-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 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 C mL
-1
, 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, two-tailed 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 predator
-1
d
-1
)
Specific growth rates of the heterotrophic dinoflagellateOxyrrhis marina on the mixotrophic dinoflagellate Biecheleria cinctaas a function of mean prey concentration (x). Symbols representtreatment means ± 1 SE. The curves are fitted according to theMichaelis-Menten equation [Eq. (2)] using all treatments in theexperiment. Growth rate (d-1) = 0.492{(x - 1.38)/[5.67 + (x - 1.38)]},r2 = 0.843.
Specific growth rates of the ciliate Strobilidium sp. on themixotrophic dinoflagellate Biecheleria cincta as a function of meanprey 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.
Ingestion rates of the heterotrophic dinoflagellate Oxyrrhismarina on the mixotrophic dinoflagellate Biecheleria cincta asa function of mean prey concentration (x). Symbols representtreatment means ± 1 SE. The curves are fitted according to theMichaelis-Menten equation [Eq. (3)] using all treatments in theexperiment. Ingestion rate (ng C predator-1 d-1) = 0.35[x/(9.22 + x)],r2 = 0.777.
Ingestion rates of the ciliate Strobilidium sp. on the mixotrophicdinoflagellate Biecheleria cincta as a function of mean prey concentration(x). Symbols represent treatment means ± 1 SE. The curvesare fitted according to the Michaelis-Menten equation [Eq. (3)] usingall treatments in the experiment. Ingestion rate (ng C predator-1 d-1) =1.98 [x/(62.2 + x)], r2 = 0.884.
Growth and grazing data for theOxyrrhis marinaandStrobilidiumsp. onBiecheleria cinctaParameters are for numerical and/or functional responses from Eqs. (2) and (3), as presented inFigs 2-5.PDV, predator’s volume (×103μm3); 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-1d-1); KIR, prey concentration sustaining 1/2 Imax(ng C mL-1); Cmax, maximum clearance rate (μL predator-1h-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.
Growth and grazing data for the Oxyrrhis marina and Strobilidium sp. on Biecheleria cincta 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.
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.
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. 6
A & B). Moreover, the growth rates were not significantly correlated with ingestion rates (p > 0.1, ANOVA) (
Fig. 6
C).
DISCUSSION
- 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. 2010
a
, 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.
- 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. 2001
b
, Kim and Jeong 2004, Yoo et al. 2013
b
). 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. 2001
b
, Kim and Jeong 2004, Yoo et al. 2013
b
). 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. 2001
b
, Kim and Jeong 2004, Yoo et al. 2013
b
). 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 (μ
max
) and ingestion rates (I
max
) of
O. marina
feeing on diverse prey items, the μ
max
of
O. marina
on
B. cincta
is similar than that on
Azadinium
cf.
poporum
(
Table 5
). However, the I
max
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 μ
max
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 I
max
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 ingestion
Comparison of maximum growth and ingestion rates ofOxyrrhis marinaandStrobilidiumspp. on diverse prey speciesRates are corrected to 20℃ 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-1d-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.aThe maximum value among the mean growth rates measured at given prey concentrations.
Comparison of maximum growth and ingestion rates of Oxyrrhis marina and Strobilidium spp. on diverse prey species Rates are corrected to 20℃ 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. aThe maximum value among the mean growth rates measured at given prey concentrations.
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 μ
max
and I
max
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 μ
max
of
O. marina
feeding on diverse prey species was not significantly correlated with the I
max
(p > 0.1, ANOVA). Therefore, for
O. marina
, the nutritional value of the different prey species, including
B. cincta
, may differ.
The μ
max
of
Strobilidium
sp. on
B. cincta
is higher than that on
A.
cf.
poporum
and the euglenophyte
Eutreptiella gymnastica
, although the I
max
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
.
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 K
GR
(the prey concentration sustaining 1/2 μ
max
) 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 K
IR
(the prey concentration sustaining 1/2 I
max
) 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.
Acknowledgements
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 (NRF-2010-0020702) and Mid-career Researcher Program (2012-R1A2A2A01-010987) award to HJ Jeong.
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