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Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs

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  • Published: 06 July 2010
  • Volume 45, pages 65–91, (2010)
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Ocean Science Journal Aims and scope Submit manuscript
Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs
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  • Hae Jin Jeong1,
  • Yeong Du Yoo1,
  • Jae Seong Kim2,
  • Kyeong Ah Seong3,
  • Nam Seon Kang1 &
  • …
  • Tae Hoon Kim4 
  • 10k Accesses

  • 540 Citations

  • 3 Altmetric

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Abstract

Planktonic mixotrophic and heterotrophic dinoflagellates are ubiquitous protists and often abundant in marine environments. Recently many phototrophic dinoflagellate species have been revealed to be mixotrophic organisms and also it is suggested that most dinoflagellates may be mixotrophic or heterotrophic protists. The mixotrophic and heterotrophic dinoflagellates are able to feed on diverse prey items including bacteria, picoeukaryotes, nanoflagellates, diatoms, other dinoflagellates, heterotrophic protists, and metazoans due to their diverse feeding mechanisms. In turn they are ingested by many kinds of predators. Thus, the roles of the dinoflagellates in marine planktonic food webs are very diverse. The present paper reviewed the kind of prey which mixotrophic and heterotrophic dinoflagellates are able to feed on, feeding mechanisms, growth and ingestion rates of dinoflagellates, grazing impact by dinoflagellate predators on natural prey populations, predators on dinoflagellates, and red tides dominated by dinoflagellates. Based on this information, we suggested a new marine planktonic food web focusing on mixotrophic and heterotrophic dinoflagellates and provided an insight on the roles of dinoflagellates in the food web.

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References

  • Adolf JE, Stoecker DK, Harding LW Jr (2006) The balance of autotrophy and heterotrophy during mixotrophic growth of Karlodinium micrum (Dinophyceae). J Plankton Res 28: 737–751

    Article  Google Scholar 

  • Adolf JE, Krupatkina D, Bachvaroff T, Place AR (2007) Karlotoxin mediates grazing by Oxyrrhis marina on strains of Karlodinium veneficum. Harmful Algae 6:400–412

    Article  Google Scholar 

  • Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil L, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263

    Article  Google Scholar 

  • Azanza RV, Fukuyo Y, Yap LG, Takayama H (2005) Prorocentrum minimum bloom and its possible link to a massive fish kill in Bolinao, Pangasinan, Northern Philippines. Harmful Algae 4:519–524

    Article  Google Scholar 

  • Baek SH, Shimode J, Kikuchi T (2008) Growth of dinoflagellates, Ceratium furca and Ceratium fusus in Sagami Bay, Japan: the role of temperature, light intensity and photoperiod. Harmful algae 7:163–173

    Article  Google Scholar 

  • Berge T, Hansen PJ, 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

    Article  Google Scholar 

  • Berggreen B, Hansen B, Kiørboe T (1988) Food size spectra, ingestion and growth of the copepod Acartia tonsa during development: implications for determination of copepod production. Mar Biol 99:341–352

    Article  Google Scholar 

  • Besiktepe S, Dam HG (2002) Coupling of ingestion and defecation as a function of diet in the calanoid copepod Acartia tonsa. Mar Ecol Prog Ser 229:151–164

    Article  Google Scholar 

  • Bhattacharya D, Medlin L (1995) The phylogeny of plastids: a review based on comparisons of small-subunit ribosomal RNA coding regions. J Phycol 31:489–498

    Article  Google Scholar 

  • Bhattacharya D, Yoon HS, Hackett JD (2003) Photosynthetic eukaryotic unite: endosymbiosis connects the dots. BioEssays 26:50–60

    Article  Google Scholar 

  • Biecheler B (1952) Recherches sur les Peridiniens. Bull Biol Fr Belg Suppl 36:1–149

    Google Scholar 

  • Bockstahler KR, Coats DW (1993a) Grazing of the mixotrophic dinoflagellate Gymnodinium sanguineum on ciliate population of Chesapeake Bay. Mar Biol 116:447–487

    Article  Google Scholar 

  • Bockstahler KR, Coats DW (1993b) Spatial and temporal aspects of mixotrophy in Chesapeake Bay dinoflagellates. J Eukaryot Microbiol 40:49–60

    Article  Google Scholar 

  • Boenigk J, Arndt H (2000) Comparative studies on the feeding behavior of two heterotrophic nanoflagellates: the filter-feeding choanoflagellate Monosiga ovata and the raptorial-feeding kinetoplastid Rhynchomonas nasuta. Aquat Microb Ecol 22:243–249

    Article  Google Scholar 

  • Broglio E, Jonasdottir SH, Calbet A, Jakobsen HH, Saiz E (2003) Effect of heterotrophic versus autotrophic food on feeding and reproduction of the calanoid copepod Acartia tonsa: relationship with prey fatty acid composition. Aquat Microb Ecol 31:267–278

    Article  Google Scholar 

  • Burkholder JAM, Glasgow HB Jr (1995) Interactions of a toxic estuarine dinoflagellate with microbial predators and prey. Arch Protistenkd 145:177–188

    Google Scholar 

  • Burkholder JAM, Glasgow HB Jr (1997) Trophic controls on stage transformations of a toxic ambush-predator dinoflagellate. J Eukaryot Microbiol 44:200–205

    Article  Google Scholar 

  • Burkholder JAM, Glibert PM, Skelton HM (2008) Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Hamful Algae 8:77–93

    Article  Google Scholar 

  • Burkholder JAM, Noga EJ, Hobbs CW, Glasgow HB Jr, Smith SA (1992) New “phantom” dinoflagellate is the causative agent of major estuarine fish kills. Nature 358:407–410

    Article  Google Scholar 

  • Bursa AS (1961) The annual oceanographic cycle at Igloolik in the Canadian Arctic II. The Phytoplakton. J Fish Res Bd Can 18:563–615

    Google Scholar 

  • Buskey EJ (1997) Behavioral components of feeding selectivity of the heterotrophic dinoflagellate Protoperidinium pellucidum. Mar Ecol Prog Ser 153:77–89

    Article  Google Scholar 

  • Buskey EJ, Coulter CJ, Brown SL (1994) Feeding, growth and bioluminescence of the heterotrophic dinoflagellate Protoperidinium huberi. Mar Biol 121:373–380

    Article  Google Scholar 

  • Calbet A, Vaque D, Felipe J, Vila M, Sala MM, Alcaraz M, Estrda M (2003) Relative grazing impact of microzooplankton and mesozooplankton on a bloom of the toxic dinoflagellate Alexandrium minutum. Mar Ecol Prog Ser 259:303–309

    Article  Google Scholar 

  • Cohen JH, Tester PA, Forward RB Jr (2007) Sublethal effects of the toxic dinoflagellate Karenia brevis on marine copepod behavior. J Plankton Res 29:301–315

    Article  Google Scholar 

  • Colin SP, Dam HG (2003) Effects of the toxic dinoflagellate Alexandrium fundyense on the copepod Acartia hudsonica: a test of the mechanisms that reduce ingestion rates. Mar Ecol Prog Ser 248:55–65

    Article  Google Scholar 

  • Daugbjerg N, Hansen G, Larsen J, Moestrup Ø (2000) Phylogeny of some major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of 3 new genera of unarmoured dinoflagellates. Phycologia 39:302–317

    Google Scholar 

  • ECOHAB (1995) The ecology and oceanography of harmful algal blooms: a national research agenda. Woods Hole Oceanographic Institute, Woods Hole, MA, 66 p

    Google Scholar 

  • Feinstein TN, Traslavina R, Sun M, Lin S (2002) Effects of light on photosynthesis, grazing, and population dynamics of the heterotrophic dinoflagellate Pfiesteria piscicida (Dinophyceae). J Phycol 38:659–669

    Article  Google Scholar 

  • Fenchel T (1987) Ecology of protozoa: the biology of free living phagotrophic protists. Springer-Verlag, New York, 197 p

    Google Scholar 

  • Gaines G, Taylor FJR (1984) Extracellular digestion in marine dinoflagellates. J Plankton Res 6:1057–1061

    Article  Google Scholar 

  • Garces E, Fernandez M, Penna A, Van Lenning K, Gutierrez A, Camp J, Zapata M (2006) Characterization of MW Mediterranean Karlodinium spp. (Dinophyceae) strains using morphological, molecular, chemical, and physiological methodologies. J Phycol 42: 1096–1112

    Article  Google Scholar 

  • Gifford DJ, Dagg MJ (1991) The microzooplankton-mesozooplankton link: consumption of planktonic protozoa by the calanoid copepods Acartia tonsa Dana and Neocalanus plumchrus Murukawa. Mar Microb Food Webs 5:161–177

    Google Scholar 

  • Glasgow HB, Lewitus AJ, Burkholder JAM (1998) Feeding behavior of the ichthyotoxic estuarine dinoflagellate, Pfiesteria piscicida, on amino acids, algal prey, and fish vs. Mammalian erythrocytes. In: Reguera B, Blanco J, Fernandez ML, Wyatt T (eds) Harmful microalgae. Intergovernmental Oceanographic Commission of UNESCO, Paris, pp 394–397

    Google Scholar 

  • Goldman JC, Dennett MR, Gordin H (1989) Dynamics of herbivorous grazing by the heterotrophic dinoflagellate Oxyrrhis marina. J Plankton Res 11:391–407

    Article  Google Scholar 

  • Granéli E, Anderson DM, Carlsson P, Maestrini SY (1997) Light and dark carbon uptake by Dinophysis species in comparison to other photosynthetic and heterotrophic dinoflagellates. Aquat Microb Ecol 13:177–186

    Article  Google Scholar 

  • Hackett JD, Anderson DM, Erdner DL, Bhattacharya D (2004) Dinoflagellates: a remarkable evolutionary experiment. Am J Bot 91:1523–1534

    Article  Google Scholar 

  • Hammer A, Pitchford J (2005) The role of mixotrophy in plankton bloom dynamics, and the consequences for system productivity. J Mar Sci 62:833–840

    Google Scholar 

  • Hansen FC, Witte HJ, Passarge J (1996) Grazing in the heterotrophic dinoflagellate Oxyrrhis marina: size selectivity and preference for calcified Emiliania hyxleyi cells. Aquat Microb Ecol 10:307–313

    Article  Google Scholar 

  • Hansen PJ (1989) The red tide dinoflagellate Alexandrium tamarense: effects on behaviour and growth of a tintinnid ciliate. Mar Ecol Prog Ser 53:105–116

    Article  Google Scholar 

  • Hansen PJ (1991) Quantitative importance and trophic role of heterotrophic dinoflagellates in a coastal pelagial food web. Mar Ecol Prog Ser 73:253–261

    Article  Google Scholar 

  • Hansen PJ (1992) Prey size selection, feeding rates and growth dynamics of heterotrophic dinoflagellates with special emphasis on Gyrodinium spirale. Mar Biol 114:327–334

    Article  Google Scholar 

  • Hansen PJ (1995) Growth and grazing response of a ciliate feeding on the red tide dinoflagellate Gyrodinium aureolum in monoculture and in mixture with a non-toxic alga. Mar Ecol Prog Ser 121:65–72

    Article  Google Scholar 

  • Hansen PJ (2002) Effect of high pH on the growth and survival of marine phytoplankton: implications for species succession. Aquat Microb Ecol 28:279–288

    Article  Google Scholar 

  • Hansen PJ, Lundholm N, Rost B (2007) Growth limitation in marine red-tide dinoflagellates: effects of pH versus inorganic carbon availability. Mar Ecol Prog Ser 334:63–71

    Article  Google Scholar 

  • Hansen PJ, Nielsen TG (1997) Mixotrophic feeding of Fragilidium subglobosum (Dinophyceae) on three species of Ceratium: effects of prey concentration, prey species and light intensity. Mar Ecol Prog Ser 147:187–196

    Article  Google Scholar 

  • Hansen PJ, Calado AJ (1999) Phagotrophic mechanisms and prey selection in free-living dinoflagellates. J Eukaryot Microbiol 46:382–389

    Article  Google Scholar 

  • Heinbokel JF, Coats DW, Henderson KW, Tyler MA (1988) Reproduction rates and secondary production of three species of the rotifer genus Synchaeta in the estuarine Potomac River. J Plankton Res 10:659–672

    Article  Google Scholar 

  • Houde SEL, Roman M (1987) Effects of food quality on the functional ingestion response of the copepod Acatria tonsa. Mar Ecol Prog Ser 40:69–77

    Article  Google Scholar 

  • Huntley M, Barthel K-G, Star JL (1983) Particle rejection by Calanus pacificus: discrimination between similarly sized particles. Mar Biol 74:151–160

    Article  Google Scholar 

  • Huntley M, Sykes P, Rohan S, Marin V (1986) Chemicallymediated rejection of dinoflagellate prey by the copepods Calanus pacificus and Paracalanus parvus: mechanism, occurrence and significance. Mar Ecol Prog Ser 28:105–120

    Article  Google Scholar 

  • Huskin I, Anadon R, lvarez-Marqus F, Harris RP (2000) Ingestion, faecal pellet and egg production rates of Calanus helgolandicus feeding coccolithophorid versus non-coccolithophorid diets. J Exp Mar Biol Ecol 248:239–254

    Article  Google Scholar 

  • Hutchinson GE (1961) The paradox of the plankton. Am Nat 95:137–145

    Article  Google Scholar 

  • Jacobson DM (1987) The ecology and feeding biology of thecate heterotrophic dinoflagellates. Ph.D. Thesis, Woods Hole Oceanographic Institution/Massachusetts Institute of Technology Joint Program, 210 p

  • Jacobson DM, Anderson DM (1986) Thecate heterotrophic dinoflagellates: feeding behavior and mechanisms. J Phycol 22:249–258

    Article  Google Scholar 

  • Jacobson DM, Andersen RA (1994) The discovery of mixotrophy in photosynthetic species of Dinophysis (Dinophyceae): light and electron microscopical observations of food vacuoles in Dinophysis acuminata, D. norvegica and two heterotrophic dinophysoid dinoflagellates. Phycologia 33:97–110

    Google Scholar 

  • Jacobson DM, Anderson DM (1996) Widespread phagocytosis of ciliates and other protists by marine mixotrophic and heterotrophic thecate dinoflagellates. J Phycol 32:279–285

    Article  Google Scholar 

  • Jakobsen HH, Hansen PJ (1997) Prey size selection, grazing and growth response of the small heterotrophic dinoflagellate Gymnodinium sp. and the ciliate Balanion comatum-a comparative study. Mar Ecol Prog Ser 158:75–86

    Article  Google Scholar 

  • Jakobsen HH, Hansen PJ, Larsen J (2000) Growth and grazing responses of two chloroplast-retaining dinoflagellates: Effect of irradiance and prey species. Mar Ecol Prog Ser 201: 121–128

    Article  Google Scholar 

  • Jeong HJ (1994a) Predation effects of the calanoid copepod Acartia tonsa on a population of the heterotrophic dinoflagellate Protoperidinium cf. divergens in the presence of co-occurring red-tide dinoflagellate prey. Mar Ecol Prog Ser 111:87–97

    Article  Google Scholar 

  • Jeong HJ (1994b) Predation by the heterotrophic dinoflagellate Protoperidinium cf. divergens on copepod eggs and early naupliar stages. Mar Ecol Prog Ser 114:203–208

    Article  Google Scholar 

  • Jeong HJ (1995) The interactions between microzooplanktonic grazers and dinoflagellates causing red tides in the open coastal waters off southern California. Ph.D. Thesis, Scripps Institution of Oceanography, University of California, San Diego, 139 p. Available on microfilm from University of Michigan, Accession Number 223882

    Google Scholar 

  • Jeong HJ (1999) The ecological roles of heterotrophic dinoflagellates in marine planktonic community. J Eukaryot Microbiol 46: 390–396

    Article  Google Scholar 

  • Jeong HJ, Latz MI (1994) Growth and grazing rates of the heterotrophic dinoflagellate Protoperidinium spp. on red tide dinoflagellates. Mar Ecol Prog Ser 106:173–185

    Article  Google Scholar 

  • Jeong HJ, Lee CW, Yih WH, Kim JS (1997) Fragilidium cf. mexicanum, a thecate mixotrophic dinoflagellate which is prey for and a predator on co-occuring thecate heterotrophic dinoflagellate Protoperidinium cf. divergens. Mar Ecol Prog Ser 151:299–305

    Article  Google Scholar 

  • Jeong HJ, Shim JH, Kim JS, Park JY, Lee CW, Lee Y (1999a) The feeding by the thecate mixotrophic dinoflagellate Fragilidium cf. mexicanum on red tide and toxic dinoflagellate. Mar Ecol Prog Ser 176:263–277

    Article  Google Scholar 

  • Jeong HJ, Shim JH, Lee CW, Kim JS, Koh SM (1999b) Growth and grazing rates of the marine planktonic ciliate Strombidinopsis sp. on red-tide and toxic dinoflagellates. J Eukaryot Microbiol 46:69–76

    Article  Google Scholar 

  • Jeong HJ, Kang HJ, Shim JH, Park JG, Kim JS, Song JY, Choi HJ (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

    Article  Google Scholar 

  • Jeong HJ, Kim SK, Kim JS, Kim ST, Yoo YD, Yoon JY (2001b) Growth and grazing rates of the heterotrophic dinoflagellate Polykrikos kofoidii on red-tide and toxic dinoflagellates. J Eukaryot Microbiol 48:298–308

    Article  Google Scholar 

  • Jeong HJ, Yoon JY, Kim JS, Yoo YD, Seong KA (2002) Growth and grazing rates of the prostomatid ciliate Tiarina fusus on red-tide and toxic algae. Aquat Microb Ecol 28:289–297

    Article  Google Scholar 

  • Jeong HJ, Kim JS, Yoo YD, Kim ST, Kim TH, Park MG, Lee CH, Seong KA, Kang NS, Shim JH (2003a) 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 Microb 50:274–282

    Article  Google Scholar 

  • Jeong HJ, Park KH, Kim JS, Kang HJ, Kim CH, Choi HJ, Kim YS, Park JY, Park MG (2003b) Reduction in the toxicity caused by a toxic dinoflagellate Gymnodinium catenatum by the feeding of the heterotrophic dinoflagellate Polykrikos kofoidii. Aquat Microb Ecol 31:307–312

    Article  Google Scholar 

  • Jeong HJ, Song JY, Lee CH, Kim ST (2004a) Feeding by the larvae of the mussel Mytilus galloprovincialis on red-tide dinoflagellates. J Shellfish Res 23:185–195

    Google Scholar 

  • Jeong HJ, Yoo YD, Kim JS, Kang NS, Kim TH, Kim JH (2004b) Feeding by the marine planktonic ciliate Strombidinopsis jeokjo on common heterotrophic dinoflagellates. Aquat Microb Ecol 36:181–187

    Article  Google Scholar 

  • Jeong HJ, Yoo YD, Kim JS, Kim TH, Kim JH, Kang NS, Yih WH (2004c) Mixotrophy in the phototrophic harmful alga Cochlodinium polykrikoides (Dinophycean): prey species, the effects of prey concentration and grazing impact. J Eukaryot Microbiol 51:563–569

    Article  Google Scholar 

  • Jeong HJ, Yoo YD, Kim ST, Kang NS (2004d) Feeding by the heterotrophic dinoflagellate Protoperidinium bipes on the diatom Skeletonema costatum. Aquat Microb Ecol 36:171–179

    Article  Google Scholar 

  • Jeong HJ, Kim JS, Kim JH, Kim ST, Seong KA, Kim TH, Song JY, Kim SK (2005a) Feeding and grazing impact by the newly described heterotrophic dinoflagellate Stoeckeria algicida on the harmful alga Heterosigma akashiwo. Mar Ecol Prog Ser 295:69–78

    Article  Google Scholar 

  • Jeong HJ, Park JY, Nho JH, Park MO, Ha JH, Seong KA, Jeng C, Seong CN, Lee KY, Yih WH (2005b) Feeding by red-tide dinoflagellates on the cyanobacterium Synechococcus. Aquat Microb Ecol 41:131–143

    Article  Google Scholar 

  • Jeong HJ, Yoo YD, Park JY, Song JY, Kim ST, Lee SH, Kim KY, Yih WH (2005c) Feeding by the phototrophic red-tide dinoflagellates: five species newly revealed and six species previously known to be mixotrophic. Aquat Microb Ecol 40:133–155

    Article  Google Scholar 

  • Jeong HJ, Yoo YD, Seong KA, Kim JH, Park JY, Kim SH, Lee SH, Ha JH, Yih WH (2005d) Feeding by the mixotrophic dinoflagellate Gonyaulax polygramma: mechanisms, prey species, the effects of prey concentration, and grazing impact. Aquat Microb Ecol 38:249–257

    Article  Google Scholar 

  • Jeong HJ, Ha JH, Park JY, Kim JH, Kang NS, Kim S, Kim JS, Yoo YD, Yih WH (2006) Distribution of the heterotrophic dinoflagellate Pfieteria piscicida in Korean waters and its feeding on mixotrophic dinoflagellates, raphidophytes, and fish blood cells. Aquat Microb Ecol 44:263–275

    Article  Google Scholar 

  • Jeong HJ, Ha JH, Yoo YD, Park JY, Kim JH, Kang NS, Kim TH, Kim HS, Yih WH (2007a) Feeding by the Pfiesteria-like heterotrophic dinoflagellate Luciella masanensis. J Eukaryot Microbiol 54:231–241

    Article  Google Scholar 

  • Jeong HJ, Song JE, Kang NS, Kim S, Yoo YD, Park JY (2007b) Feeding by heterotrophic dinoflagellates on the common marine heterotrophic nanoflagellate Cafeteria sp. Mar Ecol Prog Ser 333:151–160

    Article  Google Scholar 

  • Jeong HJ, Kim JS, Song JY, Kim JH, Kim TH, Kim SK, Kang NS (2007c) Feeding by heterotrophic protists and copepods on the heterotrophic dinoflagellates Pfiesteria pisicicida, Stoeckeria algicida, and Luciella masanensis. Mar Ecol Prog Ser 349:199–211

    Article  Google Scholar 

  • Jeong HJ, Seong KA, Yoo YD, Kim TH, Kang NS, Kim S, Park JY, Kim JS, Kim GH, Song JY (2008) Feeding and grazing impact by small marine heterotrophic dinoflagellates on hetertrophic bacteria. J Eukaryot Microbiol 55:271–288

    Article  Google Scholar 

  • Jeong HJ, Yoo YD, Kang NS, Rho JR, Seong KA, Park JW, Nam GS, Yih WH (2010) Ecology of Gymnodinium aureolum. I. Feeding in western Korean water. Aquat Microb Ecol 59:239–255

    Article  Google Scholar 

  • Jost C, Lawrence CA, Campolongo F, van de Bund W, Hill S, DeAngelis DL (2004) The effects of mixotrophy on the stability and dynamics of a simple planktonic food web model. Theoret Popul Biol 66:37–51

    Article  Google Scholar 

  • Kamiyama T, Arima S (2001) Feeding characteristics of two tintinnid ciliate species on phytoplankton including harmful species: effects of prey size on ingestion rates and selectivity. J Exp Mar Biol Ecol 257:281–296

    Article  Google Scholar 

  • Kang NS, Jeong HJ, Moestrup Ø, Shin WG, Nam SW, Park JY, de Salas MF, Kim KW, Noh JH (2010) Description of a new planktonic mixotrophic dinoflagellate Paragymnodinium shiwhaense n. gen., n. sp. from the coastal waters off western Korea: morphology, pigments, and ribosomal DNA gene sequence. J Eukaryot Microbiol 57:121–144

    Article  Google Scholar 

  • Kim JS, Jeong HJ (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

    Article  Google Scholar 

  • Kondo K, Seike Y, Date Y (1990) Red tides in the brackish Lake Nakanoumi. (II). Relationships between the occurrence of Prorocentrum minimum red tide and environmental conditions. Bull Plankt Soc Japan Hiroshima 37:19–34

    Google Scholar 

  • Koski M, Riser CW (2006) Post-bloom feeding of Calanus finmarchicus copepodites: selection for autotrophic versus heterotrophic prey. Mar Biol Res 2:109–119

    Article  Google Scholar 

  • Larsen J (1988) An ultrastructural study of Amphidinium poecilochroum (Dinophyceae), a phagotrophic dinoflagellate feeding on small species of cryptophytes. Phycologia 27:366–377

    Google Scholar 

  • Lee CW (1998) Growth and grazing rates of the heterotrophic dinoflagellate Oxyrrhis marina and the ciliate Stormbidinopsis sp. on Prorocentrum spp. M.A. Thesis, Kunsan National University, 36 p (In Korean with English abstract)

  • Lee SH (2006) Feeding by mixotrophic red-tide algae on photosynthetic picoeukaryotes. M.A. Thesis, Seoul National University, 55 p (In Korean with English abstract)

  • Legrand C, Graneli E, Carlsson P (1998) Induced phagotrophy in the photosynthetic dinoflagellate Heterocapsa triquetra. Aquat Microb Ecol 15:65–75

    Article  Google Scholar 

  • Lessard EJ (1984) Oceanic heterotrophic dinoflagellates: distribution, abundance and role as microzooplankton. Ph.D. Thesis, University of Rhode Island, Kingstown, 166 p

    Google Scholar 

  • Lessard EJ, Swift E (1985) Species-specific grazing rates of heterotrophic dinoflagellates in oceanic waters, measured with a dual-label radioisotope technique. Mar Biol 87:289–296

    Article  Google Scholar 

  • Li A, Stoecker DK, Coats DW, Adam EJ (1996) Ingestion of fluorescently-labeled and phycoerythrin-containing prey by photosynthetic dinoflagellates. Aquat Microb Ecol 10:139–147

    Article  Google Scholar 

  • Li A, Stoecker DK, Coats DW (2000) Mixotrophy in Gyrodinium galatheanum (dinophyceae): grazing responses to light intensity and inorganic nutrients. J Phycol 36:33–45

    Article  Google Scholar 

  • Liu S, Wang W-X (2002) Feeding and reproductive responses of marine copepods in South China Sea to toxic and nontoxic phytoplankton. Mar Biol 140:595–603

    Article  Google Scholar 

  • Maneiro I, Frangopulos M, Guisande C, Fernandez M, Reguera B, Riveiro I (2000) Zooplankton as a potential vector of diarrhetic shellfish poisoning toxins through the food web. Mar Ecol Prog Ser 201:155–163

    Article  Google Scholar 

  • Mason PL, Litaker RW, Jeong HJ, Ha JH, Reece KS, Vogelbein WK, Stokes NA, Park JY, Steidinger KA, Vandersea MW, Kibler S, Tester PA, Vogelbein WK (2007) Description of a new genus of Pfiesteria-like dinoflagellate, Luciella gen. nov. (dinophyceae), including two new species: Luciella masanensis sp. nov. and Luciella atlantis sp. nov. J Phycol 43:799–810

    Article  Google Scholar 

  • Matsubara T, Nagasoe S, Amasaki Y, Shikata T, Shimasaki Y, Oshima Y, Honjo T (2007) Effects of temperature, salinity, and irradiance on the growth of the dinoflagellate Akashiwo sanguinea. J Exp Mar Biol Ecol 342:226–230

    Article  Google Scholar 

  • McFadden GI (2001) Primary and secondary endosymbiosis and the origin of plastids. J Phycol 37:951–959

    Article  Google Scholar 

  • Menden-Deuer S, Lessard EJ, Sattergerg J, Grnbaum D (2005) Growth rates and starvation survival of three species of the pallium-feeding, thecate dinoflagellate genus Protoperidinium. Aquat Microb Ecol 41:145–152

    Article  Google Scholar 

  • Mitsui A, Cao S, Takahashi A, Arai T (1986) Growth synchrony and cellular parameters of the unicellular nitrogen-fixing marine cyanobacterium, Synechococcus sp. strain Miami BG 043511 under continuous illumination. Physiol Plant 69:1–8

    Article  Google Scholar 

  • Nagasoe S, Kim DI, Shimasaki Y, Oshima Y, Yamaguchi M, Honjo T (2006) Effects of temperature, salinity and irradiance on the growth of the red tide dinoflagellate Gyrodinium instriatum Freudenthal et Lee. Harmful algae 5:20–25

    Article  Google Scholar 

  • Nakamura Y, Suzuki S, Hiromi J (1995) Population dynamics of heterotiophic dinoflagellates during a Gymnodinium mikimotoi red tide in the Seto Inland Sea. Mar Ecol Prog Ser 125:269–277

    Article  Google Scholar 

  • Nakamura Y, Yamazaki Y, Hiromi J (1992) Growth and grazing of a heterotrophic dinoflagellate, Gyrodinium dominans, feeding on a red tide flagellate, Chattonella antiqua. Mar Ecol Prog Ser 82:275–279

    Article  Google Scholar 

  • Naustvoll L-J (1998) Growth and grazing by the thecate heterotrophic dinoflagellate Diplopsalis lenticula (Diplopsalidaceae, Dinophyceae). Phycologia 37:1–9

    Google Scholar 

  • Naustvoll L-J (2000) Prey size spectra and food preferences in thecate heterotrophic dinoflagellates. Phycologia 39:187–198

    Google Scholar 

  • Navarro JM, Muoz MG, Contreras AM (2006) Temperature as a factor regulating growth and toxin content in the dinoflagellate Alexandrium catenella. Harmful algae 5:762–769

    Article  Google Scholar 

  • Nygaard K, Tobiesen A (1993) Bacterivory in algae: a survival strategy during nutrient limitation. Limnol Oceanogr 38:273–279

    Article  Google Scholar 

  • Park MG, Kim SJ, Kim HS, Myung GO, Kang IG, Yih WH (2006) First successful culture of the marine dinoflagellate Dinophysis acuminata. Aquat Microb Ecol 45:101–106

    Article  Google Scholar 

  • Parrow MW, Glasgow HB, Burkholder JM, Zhang C (2001) Comparative response to algal prey by Pfiesteria piscicida, Pfiesteria shumwayae and an estuarine ‘lookalike’ species. In: Hallegraeff GM, Blackburn S, Bolch C, Lewis R (eds) Intergovernmental Oceanographic Commission of UNESCO, Paris, pp 101–104

    Google Scholar 

  • Radi T, Pospelova V, de Vernal A, Vaughn Barrie J (2007) Dinoflagellate cysts as indicators of water quality and productivity in British Columbia estuarine environments. Mar Micropaleontol 62:269–297

    Article  Google Scholar 

  • Richardson TL, Pinckney JL, Walker EA, Marshalonis DM (2006) Photopigment radiolabelling as a tool for determining in situ growth rates of the toxic dinoflagellate Karenia brevis (Dinophyceae) Eur J Phycol 41:415–423

    Article  Google Scholar 

  • Roman M, Reaugh M, Zhang X (2006) Ingestion of the dinoflagellate, Pfiesteria piscicida, by the calanoid copepod, Acartia tonsa. Harmful algae 5:435–441

    Article  Google Scholar 

  • Rublee PA, Allen C, Schaefer Rhodes EL, Adamson J, Lapworth C, Burkholder J, Glasgow H (2004) Global distribution of toxic Pfiesteria complex species detected by PCR asssay. In: Steidinger KA, Landsberg JH, Tomas CR, Vargo G (eds) Harmful algae 2002. Intergovernmental Oceanographic Commission of UNESCO, Paris, pp 320–322

    Google Scholar 

  • Scura ED, Jerde C (1977) Various species of phytoplankton as food for larval northern anchovy, Engraulis mordax, and relative nutritional values of the dinoflagellate Gymnodinuim splendens and Gonyaulax polyedra. Fish Bull 75:577–583

    Google Scholar 

  • Seong KA, Jeong HJ, Kim S, Kim GH, Kang JH (2006) Bacterivory by co-occurring red-tide algae, heterotrophic nanoflagellates, and ciliates on marine bacteria. Mar Ecol Prog Ser 322:85–97

    Article  Google Scholar 

  • Sherr EB, Sherr BF (2002) Significance of predation by protests in aquatic microbial food webs. Ant van Leeuwenh 81:293–308

    Article  Google Scholar 

  • Siano R, Montresor M (2005) Morphology, ultrastructure and feeding behaviour of Protoperidinium vorax sp. nov. (Dinophyceae, Peridiniales). Eur J Phycol 40:221–232

    Article  Google Scholar 

  • Skovgaard A (1996a) Engulfment of Ceratium spp. (Dinophyceae) by the thecate photosynthetic dinoflagellate Fragilidium subglobosum. Phycologia 35:490–499

    Google Scholar 

  • Skovgaard A (1996b) Mixotrophy in Fragilidium subglobosum (Dinophyceae): growth and grazing responses as functions of light intensity. Mar Ecol Prog Ser 143:247–253

    Article  Google Scholar 

  • Skovgaard A (1998) Role of chloroplast retention in a marine dinoflagellate. Aquat Microb Ecol 15:293–301

    Article  Google Scholar 

  • Skovgaard A (2000) A phagotrophically derivable growth factor in the plastidic dinoflagellate Gyrodinium resplendens (Dinophyceae). J Phycol 36:1069–1078

    Article  Google Scholar 

  • Skovgaard A, Hansen PJ, Stoecker DK (2000) Physiology of the mixotrophic dinoflagellate Fragilidium subglobosum. 1. Effects of phagotrophy and irradiance on photosynthesis and carbon content. Mar Ecol Prog Ser 201:129–136

    Article  Google Scholar 

  • Sleigh MA (1989) Protozoa and other protists. Edward Arnold, London, 342 p

    Google Scholar 

  • Smalley GW, Coats DW (2002) Ecology of the red-tide dinoflagellate Ceratium furca: distribution, mixotrophy, and grazing impact on ciliate populations of Chesapeake Bay. J Eukaryot Microbiol 49:63–73

    Article  Google Scholar 

  • Smalley GW, Coats DW, Adam EJ (1999) A new method using fluorescent microspheres to determine grazing on ciliates by the mixotrophic dinoflagellate Ceratium furca. Aquat Microb Ecol 17:167–179

    Article  Google Scholar 

  • Smalley GW, Coats DW, Stoecker DK (2003) Feeding in the mixotrophic dinoflagellate Ceratium furca is influenced by intracellular nutrient concentrations. Mar Ecol Prog Ser 262:137–151

    Article  Google Scholar 

  • Smayda TJ (1997) Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol Oceanogr 42:1137–1153

    Article  Google Scholar 

  • Steidinger KA, Burkholder JM, Glasgow HB Jr, Hobbs CW, Garrett JK, Truby EW, Noga EJ, Smith SA (1996) Pfiesteria piscicida gen. et sp. nov. (Pfiesteriaceae fam. nov.), a new toxic dinoflagellate with a complex life cycle and behavior. J Phycol 32:157–164

    Article  Google Scholar 

  • Stickney HL, Hood RR, Stoecker DK (2000) The impact of mixotrophy on planktonic trophic dynamics in marine ecosystems. Ecol Model 125:203–230

    Article  Google Scholar 

  • Stoecker DK (1998) Conceptual models of mixotrophy in planktonic protists and some ecological and evolutionary implications. Eur J Protistol 34:281–290

    Google Scholar 

  • Stoecker DK (1999) Mixotrophy among dinoflagellates. J Eukaryot Microbiol 46:397–401

    Article  Google Scholar 

  • Stoecker DK, Evans GT (1985) Effects of protozoan herbivory and carnivory in a microplankton food web. Mar Ecol Prog 25:159–167

    Article  Google Scholar 

  • Stoecker DK, Guillard RRL, Kavee RM (1981) Selective predation by Favella ehrenbergii (Tintinnida) on and among dinoflagellates. Biol Bull 160:136–145

    Article  Google Scholar 

  • Stoecker DK, Li A, Coats DW, Gustafson DE, Nannen MK (1997) Mixotrophy in the dinoflagellate Prorocentrum minimum. Mar Ecol Prog Ser 152:1–12

    Article  Google Scholar 

  • Stoecker DK, Parrow MW, Burkholder JM, Glasgow HB Jr (2002) Grazing by microzooplankton on Pfiesteria piscicida cultures with different histories of toxicity Aquat Microb Ecol 28:79–85

    Article  Google Scholar 

  • Strom SL (1991) Growth and grazing rates of the herbivorous dinoflagellate Gymnodinium sp. from the open subarctic Pacific Ocean. Mar Ecol Prog Ser 78:103–113

    Article  Google Scholar 

  • Strom SL, Buskey EJ (1993) Feeding, growth, and behavior of the thecate heterotrophic dinoflagellate Oblea rotunda. Limnol Oceanogr 38:965–977

    Article  Google Scholar 

  • Tester PA, Turner JT, Shea D (2000) Vectorial transport of toxins from the dinoflagellate Gymnodinium breve through copepods to fish. J Plankton Res 22:47–62

    Article  Google Scholar 

  • Tezuka Y (1990) Bacterial regeneration of ammonium and phosphate as affected by the carbon: nitrogen: phosphorus ratio of organic substrates. Microb Ecol 19:227–238

    Article  Google Scholar 

  • Tillmann U (2004) Interactions between planktonic microalgae and protozoan grazers. J Eukaryot Microbiol 51:156–168

    Article  Google Scholar 

  • Tillmann U, John U (2002) Toxic effects of Alexandrium spp. On heterotrophic dinoflagellates: an allelochemical defence mechanism independent of PSP-toxin content. Mar Ecol Prog Ser 230:47–58

    Article  Google Scholar 

  • Turner JT, Anderson DM (1983) Zooplankton grazing during dinoflagellate blooms in a Cape Cod embayment, with observations of predation upon tintinnids by copepods. Mar Ecol 4:359–374

    Article  Google Scholar 

  • Turner JT, Tester PA (1997) Toxic marine phytoplankton, zooplankton grazers, and pelagic food webs. Limnol Oceanogr 42:1203–1214

    Article  Google Scholar 

  • Uchida T, Kamiyama T, Matsuyama Y (1997) Predation by a photosynthetic dinoflagellate Gyrodinium instriatum on loricated ciliates. J Plankton Res 19:603–608

    Article  Google Scholar 

  • Uye SI, Takamatsu K (1990) Feeding interactions between planktonic copepods and red-tide flagellates from Japanese coastal waters. Mar Ecol Prog Ser 59:97–107

    Article  Google Scholar 

  • Verity PG, Paffenhöfer G-A (1996) On assessment of prey ingestion by copepods. J Plankton Res 18:1767–1779

    Article  Google Scholar 

  • Watanabe MM, Suda S, Inouye I, Sawaguchi T, Chihara M (1990) Lepidodinium viride gen. et sp. nov. (Gymnodiniales, Dinophyta), a green dinoflagellate with a chlorophyll a- and b-containing endosymbiont. J Phycol 26:741–751

    Article  Google Scholar 

  • Watras CJ, Garcon VC, Olson RJ, Chisholm SW, Anderson DM (1985) The effect of zooplankton grazing on estuarine blooms of the toxic dinoflagellate Gonyaulax tamarensis. J Plankton Res 7:891–908

    Article  Google Scholar 

  • Yamaguch M, Shigeru I, Nagasaki K, Matsuyama Y, Uchida T, Imai I (1997) Effects of temperature and salinity on the growth of the red tide flagellates Heterocapsa circularisquama (Dinophyceae) and Chattonella verruculosa (Raphidophyceae). J Plankton Res 19:1167–1174

    Article  Google Scholar 

  • Yamamoto T, Tarutani K (1997) Effects of temperature, salinity and irradiance on the growth of toxic dinoflagellate Alexandrium tamarense isolated from Hiroshima bay, Japan. Japanese J Phycol 45:95–101 (In Japanese with English abstract)

    Google Scholar 

  • Yoo YD, Jeong HJ, Kim MS, Kang NS, Song JY, Shin WG, Kim KY, Lee KT (2009) Feeding by phototrophic red-tide dinoflagellates on the ubiquitous marine diatom Skeletonema costatum. J Eukaryot Microbiol 56:413–420

    Article  Google Scholar 

  • Yoo YD, Jeong HJ, Kang NS, Song JY, Kim KY, Lee KT, Kim JH (2010) Feeding by the newly described mixotrophic dinoflagellate Paragymnodinium shiwhaense: feeding mechanism, prey species, and effect of prey concentration. J Eukaryot Microbiol 57:145–158

    Article  Google Scholar 

  • Yoon HS, Hackett JD, Pinto G, Bhattacharya D (2002) The single, ancient origin of chromist plastids. Proc Natl Acad Sci USA 99:15507–15512

    Article  Google Scholar 

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Authors and Affiliations

  1. School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University, Seoul, 151-747, Korea

    Hae Jin Jeong, Yeong Du Yoo & Nam Seon Kang

  2. Red Tide Research Center, Kunsan National University, Kunsan, 573-701, Korea

    Jae Seong Kim

  3. Saemankeum Environmental Research Center, Kunsan National University, Kunsan, 573-701, Korea

    Kyeong Ah Seong

  4. Research Institute of Oceanography, College of Natural Sciences, Seoul National University, Seoul, 151-747, Korea

    Tae Hoon Kim

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Jeong, H.J., Yoo, Y.D., Kim, J.S. et al. Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci. J. 45, 65–91 (2010). https://doi.org/10.1007/s12601-010-0007-2

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  • Received: 15 March 2010

  • Revised: 28 April 2010

  • Accepted: 02 May 2010

  • Published: 06 July 2010

  • Issue date: June 2010

  • DOI: https://doi.org/10.1007/s12601-010-0007-2

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Key words

  • grazing
  • harmful algal bloom
  • ingestion
  • predation
  • predator
  • prey
  • protist
  • red tide

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