Differential interactions between the nematocyst-bearing mixotrophic dinoflagellate Paragymnodinium shiwhaense and common heterotrophic protists and copepods: Killer or prey
Introduction
Dinoflagellates are ubiquitous protists in marine environments and occasionally form red tides or harmful algal blooms (Bockstahler and Coats, 1993a, Bockstahler and Coats, 1993b, Stoecker, 1999, Adolf et al., 2008, Hall et al., 2008, Menden-Deuer and Montalbano, 2015, Wolny et al., 2015, Lee et al., 2016a). Mixotrophic dinoflagellates play diverse ecological roles in marine planktonic communities (Smalley et al., 1999, Seong et al., 2006, Stoecker et al., 2006, Carvalho et al., 2008, Jeong et al., 2012, Lim et al., 2014); they are predators on diverse prey items (Bockstahler and Coats, 1993a, Burkholder et al., 2008, Yoo et al., 2009, Jeong et al., 2005b, Nishitani et al., 2008a, Lee et al., 2014c, Johnson, 2015) and are themselves important prey items for other mixotrophic dinoflagellates (Skovgaard, 1996, Jeong et al., 2005a, Jeong et al., 2016, Lee et al., 2014a, Lee et al., 2016a, Lee et al., 2016b), heterotrophic dinoflagellates (Hansen, 1992, Jacobson and Anderson, 1996, Johnson et al., 2003, Adolf et al., 2007), ciliates (Kamiyama and Matsuyama, 2005), and several varieties of metazooplankton (Stoecker and Sanders, 1985, Turner and Borkman, 2005). Owing to their diverse and important roles in marine ecosystems, studies have suggested that they form one of the major functional groups (e.g., Mitra et al., 2016). Therefore, to understand the roles of mixotrophic dinoflagellates in marine ecosystems, it is important to understand their prey items and predators among co-occurring plankton, and their growth, ingestion, and mortality rates caused by predation of the species implied in the predator-prey relationships of the targeted dinoflagellates (e.g., Jeong et al., 2015).
Heterotrophic protists and copepods are major microzooplankton and macrozooplankton, respectively, in marine ecosystems and play important roles in marine food webs (Stoecker and Sanders, 1985, Sherr and Sherr, 1994, Sherr and Sherr, 2016, Jeong, 1999, Calbet and Landry, 2004, Calbet et al., 2009, Yoo et al., 2013b, Yoo et al., 2015, Lee et al., 2014b, Turner, 2014, Petitpas et al., 2015, Jang et al., 2016). Heterotrophic protists such as heterotrophic dinoflagellates and ciliates have been revealed as effective grazers on many mixotrophic dinoflagellates (Jeong et al., 2001, Jeong et al., 2014, Tillmann, 2004, John et al., 2015). Furthermore, the grazing impacts by heterotrophic protists on populations of mixotrophic dinoflagellates are sometimes high enough to control prey populations (e.g., Yoo et al., 2013a). Copepods are known to feed on a diverse range of mixotrophic dinoflagellates (Turner and Tester, 1997, Jeong et al., 2010, Kim et al., 2013). Therefore, mortality due to predation by heterotrophic protists and copepods should be studied to understand mixotrophic dinoflagellate dynamics in marine ecosystems.
The mixotrophic dinoflagellate Paragymnodinium shiwhaense isolated from Shiwha Bay, Korea is a newly described species (Kang et al., 2010). Cell length and width of live cells of P. shiwhaense fed the mixotrophic dinoflagellate Amphidinium carterae were ca. 8–19 μm and ca. 6–16 μm, respectively. P. shiwhaense has an amphiesmal plate pattern similar to woloszynskioid dinoflagellates, but it does not have an apical groove or an eyespot (Kang et al., 2010). Furthermore, P. shiwhaense does not have any of the three characters that define species of genus Gymnodinium (i.e., nuclear envelope chambers, horseshoe-like apical groove, or nuclear fibrous connective) (Daugbjerg et al., 2000). However, it does have both chloroplasts and nematocysts (Kang et al., 2010), with only a few other dinoflagellate species (e.g., Polykrikos lebourae and Polykrikos hartmannii) having both these organelles (Hoppenrath and Leander, 2007, Kim et al., 2015). In addition, a study by Yoo et al. (2010b) discovered the maximum growth rate (mixotrophic growth) of P. shiwhaense feeding on A. carterae exceeded 1.0 d−1, yet the rate without added prey (autotrophic growth) was negative. Based on the presence of nematocysts and potential for negative autotrophic growth, P. shiwhaense is possibly close to heterotrophic dinoflagellates in the spectrum of mixotrophic dinoflagellates. P. shiwhaense formed dense blooms in Shiwha Bay (maximum abundance = 1375 cells ml−1) (our unpublished data). Thus, there is a high possibility that this species causes harmful effects on marine organisms during or after dense blooms.
For better understanding of the ecology of P. shiwhaense in marine ecosystems, further studies on the interactions between P. shiwhaense and potential predatory plankton are required. Therefore, in the present study, (1) feeding behaviors of the common heterotrophic dinoflagellates (Oxyrrhis marina and Gyrodinium dominans) and the oligotrich ciliates (Strobilidium sp. and Strombidinopsis sp.) on P. shiwhaense and vice versa were observed; (2) experiments to measure the growth and ingestion rates of each of the heterotrophic dinoflagellates and ciliates and the calanoid copepods Acartia spp. (A. hongi and A. omorii) as a function of P. shiwhaense concentration were conducted; and (3) the growth rates of heterotrophic dinoflagellates in filtrates from experimental (P. shiwhaense + target heterotrophic dinoflagellate) and control (P. shiwhaense only, target heterotrophic dinoflagellate only, filtered seawater only) bottles were measured to test the effect of potential toxic materials exudated by P. shiwhaense. The results of the present study provide a basis on understanding the interactions between P. shiwhaense and common heterotrophic protist and copepod species, and their ecological roles in the marine planktonic community.
Section snippets
Preparation of experimental organisms
For the isolation and culture of Paragymnodinium shiwhaense, plankton samples were collected with a water sampler from surface waters in Shiwha Bay, Korea, during May 2006 when the water temperature and salinity were 18.8 °C and 30.4, respectively (Kang et al., 2010). The samples were screened gently through a 154-μm Nitex mesh and placed in 6-well tissue culture plates. Clonal cultures of P. shiwhaense were established by two serial single cell isolations. The mixotrophic dinoflagellate
Interactions
Cells of Oxyrrhis marina, Gyrodinium dominans, and Strombidinopsis sp. were able to feed on Paragymnodinium shiwhaense cells, but cells of Strobilidium sp. were not (Fig. 1A–C). Cells of O. marina and G. dominans contained 1–2 ingested prey cells, while Strombidinopsis sp. contained 5–6 prey cells. On the contrary, P. shiwhaense was also able to feed on O. marina and Strobilidium sp. (Fig. 1D, E). Thus, P. shiwhaense and O. marina can feed on each other (i.e. reciprocal predation). However, P.
Interactions
The present study clearly showed that the mixotrophic dinoflagellate Paragymnodinium shiwhaense attacked some heterotrophic protists and the P. shiwhaense population adversely affected the populations of the heterotrophic protists. Previously, there have been a few reports on feeding by marine mixotrophic dinoflagellates on heterotrophic dinoflagellates, whereas several reports on feeding by marine mixotrophic dinoflagellates on ciliates (Table 3); the mixotrophic dinoflagellate Fragilidium cf.
Acknowledgments
We thank Sung Yeon Lee, Hee Mahn Lee, and Éric Potvin for technical support. This research was supported by the Useful Dinoflagellate program of Korea Institute of Marine Science and Technology Promotion (KIMST) funded by the Ministry of Oceans and Fisheries (MOF) and Management of marine organisms causing ecological disturbance and harmful effect Program of KIMST and the National Research Foundation (NRF) funded by the Ministry of Science, ICT & Future Planning (NRF-2015M1A5A1041806) award to
References (94)
- et al.
Karlotoxin mediates grazing by Oxyrrhis marina on strains of Karlodinium venificum
Harmful Algae
(2007) - et al.
Can cryptophyte abundance trigger toxic Karlodinium venificum blooms in eutrophic estuaries?
Harmful Algae
(2008) - et al.
Toxic mucus traps: a novel mechanism that mediates prey uptake in the mixotrophic dinoflagellate Alexandrium pseudogonyaulax
Harmful Algae
(2012) - et al.
Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters
Harmful Algae
(2008) - et al.
Zooplankton grazing in the Atlantic Ocean: a latitudinal study
Deep Sea Res Part II Top. Stud. Oceanogr.
(2009) - et al.
Morphology and phylogeny of the pseudocolonial dinofagellates Polykrikos lebourae and Polykrikos herdmanae n. sp
Protist
(2007) - et al.
A hierarchy of conceptual models of red-tide generation: nutrition, behavior, and biological interactions
Harmful Algae
(2015) - et al.
Mixotrophy in the phototrophic dinoflagellate Takayama helix (family Kareniaceae): Predator of diverse toxic and harmful dinoflagellates
Harmful Algae
(2016) - et al.
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
(2013) - et al.
Killing potential protist predators as a survival strategy of the newly described dinoflagellate Alexandrium pohangense
Harmful Algae
(2016)
Feeding by the newly described mixotrophic dinoflagellate Gymnodinium smaydae: Feeding mechanism, prey species, and effect of prey concentration
J. Exp. Mar. Biol. Ecol.
Mixotrophy in the nematocyst–taeniocyst complex-bearing phototrophic dinoflagellate Polykrikos hartmannii
Harmful Algae
Mixotrophic ability of the phototrophic dinoflagellates Alexandrium andersonii, A. affine, and A. fraterculus
Harmful Algae
Feeding by the newly described heterotrophic dinoflagellate Stoeckeria changwonensis: a comparison with other species in the family Pfiesteriaceae
Harmful Algae
Mixotrophy in the newly described dinoflagellate Alexandrium pohangense: a specialist for feeding on the fast-swimming ichthyotoxic dinoflagellate Cochlodinium polykrikoides
Harmful Algae
Bloom formation potential in the harmful dinoflagellate Akashiwo sanguinea: clues from movement behaviors and growth characteristics
Harmful Algae
Defining planktonic protist functional groups on mechanisms for energy and nutrient acquisition: incorporation of diverse mixotrophic strategies
Protist
Zooplankton community grazing impact on a toxic bloom of Alexandrium fundyense in the Nauset Marsh system Cape Cod, Massachusetts
U. S. A. Harmful Algae
Ingestion of the dinoflagellate, Pfiesteria piscicida, by the calanoid copepod, Acartia tonsa
Harmful Algae
Allelochemical interactions and short-term effects of the dinoflagellate Alexandrium on selected photoautotrophic and heterotrophic protists
Harmful Algae
Bioactive compounds of marine dinoflagellate isolates from western Greenland and their phylogenetic association within the genus Alexandrium
Harmful Algae
Impact of zooplankton grazing on Alexandrium blooms in the offshore Gulf of Maine
Deep Sea Res.
Planktonic marine copepods and harmful algae
Harmful Algae
Feeding by heterotrophic protists on the toxic dinoflagellate Ostreopsis cf. ovata
Harmful Algae
Feeding mechanism, prey specificity and growth in light and dark of the plastidic dinoflagellate Karlodinium armiger
Aquat. Microb. Ecol.
Coupling of ingestion and defecation as a function of diet in the calanoid copepod Acartia tonsa
Mar. Ecol. Prog. Ser.
Grazing of the mixotrophic dinoflagellate Gymnodinium sanguineum on a ciliate population of Chesapeake Bay
Mar. Biol.
Spatial and temporal aspects of mixotrophy in Chesapeake Bay dinoflagellates
J. Eukaryot. Microbiol.
Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems
Limnol. Oceanogr.
Dinophysis norvegica (Dinophyceae), more a predator than a producer
Harmful Algae
Cell lysis of a phagotrophic dinoflagellate, Polykrikos kofoidii
Plankton Biol. Ecol.
Phylogeny of some of the major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of three new genera of unarmoured dinoflagellates
Phycologia
Sterol-specific membrane interactions with the toxins from Karlodinium micrum (Dinophyceae)—a strategy for self-protection?
Afr. J. Mar. Sci.
Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus
Limnol. Oceanogr.
Harmful effects of the toxic dinoflagellate Alexandrium tamarense on the tintinnids Favella taraikaensis and Eutintinnus sp
J. Mar. Biol. Assoc. U. K
Environmental factors contributing to the development and demise of a toxic dinoflagellate (Karlodinium veneficum) bloom in a shallow eutrophic, lagoonal estuary
Estuar. Coast
The red tide dinoflagellate Alexandria tamarense: effects on behaviour and growth of a tintinnid ciliate
Mar. Ecol. Prog. Ser.
Dinophysis-a planktonic dinoflagellate genus which can act both as a prey and a predator of a ciliate
Mar. Ecol. Prog. Ser.
Prey size selection, feeding rates and growth dynamics of heterotrophic dinoflagellates with special emphasis on Gyrodinium spirale
Mar. Biol.
Zooplankton grazing and growth: scaling within the 2–2,000-μm body size range
Limnol. Oceanogr.
Studies on the functional role of tintinnids in the Southern California Bight: I. Grazing and growth rates in laboratory cultures
Mar. Biol.
Widespread phagocytosis of ciliates and other protists by marine mixotrophic and heterotrophic thecate dinoflagellates
J. Phycol.
Feeding by the newly described heterotrophic dinoflagellate Aduncodinium glandula: having the most diverse prey species in the family Pfiesteriaceae
Algae
The ecological roles of heterotrophic dinoflagellates in marine planktonic community
J. Eukaryot. Microbiol.
Growth and grazing rates of the heterotrophic dinoflagellate Protoperidinium spp. on red tide dinoflagellates
Mar. Ecol. Prog. Ser.
Fragilidium cf. mexicanum, a thecate mixotrophic dinoflagellate, which is prey for and a predator on co-occurring thecate heterotrophic dinoflagellate Protoperidinium cf. divergens
Mar. Ecol. Prog. Ser.
Growth and grazing rates of the marine planktonic ciliate Strombidinopsis sp. on red-tide and toxic dinoflagellates
J. Eukaryot. Microbiol.
Cited by (17)
Community assembly and network stability of picoeukaryotic plankton communities in the northeast Indian Ocean
2023, Progress in OceanographyEffects of light intensity, temperature, and salinity on the growth and ingestion rates of the red-tide mixotrophic dinoflagellate Paragymnodinium shiwhaense
2018, Harmful AlgaeCitation Excerpt :In contrast, effective predators of P. shiwhaense are lacking (Jeong et al., 2017a); the growth rates of the common heterotrophic protists Oxyrrhis marina (Dinophyceae), Gyrodinium dominans (Dinophyceae), and Strombidinopsis sp. (Oligotrichea, ciliate) feeding on P. shiwhaense were very low or negative, although they were able to feed on P. shiwhaense. In addition, the maximum ingestion rate of Strombidinopsis sp. on P. shiwhaense was much lower than ingestion rates reported for other mixotrophic dinoflagellate prey species (Jeong et al., 2017a), and it was suggested that P. shiwhaense has defense mechanisms against potential protistan predators. For mixotrophic dinoflagellates, biological properties such as suitable prey availability, and physical/chemical properties such as nutrients, light, temperature, and/or salinity have been shown to affect growth and ingestion rates (Li et al., 2000; Skovgaard et al., 2000; Montagnes et al., 2003; Guerrini et al., 2007; Salgado et al., 2015).
Newly discovered role of the heterotrophic nanoflagellate Katablepharis japonica, a predator of toxic or harmful dinoflagellates and raphidophytes
2017, Harmful AlgaeCitation Excerpt :Marine phytoplankton are a major component of marine ecosystems and major primary producers in the sea, and in turn, they are important prey items for diverse mixotrophic and heterotrophic organisms (Sanders, 1991; Stoecker, 1998; Jeong et al., 1999; Tillmann, 2004; Jeong et al., 2010b, 2015, 2016; Lim et al., 2017). Some phytoplankton species are toxic or harmful to other marine organisms and humans (Smayda, 1997; Basti et al., 2016; Jeong et al., 2017). Furthermore, some species are primarily responsible for harmful algal blooms (HAB) or red tides, which cause large-scale mortality of fish or human illnesses (Hallegraeff, 1993; Anderson, 1989; Park et al., 2013; Lim et al., 2015; Reich et al., 2015; Lee et al., 2016; Grattan et al., 2016).
Interactions between the mixotrophic dinoflagellate Takayama helix and common heterotrophic protists
2017, Harmful AlgaeCitation Excerpt :Furthermore, the dominancy of T. helix over O. marina became more pronounced with increasing mean T. helix concentration. Moreover, P. shiwhaense has also been shown to predominate over O. marina (Jeong et al., 2017a), and F. cf. mexicanum was observed to predominate over P. divergens (Jeong et al., 1997). Thus, although a reciprocal predation between two dinoflagellates occurs, one species tends to predominate over the other species.