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 . 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. 2010 a , 2013 b ). 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. 2013 a ). 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. 2013 b ). Furthermore, phototrophic dinoflagellates play diverse roles in marine planktonic food webs (Anderson et al. 2002, Yoo et al. 2009, Jeong et al. 2010 b , 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. 2010 b , Jeong et al. 2012), and, in turn, act as prey for diverse predators (Jeong and Latz 1994, Jeong 1999, Tillmann 2004, Jeong et al. 2010 b , Kim et al. 2013, Yoo et al. 2013 b ). 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 brick-like 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. 2013 a ). Heterotrophic dinoflagellates and ciliates are the major components of heterotrophic protist communities (Sherr and Sherr 2007, Jeong et al. 2011, Yoo et al. 2013 a ). They are effective grazers on many phototrophic dinoflagellates (Eppley and Harrison 1975, Jeong et al. 2013 a , Yoo et al. 2013 b ). 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 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. 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℃ 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℃ 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. (2008 a ). 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. (2008 b ) and Jeong et al. (2008 a ) for O. marina and Strobilidium sp., respectively. 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 × 10 ⁵ 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 plankton wheel rotating at 0.9 rpm and incubated at 20℃ 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. 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℃ 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 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: , where G ₀ and G _t 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: , 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), and K _GR = the prey concentration sustaining 1/2 μ _max . 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: , 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 . 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 concentrations 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℃ 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. 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. 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 . The specific growth rates of O. marina on B. cincta increased rapidly with increasing mean prey concentration ^-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 ^-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 ^-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 μL

Fig. 1.

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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.

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 ^-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 )

Fig. 2.

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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.

Fig. 3.

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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.

Fig. 4.

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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.

Fig. 5.

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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.

Table 4.

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.

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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); μ_max, maximum growth rate (d^-1); K_GR, prey concentration sustaining 1/2 μ_max (ng C mL^-1); x’, threshold prey concentration (ng C mL^-1); I_max, maximum ingestion rate (ng C predator^-1 d^-1); K_IR, prey concentration sustaining 1/2 I_max (ng C mL^-1); C_max, 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.

Fig. 6.

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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

Table 5.

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.

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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); μ_max, maximum growth rate (d^-1); I_max, 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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1.

Adolf J. E. , Krupatkina D. , Bachvaroff T. , Place A. R. 2007 Karlotoxin mediates grazing by Oxyrrhis marina on strains of Karlodinium veneficum. Harmful Algae 6 400 - 412    DOI : 10.1016/j.hal.2006.12.003

2.

Anderson D. M. , Glibert P. M. , Burkholder J. M. 2002 Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 25 704 - 726    DOI : 10.1007/BF02804901

3.

Balzano S. , Gourvil P. , Siano R. , Chanoine M. , Marie D. , Lessard S. , Sarno D. , Vaulot D. 2012 Diversity of cultured photosynthetic flagellates in the north east Pacific and Artic Oceans in summer. Biogeosciences 9 6219 - 6259    DOI : 10.5194/bg-9-4553-2012

4.

Berge T. , Hansen P. J. , Moestrup Ø. 2008 Feeding mechanism, prey specificity and growth in light and dark of the plastidic dinoflagellate Karlodinium armiger. Aquat. Microb. Ecol. 50 279 - 288    DOI : 10.3354/ame01165

5.

Burkholder J. M. , Glibert P. M. , Skelton H. M. 2008 Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae 8 77 - 93    DOI : 10.1016/j.hal.2008.08.010

6.

Eppley R. W. , Harrison W. G. 1975 Physiological ecology of Gonyaulax polyedrum, a red tide water dinoflagellate of southern California. In Locicero, V. R. (Ed.) Proc. First Int. Conf. Toxic Dinoflagellate Bloom. Massachusetts Science and Technology Foundation Wakefield, MA 11 - 22

7.

Frost B. W. 1972 Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus. Limnol. Oceanogr. 17 805 - 815    DOI : 10.4319/lo.1972.17.6.0805

8.

Goldman J. C. , Dennett M. R. , Gordin H. 1989 Dynamics of herbivorous grazing by the heterotrophic dinoflagellate Oxyrrhis marina. J. Plankton Res. 11 391 - 407    DOI : 10.1093/plankt/11.2.391

9.

Guillard R. R. L. , Ryther J. H. 1962 Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea (Cleve) Grun. Can. J. Microbiol. 8 229 - 239    DOI : 10.1139/m62-029

10.

Hansen P. J. 2011 The role of photosynthesis and food uptake for the growth of marine mixotrophic dinoflagellates. J. Eukaryot. Microbiol. 58 203 - 214    DOI : 10.1111/j.1550-7408.2011.00537.x

11.

Hansen P. J. , Bjornsen P. K. , Hansen B. W. 1997 Zooplankton grazing and growth: scaling within the 2-2,000-μm body size range. Limnol. Oceanogr. 42 687 - 704    DOI : 10.4319/lo.1997.42.4.0687

12.

Hallegraeff G. M. 1993 A review of harmful algal blooms and their apparent global increase. Phycologia 32 79 - 99    DOI : 10.2216/i0031-8884-32-2-79.1

13.

Heinbokel J. F. 1978 Studies on the functional role of tintinnids in the Southern California Bight. I. Grazing and growth rates in laboratory cultures. Mar. Biol. 47 177 - 189    DOI : 10.1007/BF00395638

14.

Jeong H. J. 1999 The ecological roles of heterotrophic dinoflagellates in marine planktonic community. J. Eukaryot. Microbiol. 46 390 - 396    DOI : 10.1111/j.1550-7408.1999.tb04618.x

15.

Jeong H. J. , Kang H. , Shim J. H. , Park J. K. , Kim J. S. , Song J. Y. , Choi H. J. 2001a Interactions among the toxic dinoflagellate Amphidinium carterae, the heterotrophic dinoflagellate Oxyrrhis marina, and the calanoid copepods Acartia spp. Mar. Ecol. Prog. Ser. 218 77 - 86    DOI : 10.3354/meps218077

16.

Jeong H. J. , Kim J. S. , Song J. Y. , Kim J. H. , Kim T. H. , Kim S. K. , Kang N. S. 2007a Feeding by protists and copepods on the heterotrophic dinoflagellates Pfiesteria piscicida, Stoeckeria algicida, and Luciella masanensis. Mar. Ecol. Prog. Ser. 349 199 - 211    DOI : 10.3354/meps07094

17.

Jeong H. J. , Kim J. S. , Yoo Y. D. , Kim S. T. , Kim T. H. , Park M. G. , Lee C. H. , Seong K. A. , Kang N. S. , Shim J. H. 2003 Feeding by the heterotrophic dinoflagellate Oxyrrhis marina on the red-tide raphidophyte Heterosigma akashiwo: a potential biological method to control red tides using mass-cultured grazers. J. Eukaryot. Microbiol. 50 274 - 282    DOI : 10.1111/j.1550-7408.2003.tb00134.x

18.

Jeong H. J. , Kim J. S. , Yoo Y. D. , Kim S. T. , Song J. Y. , Kim T. H. , Seong K. A. , Kang N. S. , Kim M. S. , Kim J. H. , Kim S. , Ryu J. , Lee H. M. , Yih W. H. 2008a Control of the harmful alga Cochlodinium polykrikoides by the naked ciliate Strombidinopsis jeokjo in mesocosm enclosures. Harmful Algae 7 368 - 377    DOI : 10.1016/j.hal.2007.12.004

19.

Jeong H. J. , Kim S. K. , Kim J. S. , Kim S. T. , Yoo Y. D. , Yoon J. Y. 2001b Growth and grazing rates of the heterotrophic dinoflagellate Polykrikos kofoidii on red-tide and toxic dinoflagellates. J. Eukaryot. Microbiol. 48 298 - 308    DOI : 10.1111/j.1550-7408.2001.tb00318.x

20.

Jeong H. J. , Kim T. H. , Yoo Y. D. , Yoon E. Y. , Kim J. S. , Seong K. A. , Kim K. Y. , Park J. Y. 2011 Grazing impact of heterotrophic dinoflagellates and ciliates on common red-tide euglenophyte Eutreptiella gymnastica in Masan Bay, Korea. Harmful Algae 10 576 - 588    DOI : 10.1016/j.hal.2011.04.008

21.

Jeong H. J. , Latz M. I. 1994 Growth and grazing rates of the heterotrophic dinoflagellate Protoperidinium spp. on red tide dinoflagellates. Mar. Ecol. Prog. Ser. 106 173 - 185    DOI : 10.3354/meps106173

22.

Jeong H. J. , Lim A. S. , Yoo Y. D. , Lee M. J. , Lee K. H. , Jang T. Y. , Lee K. 2013a Feeding by heterotrophic dinoflagellates and ciliates on the free-living dinoflagellate Symbiodinium sp. (Clade E). J. Eukaryot. Microbiol. Advance online publication.    DOI : 10.1111/jeu.12083

23.

Jeong H. J. , Seong K. A. , Yoo Y. D. , Kim T. H. , Kang N. S. , Kim S. , Park J. Y. , Kim J. S. , Kim K. H. , Song J. Y. 2008b Feeding and grazing impact by the small marine heterotrophic dinoflagellates on heterotrophic bacteria. J. Eukaryot. Microbiol. 55 271 - 288    DOI : 10.1111/j.1550-7408.2008.00336.x

24.

Jeong H. J. , Song J. E. , Kang N. S. , Kim S. , Yoo Y. D. , Park J. Y. 2007b Feeding by heterotrophic dinoflagellates on the common marine heterotrophic nanoflagellate Cafeteria sp. Mar. Ecol. Prog. Ser. 333 151 - 160    DOI : 10.3354/meps333151

25.

Jeong H. J. , Yoo Y. D. , Kang N. S. , Lim A. S. , Seong K. A. , Lee S. Y. , Lee M. J. , Lee K. H. , Kim H. S. , Shin W. , Nam S. W. , Yih W. , Lee K. 2012 Heterotrophic feeding as a newly identified survival strategy of the dinoflagellate Symbiodinium. Proc. Natl. Acad. Sci. U. S. A. 109 12604 - 12609    DOI : 10.1073/pnas.1204302109

26.

Jeong H. J. , Yoo Y. D. , Kang N. S. , Rho J. R. , Seong K. A. , Park J. W. , Nam S. , Yih W. H. 2010a Ecology of Gymnodinium aureolum. I. Feeding in western Korean waters. Aquat. Microb. Ecol. 59 239 - 255    DOI : 10.3354/ame01394

27.

Jeong H. J. , Yoo Y. D. , Kim J. S. , Seong K. A. , Kang N. S. , Kim T. H. 2010b Growth, feeding, and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci. J. 45 65 - 91    DOI : 10.1007/s12601-010-0007-2

28.

Jeong H. J. , Yoo Y. D. , Lee K. H. , Kim T. H. , Seong K. A. , Kang N. S. , Lee K. H. , Lee S. Y. , Kim J. S. , Kim S. , Yih W. H. 2013b Red tides in Masan Bay, Korea in 2004-2005: I. Daily variations in the abundance of red-tide organisms and environmental factors. Harmful Algae 30S S75 - S88    DOI : 10.1016/j.hal.2013.10.008

29.

Kang N. S. , Jeong H. J. , Yoo Y. D. , Yoon E. Y. , Lee K. H. , Lee K. , Kim G. 2011 Mixotrophy in the newly described phototrophic dinoflagellate Woloszynskia cincta from western Korean waters: feeding mechanism, prey species, and effect of prey concentration. J. Eukaryot. Microbiol. 58 152 - 170    DOI : 10.1111/j.1550-7408.2011.00531.x

30.

Kang N. S. , Lee K. H. , Jeong H. J. , Yoo Y. D. , Seong K. A. , Potvin É , Hwang Y. J. , Yoon E. Y. 2013 Red tides in Shiwha Bay, western Korea: a huge dike and tidal power plant established in a semi-enclosed embayment system. Harmful Algae 30S S114 - S130    DOI : 10.1016/j.hal.2013.10.011

31.

Kim J. S. , Jeong H. J. 2004 Feeding by the heterotrophic dinoflagellates Gyrodinium dominans and G. spirale on the red-tide dinoflagellate Prorocentrum minimum. Mar. Ecol. Prog. Ser. 280 85 - 94    DOI : 10.3354/meps280085

32.

Kim J. S. , Jeong H. J. , Yoo Y. D. , Kang N. S. , Kim S. K. , Song J. Y. , Lee M. J. , Kim S. T. , Kang J. H. , Seong K. A. , Yih W. H. 2013 Red tides in Masan Bay, Korea in 2004-2005: III. Daily variation in the abundance of mesozooplankton and their grazing impacts on red-tide organisms. Harmful Algae 30S S102 - S113    DOI : 10.1016/j.hal.2013.10.010

33.

Lindberg K. , Moestrup Ø. , Daugbjerg N. 2005 Studies on woloszynskioid dinoflagellates I: Woloszynskia coronata re-examined using light and electron microscopy and partial LSU rDNA sequences, with description of Tovellia gen. nov. and Jadwigia gen. nov. (Tovelliaceae fam. nov.). Phycologia 44 416 - 440    DOI : 10.2216/0031-8884(2005)44[416:SOWDIW]2.0.CO;2

34.

Luo Z. , Yang W. , Xu B. , Gu H. 2013 First record of Biecheleria cincta (Dinophyceae) from Chinese coasts, with morphological and molecular characterization of the strains. Chin. J. Oceanol. Limnol. 31 835 - 845    DOI : 10.1007/s00343-013-2315-8

35.

Menden-Deuer S. , Lessard E. J. 2000 Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol. Oceanogr. 45 569 - 579    DOI : 10.4319/lo.2000.45.3.0569

36.

Moestrup Ø. , Lindberg K. , Daugbjerg N. 2009 Studies on woloszynskioid dinoflagellates IV: The genus Biecheleria gen. nov. Phycol. Res. 57 203 - 220    DOI : 10.1111/j.1440-1835.2009.00540.x

37.

Park J. Y. , Jeong H. J. , Yoo Y. D. , Yoon E. Y. 2013a Mixotrophic dinoflagellate red tides in Korean waters: distribution and ecophysiology. Harmful Algae 30S S28 - S40    DOI : 10.1016/j.hal.2013.10.004

38.

Park M. G. , Kim S. , Kim H. S. , Myung G. , Kang Y. G. , Yih W. 2006 First successful culture of the marine dinoflagellate Dinophysis acuminata. Aquat. Microb. Ecol. 45 101 - 106    DOI : 10.3354/ame045101

39.

Park T. G. , Lim W. A. , Park Y. T. , Lee C. K. , Jeong H. J. 2013b Economic impact, management and mitigation of red tides in Korea. Harmful Algae 30S S131 - S143    DOI : 10.1016/j.hal.2013.10.012

40.

Porter K. G. , Sherr E. B. , Sherr B. F. , Pace M. , Sanders R. W. 1985 Protozoa in planktonic food webs. J. Eukaryot. Microbiol. 32 409 - 415

41.

Potvin É , Hwang Y. J. , Yoo Y. D. , Kim J. S. , Jeong H. J. 2013 Feeding by heterotrophic protists and copepods on the photosynthetic dinoflagellate Azadinium cf. poporum from western Korean waters. Aquat. Microb. Ecol. 68 143 - 158    DOI : 10.3354/ame01603

42.

Sherr E. B. , Sherr B. F. 2007 Heterotrophic dinoflagellates: a significant component of microzooplankton biomass and major grazers of diatoms in the sea. Mar. Ecol. Prog. Ser. 352 187 - 197    DOI : 10.3354/meps07161

43.

Siano R. , Kooistra W. H. C. F. , Montresor M. , Zingone A. 2009 Unarmoured and thin-walled dinoflagellates from the Gulf of Naples, with the description of Woloszynskia cincta sp. nov. (Dinophyceae, Suessiales). Phycologia 48 44 - 65    DOI : 10.2216/08-61.1

44.

Tillmann U. 2004 Interactions between planktonic microalgae and protozoan grazers. J. Eukaryot. Microbiol. 51 156 - 168    DOI : 10.1111/j.1550-7408.2004.tb00540.x

45.

Tillmann U. , Elbrähter M. , Krock B. , John U. , Cembella A. 2009 Azadinium spinosum gen. et sp. nov. (Dinophyceae) identified as a primary producer of azaspiracid toxins. Eur. J. Phycol. 44 63 - 79    DOI : 10.1080/09670260802578534

46.

Tillmann U. , Reckermann M. 2002 Dinoflagellate grazing on the raphidophyte Fibrocapsa japonica. Aquat. Microb. Ecol. 26 247 - 257    DOI : 10.3354/ame026247

47.

Turner J. T. 2006 Harmful algae interactions with marine planktonic grazers. In Granéi, E. & Turner, J. T. (Eds.) Ecology of Harmful Algae. Springer-Verlag Berlin 259 - 270

48.

Watras C. J. , Garcon V. C. , Olson R. J. , Chisholm S. W. , Anderson D. M. 1985 The effect of zooplankton grazing on estuarine blooms of the toxic dinoflagellate Gonyaulax tamarensis. J. Plankton Res. 7 891 - 908    DOI : 10.1093/plankt/7.6.891

49.

Yoon E. Y. , Kang N. S. , Jeong H. J. 2012 Gyrodinium moestrupii n. sp. a new planktonic heterotrophic dinoflagellate from the coastal waters of western Korea: morphology and ribosomal DNA gene sequence. J. Eukaryot. Microbiol. 59 571 - 586    DOI : 10.1111/j.1550-7408.2012.00632.x

50.

Yoo Y. D. , Jeong H. J. , Kang N. S. , Kim J. S. , Kim T. H. , Yoon E. Y. 2010a Ecology of Gymnodinium aureolum. II. Predation by common heterotrophic dinoflagellates and a ciliate. Aquat. Microb. Ecol. 59 257 - 272    DOI : 10.3354/ame01401

51.

Yoo Y. D. , Jeong H. J. , Kang N. S. , Song J. Y. , Kim K. Y. , Lee G. , Kim J. 2010b Feeding by the newly described mixotrophic dinoflagellate Paragymnodinium shiwhaense: feeding mechanism, prey species, and effect of prey concentration. J. Eukaryot. Microbiol. 57 145 - 158    DOI : 10.1111/j.1550-7408.2009.00448.x

52.

Yoo Y. D. , Jeong H. J. , Kim J. S. , Kim T. H. , Kim J. H. , Seong K. A. , Lee S. H. , Kang N. S. , Park J. W. , Park J. , Yih W. H. 2013a Red tides in Masan Bay, Korea in 2004-2005: II. Daily variations in the abundance of heterotrophic protists and their grazing impact on red-tide organisms. Harmful Algae 30S S89 - S101    DOI : 10.1016/j.hal.2013.10.009

53.

Yoo Y. D. , Jeong H. J. , Kim M. S. , Kang N. S. , Song J. Y. , Shin W. , Kim K. Y. , Lee K. 2009 Feeding by phototrophic red-tide dinoflagellates on the ubiquitous marine diatom Skeletonema costatum. J. Eukaryot. Microbiol. 56 413 - 420    DOI : 10.1111/j.1550-7408.2009.00421.x

54.

Yoo Y. D. , Yoon E. Y. , Jeong H. J. , Lee K. H. , Hwang Y. J. , Seong K. A. , Kim J. S. , Park J. Y. 2013b The newly described heterotrophic dinoflagellate Gyrodinium moestrupii, an effective protistan grazer of toxic dinoflagellates. J. Eukaryot. Microbiol. 60 13 - 24    DOI : 10.1111/jeu.12002