Ocean Science Journal

, Volume 45, Issue 2, pp 65–91 | Cite as

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

  • Hae Jin Jeong
  • Yeong Du Yoo
  • Jae Seong Kim
  • Kyeong Ah Seong
  • Nam Seon Kang
  • Tae Hoon Kim
Open Access
Review

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.

Key words

grazing harmful algal bloom ingestion predation predator prey protist red tide 

References

  1. 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: 737–751CrossRefGoogle Scholar
  2. Adolf JE, Krupatkina D, Bachvaroff T, Place AR (2007) Karlotoxin mediates grazing by Oxyrrhis marina on strains of Karlodinium veneficum. Harmful Algae 6:400–412CrossRefGoogle Scholar
  3. 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 10:257–263CrossRefGoogle Scholar
  4. 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 4:519–524CrossRefGoogle Scholar
  5. 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 7:163–173CrossRefGoogle Scholar
  6. 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: 279–288CrossRefGoogle Scholar
  7. 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 99:341–352CrossRefGoogle Scholar
  8. 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 229:151–164CrossRefGoogle Scholar
  9. Bhattacharya D, Medlin L (1995) The phylogeny of plastids: a review based on comparisons of small-subunit ribosomal RNA coding regions. J Phycol 31:489–498CrossRefGoogle Scholar
  10. Bhattacharya D, Yoon HS, Hackett JD (2003) Photosynthetic eukaryotic unite: endosymbiosis connects the dots. BioEssays 26:50–60CrossRefGoogle Scholar
  11. Biecheler B (1952) Recherches sur les Peridiniens. Bull Biol Fr Belg Suppl 36:1–149Google Scholar
  12. Bockstahler KR, Coats DW (1993a) Grazing of the mixotrophic dinoflagellate Gymnodinium sanguineum on ciliate population of Chesapeake Bay. Mar Biol 116:447–487CrossRefGoogle Scholar
  13. Bockstahler KR, Coats DW (1993b) Spatial and temporal aspects of mixotrophy in Chesapeake Bay dinoflagellates. J Eukaryot Microbiol 40:49–60CrossRefGoogle Scholar
  14. 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 22:243–249CrossRefGoogle Scholar
  15. 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 31:267–278CrossRefGoogle Scholar
  16. Burkholder JAM, Glasgow HB Jr (1995) Interactions of a toxic estuarine dinoflagellate with microbial predators and prey. Arch Protistenkd 145:177–188Google Scholar
  17. Burkholder JAM, Glasgow HB Jr (1997) Trophic controls on stage transformations of a toxic ambush-predator dinoflagellate. J Eukaryot Microbiol 44:200–205CrossRefGoogle Scholar
  18. Burkholder JAM, Glibert PM, Skelton HM (2008) Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Hamful Algae 8:77–93CrossRefGoogle Scholar
  19. 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 358:407–410CrossRefGoogle Scholar
  20. Bursa AS (1961) The annual oceanographic cycle at Igloolik in the Canadian Arctic II. The Phytoplakton. J Fish Res Bd Can 18:563–615Google Scholar
  21. Buskey EJ (1997) Behavioral components of feeding selectivity of the heterotrophic dinoflagellate Protoperidinium pellucidum. Mar Ecol Prog Ser 153:77–89CrossRefGoogle Scholar
  22. Buskey EJ, Coulter CJ, Brown SL (1994) Feeding, growth and bioluminescence of the heterotrophic dinoflagellate Protoperidinium huberi. Mar Biol 121:373–380CrossRefGoogle Scholar
  23. 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 259:303–309CrossRefGoogle Scholar
  24. Cohen JH, Tester PA, Forward RB Jr (2007) Sublethal effects of the toxic dinoflagellate Karenia brevis on marine copepod behavior. J Plankton Res 29:301–315CrossRefGoogle Scholar
  25. 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 248:55–65CrossRefGoogle Scholar
  26. 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 39:302–317Google Scholar
  27. ECOHAB (1995) The ecology and oceanography of harmful algal blooms: a national research agenda. Woods Hole Oceanographic Institute, Woods Hole, MA, 66 pGoogle Scholar
  28. 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 38:659–669CrossRefGoogle Scholar
  29. Fenchel T (1987) Ecology of protozoa: the biology of free living phagotrophic protists. Springer-Verlag, New York, 197 pGoogle Scholar
  30. Gaines G, Taylor FJR (1984) Extracellular digestion in marine dinoflagellates. J Plankton Res 6:1057–1061CrossRefGoogle Scholar
  31. 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: 1096–1112CrossRefGoogle Scholar
  32. 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 5:161–177Google Scholar
  33. 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 394–397Google Scholar
  34. Goldman JC, Dennett MR, Gordin H (1989) Dynamics of herbivorous grazing by the heterotrophic dinoflagellate Oxyrrhis marina. J Plankton Res 11:391–407CrossRefGoogle Scholar
  35. 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 13:177–186CrossRefGoogle Scholar
  36. Hackett JD, Anderson DM, Erdner DL, Bhattacharya D (2004) Dinoflagellates: a remarkable evolutionary experiment. Am J Bot 91:1523–1534CrossRefGoogle Scholar
  37. Hammer A, Pitchford J (2005) The role of mixotrophy in plankton bloom dynamics, and the consequences for system productivity. J Mar Sci 62:833–840Google Scholar
  38. 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 10:307–313CrossRefGoogle Scholar
  39. Hansen PJ (1989) The red tide dinoflagellate Alexandrium tamarense: effects on behaviour and growth of a tintinnid ciliate. Mar Ecol Prog Ser 53:105–116CrossRefGoogle Scholar
  40. Hansen PJ (1991) Quantitative importance and trophic role of heterotrophic dinoflagellates in a coastal pelagial food web. Mar Ecol Prog Ser 73:253–261CrossRefGoogle Scholar
  41. Hansen PJ (1992) Prey size selection, feeding rates and growth dynamics of heterotrophic dinoflagellates with special emphasis on Gyrodinium spirale. Mar Biol 114:327–334CrossRefGoogle Scholar
  42. 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 121:65–72CrossRefGoogle Scholar
  43. Hansen PJ (2002) Effect of high pH on the growth and survival of marine phytoplankton: implications for species succession. Aquat Microb Ecol 28:279–288CrossRefGoogle Scholar
  44. 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 334:63–71CrossRefGoogle Scholar
  45. 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 147:187–196CrossRefGoogle Scholar
  46. Hansen PJ, Calado AJ (1999) Phagotrophic mechanisms and prey selection in free-living dinoflagellates. J Eukaryot Microbiol 46:382–389CrossRefGoogle Scholar
  47. 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 10:659–672CrossRefGoogle Scholar
  48. Houde SEL, Roman M (1987) Effects of food quality on the functional ingestion response of the copepod Acatria tonsa. Mar Ecol Prog Ser 40:69–77CrossRefGoogle Scholar
  49. Huntley M, Barthel K-G, Star JL (1983) Particle rejection by Calanus pacificus: discrimination between similarly sized particles. Mar Biol 74:151–160CrossRefGoogle Scholar
  50. 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 28:105–120CrossRefGoogle Scholar
  51. 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 248:239–254CrossRefGoogle Scholar
  52. Hutchinson GE (1961) The paradox of the plankton. Am Nat 95:137–145CrossRefGoogle Scholar
  53. 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 pGoogle Scholar
  54. Jacobson DM, Anderson DM (1986) Thecate heterotrophic dinoflagellates: feeding behavior and mechanisms. J Phycol 22:249–258CrossRefGoogle Scholar
  55. 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 33:97–110Google Scholar
  56. Jacobson DM, Anderson DM (1996) Widespread phagocytosis of ciliates and other protists by marine mixotrophic and heterotrophic thecate dinoflagellates. J Phycol 32:279–285CrossRefGoogle Scholar
  57. 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 158:75–86CrossRefGoogle Scholar
  58. 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: 121–128CrossRefGoogle Scholar
  59. 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 111:87–97CrossRefGoogle Scholar
  60. Jeong HJ (1994b) Predation by the heterotrophic dinoflagellate Protoperidinium cf. divergens on copepod eggs and early naupliar stages. Mar Ecol Prog Ser 114:203–208CrossRefGoogle Scholar
  61. 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 223882Google Scholar
  62. Jeong HJ (1999) The ecological roles of heterotrophic dinoflagellates in marine planktonic community. J Eukaryot Microbiol 46: 390–396CrossRefGoogle Scholar
  63. Jeong HJ, Latz MI (1994) Growth and grazing rates of the heterotrophic dinoflagellate Protoperidinium spp. on red tide dinoflagellates. Mar Ecol Prog Ser 106:173–185CrossRefGoogle Scholar
  64. 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 151:299–305CrossRefGoogle Scholar
  65. 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 176:263–277CrossRefGoogle Scholar
  66. 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 46:69–76CrossRefGoogle Scholar
  67. 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 218:77–86CrossRefGoogle Scholar
  68. 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 48:298–308CrossRefGoogle Scholar
  69. 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 28:289–297CrossRefGoogle Scholar
  70. 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 50:274–282CrossRefGoogle Scholar
  71. 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 31:307–312CrossRefGoogle Scholar
  72. 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 23:185–195Google Scholar
  73. 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 36:181–187CrossRefGoogle Scholar
  74. 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 51:563–569CrossRefGoogle Scholar
  75. Jeong HJ, Yoo YD, Kim ST, Kang NS (2004d) Feeding by the heterotrophic dinoflagellate Protoperidinium bipes on the diatom Skeletonema costatum. Aquat Microb Ecol 36:171–179CrossRefGoogle Scholar
  76. 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 295:69–78CrossRefGoogle Scholar
  77. 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 41:131–143CrossRefGoogle Scholar
  78. 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 40:133–155CrossRefGoogle Scholar
  79. 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 38:249–257CrossRefGoogle Scholar
  80. 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 44:263–275CrossRefGoogle Scholar
  81. 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 54:231–241CrossRefGoogle Scholar
  82. 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 333:151–160CrossRefGoogle Scholar
  83. 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 349:199–211CrossRefGoogle Scholar
  84. 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 55:271–288CrossRefGoogle Scholar
  85. 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 59:239–255CrossRefGoogle Scholar
  86. 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 66:37–51CrossRefGoogle Scholar
  87. 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 257:281–296CrossRefGoogle Scholar
  88. 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 57:121–144CrossRefGoogle Scholar
  89. 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 280:85–94CrossRefGoogle Scholar
  90. 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 37:19–34Google Scholar
  91. Koski M, Riser CW (2006) Post-bloom feeding of Calanus finmarchicus copepodites: selection for autotrophic versus heterotrophic prey. Mar Biol Res 2:109–119CrossRefGoogle Scholar
  92. Larsen J (1988) An ultrastructural study of Amphidinium poecilochroum (Dinophyceae), a phagotrophic dinoflagellate feeding on small species of cryptophytes. Phycologia 27:366–377Google Scholar
  93. 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)Google Scholar
  94. 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)Google Scholar
  95. Legrand C, Graneli E, Carlsson P (1998) Induced phagotrophy in the photosynthetic dinoflagellate Heterocapsa triquetra. Aquat Microb Ecol 15:65–75CrossRefGoogle Scholar
  96. Lessard EJ (1984) Oceanic heterotrophic dinoflagellates: distribution, abundance and role as microzooplankton. Ph.D. Thesis, University of Rhode Island, Kingstown, 166 pGoogle Scholar
  97. Lessard EJ, Swift E (1985) Species-specific grazing rates of heterotrophic dinoflagellates in oceanic waters, measured with a dual-label radioisotope technique. Mar Biol 87:289–296CrossRefGoogle Scholar
  98. Li A, Stoecker DK, Coats DW, Adam EJ (1996) Ingestion of fluorescently-labeled and phycoerythrin-containing prey by photosynthetic dinoflagellates. Aquat Microb Ecol 10:139–147CrossRefGoogle Scholar
  99. Li A, Stoecker DK, Coats DW (2000) Mixotrophy in Gyrodinium galatheanum (dinophyceae): grazing responses to light intensity and inorganic nutrients. J Phycol 36:33–45CrossRefGoogle Scholar
  100. Liu S, Wang W-X (2002) Feeding and reproductive responses of marine copepods in South China Sea to toxic and nontoxic phytoplankton. Mar Biol 140:595–603CrossRefGoogle Scholar
  101. 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 201:155–163CrossRefGoogle Scholar
  102. 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 43:799–810CrossRefGoogle Scholar
  103. 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 342:226–230CrossRefGoogle Scholar
  104. McFadden GI (2001) Primary and secondary endosymbiosis and the origin of plastids. J Phycol 37:951–959CrossRefGoogle Scholar
  105. 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 41:145–152CrossRefGoogle Scholar
  106. 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 69:1–8CrossRefGoogle Scholar
  107. 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 5:20–25CrossRefGoogle Scholar
  108. 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 125:269–277CrossRefGoogle Scholar
  109. 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 82:275–279CrossRefGoogle Scholar
  110. Naustvoll L-J (1998) Growth and grazing by the thecate heterotrophic dinoflagellate Diplopsalis lenticula (Diplopsalidaceae, Dinophyceae). Phycologia 37:1–9Google Scholar
  111. Naustvoll L-J (2000) Prey size spectra and food preferences in thecate heterotrophic dinoflagellates. Phycologia 39:187–198Google Scholar
  112. Navarro JM, Muoz MG, Contreras AM (2006) Temperature as a factor regulating growth and toxin content in the dinoflagellate Alexandrium catenella. Harmful algae 5:762–769CrossRefGoogle Scholar
  113. Nygaard K, Tobiesen A (1993) Bacterivory in algae: a survival strategy during nutrient limitation. Limnol Oceanogr 38:273–279CrossRefGoogle Scholar
  114. 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 45:101–106CrossRefGoogle Scholar
  115. 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 101–104Google Scholar
  116. 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 62:269–297CrossRefGoogle Scholar
  117. 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 41:415–423CrossRefGoogle Scholar
  118. Roman M, Reaugh M, Zhang X (2006) Ingestion of the dinoflagellate, Pfiesteria piscicida, by the calanoid copepod, Acartia tonsa. Harmful algae 5:435–441CrossRefGoogle Scholar
  119. 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 320–322Google Scholar
  120. 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 75:577–583Google Scholar
  121. 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 322:85–97CrossRefGoogle Scholar
  122. Sherr EB, Sherr BF (2002) Significance of predation by protests in aquatic microbial food webs. Ant van Leeuwenh 81:293–308CrossRefGoogle Scholar
  123. Siano R, Montresor M (2005) Morphology, ultrastructure and feeding behaviour of Protoperidinium vorax sp. nov. (Dinophyceae, Peridiniales). Eur J Phycol 40:221–232CrossRefGoogle Scholar
  124. Skovgaard A (1996a) Engulfment of Ceratium spp. (Dinophyceae) by the thecate photosynthetic dinoflagellate Fragilidium subglobosum. Phycologia 35:490–499Google Scholar
  125. Skovgaard A (1996b) Mixotrophy in Fragilidium subglobosum (Dinophyceae): growth and grazing responses as functions of light intensity. Mar Ecol Prog Ser 143:247–253CrossRefGoogle Scholar
  126. Skovgaard A (1998) Role of chloroplast retention in a marine dinoflagellate. Aquat Microb Ecol 15:293–301CrossRefGoogle Scholar
  127. Skovgaard A (2000) A phagotrophically derivable growth factor in the plastidic dinoflagellate Gyrodinium resplendens (Dinophyceae). J Phycol 36:1069–1078CrossRefGoogle Scholar
  128. 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 201:129–136CrossRefGoogle Scholar
  129. Sleigh MA (1989) Protozoa and other protists. Edward Arnold, London, 342 pGoogle Scholar
  130. 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 49:63–73CrossRefGoogle Scholar
  131. 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 17:167–179CrossRefGoogle Scholar
  132. Smalley GW, Coats DW, Stoecker DK (2003) Feeding in the mixotrophic dinoflagellate Ceratium furca is influenced by intracellular nutrient concentrations. Mar Ecol Prog Ser 262:137–151CrossRefGoogle Scholar
  133. Smayda TJ (1997) Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol Oceanogr 42:1137–1153CrossRefGoogle Scholar
  134. 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 32:157–164CrossRefGoogle Scholar
  135. Stickney HL, Hood RR, Stoecker DK (2000) The impact of mixotrophy on planktonic trophic dynamics in marine ecosystems. Ecol Model 125:203–230CrossRefGoogle Scholar
  136. Stoecker DK (1998) Conceptual models of mixotrophy in planktonic protists and some ecological and evolutionary implications. Eur J Protistol 34:281–290Google Scholar
  137. Stoecker DK (1999) Mixotrophy among dinoflagellates. J Eukaryot Microbiol 46:397–401CrossRefGoogle Scholar
  138. Stoecker DK, Evans GT (1985) Effects of protozoan herbivory and carnivory in a microplankton food web. Mar Ecol Prog 25:159–167CrossRefGoogle Scholar
  139. Stoecker DK, Guillard RRL, Kavee RM (1981) Selective predation by Favella ehrenbergii (Tintinnida) on and among dinoflagellates. Biol Bull 160:136–145CrossRefGoogle Scholar
  140. Stoecker DK, Li A, Coats DW, Gustafson DE, Nannen MK (1997) Mixotrophy in the dinoflagellate Prorocentrum minimum. Mar Ecol Prog Ser 152:1–12CrossRefGoogle Scholar
  141. 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 28:79–85CrossRefGoogle Scholar
  142. Strom SL (1991) Growth and grazing rates of the herbivorous dinoflagellate Gymnodinium sp. from the open subarctic Pacific Ocean. Mar Ecol Prog Ser 78:103–113CrossRefGoogle Scholar
  143. Strom SL, Buskey EJ (1993) Feeding, growth, and behavior of the thecate heterotrophic dinoflagellate Oblea rotunda. Limnol Oceanogr 38:965–977CrossRefGoogle Scholar
  144. Tester PA, Turner JT, Shea D (2000) Vectorial transport of toxins from the dinoflagellate Gymnodinium breve through copepods to fish. J Plankton Res 22:47–62CrossRefGoogle Scholar
  145. Tezuka Y (1990) Bacterial regeneration of ammonium and phosphate as affected by the carbon: nitrogen: phosphorus ratio of organic substrates. Microb Ecol 19:227–238CrossRefGoogle Scholar
  146. Tillmann U (2004) Interactions between planktonic microalgae and protozoan grazers. J Eukaryot Microbiol 51:156–168CrossRefGoogle Scholar
  147. 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 230:47–58CrossRefGoogle Scholar
  148. 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 4:359–374CrossRefGoogle Scholar
  149. Turner JT, Tester PA (1997) Toxic marine phytoplankton, zooplankton grazers, and pelagic food webs. Limnol Oceanogr 42:1203–1214CrossRefGoogle Scholar
  150. Uchida T, Kamiyama T, Matsuyama Y (1997) Predation by a photosynthetic dinoflagellate Gyrodinium instriatum on loricated ciliates. J Plankton Res 19:603–608CrossRefGoogle Scholar
  151. Uye SI, Takamatsu K (1990) Feeding interactions between planktonic copepods and red-tide flagellates from Japanese coastal waters. Mar Ecol Prog Ser 59:97–107CrossRefGoogle Scholar
  152. Verity PG, Paffenhöfer G-A (1996) On assessment of prey ingestion by copepods. J Plankton Res 18:1767–1779CrossRefGoogle Scholar
  153. 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 26:741–751CrossRefGoogle Scholar
  154. 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 7:891–908CrossRefGoogle Scholar
  155. 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 19:1167–1174CrossRefGoogle Scholar
  156. 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
  157. 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 56:413–420CrossRefGoogle Scholar
  158. 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 57:145–158CrossRefGoogle Scholar
  159. Yoon HS, Hackett JD, Pinto G, Bhattacharya D (2002) The single, ancient origin of chromist plastids. Proc Natl Acad Sci USA 99:15507–15512CrossRefGoogle Scholar

Copyright information

© Korea Ocean Research & Development Institute (KORDI) and the Korean Society of Oceanography (KSO) and Springer Netherlands 2010

Authors and Affiliations

  • Hae Jin Jeong
    • 1
  • Yeong Du Yoo
    • 1
  • Jae Seong Kim
    • 2
  • Kyeong Ah Seong
    • 3
  • Nam Seon Kang
    • 1
  • Tae Hoon Kim
    • 4
  1. 1.School of Earth and Environmental Sciences, College of Natural SciencesSeoul National UniversitySeoulKorea
  2. 2.Red Tide Research CenterKunsan National UniversityKunsanKorea
  3. 3.Saemankeum Environmental Research CenterKunsan National UniversityKunsanKorea
  4. 4.Research Institute of Oceanography, College of Natural SciencesSeoul National UniversitySeoulKorea

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