Feeding by Phototrophic Red‐Tide Dinoflagellates on the Ubiquitous Marine Diatom Skeletonema costatum

Abstract

We investigated feeding by phototrophic red-tide dinoflagellates on the ubiquitous diatom Skeletonema costatum to explore whether dinoflagellates are able to feed on S. costatum, inside the protoplasm of target dinoflagellate cells observed under compound microscope, confocal microscope, epifluorescence microscope, and transmission electron microscope (TEM) after adding living and fluorescently labeled S. costatum (FLSc). To explore effects of dinoflagellate predator size on ingestion rates of S. costatum, we measured ingestion rates of seven dinoflagellates at a single prey concentration. In addition, we measured ingestion rates of the common phototrophic dinoflagellates Prorocentrum micans and Gonyaulax polygramma on S. costatum as a function of prey concentration. We calculated grazing coefficients by combining field data on abundances of P. micans and G. polygramma on co-occurring S. costatum with laboratory data on ingestion rates obtained in the present study. All phototrophic dinoflagellate predators tested (i.e. Akashiwo sanguinea, Amphidinium carterae, Alexandrium catenella, Alexandrium tamarense, Cochlodinium polykrikoides, G. polygramma, Gymnodinium catenatum, Gymnodinium impudicum, Heterocapsa rotundata, Heterocapsa triquetra, Lingulodinium polyedrum, Prorocentrum donghaiense, P. micans, Prorocentrum minimum, Prorocentrum triestinum, and Scrippsiella trochoidea) were able to ingest S. costatum. When mean prey concentrations were 170-260 ng C/ml (i.e. 6,500-10,000 cells/ml), the ingestion rates of G. polygramma, H. rotundata, H. triquetra, L. polyedrum, P. donghaiense, P. micans, and P. triestinum on S. costatum (0.007-0.081 ng C/dinoflagellate/d [0.2-3.0 cells/dinoflagellate/d]) were positively correlated with predator size. With increasing mean prey concentration of ca 1-3,440 ng C/ml (40-132,200 cells/ml), the ingestion rates of P. micans and G. polygramma on S. costatum continuously increased. At the given prey concentrations, the maximum ingestion rates of P. micans and G. polygramma on S. costatum (0.344-0.345 ng C/grazer/d; 13 cells/grazer/d) were almost the same. The maximum clearance rates of P. micans and G. polygramma on S. costatum were 0.165 and 0.020 microl/grazer/h, respectively. The calculated grazing coefficients of P. micans and G. polygramma on co-occurring S. costatum were up to 0.100 and 0.222 h, respectively (i.e. up to 10% and 20% of S. costatum populations were removed by P. micans and G. polygramma populations in 1 h, respectively). Our results suggest that P. micans and G. polygramma sometimes have a considerable grazing impact on populations of S. costatum.

Feeding and Growth Characteristics of a Diatom-Feeding Flagellate Isolated from the Bottom Sediment of Onagawa Bay, Northeastern Japan

“…OJMS that feed on diatoms [18]. Previous investigators have generally reported that growth rates could be described as a Michaelis-Menten function of food concentration [16,19,20]. The results obtained in this study are generally consistent with this growth model in that growth rates increase with increasing food concentrations but then tend to level off above a moderate level of food.…”

Feeding and Growth Characteristics of a Diatom-Feeding Flagellate Isolated from the Bottom Sediment of Onagawa Bay, Northeastern Japan

“…OJMS that feed on diatoms [18]. Previous investigators have generally reported that growth rates could be described as a Michaelis-Menten function of food concentration [16,19,20]. The results obtained in this study are generally consistent with this growth model in that growth rates increase with increasing food concentrations but then tend to level off above a moderate level of food.…”

Diversity and Vertical Distribution of Microbial Eukaryotes in the Snow, Sea Ice and Seawater Near the North Pole at the End of the Polar Night

“…In fact, mixotrophy, a nutritional mode that combines autotrophy and heterotrophy, has been proposed to be a much more widespread strategy in marine and freshwater ecosystems than previously thought (Sanders, 1991; Jones, 2000), with a prominent role particularly in polar environments (Moorthi et al, 2009). Likely mixotrophic candidates in our samples were several of the dinoflagellate phylotypes, especially those closely related to species of the genera Gyrodinium , Gymnodinium , Blastodinium , Katodinium , Prorocentrum , and Woloszynskia (Sherr and Sherr, 2007; Yoo et al, 2009; Kang et al, 2011), some of them at relatively high frequencies (Figure 6), as well as the ciliate phylotypes closely related to Myrionecta rubra and Strombidium conicum , which possess plasts obtained from partial digestion of algal prey (Gustafson et al, 2000; Johnson and Stoecker, 2005; Myung et al, 2006). These observations suggest that mixotrophy was probably more prevalent than strict phototrophy in our samples.…”

Selective Algicidal Action of Peptides against Harmful Algal Bloom Species

“…After pre-culturing both types of algal cells, S. costatum cultures (4.2×10 4 cells/mL) were mixed with H. akashiwo or P. minimum cultures (2.1×10 4 cells/mL) in different cell densities because S. costatum can be preyed upon by HAB [19], [20]. HPA3NT3 was introduced to combinations of co-cultured cells at concentrations of 2 µM or 8 µM (IC 90 against H. akashiwo and P. minimum , respectively).…”

Feeding and Growth Characteristics of a Diatom-Feeding Flagellate Isolated from the Bottom Sediment of Onagawa Bay, Northeastern Japan

“…OJMS that feed on diatoms [18]. Previous investigators have generally reported that growth rates could be described as a Michaelis-Menten function of food concentration [16,19,20]. The results obtained in this study are generally consistent with this growth model in that growth rates increase with increasing food concentrations but then tend to level off above a moderate level of food.…”

Diversity and Vertical Distribution of Microbial Eukaryotes in the Snow, Sea Ice and Seawater Near the North Pole at the End of the Polar Night

“…In fact, mixotrophy, a nutritional mode that combines autotrophy and heterotrophy, has been proposed to be a much more widespread strategy in marine and freshwater ecosystems than previously thought (Sanders, 1991; Jones, 2000), with a prominent role particularly in polar environments (Moorthi et al, 2009). Likely mixotrophic candidates in our samples were several of the dinoflagellate phylotypes, especially those closely related to species of the genera Gyrodinium , Gymnodinium , Blastodinium , Katodinium , Prorocentrum , and Woloszynskia (Sherr and Sherr, 2007; Yoo et al, 2009; Kang et al, 2011), some of them at relatively high frequencies (Figure 6), as well as the ciliate phylotypes closely related to Myrionecta rubra and Strombidium conicum , which possess plasts obtained from partial digestion of algal prey (Gustafson et al, 2000; Johnson and Stoecker, 2005; Myung et al, 2006). These observations suggest that mixotrophy was probably more prevalent than strict phototrophy in our samples.…”

Selective Algicidal Action of Peptides against Harmful Algal Bloom Species

“…After pre-culturing both types of algal cells, S. costatum cultures (4.2×10 4 cells/mL) were mixed with H. akashiwo or P. minimum cultures (2.1×10 4 cells/mL) in different cell densities because S. costatum can be preyed upon by HAB [19], [20]. HPA3NT3 was introduced to combinations of co-cultured cells at concentrations of 2 µM or 8 µM (IC 90 against H. akashiwo and P. minimum , respectively).…”

Feeding and Growth Characteristics of a Diatom-Feeding Flagellate Isolated from the Bottom Sediment of Onagawa Bay, Northeastern Japan

“…OJMS that feed on diatoms [18]. Previous investigators have generally reported that growth rates could be described as a Michaelis-Menten function of food concentration [16,19,20]. The results obtained in this study are generally consistent with this growth model in that growth rates increase with increasing food concentrations but then tend to level off above a moderate level of food.…”

Diversity and Vertical Distribution of Microbial Eukaryotes in the Snow, Sea Ice and Seawater Near the North Pole at the End of the Polar Night

“…In fact, mixotrophy, a nutritional mode that combines autotrophy and heterotrophy, has been proposed to be a much more widespread strategy in marine and freshwater ecosystems than previously thought (Sanders, 1991; Jones, 2000), with a prominent role particularly in polar environments (Moorthi et al, 2009). Likely mixotrophic candidates in our samples were several of the dinoflagellate phylotypes, especially those closely related to species of the genera Gyrodinium , Gymnodinium , Blastodinium , Katodinium , Prorocentrum , and Woloszynskia (Sherr and Sherr, 2007; Yoo et al, 2009; Kang et al, 2011), some of them at relatively high frequencies (Figure 6), as well as the ciliate phylotypes closely related to Myrionecta rubra and Strombidium conicum , which possess plasts obtained from partial digestion of algal prey (Gustafson et al, 2000; Johnson and Stoecker, 2005; Myung et al, 2006). These observations suggest that mixotrophy was probably more prevalent than strict phototrophy in our samples.…”

Selective Algicidal Action of Peptides against Harmful Algal Bloom Species

“…After pre-culturing both types of algal cells, S. costatum cultures (4.2×10 4 cells/mL) were mixed with H. akashiwo or P. minimum cultures (2.1×10 4 cells/mL) in different cell densities because S. costatum can be preyed upon by HAB [19], [20]. HPA3NT3 was introduced to combinations of co-cultured cells at concentrations of 2 µM or 8 µM (IC 90 against H. akashiwo and P. minimum , respectively).…”