Research Article
Algae 2013, 28(4): 343-354
http://dx.doi.org/10.4490/algae.2013.28.4.343
Open Access
Growth and ingestion rates of heterotrophic dinoflagellates and a
ciliate on the mixotrophic dinoflagellate Biecheleria cincta
Yeong Du Yoo1,*, Eun Young Yoon2, Kyung Ha Lee3, Nam Seon Kang3 and Hae Jin Jeong3
Marine Biology Research Division, Scripps Institution of Oceanography, University of California at San Diego, La Jolla,
CA 92093-0202, USA
2
Advanced Institutes of Convergence Technology, Seoul National University-Gyeonggi Province, Suwon 443-270, Korea
3
School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University, Seoul 151-747, Korea
1
To explore the interactions between the mixotrophic dinoflagellate Biecheleria cincta (previously Woloszynskia cincta)
and heterotrophic protists, we investigated whether the common heterotrophic dinoflagellates Gyrodinium dominans,
Gyrodinium moestrupii, Gyrodinium spirale, Oxyrrhis marina, and Polykrikos kofoidii, and the ciliate Strobilidium sp.
were able to feed on B. cincta. We also measured growth and ingestion rates of O. marina and Strobilidium sp. on B. cincta
as a function of prey concentration. In addition, these rates were measured for other predators at single prey concentrations at which the growth and ingestion rates of O. marina and Strobilidium sp. were saturated. All grazers tested in the
present study were able to feed on B. cincta. B. cincta clearly supported positive growth of O. marina, G. dominans, and
Strobilidium sp., but it did not support that of G. moestrupii, G. spirale, and P. kofoidii. The maximum growth rates of
Strobilidium sp. and O. marina on B. cincta (0.91 and 0.49 d-1, respectively) were much higher than that of G. dominans
(0.07 d-1). With increasing the mean prey concentration, the specific growth rates of O. marina and Strobilidium sp. on B.
cincta increased, but either became saturated or slowly increased. The maximum ingestion rate of Strobilidium sp. (1.60
ng C predator-1 d-1) was much higher than that of P. kofoidii and O. marina (0.55 and 0.34 ng C predator-1 d-1) on B. cincta.
The results of the present study suggest that O. marina and Strobilidium sp. are effective protistan grazers of B. cincta.
Key Words: graze; growth; harmful algal bloom; ingestion; protist; red tide
INTRODUCTION
Phototrophic dinoflagellates are ubiquitous and sometimes dominate the abundance and biomass of plankton
assemblages in marine environments (Porter et al. 1985,
Hallegraeff 1993, Lindberg et al. 2005, Jeong et al. 2010a,
2013b). They can sometimes form dense blooms so called
red tides or harmful algal blooms in marine ecosystem
(Eppley and Horrison 1975, Burkholder et al. 2008, Kang
et al. 2013, Park et al. 2013a). Dense blooms dominated
by phototrophic dinoflagellates can upset the balance
of food webs and cause great loss to the aquaculture
and tourist industries in many countries (e.g., Park et al.
2013b). Furthermore, phototrophic dinoflagellates play
diverse roles in marine planktonic food webs (Anderson et al. 2002, Yoo et al. 2009, Jeong et al. 2010b, Hansen
2011); they are primary producers (Tillmann et al. 2009),
predators feeding on diverse prey items (Park et al. 2006,
Berge et al. 2008, Yoo et al. 2010b, Jeong et al. 2012), and,
in turn, act as prey for diverse predators (Jeong and Latz
This is an Open Access article distributed under the terms of the
Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted
non-commercial use, distribution, and reproduction in any medium,
provided the original work is properly cited.
Received July 30, 2013, Accepted November 17, 2013
Copyright © The Korean Society of Phycology
*Corresponding Author
E-mail: ydyoo@ucsd.edu
Tel: +1-858-534-7110, Fax: +1-858-534-7313
343
http://e-algae.kr pISSN: 1226-2617 eISSN: 2093-0860
Algae 2013, 28(4): 343-354
1994, Jeong 1999, Tillmann 2004, Jeong et al. 2010b, Kim
et al. 2013, Yoo et al. 2013b). Therefore, to understand the
roles of phototrophic dinoflagellates in the food web, we
must collate data on growth and mortality due to predation.
The phototrophic dinoflagellate Biecheleria cincta was
previously named Woloszynskia cincta (Siano et al. 2009,
Kang et al. 2011). However, this dinoflagellate has since
been reclassified and moved from the genus Woloszynskia to the genus Biecheleria because it has genetic and
morphological characteristics that more closely resemble
Biecheleria, including an apical furrow apparatus formed
by a single elongated narrow vesicle extending over the
apex from the ventral to the dorsal side of the cell (Moestrup et al. 2009, Kang et al. 2011, Balzano et al. 2012, Luo
et al. 2013). In addition, it has chloroplasts and eyespots
that are formed by a stack of cisternae containing bricklike material (type E sensu) (Moestrup et al. 2009, Kang et
al. 2011). The presence of this species has been reported
in the coastal waters of Korea (Kang et al. 2011).
Recently, Kang et al. (2011) discovered that B. cincta,
originally thought to be an exclusively phototrophic dinoflagellate, is a mixotrophic dinoflagellate; it feeds on
diverse prey such as the haptophyte Isochrysis galbana,
the cryptophytes Teleaulax sp. and Rhodomonas salina,
the raphidophyte Heterosigma akashiwo, the euglenophyte Eutreptiella gymnastica, and the dinoflagellates
Heterocapsa rotundata and Amphidinium carterae. However, to date, there have been no studies on the mortality of B. cincta due to predation. Grazing pressure sometimes plays an important role in controlling populations
of phototrophic dinoflagellates (Watras et al. 1985, Turner
2006, Kang et al. 2013, Yoo et al. 2013a). Heterotrophic dinoflagellates and ciliates are the major components of
heterotrophic protist communities (Sherr and Sherr 2007,
Jeong et al. 2011, Yoo et al. 2013a). They are effective grazers on many phototrophic dinoflagellates (Eppley and
Harrison 1975, Jeong et al. 2013a, Yoo et al. 2013b). Thus,
to understand the population dynamics of B. cincta, the
predator-prey relationships between B. cincta and common heterotrophic dinoflagellates and ciliates should be
investigated.
We established a clonal culture of Biecheleria cincta
isolated from Shiwha Bay, Korea in 2009. In the present
study, using this culture we investigated feeding by five
common heterotrophic dinoflagellates and one ciliate
on this dinoflagellate; 1) we tested whether the common
heterotrophic dinoflagellates Gyrodinium dominans, G.
moestrupii, G. spirale, Oxyrrhis marina, and Polykrikos
kofoidii and the ciliate Strobilidium sp. were able to
http://dx.doi.org/10.4490/algae.2013.28.4.343
feed on B. cincta. 2) We also measured the growth and/
or ingestion rates of O. marina and Strobilidium sp. on
B. cincta as a function of prey concentration. 3) In addition, the growth and ingestion rates were measured for
G. dominans, G. moestrupii, G. spirale, and P. kofoidii at
single prey concentrations at which these rates of O. marina and Strobilidium sp. were saturated. 4) Additionally,
we compared the growth and ingestion rates of heterotrophic protists in the present study of B. cincta to those of
other prey species reported in the literature.
The results of the present study provide a basis for understanding the interactions between B. cincta and heterotrophic protists and their population dynamics in marine planktonic food webs.
MATERIALS AND METHODS
Preparation of experimental organisms
For isolation and culture of Biecheleria cincta (GenBank accession No. FR690459), plankton samples collected with water samplers were taken from Shiwha Bay,
Korea during June 2009 when the water temperature and
salinity were 22.0°C and 29.3, respectively (Table 1). These
samples were screened gently through a 154-µm Nitex
mesh and placed in 6-well tissue culture plates. A clonal
culture of B. cincta was established by two serial single
cell isolations as described by Kang et al. (2011).
For the isolation and culture of the heterotrophic dinoflagellate predators Gyrodinium dominans, G. moestrupii, G. spirale, Oxyrrhis marina, and Polykrikos kofoidii,
plankton samples collected with water samplers were
taken from the coastal waters off Masan, Saemankeum,
or Keum estuary, Korea in 2001-2009, and a clonal culture
of each species was established by two serial single-cell
isolations (Table 1).
For the isolation and culture of Strobilidium sp., plankton samples collected with water samplers were taken
from a pier in Shiwha Bay, Korea, during May 2010 when
the water temperature and salinity were 17.7°C and 27.8,
respectively (Table 1). A clonal culture of Strobilidium sp.
(30-50 µm in cell length) was established by two serial
single cell isolations as described by Jeong et al. (2008a).
The carbon contents for B. cincta (0.1 ng C per cell),
the heterotrophic dinoflagellates, and the ciliate were estimated from the cell volume according to the methods
described by Menden-Deuer and Lessard (2000). The cell
volume of the predators was estimated using the methods
described by Jeong et al. (2008b) and Jeong et al. (2008a)
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Yoo et al. Feeding by Predators on Biecheleria
for O. marina and Strobilidium sp., respectively.
ton wheel rotating at 0.9 rpm and incubated at 20°C under an illumination of 20 µmol photons m-2 s-1 on a 14 : 10
h light-dark cycle.
Five milliliters aliquots were removed from each bottle
after 1, 2, 6, 24, and 48-h incubation periods and then
transferred into 6-well plate chambers (or slide glasses).
Approximately 100 cells of predators at different stages of the feeding process in the plate chamber (or slide
glasses) were observed under a dissecting microscope
(or inverted microscope) at a magnification of ×20-90 (or
×100-630) to determine whether the predators were able
to feed on B. cincta. Cells from those predators that contained ingested B. cincta cells were photographed using a
digital camera (Zeiss AxioCam HRc5; Carl Zeiss Ltd., Göttingen, Germany) on the microscope at a magnification
of ×400-630.
Feeding occurrence
Experiment 1 was designed to investigate whether G.
dominans, G. moestrupii, G. spirale, O. marina, P. kofoidii,
and Strobilidium sp. were able to feed on B. cincta (Table
2). The concentrations of each predator species offered
were similar in terms of carbon biomass.
Approximately 4.8 × 105 B. cincta cells were added to
each of two 80 mL polycarbonate (PC) bottles containing G. dominans, G. moestrupii, G. spirale (100-500 cells
mL-1), P. kofoidii (30 cells mL-1), and Strobilidium sp. (30
cells mL-1) (final B. cincta prey concentration = ca. 6,000
cells mL-1). One control bottle (without prey) was set up
for each experiment. The bottles were placed on a plank-
Table 1. Isolation and maintenance conditions of the experimental organisms
Organism
Location
Date
T
S
Prey species
Concentration
Amphidinium
carterae
Alexandrium
minutum
Prorocentrum
minimum
Amphidinium
carterae
Lingulodinium
polyedrum
30,000-40,000
Teleaulax sp.
Heterosigma
akashiwo
50,000-60,000
10,000-15,000
Gyrodinium dominans (HTD)
Masan Bay
Apr 2007
15.1
33.4
Gyrodinium moestrupii (HTD)
Off Saemankeum
Oct 2009
21.2
31.0
Gyrodinium spirale (HTD)
Masan Bay
May 2009
19.7
31.0
Oxyrrhis marina (HTD)
Keum Estuary
May 2001
16.0
27.7
Polykrikos kofoidii (HTD)
Masan Bay
Jun 2007
20.2
32.2
Strobilidium sp. (CIL)
Biecheleria cincta (MTD)
Shiwha Bay
Shiwha Bay
May 2010
Jun 2009
17.7
22.0
27.8
29.3
8,000-10,000
20,000-30,000
8,000
4,000
Sampling location and date, water temperature (T, oC), salinity (S, practical salinity units) for isolation, and prey species and concentrations (cells
mL-1) for maintenance.
HTD, heterotrophic dinoflagellate; CIL, ciliate; MTD, mixotrophic dinoflagellate.
Table 2. Design of the experiments
Exp. no.
1
Prey
Predator
Species
Density
Biecheleria cincta
6,000
Species
Density
Feeding
Gyrodinium dominans
500
Y
Gyrodinium moestrupii
200
Y
Gyrodinium spirale
100
Y
Oxyrrhis marina
500
Y
Polykrikos kofoidii
30
Y
Strobilidium sp.
30
Y
2
Biecheleria cincta
20, 60, 130, 510, 1,690, 3,670, 6,420
Oxyrrhis marina
3, 4, 6, 12, 19, 39, 73, (6)
-
3
Biecheleria cincta
20, 80, 240, 850, 2,640, 5,310, 6,930
Strobilidium sp.
5, 12, 14, 24, 23, 35, 35, (12)
-
The numbers in the prey and predator columns are the actual initial densities (cells mL-1) of the prey and predator. Values in the parentheses in
the predator column are the predator densities in the control bottles. Feeding occurrence of each predator fed Biecheleria cincta is represented by
Y (feeding observed).
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Algae 2013, 28(4): 343-354
Effects of prey concentration on growth and
ingestion rates
was taken from each bottle after a 48-h incubation period
and fixed with 5% Lugol’s solution, and the abundance of
O. marina (or Strobilidium sp.) and B. cincta were determined by counting all or >200 cells in three 1-mL SRCs.
Prior to taking the subsamples, the conditions of O. marina (or Strobilidium sp.) and its prey were assessed using a dissecting microscope, as described earlier in this
section.
The specific growth rate of O. marina (or Strobilidium
sp.), µ (d-1) was calculated as follows:
Experiments 2 and 3 were designed to measure the
growth, ingestion, and clearance rates of O. marina and
Strobilidium sp. as a function of the prey concentrations
when fed on B. cincta (Table 2).
A dense culture of ~15,000 cells mL–1 of B. cincta
grown mixotrophically on the raphidophyte Heterosigma
akashiwo in the f/2 medium (Guillard and Ryther 1962,
Kang et al. 2011) under the illumination of 20 µmol photons m-2 s-1 on a 14 : 10 h light : dark cycle was transferred
to a 250-mL PC bottle containing the f/2 medium wherein H. akashiwo was undetectable. This culture was maintained in the f/2 medium for 2 d under the illumination of
20 µmol photons m-2 s-1 on a 14 : 10 h light : dark cycle and
then transferred to another 250-mL PC bottle containing filtered seawater. Three 1-mL aliquots from the bottle
were examined using a light microscope to determine
the concentration of B. cincta cells, and the cultures were
then used in further experiments.
Furthermore, dense cultures of O. marina (or Strobilidium sp.) growing on algal prey were transferred into
250-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°C under the illumination of 20
mol photons m-2 s-1 on a 14 : 10 h light : dark cycle.
For each experiment, the initial concentrations of O.
marina (or Strobilidium sp.) and B. cincta were established using an autopipette to deliver predetermined
volumes of known cell concentrations to the bottles.
Triplicate 42-mL PC experimental bottles (mixtures of
predator and prey) and triplicate control bottles (prey
only) were set up for each predator-prey combination.
Triplicate control bottles containing only O. marina (or
Strobilidium sp.) were also established for a single predator concentration. All the bottles were 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 then examined
under a light microscope to determine predator and prey
abundance by enumerating 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
earlier in this section. Dilution of cultures associated with
the refilling of bottles was taken into consideration when
calculating growth and ingestion rates. A 10-mL aliquot
http://dx.doi.org/10.4490/algae.2013.28.4.343
µ = [ln (Gt/G0)] / t
(1)
, where G0 and Gt are the concentration of O. marina (or
Strobilidium sp.) at time (t) 0 and 2 d, respectively.
Data for O. marina (or Strobilidium sp.) growth rates
were fitted to a modified Michaelis-Menten equation:
µ
µ=
max
(x – x')
K GR + (x – x')
(2)
, where µmax = 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), and
KGR = the prey concentration sustaining 1/2 µmax. Data
were iteratively fitted to the model using DeltaGraph
(Delta Point Inc., Monterey, CA, USA).
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 growth rate. Data for
O. marina (or Strobilidium sp.) ingestion rates (IR, cells
predator-1 d-1 or ng C predator-1 d-1) were fitted to a modified Michaelis-Menten equation:
IR =
Imax(x)
K IR + (x)
(3)
, where Imax = 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 KIR = the prey concentration sustaining 1/2 Imax.
Comparison of growth and ingestion rates at
single prey concentrations
Experiment 4 was designed to compare the growth and
ingestion rates of G. dominans, G. moestrupii, G. spirale,
and P. kofoidii when B. cincta was provided at a single
prey concentration (Table 3). Growth and ingestion rates
of O. marina and Strobilidium sp. at single prey concen-
346
Yoo et al. Feeding by Predators on Biecheleria
trations were obtained in Experiment 2 and 3.
The B. cincta culture was prepared as described earlier
in this section. In addition, G. dominans, G. moestrupii, G.
spirale, and P. kofoidii were cultured in the same manner
as described earlier in this section.
The initial concentrations of G. dominans (or another
predator) and B. cincta were established using an autopipette to deliver predetermined volumes of known cell
concentrations to the bottles. Triplicate 42-mL PC experimental bottles containing mixtures of G. dominans (or
another predator) and B. cincta, triplicate prey control
bottles containing B. cincta only, and triplicate predator control bottles containing only G. dominans (or another predator) were set up for B. cincta. Next, 5 mL of
the f/2 medium was added to all the bottles, which were
then filled to capacity with freshly filtered seawater and
capped. To determine the predator and prey concentrations at the beginning of the experiment and the prey
concentrations after 2 d, a 5-mL aliquot was removed
from each bottle and fixed with 5% (v/v) Lugol’s solution;
then, all or >200 predator and prey cells from three 1-mL
SRCs were enumerated. Prior to taking subsamples, the
conditions of G. dominans (or other predators) and B.
cincta were assessed using a dissecting microscope. The
bottles were, again, filled to capacity with freshly filtered
seawater, capped, and placed on a rotating wheel at 0.9
rpm at 20°C under the illumination of 20 µmol photons
m-2 s-1 on a 14 : 10 h light : dark cycle. The dilution of the
cultures associated with the refilling of bottles was taken
into consideration when calculating the growth and ingestion rates.
The growth and ingestion rates were measured in the
same manner as described for Experiments 2 and 3.
Gross growth efficiency (GGE)
GGE, defined as grazer biomass produced (+) or lost (–)
per prey biomass ingested, was calculated from the estimates of carbon contents per cell based on the cell volume for each mean prey concentration.
RESULTS
Feeding occurrence and growth
It was observed that G. dominans, G. moestrupii, G. spirale, O. marina, P. kofoidii, and Strobilidium sp. fed on B.
cincta (Table 2, Fig. 1). All predators in the present study
fed on prey by engulfing the prey cells.
B. cincta clearly supported positive growth rates for O.
marina, G. dominans, and Strobilidium sp. but did not
support the growth of G. moestrupii, G. spirale, or P. kofoidii.
Effects of prey concentrations on growth and
ingestion rates
The specific growth rates of O. marina on B. cincta increased rapidly with increasing mean prey concentration
<ca. 12 ng C mL-1 (120 cells mL-1), but became saturated
or slowly increased at higher concentrations (Fig. 2).
When the data were fitted to Eq. (2), the maximum specific growth rates of O. marina was 0.49 d-1. The feeding
threshold prey concentration for the growth of O. marina
was 1.4 ng C mL-1 (14 cells mL-1).
The specific growth rates of Strobilidium sp. on B.
cincta increased rapidly with increasing mean prey concentration <ca. 71 ng C mL-1 (710 cells mL-1), but became
slowly increased at higher concentrations (Fig. 3). When
the data were fitted to Eq. (2), the maximum specific
growth rates of Strobilidium sp. was 0.91 d-1. The feeding
threshold prey concentration for the growth of Strobilidium sp. was 11.8 ng C mL-1 (118 cells mL-1).
The ingestion rates of O. marina on B. cincta increased
rapidly with increasing mean prey concentration <ca. 45
ng C mL-1 (450 cells mL-1), but became saturated or slowly
increased at higher concentrations (Fig. 4). When the data
were fitted to Eq. (3), the maximum ingestion rates of O.
marina was 0.35 ng C predator-1 d-1 (3.5 cells predator-1
d-1). The maximum clearance rate of O. marina was 1.47
Table 3. Comparison in growth (GR, d-1) and ingestion rates (IR, ng
C predator-1 d-1) (means ± standard errors, n = 3) protistan predators
on mixotrophic dinoflagellate Biecheleria cincta at single mean prey
concentrations (MPC, ng C mL-1) where GR and IR of Oxyrrhis marina
and Strobilidium sp. on B. cincta were saturated
Predators
MPC
GR
IR
Oxyrrhis marina (HTD)
600
Gyrodinium dominans (HTD)
562
Gyrodinium moestrupii (HTD)
487
Gyrodinium spirale (HTD)
512
Polykrikos kofoidii (HTD)
481
Strobilidium sp. (CIL)
504
0.436
(0.023)
0.069
(0.018)
-0.086
(0.037)
-0.198
(0.020)
-0.253
(0.009)
0.706
(0.054)
0.34
(0.03)
0.13
(0.02)
0.10
(0.03)
0.04
(0.02)
0.55
(0.05)
1.60
(0.17)
HTD, heterotrophic dinoflagellate; CIL, ciliate.
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Algae 2013, 28(4): 343-354
A
C
B
D
E
Fig. 1. Feeding by heterotrophic dinoflagellates (A-D) and a ciliate (E) on the mixotrophic dinoflagellate Biecheleria cincta. (A) Gyrodinium
dominans with an ingested B. cincta cell. (B) Gyrodinium spirale with an ingested B. cincta cell. (C) Oxyrrhis marina with several ingested B. cincta
cells. (D) Polykrikos kofoidii with two ingested B. cincta cells. (E) Strobilidium sp. with two ingested B. cincta cells. Arrows indicate ingested prey
cells. All photographs were taken using an inverted microscope. Scale bars represent: A-E, 10 µm.
µL predator-1 h-1. GGEs of O. marina on B. cincta at prey
concentrations where the ingestion rates were saturated
were 45-53% (Table 4).
The ingestion rates of Strobilidium sp. on B. cincta increased rapidly with increasing mean prey concentration
<ca. 236 ng C mL-1 (2,360 cells mL-1), but became slowly
increased at higher concentrations (Fig. 5). When the
data were fitted to Eq. (3), the maximum ingestion rates
of Strobilidium sp. was 2.0 ng C predator-1 d-1 (20.0 cells
predator-1 d-1). The maximum clearance rate of Strobilidium sp. was 1.72 µl predator-1 h-1. GGEs of Strobilidium sp.
on B. cincta at prey concentrations where the ingestion
http://dx.doi.org/10.4490/algae.2013.28.4.343
rates increased slowly were 25-32% (Table 4).
Comparison of growth and ingestion rates at
single prey concentrations
When the mean prey concentrations were 480-600 ng
-1
C mL , the specific growth rate of Strobilidium sp. (0.71
d-1) on B. cincta was significantly higher than that of O.
marina (0.44 d-1) or G. dominans (0.07 d-1) (p < 0.01, twotailed t-test). However, the growth rates of G. moestrupii,
G. spirale, and P. kofoidii were negative (Table 3).
The ingestion rate of Strobilidium sp. (1.60 ng C preda-
348
Yoo et al. Feeding by Predators on Biecheleria
Fig. 2. Specific growth rates of the heterotrophic dinoflagellate
Fig. 3. Specific growth rates of the ciliate Strobilidium sp. on the
Fig. 4. Ingestion rates of the heterotrophic dinoflagellate Oxyrrhis
Fig. 5. Ingestion rates of the ciliate Strobilidium sp. on the mixotro-
Oxyrrhis marina on the mixotrophic dinoflagellate Biecheleria cincta
as a function of mean prey concentration (x). Symbols represent
treatment means ± 1 SE. The curves are fitted according to the
Michaelis-Menten equation [Eq. (2)] using all treatments in the
experiment. Growth rate (d-1) = 0.492{(x - 1.38)/[5.67 + (x - 1.38)]},
r2 = 0.843.
mixotrophic dinoflagellate Biecheleria cincta as a function of mean
prey concentration (x). Symbols represent treatment means ± 1 SE.
The curves are fitted according to the Michaelis-Menten equation [Eq.
(2)] using all treatments in the experiment. Growth rate (d-1) = 0.910
{(x - 11.8)/[34.8 + (x - 11.8)]}, r2 = 0.911.
phic dinoflagellate Biecheleria cincta as a function of mean prey concentration (x). Symbols represent treatment means ± 1 SE. The curves
are fitted according to the Michaelis-Menten equation [Eq. (3)] using
all treatments in the experiment. Ingestion rate (ng C predator-1 d-1) =
1.98 [x/(62.2 + x)], r2 = 0.884.
marina on the mixotrophic dinoflagellate Biecheleria cincta as
a function of mean prey concentration (x). Symbols represent
treatment means ± 1 SE. The curves are fitted according to the
Michaelis-Menten equation [Eq. (3)] using all treatments in the
experiment. Ingestion rate (ng C predator-1 d-1) = 0.35[x/(9.22 + x)],
r2 = 0.777.
Table 4. Growth and grazing data for the Oxyrrhis marina and Strobilidium sp. on Biecheleria cincta
Predator
Oxyrrhis marina (HTD)
Strombilidium sp. (CIL)
PDV
µmax
KGR
x'
Imax
KIR
Cmax
GGE
1.1
11.4
0.49
0.91
5.67
34.8
1.38
11.8
0.35
1.98
9.22
62.2
1.47
1.72
45-53
25-32
Parameters are for numerical and/or functional responses from Eqs. (2) and (3), as presented in Figs 2-5.
PDV, predator’s volume (×103 µm3); µmax, maximum growth rate (d-1); KGR, prey concentration sustaining 1/2 µmax (ng C mL-1); x’, threshold prey
concentration (ng C mL-1); Imax, maximum ingestion rate (ng C predator-1 d-1); KIR, prey concentration sustaining 1/2 Imax (ng C mL-1); Cmax, maximum
clearance rate (µL predator-1 h-1); GGE, gross growth efficiency, %, of predators feeding on B. cincta at the prey concentrations where the ingestion
rates were saturated or the 3 highest ingestion rates were achieved; HTD, heterotrophic dinoflagellate; CIL, ciliate.
349
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Algae 2013, 28(4): 343-354
DISCUSSION
A
Feeding occurrence and growth
To the best of our knowledge, this study is the first report on feeding by heterotrophic protistan predators on
B. cincta. All heterotrophic protistan predators investigated in the present study were able to feed on B. cincta
by engulfing the cells. These heterotrophic protists commonly occur in many marine environments (Goldman
et al. 1989, Yoo et al. 2010a, Jeong et al. 2011, Yoon et al.
2012). Thus, heterotrophic protists should be considered
predators of B. cincta in marine food webs.
O. marina, G. dominans, and Strobilidium sp. exhibited positive growth rates when feeding on B. cincta but G.
moestrupii, G. spirale, and P. kofoidii did not. Thus, during
blooms dominated by B. cincta, O. marina, G. dominans,
and Strobilidium sp. are likely to be abundant, while G.
moestrupii, G. spirale, and P. kofoidii may not be present.
B. cincta can be a critical prey for selecting dominant species among heterotrophic protistan communities.
B
C
Growth and ingestion rates
The growth rates for G. moestrupii, G. spirale, and P. kofoidii feeding on B. cincta were negative, while those for
O. marina or Strobilidium sp. were relatively high (Table
3). For G. moestrupii, G. spirale, and P. kofoidii feeding on
B. cincta, their ingestion rates (0.10, 0.04, and 0.55 ng C
predator-1 d-1, respectively) were much lower than their
carbon contents (0.4, 1.3, and 4.2 ng C cell-1, respectively)
(Jeong et al. 2001b, Kim and Jeong 2004, Yoo et al. 2013b).
Thus, low ingestion rates for G. moestrupii, G. spirale,
and P. kofoidii on B. cincta are likely responsible for their
negative growth rates. However, growth rates for G. moestrupii, G. spirale, and P. kofoidii are high when feeding on
algal prey (Jeong et al. 2001b, Kim and Jeong 2004, Yoo et
al. 2013b). The maximum growth rates for G. moestrupii,
G. spirale, and P. kofoidii when feeding on optimal prey
(e.g., Alexandrium minutum, Prorocentrum minimum,
and Gymnodinium catenatum) are as high as 1.60, 1.13,
and 1.12 d-1, respectively (Jeong et al. 2001b, Kim and
Jeong 2004, Yoo et al. 2013b). We assume that the ecological niches of G. moestrupii, G. spirale, and P. kofoidii may
be different from those of O. marina or Strobilidium sp.,
and competition among these protistan grazers might reduce when feeding on certain prey.
Among the maximum growth (µmax) and ingestion rates
(Imax) of O. marina feeing on diverse prey items, the µmax
of O. marina on B. cincta is similar than that on Azadini-
Fig. 6. Growth (GR) and ingestion rates (IR) of heterotrophic
dinoflagellates and the ciliate on the mixotrophic dinoflagellate
Biecheleria cincta as a single prey concentration where the growth
and ingestion rates of Oxyrrhis marina and Strobilidium sp. were
saturated. GR (A) and IR (B) of the predators on B. cincta as a function
of predator size (equivalent spherical diameter, ESD, µm). (C) The GR
of predators on B. cincta as a function of the IR (as shown in Table
3). The p-values in (A), (B), and (C) were all p > 0.1 (linear regression
ANOVA). Gd, Gyrodinium dominans; Gm, Gyrodinium moestrupii;
Gs, Gyrodinium spirale; Om, O. marina; Pk, Polykrikos kofoidii; St,
Strobilidium sp.
tor-1 d-1) on B. cincta was significantly higher than that of
P. kofoidii (0.55 ng C predator -1 d-1), O. marina (0.34 ng C
predator -1 d-1), G. dominans (0.13 ng C predator -1 d-1), G.
moestrupii (0.10 ng C predator -1 d-1), or G. spirale (0.04 ng
C predator -1 d-1) (p < 0.01, two-tailed t-test).
Both growth and ingestion rates of the heterotrophic
protists feeding on B. cincta in the present study were not
significantly correlated with the predators’ equivalent
spherical diameter (p > 0.1, linear regression analysis of
variance [ANOVA]) (Fig. 6A & B). Moreover, the growth
rates were not significantly correlated with ingestion
rates (p > 0.1, ANOVA) (Fig. 6C).
http://dx.doi.org/10.4490/algae.2013.28.4.343
350
Yoo et al. Feeding by Predators on Biecheleria
um cf. poporum (Table 5). However, the Imax of O. marina
on B. cincta is lower than that on A. cf. poporum (Potvin
et al. 2013). Therefore, the nutritional value of B. cincta
for growth of O. marina may be greater than that of A.
cf. poporum. The µmax of O. marina feeding on B. cincta
is lower than that on the other algal prey species except
a toxic strain of Karlodinium veneficum, but higher than
that on the heterotrophic nanoflagellate Cafeteria sp. and
the heterotrophic dinoflagellates Luciella masanensis
and Stoeckeria algicida (Table 5). Therefore, B. cincta is a
better prey item for O. marina than these heterotrophic
nanoflagellate and heterotrophic dinoflagellates, but less
favorable prey than the other algal prey species, except
K. veneficum. The Imax of O. marina feeding on B. cincta is
lower than that on the other algal prey species except the
mixotrophic dinoflagellate Gymnodinium aureolum, but
higher than that on Cafeteria sp., Pfiesteria piscicida, L.
masanensis, and S. algicida (Table 5). Therefore, the lower
ingestion rate of O. marina feeding on B. cincta than that
on the other algal prey species except one species may be
responsible for its lower growth rates, but the higher in-
gestion rate of O. marina feeding on B. cincta than that on
the heterotrophic nanoflagellate and heterotrophic dinoflagellates may be responsible for its higher growth rates.
O. marina may capture and ingest B. cincta with more
difficulty than the other algal prey, except some unpalatable ones, but more easily than heterotrophic nanoflagellate and dinoflagellates. Both the µmax and Imax of O. marina feeding on diverse prey species, including B. cincta,
were not significantly correlated with the prey’s equivalent spherical diameter (p > 0.1, ANOVA). Moreover, the
µmax of O. marina feeding on diverse prey species was not
significantly correlated with the Imax (p > 0.1, ANOVA).
Therefore, for O. marina, the nutritional value of the different prey species, including B. cincta, may differ.
The µmax of Strobilidium sp. on B. cincta is higher than
that on A. cf. poporum and the euglenophyte Eutreptiella
gymnastica, although the Imax of Strobilidium sp. on B.
cincta is comparable to or lower than that on A. cf. poporum and E. gymnastica (Table 5). Therefore, for Strobilidium sp., B. cincta may have higher nutritional value than
A. cf. poporum or E. gymnastica.
Table 5. Comparison of maximum growth and ingestion rates of Oxyrrhis marina and Strobilidium spp. on diverse prey species
Predator
Oxyrrhis marina (HTD)
Strobilidium spp. (CIL)
Prey species
ESD
µmax
Imax
Cafeteria sp. (HNF)
3.5
0.19
0.3
Jeong et al. (2007b)
Phaeodactylum tricornutum (DIA)
4.2
1.30
1.9
Goldman et al. (1989)
Isochrysis galbana (PRY)
5.1
0.80
2.2
Goldman et al. (1989)
Dunaliella tertiolecta (CHL)
5.1
0.80
1.5
Goldman et al. (1989)
Karlodinium veneficum_NT (MTD)
9.1
0.90
6.4
Adolf et al. (2007)
Amphidinium carterae (MTD)
9.7
1.17
2.8
Jeong et al. (2001a)
Azadinium cf. poporum (PTD)
10.0
0.50
5.0
Potvin et al. (2013)
Karlodinium veneficum_T (MTD)
10.5
0.25
2.2
Adolf et al. (2007)
Heterosigma akashiwo (RAP)
11.5
1.43
1.3
Jeong et al. (2003)
Biecheleria cincta (MTD)
12.2
0.49
0.91
This study
Eutreptiella gymnastica (EUG)
12.6
0.81
2.7
Jeong et al. (2011)
Pfiesteria piscicida (HTD)
13.5
0.66
0.33
Jeong et al. (2007a)
Luciella masanensis (HTD)
13.5
0.04a
0.07
Jeong et al. (2007a)
Stoeckeria algicida (HTD)
13.9
0.22
0.14
Jeong et al. (2007a)
Gymnodinium aureolum (MTD)
19.4
0.71
0.51
Yoo et al. (2010a)
Fibrocapsa japonica (RAP)
20.4
0.72
1.2
Tillmann and Reckermann (2002)
Azadinium cf. poporum (PTD)
10.0
0.64
Biecheleria cincta (MTD)
12.2
0.91
1.98
This study
Eutreptiella gymnastica (EUG)
12.6
-0.94a
2.2
Jeong et al. (2011)
179
Reference
Potvin et al. (2013)
Rates are corrected to 20°C using Q10 = 2.8 (Hansen et al. 1997).
ESD, equivalent spherical diameter (µm); µmax, maximum growth rate (d-1); Imax, maximum ingestion rate (ng C predator-1 d-1); HTD, heterotrophic
dinoflagellate; HNF, heterotrophic nanoflagellate; DIA, diatom; PRY, prymnesiophyte; CHL, chlorophyte; NT, non-toxic; MTD, mixotrophic dinoflagellate; PTD, phototrophic dinoflagellate; T, toxic; RAP, raphidophyte; EUG, euglenophyte; CIL, ciliate.
a
The maximum value among the mean growth rates measured at given prey concentrations.
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Algae 2013, 28(4): 343-354
Both growth and ingestion rates of O. marina and Strobilidium sp. on B. cincta are affected by prey concentrations. The threshold prey concentration for growth of O.
marina on B. cincta (1.4 ng C mL-1) was lower than that for
the growth rate of Strobilidium sp. on the same prey (11.8
ng C mL-1). Therefore, O. marina is likely to survive at low
B. cincta concentrations but Strobilidium sp. is not. The
KGR (the prey concentration sustaining 1/2 µmax) of 5.7 ng
C mL-1 for O. marina feeding on B. cincta was also lower
than that of Strobilidium sp. (34.8 ng C mL-1) feeding on
the same algal prey. Thus, O. marina is likely to grow rapidly at low B. cincta concentrations but Strobilidium sp.
would not. Additionally, the KIR (the prey concentration
sustaining 1/2 Imax) of 9.2 ng C mL-1 for O. marina feeding on B. cincta was also lower than that of Strobilidium
sp. (62.2 ng C mL-1) feeding on the same algal prey. Thus,
these results indicate that, at low prey concentrations, the
growth and ingestion rates of O. marina would respond
more readily to changes in prey concentrations than
those of Strobilidium sp.
We could not estimate the grazing impact by O. marina
and Strobilidium sp. on B. cincta in this study because
data on the abundance of B. cincta, O. marina, and Strobilidium sp. are not available. Therefore, to understand
the population dynamics of B. cincta and heterotrophic
protists and their interactions, the abundance of B. cincta and its predators in natural environments need to be
quantified.
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We thank Yeong Jong Hwang and Eric Potvin for technical support. This paper was supported by Basic Research
Program through the National Research Foundation of
Korea (NRF) grant funded by Ministry of Science, ICT
and Future Planning (MSICTFP), the Korean Government NRF/MEST (2012R1A6A3A03040333) award to
YD Yoo and the NRF grant funded by MSICTFP (NRF2010-0020702) and Mid-career Researcher Program
(2012-R1A2A2A01-010987) award to HJ Jeong.
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