Feeding by common heterotrophic protists on the mixotrophic dinoflagellate Ansanella granifera (Suessiaceae, Dinophyceae)
Article information
Abstract
The mortality rate of red-tide dinoflagellates owing to predation is a major parameter that affects their population dynamics. The dinoflagellates Ansanella granifera and Ansanella sp. occasionally cause red tides. To understand the interactions between common heterotrophic protists and A. granifera, we explored the feeding occurrence of nine heterotrophic protists on A. granifera and the growth and ingestion rates of the heterotrophic dinoflagellate Gyrodinium dominans on A. granifera as a function of prey concentration and those of Oxyrrhis marina at a single high prey concentration. The heterotrophic dinoflagellates Aduncodinium glandula, G. dominans, Gyrodinium moestrupii, Luciella masanensis, Oblea rotunda, O. marina, Polykrikos kofoidii, and Pfiesteria piscicida and the naked ciliate Strombidium sp. were able to feed on A. granifera. With increasing mean prey concentrations, the growth and ingestion rates of G. dominans feeding on A. granifera rapidly increased and became saturated or slowly increased. The maximum growth and ingestion rates of G. dominans on A. granifera were 0.305 d−1 and 0.42 ng C predator−1 d−1 (3.8 cells predator−1 d−1), respectively. Furthermore, the growth and ingestion rates of O. marina on A. granifera at 1,700 ng C mL−1 (15,454 cells mL−1) were 0.037 d−1 and 0.19 ng C predator−1 d−1 (1.7 cells predator−1 d−1), respectively. The growth and ingestion rates of G. dominans and O. marina feeding on A. granifera were almost the lowest among those on the dinoflagellate prey species. Therefore, G. dominans and O. marina may prefer A. granifera less than other dinoflagellate prey species. The low mortality rate of A. granifera may positively affect its bloom formation.
INTRODUCTION
Dinoflagellates are ubiquitous and one of the major components of marine ecosystems (Taylor et al. 2008, Stern et al. 2010, Kang et al. 2019b, Jeong et al. 2021, Lim and Jeong 2021, Ok et al. 2021). They play diverse ecological roles in marine food webs as primary producers, predators, prey, symbiotic partners, and parasites (Coats 1999, Jeong et al. 2010b, Hansen 2011, Stoecker et al. 2017, LaJeunesse et al. 2018, Eom et al. 2021, Lim and Jeong 2022). They have three trophic modes: autotrophy, mixotrophy (i.e., autotrophy + heterotrophy), and heterotrophy (Stoecker 1999, Jeong et al. 2010b). Many mixotrophic dinoflagellate species form red tides or harmful algal blooms (HABs), which often cause mass mortality in various marine organisms and significant economic damage to the aquaculture industry (Hallegraeff 1995, Jeong et al. 2021, Sakamoto et al. 2021). Thus, to minimize economic losses owing to red tides or HABs by mixotrophic dinoflagellate species, the growth rate of the species under given conditions should be determined (Jeong et al. 2015). The growth of a species can be lowered if effective predators of the species are abundant (Yoo et al. 2013a, Lim et al. 2017, You et al. 2020). To understand and predict the outbreak of red tides or HABs by mixotrophic dinoflagellate species, the type of predators that are able to feed on the species as well as the growth and ingestion rates of predators on the prey species should be determined (Matsuyama et al. 1999, Jeong et al. 2017, Ok et al. 2017).
The dinoflagellate Ansanella granifera was formally described as a new species and genus in the order Suessiales in 2014 (Jeong et al. 2014a). Subsequently, Ansanella natalensis from South Africa and A. catalana from the NW Mediterranean Sea were formally described in 2018 and 2022, respectively (Dawut et al. 2018, Sampedro et al. 2022). All these species have a type E eyespot and small sizes with ranges of 9.6–15.5 μm in length and 7.3–12.4 μm in width (Jeong et al. 2014a, Dawut et al. 2018, Sampedro et al. 2022). These species have been found in many regions globally as vegetative cells or cysts (Jeong et al. 2014a, Belevich et al. 2021, Reñé et al. 2021, Liu et al. 2022, 2023, Pratomo et al. 2022, Sampedro et al. 2022). The presence of A. granifera has been reported in Korea, China, Indonesia, the Yellow Sea, and the Kara Sea (Jeong et al. 2014a, Belevich et al. 2021, Liu et al. 2022, 2023, Pratomo et al. 2022). Furthermore, A. granifera caused huge red tides in Manzanillo City, southeastern Cuba in August 2018, with a maximum concentration of 2.16 × 105 cells mL−1 (Moreira-González et al. 2021). Moreover, Ansanella sp. caused mixed blooms with the mixotrophic dinoflagellate Karenia mikimotoi within East Johor Straits, Singapore in January 2016, and the highest concentration of Ansanella sp. was 2.45 × 103 cells mL−1 (Kok and Leong 2019). Ansanella granifera has been revealed to be mixotrophic and its maximum growth rate is as high as 1.426 d−1 (Lee et al. 2014b). However, the type of predators that are able to feed on A. granifera and the growth and ingestion rates of the predators on A. granifera have not yet been explored.
Heterotrophic protists, such as heterotrophic dinoflagellates (HTDs) and ciliates, are major predators of mixotrophic dinoflagellates in marine ecosystems (Pierce and Turner 1992, Sherr and Sherr 2002, Kang et al. 2020). In general, the grazing impact of heterotrophic protists on populations of mixotrophic dinoflagellates is usually greater than that of metazoan predators because of the much higher abundance of heterotrophic protists than metazoan predators (Lee et al. 2017, Lim et al. 2017). The high grazing impact of heterotrophic protists sometimes prevents the outbreak of red tides or HABs by mixotrophic dinoflagellates (Yoo et al. 2013a, Lim et al. 2017, Kang et al. 2018). The HTDs Aduncodinium glandula, Gyrodinium dominans, Gyrodinium moestrupii, Luciella masanensis, Oblea rotunda, Oxyrrhis marina, Polykrikos kofoidii, and Pfiesteria piscicida and the naked ciliate Strombidium sp. are commonly found in many marine environments (Strom and Buskey 1993, Claessens et al. 2008, Taylor et al. 2008, Watts et al. 2010, Tillmann and Hoppenrath 2013, Lee et al. 2021). These potential heterotrophic protistan predators have different sizes, shapes, edible prey species, feeding mechanisms, and growth and ingestion rates on the same prey species (e.g., Mason et al. 2007, Jeong et al. 2010b, Lowe et al. 2011, Guo et al. 2013, Kang et al. 2015, 2020, Jang et al. 2016).
In the present study, the feeding occurrence of these eight HTDs and one naked ciliate on A. granifera was examined. Furthermore, the growth and ingestion rates of G. dominans feeding on A. granifera as a function of prey concentration and those of O. marina feeding on A. granifera at a single high prey concentration were measured because only these two predator species had positive growth rates in our preliminary tests. The growth and ingestion rates of G. dominans and O. marina feeding on A. granifera were compared with those of G. dominans and O. marina feeding on other dinoflagellate prey species. This study provides a better understanding of the interactions between A. granifera and common heterotrophic protists, as well as the population dynamics of A. granifera and its predators.
MATERIALS AND METHODS
Preparation of experimental organisms
Sediment samples were collected from Shiwha Bay, Korea, in September 2010, when the temperature and salinity of ambient waters were 21.3°C and 15.6, respectively (Table 1) (Jeong et al. 2014a). After germinating cysts in the samples, a clonal culture of A. granifera AGSW10 was established using two consecutive single-cell isolations. The culture of A. granifera with fresh f/2-Si medium in 500-mL bottles on a shelf was incubated at 20°C under an irradiance of 20 μE m−2 s−1 provided by cool white fluorescent lights and a 14 : 10 h light : dark (L : D) cycle.
Information for the isolation and maintenance of the prey and predator species used in this study
For the isolation of the HTDs used in this study, plankton samples were collected off the coasts of Masan, Jeongok, Saemankeum, Jinhae, Kunsan, and Jangheung, Korea from 2001–2019 using water samplers (Table 1). The culture of P. piscicida was obtained from the National Center for Marine Algae and Microbiota. The naked ciliate Strombidium sp. was isolated from plankton samples collected using a 20-μm mesh net off the coasts of Kunsan in January 2023 (Table 1). To obtain clonal cultures of each HTD and ciliate species, two consecutive single-cell isolations were used.
The carbon contents of A. granifera and predator species were obtained from previous studies (Jeong et al. 2001b, 2007, 2008, Lee et al. 2014b, Jang et al. 2016, Ok et al. 2017, Kang et al. 2020). The carbon content of Strombidium sp. was estimated from cell volumes in this study using the equation suggested by Menden-Deuer and Lessard (2000).
Interactions between Ansanella granifera and heterotrophic protists
In experiment 1, feeding by each of the HTDs and ciliates on A. granifera was investigated (Table 2). Dense cultures of A. granifera (ca. 20,000 cells mL−1) and each of the HTDs and ciliates (ca. 20–4,000 cells mL−1) were added to each 42-mL PC bottle using an autopipette (Table 2). For each experiment, one experiment (mixtures of prey and predator), one prey control (only prey without predator), and one predator control (only predator without prey) bottle were set up. The bottles were placed on a 0.00017 g (0.9 rpm) rotating wheel, whereas those for the benthic species A. glandula were placed on a shelf. All bottles were incubated at 20°C under an illumination of 20 μE m−2 s−1 and a 14 : 10 h L : D cycle.
Experimental design
After 2, 24, and 48 h of incubation, 5 mL aliquots were taken from each bottle and transferred into the wells of a 6-well cell culture plate. To determine whether each predator could feed on A. granifera, each predator cell (n ≥ 30) was tracked for 2 min under a dissection microscope at 20–63× magnification. The feeding process of predators on A. granifera was photographed on a confocal dish with cover glasses at 200–1,000× magnification using a digital camera (Zeiss-AxioCam 506; Carl Zeiss Ltd., Göttingen, Germany) attached to an inverted light microscope (Zeiss-Axiovert 200 M; Carl Zeiss Ltd.).
Growth and ingestion rates of Gyrodinium dominans feeding on Ansanella granifera as a function of prey concentration
In experiment 2, the growth and ingestion rates of G. dominans feeding on A. granifera as a function of prey concentration were measured (Table 2). In preliminary tests, A. granifera supported only the growth of G. dominans and O. marina among the heterotrophic protists tested, and the growth rate of G. dominans on A. granifera was the highest.
Dense cultures of G. dominans grown on Amphidinium carterae were transferred into 250-mL PC bottles one day after cells of A. carterae were not observed. The bottles were filled with freshly filtered seawater, capped, placed on a 0.00017 g rotating plankton wheel, and incubated at 20°C under illumination of 20 μE m−2 s−1 and a 14 : 10 h L : D cycle. This was conducted to minimize possible residual growth from the ingested prey in their body. After one day, three 1 mL aliquots from each bottle were taken using an autopipette and enumerated using a compound microscope to determine the cell concentration. After determining that there was no residual growth, the cultures were used in further experiments.
The initial concentrations of G. dominans and A. granifera were established in six different combinations (Table 2). Triplicate 42-mL PC experimental bottles (mixtures of predator and prey) and triplicate control bottles (prey only) were set up for each of the six predator-prey combinations, and triplicate control bottles (predator only) were established at a single high predator concentration. Predetermined volumes of G. dominans and A. granifera were added to each bottle using autopipettes. To provide similar water conditions in experimental and control bottles, the predator culture was filtered through a 0.2-μm disposable syringe filter (DISMIC-25CS type, 25 mm; Advantec, Toyo Roshi Kaisha Ltd., Chiba, Japan), and then for each predator-prey combination, an amount equal to the amount of predator volume added to the experimental bottle was added to the prey control bottles. Similarly, the prey culture was filtered through a 0.2-μm disposable syringe filter, and then an amount equal to the prey volume added to the experimental bottles was added to the predator control bottles. To provide sufficient nutrients to A. granifera, 5 mL of f/2-Si medium was added to all bottles, which were then filled with freshly filtered seawater and capped. To determine the initial predator and prey densities at the beginning of the experiment, a 5 mL aliquot was taken from each bottle, fixed with 5% Lugol’s solution, and counted in three 1-mL Sedgewick Rafter chambers (SRCs) using a microscope. The bottles were then filled to capacity with freshly filtered seawater, capped, and placed on 0.00017 g rotating wheels under the conditions described above. The dilution of the cultures in this process was considered when calculating the growth and ingestion rates. A 10 mL aliquot was taken from each bottle after 48 h and fixed with 5% Lugol’s solution, and the abundances of predators and prey were then examined by counting all or >200 cells in three 1-mL SRCs.
The specific growth rate of the predator μ (d−1) was calculated using the following equation:
, where P0 and Pt represent the predator concentrations at 0 and 2 d, respectively.
Data for G. dominans growth rates were fitted to a modified Michaelis–Menten equation:
, where μmax is the maximum growth rate (d−1), x is the prey concentration (cells mL−1 or ng C mL−1), x′ is the threshold of prey concentration (prey concentration where μ = 0), and KGR is the prey concentration sustaining 1/2 μmax. The data were iteratively fitted to the model using DeltaGraph (Red Rock Software Inc., Salt Lake, UT, USA).
Ingestion rate and mean prey concentration were calculated using the modified equations of Frost (1972) and Heinbokel (1978). Data for G. dominans ingestion rates (IR, cells predator−1 d−1 or ng C predator−1 d−1) were fitted into a modified Michaelis–Menten equation:
, where Imax is the maximum ingestion rate (cells predator−1 d−1 or ng C predator−1 d−1), x is the prey concentration (cells mL−1 or ng C mL−1), and KIR is the prey concentration that sustains 1/2 Imax.
Growth and ingestion rates of Oxyrrhis marina feeding on Ansanella granifera at a single prey concentration
Experiment 3 was designed to measure the growth and ingestion rates of O. marina feeding on A. granifera at a single high prey concentration at which the growth and ingestion rates of G. dominans on A. granifera were saturated. The growth and ingestion rates of O. marina feeding on A. granifera were determined as described above.
Statistical analysis
Pearson’s correlation analysis was used to investigate the relationships between variables (i.e., the growth and ingestion rates of G. dominans or O. marina feeding on each prey species, and the equivalent spherical diameter and maximum swimming speed (MSS) of each prey species). All analyses were performed using SPSS version 25.0 (IBM-SPSS Inc., Armonk, NY, USA).
RESULTS AND DISCUSSION
Interactions between Ansanella granifera and heterotrophic protists
All tested HTDs, A. glandula, G. dominans, G. moestrupii, O. marina, L. masanensis, P. piscicida, P. kofoidii, O. rotunda and the ciliate Strombidium sp., were able to feed on A. granifera AGSW10 (Table 1). The cells of the engulfment feeders G. dominans, G. moestrupii, O. marina, P. kofoidii, and Strombidium sp. ingested A. granifera cells (Fig. 1), whereas the peduncle feeders A. glandula, L. masanensis, and P. piscicida fed on A. granifera cells using a peduncle (Fig. 2). A pallium feeder, O. rotunda ingested A. granifera cells using a pallium (feeding veil) after capturing the A. granifera cell using a tow filament.
Feeding by engulfment feeding heterotrophic dinoflagellates on Ansanella granifera (Ang). (A & B) Intact Ang cells. (C) Unfed Gyrodinium dominans (Gd). (D) Gd (blue arrow) with two ingested Ang cells (red arrows). (E) Unfed Gyrodinium moestrupii (Gm). (F) Gm (blue arrow) with two ingested Ang cells (red arrows). (G) Unfed Oxyrrhis marina (Om). (H) Om (blue arrow) with two ingested Ang cells (red arrows). (I) Unfed Polykrikos kofoidii (Pk). (J) Pk (blue arrow) with an ingested Ang cell (red arrow). (K) Unfed Strombidium sp. (Str). (L) Str (blue arrow) with several ingested Ang cells (red arrows). Scale bars represent: A–J, 10 μm; K & L, 50 μm.
Feeding by peduncle feeding heterotrophic dinoflagellates on Ansanella granifera (Ang). (A) Unfed Aduncodinium glandula (Adg). (B) Adg (blue arrow) with ingested Ang cells (red arrow). (C & D) Adg (blue arrows) feeding on an Ang cell (red arrows) using a peduncle. Each Adg cell in (A–D) is a different cell. (E) Unfed Pfiesteria piscicida (Pp). (F) Pp (blue arrow) with ingested Ang cells (red arrow). (G) Unfed Luciella masanensis (Lm). (H) Lm (blue arrow) with ingested Ang cells (red arrows). Scale bars represent: A–H, 10 μm.
Growth and ingestion rates of Gyrodinium dominans feeding on Ansanella granifera as a function of prey concentration
With increasing mean prey concentrations, the specific growth rate of G. dominans feeding on A. granifera AGSW10 increased at mean A. granifera concentrations <69 ng C mL−1 (631 cells mL−1) but became saturated at higher mean prey concentrations (Fig. 3). When the data were fitted to Eq. (2), the maximum growth rate (μmax) of G. dominans on A. granifera was 0.305 d−1.
Specific growth rates of the heterotrophic dinoflagellate Gyrodinium dominans on Ansanella granifera as a function of mean prey concentration (x, ng C mL−1). The curves are fitted by a Michaelis-Menten equation [Eq. (2)] using all treatments in the experiment. Growth rate (d−1) = 0.305 [(x − 1.12)/(9.48 + (x − 1.12)], r2 = 0.726. Symbols represent treatment means ± standard error (n = 3).
With increasing mean prey concentrations, the ingestion rate of G. dominans feeding on A. granifera increased rapidly with increasing mean prey concentrations < 69 ng C mL−1 (631 cells mL−1) but slowly increased at higher concentrations (Fig. 4). When the data were fitted to Eq. (3), the maximum ingestion rate (Imax) of G. dominans on A. granifera was 0.42 ng C predator−1 d−1 (3.8 cells predator−1 d−1).
Ingestion rates of the heterotrophic dinoflagellate Gyrodinium dominans on Ansanella granifera as a function of mean prey concentration (x, ng C mL−1). The curves are fitted by a Michaelis-Menten equation [Eq. (3)] using all treatments in the experiment. Ingestion rate (ng C predator−1 d−1) = 0.42 [x/(113 + x)], r2 = 0.762. Symbols represent treatment means ± standard error (n = 3).
Growth and ingestion rates of Oxyrrhis marina feeding on Ansanella granifera at a single prey concentration
At a single high mean prey concentration of 1,700 ng C mL−1 (15,454 cells mL−1), the specific growth and ingestion rates of O. marina on A. granifera were 0.037 d−1 and 0.19 ng C predator−1 d−1 (1.7 cells predator−1 d−1), respectively.
The present study clearly showed that all nine common heterotrophic protists tested were able to feed on A. granifera AGSW10, although they had diverse sizes, shapes, feeding mechanisms, and behaviors. The types of heterotrophic protist predators that can feed on A. granifera are similar to those on Effrenium voratum and Biecheleria cincta which belong to the same order (Table 3). Thus, heterotrophic protist predators may compete for A. granifera, E. voratum, or B. cincta in marine environments. However, in the order Suessiales, unlike A. granifera, only O. marina, A. glandula, and a naked ciliate can feed on Yihiella yeosuensis (Jeong et al. 2018a). Thus, A. granifera might be more vulnerable to common heterotrophic protist predators than Y. yeosuensis.
Feeding occurrence of heterotrophic dinoflagellates and naked ciliates on five dinoflagellate prey species in the order Suessiales
When the μmax and Imax of G. dominans on A. granifera AGSW10 were compared with those on the dinoflagellate prey species belonging to diverse orders, the μmax and Imax of G. dominans on A. granifera were higher than those on the mixotrophic dinoflagellates Paragymnodinium shiwhaense and B. cincta, but lower than those on the mixotrophic dinoflagellates Gymnodinium aureolum, Heterocapsa steinii, Prorocentrum cordatum, P. donghaiense, and E. voratum belonging to the orders Gymnodiniales, Peridiniales, Prorocentrales, and Suessiales (Table 4). The smallest size and fastest swimming speed of A. granifera among the dinoflagellate prey species may be partially responsible for the low μmax and Imax values of G. dominans on A. granifera. Therefore, if A. granifera is abundant in natural marine environments, G. dominans will possibly be less abundant than when G. aureolum, H. steinii, P. cordatum, P. donghaiense, or E. voratum is abundant. In contrast, G. dominans may be more abundant when A. granifera is abundant than when P. shiwhaense or B. cincta is abundant. Therefore, A. granifera may not be the preferred prey for G. dominans except for P. shiwhaense and B. cincta. The μmax or Imax of G. dominans on dinoflagellate prey species was not significantly correlated with prey size (Pearson’s correlation test, p > 0.1) (Fig. 5A & B). The μmax of G. dominans on dinoflagellate prey species was not significantly correlated with the Imax (Pearson’s correlation test, p > 0.1) (Fig. 5C). This suggests that factors other than prey size affected the μmax and Imax of G. dominans on dinoflagellate prey species, and that there was a difference in the nutritional values of prey species. The μmax or Imax of G. dominans on dinoflagellate prey species was also not correlated with the MSS of the prey species.
The maximum growth (μmax, d−1) and ingestion (Imax, ng C predator−1 d−1) rates of Gyrodinium dominans on dinoflagellate prey species
Maximum growth (μmax) and ingestion (Imax) rates of Gyrodinium dominans on the dinoflagellate prey species. (A) μmax as a function of equivalent spherical diameter (ESD, μm) of prey species. (B) Imax as a function of ESD of prey species. (C) μmax as a function of Imax. Ag, Ansanella granifera; Bc, Biecheleria cincta; Ev, Effrenium voratum; Ga, Gymnodinium aureolum; Hs, Heterocapsa steinii; Pc, Prorocentrum cordatum; Pd, Prorocentrum donghaiense. See Table 4 for details. Only positive values of μmax and Imax were included in this figure.
When the growth and ingestion rates of O. marina feeding on A. granifera at a single high prey concentration were compared with μmax and Imax of O. marina feeding on other dinoflagellate prey species belonging to diverse orders, the growth and ingestion rates of O. marina feeding on A. granifera were higher than the μmax and Imax of O. marina feeding on P. shiwhaense and Y. yeosuensis, but lower than those of O. marina feeding on most other dinoflagellate prey (Table 5). The μmax or Imax of O. marina on dinoflagellate prey species was not significantly correlated with prey size (Pearson’s correlation test, p > 0.1) (Fig. 6A & B). Furthermore, the μmax of O. marina on dinoflagellate prey species was not significantly correlated with Imax (Pearson’s correlation test, p > 0.1) (Fig. 6C). However, the μmax of O. marina was significantly and negatively correlated with the MSS of dinoflagellate prey species (Pearson’s correlation test, p < 0.01) (Fig. 6D). This suggests that the μmax of O. marina is likely to be affected by the MSS of dinoflagellate prey species, but not by prey species. Cells of O. marina may spend more energy to catch and ingest faster-swimming prey species such as A. granifera than slow-swimming prey species (Table 5).
The maximum growth (μmax, d−1) and ingestion (Imax, ng C predator−1 d−1) rates of Oxyrrhis marina on dinoflagellate prey species
Maximum growth (μmax) and ingestion (Imax) rates of Oxyrrhis marina on the dinoflagellate prey species. (A) μmax as a function of equivalent spherical diameter (ESD, μm) of prey species. (B) Imax as a function of ESD of prey species. (C) μmax as a function of Imax. (D) μmax as a function of maximum swimming speed (MSS, x) of prey species. Maximum growth (μmax, d−1) = −0.0007x + 0.96, r2 = 0.627. Ag, Ansanella granifera; Ba, Biecheleriopsis adriatica; Kv, non-toxic Karlodinium veneficum; Sa, Stoeckeria algicida. See Table for details. Only positive values of μmax and Imax were included in this figure.
To estimate the grazing impact of G. dominans on populations of A. granifera, data on the abundance of G. dominans and A. granifera in the same water parcel are needed. However, there are no data on the abundances of G. dominans and A. granifera that co-occur yet. There are data on the abundance of A. granifera and Ansanella sp. in the waters of the three regions in which there are data on the abundance of G. dominans or Gyrodinium spp., but they are not in the same water parcels (Table 6). The highest abundance of A. granifera in the Caribbean Sea was 216,000 cells mL−1 (Moreira-González et al. 2021). When using the equation in Figs 3 & 4 and the abundance of A. granifera in Caribbean Sea, the calculated growth and ingestion rates of G. dominans on A. granifera were 0.3 d−1 and 3.8 cells predator−1 d−1, respectively (Table 6). If all cells of Gyrodinium spp. feed on A. granifera at the same rate that G. dominans feeds on A. granifera, the population of Gyrodinium spp. (0.2 cells mL−1) in the Caribbean Sea is calculated to eliminate 0.6 Ansanella cells in a day. Similarly, the highest abundance of Ansanella sp. in the waters off Singapore was 2,450 cells mL−1 (Kok and Leong 2019). When using the equation in Figs 3 & 4 and the abundance of Ansanella sp. in the waters off Singapore and assuming that the ingestion rate of G. dominans on Ansanella sp. is the same as that on A. granifera, the calculated growth and ingestion rates of G. dominans on Ansanella sp. were 0.3 d−1 and 2.7 cells predator−1 d−1, respectively (Table 6). The population of G. dominans (2.0 cells mL−1) in the waters off Singapore is calculated to eliminate 5.4 Ansanella cells in a day. Furthermore, the highest abundance of Ansanella sp. in the NW Mediterranean Sea was 49 cells mL−1 (Reñé et al. 2021). When using the equation in Fig. 3 & 4 and the abundance of Ansanella sp. in the NW Mediterranean Sea and assuming that the ingestion rate of G. dominans on Ansanella sp. is the same as that on A. granifera, the calculated growth and ingestion rates of G. dominans on Ansanella sp. were 0.1 d−1 and 0.2 cells predator−1 d−1, respectively (Table 6). The population of G. dominans (0.1 cells mL−1) in the NW Mediterranean Sea is calculated to eliminate 0.02 Ansanella cells in a day. Data on the abundance of co-occurring prey and predators should be obtained to better estimate the grazing impact of heterotrophic protist predators on the Ansanella spp.
The reported abundances of Ansanella granifera or Ansanella sp. and Gyrodinium dominans or Gyrodinium spp. in the global ocean and calculated growth and ingestion rates of G. dominans or Gyrodinium spp. on A. granifera or Ansanella sp.
CONCLUSION
The growth and ingestion rates of G. dominans and O. marina feeding on A. granifera were almost the lowest among those on the dinoflagellate prey species. Therefore, G. dominans and O. marina may prefer A. granifera less than other dinoflagellate prey species. The low mortality rate of A. granifera may be helpful in forming blooms, and A. granifera may have an advantage over other competing prey species regarding survival.
ACKNOWLEDGEMENTS
We thank Dr. Yeong Du Yoo and Se Hyeon Jang for their support and editors and reviewers for their valuable comments. This research was supported by the National Research Foundation funded by the Ministry of Science and ICT (NRF-2020M3F6A1110582; NRF-2021M3I6A1091272; NRF-2021R1A2C1093379) award to HJJ.
Notes
The authors declare that they have no potential conflicts of interest.