey concentration where μ = 0), K
GR
= the prey concentration sustaining 1/2 μ
max
. Data were iteratively fitted to the model using DeltaGraph (Delta Point).
Ingestion and clearance rates were calculated using the equations of
Frost (1972)
and
Heinbokel (1978)
. The incubation time for calculating ingestion and clearance rates was the same as that for estimating the growth rate. Ingestion rate data for
G. dominans
were also fitted to a Michaelis-Menten equation:
, where I
max
= the maximum ingestion rate (cells predator
-1
d
-1
or ng C predator
-1
d
-1
); x = prey concentration (cells mL
-1
or ng C mL
-1
), and K
IR
= the prey concentration sustaining 1/2 I
max
.
Additionally, the growth and ingestion rates of
L. masanensis, O. rotunda
, and
Strombidium
sp. on
M. rubrum
prey at a single prey concentration at which both growth and ingestion rates of
G. dominans
on
M. rubrum
were saturated were measured as described above.
- Cell volume ofGyrodinium dominans
After the 2-d incubation, the cell length and maximum width of
G. dominans
preserved in 5% acid Lugol’s solution (n = 20-30 for each prey concentration) were measured using an image analysis system on images collected with an inverted microscope (AxioVision 4.5; Carl Zeiss Ltd.). The shape of
G. dominans
was estimated to 2 cones joined at the cell equator (= maximum width of the cell). The carbon content was estimated from cell volume according to
Menden-Deuer and Lessard (2000)
.
- Grazing impact
We estimated grazing coefficients attributable to small heterotrophic
Gyrodinium
spp. (25-35 μm in cell length) on
Mesodinium
by combining field data on abundances of small
Gyrodinium
spp. and prey with ingestion rates of the predators on the prey obtained in the present study. We assumed that the ingestion rates of the other small heterotrophic
Gyrodinium
spp. on
M. rubrum
are the same as that of
G. dominans
. The data on the abundances of
M. rubrum
and co-occurring small heterotrophic
Gyrodinium
spp. used in this estimation were obtained from water samples collected in 2004-2005 from Masan Bay and in 2008-2009 from Shiwha Bay.
The grazing coefficients (g, h
-1
) were calculated as:
, where CR is the clearance rate (mL predator
-1
h
-1
) of a predator on
M. rubrum
at a given prey concentration and GC is the predator concentration (cells mL
-1
). CR’s were calculated as:
, where IR (h) is the ingestion rate (cells eaten predator
-1
h
-1
) of the predator on the prey and x is the prey concentration (cells mL
-1
). CR’s were corrected using Q
10
= 2.8 (
Hansen et al. 1997
) because in situ water temperatures and the temperature used in the laboratory for this experiment (20℃) were sometimes different.
RESULTS
- Feeding occurrence
Among the predators tested in the present study,
G. dominans, L. masanensis, O. rotunda, P. kofoidii
, and
Strombidium
sp. preyed on
M. rubrum
(
Table 1
,
Fig. 1
). However,
G. shiwhaense, G. spirale, O. marina, P. piscicida, P. bipes
, and
S. algicida
did not attempt to attack, even when it encountered
M. rubrum
.
Feeding by heterotrophic protistan predators on Mesodinium rubrum. (A & B) Gyrodinium dominans having 1-2 ingested M. rubrum cells. (C) Polykrikos kofoidii. (D) Strombidium sp. (E) Luciella masanensis. (F) Oblea rotunda. White arrows indicate prey (M. rubrum) materials. Scale bars represent: A-F, 10 μm.
- Growth and ingestion rates
The specific growth rates of
G. dominans
on
M. rubrum
increased rapidly with increasing mean prey concentration up to ca. 321 ng C mL
-1
(746 cells mL
-1
), but slowly at higher concentrations (
Fig. 2
). When the data were fitted to Eq. (2), the maximum specific growth rate (μ
max
) of
G. dominans
on
M. rubrum
was 0.48 d
-1
. The feeding threshold prey concentration for the growth of
G. dominans
(i.e., no growth) was 23.3 ng C mL
-1
(54 cells mL
-1
).
Specific growth rate of the heterotrophic dinoflagellate Gyrodinium dominans on Mesodinium rubrum as a function of mean prey concentration (x). Symbols represent treatment means ± 1 standard error. The curves are fitted by the Michaelis-Menten equation [Eq. (2)] using all treatments in the experiment. Growth rate (d-1) = 0.48 [(x - 23.3) / (325.7 + [x - 23.3])], r2 = 0.881.
The ingestion rates of
G. dominans
on
M. rubrum
increased rapidly with increasing mean prey concentration up to ca. 321 ng C mL
-1
(746 cells mL
-1
), but became saturated at higher concentrations (
Fig. 3
). When the data were fitted to Eq. (3), the maximum ingestion rate (I
max
) of
G. dominans
on
M. rubrum
was 0.55 ng C predator
-1
d
-1
(1.3 cells predator
-1
d
-1
). The maximum clearance rate of
G. dominans
on
M. rubrum
was 0.14 μL predator
-1
h
-1
.
Specific ingestion rates of the heterotrophic dinoflagellate Gyrodinium dominans on Mesodinium rubrum as a function of mean prey concentration (x). Symbols represent treatment means ± 1 standard error. The curves are fitted by the Michaelis-Menten equation [Eq. (3)] using all treatments in the experiment. Ingestion rate (ng C predator-1 d-1 = 0.55 [x / (94.6 + x)], r2 = 0.453.
The growth rates of
L. masanensis, O. rotunda
, and
Strombidium
sp. on
M. rubrum
prey at single prey concentrations (995-1,130 ng C mL
-1
) at which both growth and ingestion rates of
G. dominans
on
M. rubrum
were saturated were negative.
- Grazing impact
When the abundances of
M. rubrum
and small heterotrophic
Gyrodinium
spp. (25-35 μm in cell length) in Masan Bay in 2004-2005 and Shiwha Bay in 2008-2009 (n = 121) were 1-1,014 cells mL
-1
and 1-1,356 cells mL
-1
, respectively, grazing coefficients attributable to small heterotrophic
Gyrodinium
spp. on co-occurring
M. rubrum
were up to 0.236 h
-1
(
Fig. 4
).
Calculated grazing coefficients of small heterotrophic Gyrodinium spp. (n = 121) in relation to the concentration of co- occurring Mesodinium rubrum (see text for calculation). Clearance rates, measured under the conditions provided in the present study, were corrected using Q10 = 2.8 (Hansen et al. 1997) because in situ water temperatures and the temperature used in the laboratory for this experiment (20℃) were sometimes different. The scales of the circles in the inset boxes are g (h-1).
DISCUSSION
- Predators
Among the heterotrophic dinoflagellates and a ciliate investigated in this study,
G. dominans, L. masanensis, O. rotunda, P. kofoidii
, and
Strombidium
sp. prey on
M. rubrum
. With respect to feeding mechanisms,
G. dominans, P. kofoidii
, and
Strombidium
sp. feed on prey by direct engulfment, but
L. masanensis
by a peduncle, and
O. rotunda
by a pallium (
Strom and Buskey 1993
,
Kim and Jeong 2004
,
Jeong et al. 2007
,
Yoo et al. 2010
). Since organisms with different feeding modalities were able to graze on
M. rubrum
, we conclude that feeding mechanisms do not generally determine the ability of heterotrophic protists to feed on
M. rubrum
. In addition, the size range of the predators that can feed on
M. rubrum
is also wide, and thus this factor is also not a critical determinant of protist feeding on
M. rubrum. G. shiwhaense, G. spirale, O. marina, P. piscicida, P. bipes
, and
S. algicida
did not even attack
M. rubrum
when they encountered the ciliate. Thus,
G. dominans, L. masanensis, O. rotunda, P. kofoidii
, and
Strombidium
sp. may have an ability to detect
M. rubrum
cells by physical and / or chemical cues, while the other organisms may lack this feature.
M. rubrum
usually stay motionless for a second, but swim or jump quickly. When it jumps, the maximum swimming speeds of
M. rubrum
are 2,217-12,000 μm s
-1
, which are comparable to or greater than that of
G. dominans, O. rotunda, P. kofoidii
, and
Strombidium
sp. (2,533, 420, 1,182, and 4,000 μm s
-1
, respectively) (Lee, unpublished data) (
Barber and Smith 1981
cited by
Smayda 2002
,
Crawford 1992
,
Buskey et al. 1993
,
Crawford and Lindholm 1997
,
Kim and Jeong 2004
,
Fenchel and Hansen 2006
). Therefore,
G. dominans, O. rotunda, P. kofoidii
, and
Strombidium
sp. are likely to capture
M. rubrum
when they are motionless or when
M. rubrum
may bump into them and then stun them.
- Growth and ingestion rates
G. dominans
was the only predator whose growth actually increased when grazing on
M. rubrum
in this study, even though
L. masanensis, O. rotunda, P. kofoidii
, and
Strombidium
sp. also fed on
M. rubrum
. In addition, the mixotrophic dinoflagellates
Amylax triacantha
and
Dinophysis acuminata
are known to grow on
M. rubrum
(
Park et al. 2006
,
2013
,
Kim et al. 2008
). Therefore, during red tides dominated by
M. rubrum, G. dominans, A. triacantha
, and
D. acuminata
are expected to be present. In contrast,
L. masanensis, O. rotunda, P. kofoidii
, and
Strombidium
sp. may be absent due to a lack of co-occurring alternative optimal prey species. The maximum growth rate of
G. dominans
on
M. rubrum
(0.48 d
-1
) is lower than the mixotrophic growth rates of
A. triacantha
and
D. acuminata
on the same prey (0.68 and 0.91 d
-1
, respectively) (
Table 2
). A lower ingestion rate of
G. dominans
on
M. rubrum
(0.55 ng C predator
-1
d
-1
) when compared with
A. triacantha
(2.54 ng C predator
-1
d
-1
) and
D. acuminata
(1.30 ng C predator
-1
d
-1
) may be partially responsible for this lower growth rate. During
M. rubrum
red tides,
G. dominans
may be less abundant than
A. triacantha
and
D. acuminata
. However,
G. dominans
can grow on diverse algal prey species, while
A. triacantha
and
D. acuminata
can only grow on
M. rubrum
(
Nakamura et al. 1992
,
1995
,
Kim and Jeong 2004
,
Park et al. 2006
,
2013
,
Kim et al. 2008
,
Yoo et al. 2010
,
2013
,
Jeong et al. 2011
,
2014
). Thus, the abundance of
G. dominans
in the period of red tides that are not associated with
M. rubrum
may be greater than those of
A. triacantha
and
D. acuminata
. We suggest that future studies should compare the relative abundances of these three predators, and their grazing impact on prey populations, during
M. rubrum
-associated red tides.
Growth and ingestion rates of dinoflagellate predators when feeding onMesodinium rubrum
ESD, equivalent spherical diameter (µm); GR, growth rate (d-1); IR, ingestion rate (ng C predator-1 d-1); HTD, heterotrophic dinoflagellate; MTD, mixotrophic dinoflagellate
The maximum growth rate (μ
max
) of
G. dominans
on
M. rubrum
(0.48 d
-1
) is comparable to that on the mixotrophic dinoflagellates
Heterocapsa triquetra
and
Karenia mikimotoi
, and the raphidophyte
Chattonella antique
, but higher than that on the mixotrophic dinoflagellate
Biecheleria cincta
, the cryptophyte
Rhodomonas salina
, and the chlorophyte
Dunaliella teriolecta
(
Table 3
). However, the μ
max
of
G. dominans
on
M. rubrum
is lower than that observed with the mixotrophic dinoflagellates
Gymnodinium aureolum, Prorocentrum minimum
, and
Symbiodinium voratum
, the euglenophyte
Eutreptiella gymnastica
, and the diatom
Thalassiosira
sp. (
Table 3
).
M. rubrum
, these mixotrophic dinoflagellates, and the raphidophyte cause red tides in the waters of many countries (
Crawford 1989
,
Heil et al. 2005
,
Jeong et al. 2011
,
2013
,
Park et al. 2013
,
Yih et al. 2013
).
G. dominans
is likely to be more abundant during
M. rubrum
red tides than during
B. cincta, R. salina
, or
D. teriolecta
red tides, but less abundant during
E. gymnastica, G. aureolum
, or
P. minimum
red tides.
Comparison of growth and grazing data forGyrodinium dominanson diverse prey species
ESD, equivalent spherical diameter (μm); MGR, maximum growth rate (d-1); KGR, the prey concentration sustaining 1/2 μmax (ng C mL-1); x', threshold prey concentration (ng C mL-1); MIR, maximum ingestion rate (ng C predator -1 d-1); KIR, the prey concentration sustaining 1/2 Imax (ng C mL-1); RMGI, ratio of MGR relative to MIR. Rates are corrected to 20℃ using Q10 = 2.8 (Hansen et al. 1997); DIA, diatom; CR, cryptophyte; CH, chlorophyte; MTD, mixotrophic dinoflagellate; EU, euglenophyte; MNC, mixotrophic naked ciliate; RA, raphidophyte.
The maximum rate at which
G. dominans
can ingest
M. rubrum
is one of the lowest among the algal prey species, with the exception of
B. cincta
and comparable to that on
R. salina
(
Table 3
). Interestingly,
M. rubrum
and
Rhodomonas
spp. exhibit jumping behaviors (
Fenchel and Hansen 2006
,
Berge et al. 2008
). These jumping behaviors of
M. rubrum
may act as an anti-predation behavior. However, the ratio of the maximum growth rate relative to the maximum ingestion rate of
G. dominans
on
M. rubrum
is greater than that on any other algal prey, with the exception of
P. minimum
. Therefore,
M. rubrum
is likely to be the most nutritious algal prey for
G. dominans, P. minimum
notwithstanding.
In the numerical response of
G. dominans
to four algal prey species, the feeding threshold prey concentration for growth of
G. dominans
on
M. rubrum
is lower than that of
E. gymnastica
or
G. aureolum
, but higher than that of
S. voratum
(
Table 3
,
Fig. 5A
). Therefore,
G. dominans
may preferentially grow on
M. rubrum
rather than on
E. gymnastica
or
G. aureolum
at low prey concentrations. The K
GR
(the prey concentration sustaining 1/2 μ
max
) of
G. dominans
on
M. rubrum
is greater than that on
G. aureolum
, and
S. voratum
, but lower than that on
E. gymnastica
. Therefore, the growth of
G. dominans
on
M. rubrum
is more sensitive to a change in prey concentration than the same parameter in
E. gymnastica
, but less sensitive than
G. aureolum
, and
S. voratum
. The functional response of
G. dominans
feeding on diverse algal prey species follows a Holling type II pattern (
Holling 1959
). With respect to the functional response of
G. dominans
to eight algal prey species, the K
IR
(the prey concentration sustaining 1/2 I
max
) when grown on
M. rubrum
is greater than that obtained with
R. salina, P. minimum, D. teriolecta
, and
H. triquetra
, but lower than that obtained with
E. gymnastica, G. aureolum
, and
S. voratum
(
Fig. 5B
). Therefore, the ingestion of
G. dominans
on
M. rubrum
is more sensitive to a change in prey concentration than
E. gymnastica, G. aureolum
, and
S. voratum
, but less sensitive than
R. salina, P. minimum, D. teriolecta
, and
H. triquetra
.
A comparison of the numerical (A) and functional (B) responses of the heterotrophic dinoflagellate Gyrodinium dominans feeding on diverse prey related to prey concentration. Rates are corrected to 20℃ using Q10 = 2.8 (Hansen et al. 1997). Eg, Eutreptiella gymnastica, euglenophyte; Ga, Gymnodinium aureolum, mixotrophic dinoflagellate; Sv, Symbiodinium voratum, mixotrophic dinoflagellate; Mr, Mesodinium rubrum, mixotrophic ciliate; Ht, Heterocapsa triquetra, mixotrophic dinoflagellate; Dt, Dunaliella tertiolecta, chlorophyte; Pm, Prorocentrum minimum, mixotrophic dinoflagellate; Rs, Rhodomonas salina, cryptophyte. All responses in (A) were fitted to Eq. 2, whereas those in (B) were fitted to Eq. 3.
- Grazing impact
To our knowledge, prior to this study, there had been no reports on the impact of protist grazing on
Mesodinium
populations. Grazing coefficients derived from studies in Masan Bay in 2004-2005 and Shiwha Bay in 2008-2009 show that up to 21% of
M. rubrum
populations can be removed by small
Gyrodinium
populations in approximately 1 d. Therefore, small heterotrophic
Gyrodinium
spp. can have a considerable grazing impact on populations of
M. rubrum
under suitable conditions.
G. dominans
is one of the few protistan grazers that are able to feed on
M. rubrum
, and is the only protistan grazer with a documented grazing impact on
M. rubrum
abundance. This finding should be taken into consideration when developing models to explain the red tide dynamics of
M. rubrum
.
Acknowledgements
We thank Dr. Yeong Du Yoo, Seong Yeon Lee, and Kila Park for technical supports. This work was supported by the National Research Foundation of Korea Grant funded by the Korea Government / Ministry of Science, ICT and Future Planning (NRF-2010-0020702 and NRF-2012R1A2A2A01010987), Pilot project for predicting the outbreak of Cochlodinium red tide funded by MICTFP (NRF-2014M4A1H5009428), and Management of marine organisms causing ecological disturbance and harmful effect Program of Korea Institute of Marine Science and Technology Promotion (KIMST) of KIMST award to HJJ.
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