DOI QR코드

DOI QR Code

Feeding by common heterotrophic protists on the phototrophic dinoflagellate Biecheleriopsis adriatica (Suessiaceae) compared to that of other suessioid dinoflagellates

  • Kang, Hee Chang (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Jeong, Hae Jin (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Jang, Se Hyeon (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Lee, Kyung Ha (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University)
  • Received : 2019.03.31
  • Accepted : 2019.05.29
  • Published : 2019.06.15

Abstract

The species in the dinoflagellate order Suessiales have 5-24 latitudinal paraplate series and include many fossil and extant species. There have been a few studies on the ecophysiology of the phototrophic species Biecheleriopsis adriatica, and no study on its predators. Thus, we explored the feeding occurrence by common heterotrophic protists on B. adriatica and the growth and ingestion rates of the heterotrophic dinoflagellate Oxyrrhis marina on B. adriatica BATY06 as a function of prey concentration. The common heterotrophic dinoflagellates Aduncodinium glandula, O. marina, Gyrodinium dominans, Gyrodinium moestrupii, Luciella masanensis, Pfiesteria piscicida, and Oblea rotunda and two naked ciliates Strombidinopsis sp. and Pelagostrobilidium sp. were able to feed on B. adriatica, but the heterotrophic dinoflagellate Polykrikos kofoidii was not. However, B. adriatica supported the positive growth of O. marina, but did not support that of G. dominans and O. rotunda. With increasing prey concentrations, the growth and ingestion rates of O. marina on B. adriatica increased and became saturated. The maximum growth rate of O. marina on B. adriatica was $0.162d^{-1}$. Furthermore, the maximum ingestion rate of O. marina on B. adriatica was $0.2ng\;C\;predator^{-1}\;d^{-1}$ ($2.0cells\;predator^{-1}\;d^{-1}$). In the order Suessiales, the feeding occurrence by common heterotrophic protists on B. adriatica is similar to that on Effrenium voratum and Biecheleria cincta, but different from that on Yihiella yeosuensis. However, the growth and ingestion rates of O. marina on B. adriatica are considerably lower than those on E. voratum and B. cincta, but higher than those on Y. yeosuensis. Therefore, B. adriatica may be less preferred prey for O. marina than E. voratum and B. cincta, but more preferred prey than Y. yeosuensis.

Keywords

Acknowledgement

Supported by : National Research Foundation (NRF)

References

  1. Adolf, J. E., Bachvaroff, T. R., Deeds, J. R. & Place, A. R. 2015. Ichthyotoxic Karlodinium veneficum (Ballantine) J Larsen in the upper Swan River estuary (western Australia): ecological conditions leading to a fish kill. Harmful Algae 48:83-93. https://doi.org/10.1016/j.hal.2015.07.006
  2. Adolf, J. E., Krupatkina, D., Bachvaroff, T. & Place, A. R. 2007. Karlotoxin mediates grazing by Oxyrrhis marina on strains of Karlodinium veneficum. Harmful Algae 6:400-412. https://doi.org/10.1016/j.hal.2006.12.003
  3. Affan, M. A., Lee, J. B., Khomayis, H. S., Touliabah, H. E. S. & Abdulwassi, N. I. 2014. Community composition and dynamics of phytoplankton at the western coast of Jeju Island, Korea. Indian J. Geo-Mar. Sci. 43:1879-1890.
  4. Benico, G. A., Takahashi, K., Lum, W. M., Yñiguez, A. T., Azanza, R. V., Leong, S. C. Y., Lim, P. T. & Iwataki, M. 2019. First report of Biecheleriopsis adriatica in Bolinao, Northwestern Philippines and its wide distribution in Southeast Asia and adjacent waters. Philipp. J. Nat. Sci. 24:34-41.
  5. Calbet, A., Isari, S., Martinez, R. A., Saiz, E., Garrido, S., Peters, J., Borrat, R. M. & Alcaraz, M. 2013. Adaptations to feast and famine in different strains of the marine heterotrophic dinoflagellates Gyrodinium dominans and Oxyrrhis marina. Mar. Ecol. Prog. Ser. 483:67-84. https://doi.org/10.3354/meps10291
  6. Calbet, A. & Landry, M. R. 2004. Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems. Limnol. Oceanogr. 49:51-57. https://doi.org/10.4319/lo.2004.49.1.0051
  7. Carlsson, P., Graneli, E. & Segatto, A. Z. 1999. Cycling of biologically available nitrogen in riverine humic substances between marine bacteria, a heterotrophic nanoflagellate and a photosynthetic dinoflagellate. Aquat. Microb. Ecol. 18:23-36. https://doi.org/10.3354/ame018023
  8. Claessens, M., Wickham, S. A., Post, A. F. & Reuter, M. 2008. Ciliate community in the oligotrophic Gulf of Aqaba, Red Sea. Aquat. Microb. Ecol. 53:181-190. https://doi.org/10.3354/ame01243
  9. Coats, D. W. 1999. Parasitic life styles of marine dinoflagellates. J. Eukaryot. Microbiol. 46:402-409. https://doi.org/10.1111/j.1550-7408.1999.tb04620.x
  10. Eppley, R. W., Renger, E. H., Venrick, E. L. & Mullin, M. M. 1973. A study of plankton dynamics and nutrient cycling in the central gyre of the north pacific ocean. Limnol. Oceanogr. 18:534-551. https://doi.org/10.4319/lo.1973.18.4.0534
  11. Frost, B. W. 1972. Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus. Limnol. Oceanogr. 17:805-815. https://doi.org/10.4319/lo.1972.17.6.0805
  12. Fuller, A. K. R. 1990. The grazing and growth rates of some marine protozoa measured in batch and continuous culture with particular reference to the heterotrophic dinoflagellate Oxyrrhis marina. Ph. D. dissertation, Royal Holloway, University of London, Egham, pp. 57-129.
  13. Hansen, P. J. 1992. Prey size selection, feeding rates and growth dynamics of heterotrophic dinoflagellates with special emphasis on Gyrodinium spirale. Mar. Biol. 114:327-334. https://doi.org/10.1007/BF00349535
  14. Hansen, P. J. 2011. The role of photosynthesis and food uptake for the growth of marine mixotrophic dinoflagellates. J. Eukaryot. Microbiol. 58:203-214. https://doi.org/10.1111/j.1550-7408.2011.00537.x
  15. Heinbokel, J. F. 1978. Studies on the functional role of tintinnids in the Southern California Bight. I. grazing and growth rates in laboratory cultures. Mar. Biol. 47:177-189. https://doi.org/10.1007/BF00395638
  16. Jang, S. H., Jeong, H. J., Kwon, J. E. & Lee, K. H. 2017. Mixotrophy in the newly described dinoflagellate Yihiella yeosuensis: a small, fast dinoflagellate predator that grows mixotrophically, but not autotrophically. Harmful Algae 62:94-103. https://doi.org/10.1016/j.hal.2016.12.007
  17. Jang, S. H., Jeong, H. J., Lim, A. S., Kwon, J. E. & Kang, N. S. 2016. Feeding by the newly described heterotrophic dinoflagellate Aduncodinium glandula: having the most diverse prey species in the family Pfiesteriaceae. Algae 31:17-31. https://doi.org/10.4490/algae.2016.31.2.2
  18. Jang, S. H., Jeong, H. J., Moestrup, O., Kang, N. S., Lee, S. Y., Lee, K. H., Lee, M. J. & Noh, J. H. 2015. Morphological, molecular and ecophysiological characterization of the phototrophic dinoflagellate Biecheleriopsis adriatica from Korean coastal waters. Eur. J. Phycol. 50:301-317. https://doi.org/10.1080/09670262.2015.1054892
  19. Jeong, H. J. 1999. The ecological roles of heterotrophic dinoflagellates in marine planktonic community. J. Eukaryot. Microbiol. 46:390-396. https://doi.org/10.1111/j.1550-7408.1999.tb04618.x
  20. Jeong, H. J., Ha, J. H., Park, J. Y., Kim, J. H., Kang, N. S., Kim, S., Kim, J. S., Yoo, Y. D. & Yih, W. H. 2006. Distribution of the heterotrophic dinoflagellate Pfiesteria piscicida in Korean waters and its consumption of mixotrophic dinoflagellates, raphidophytes and fish blood cells. Aquat. Microb. Ecol. 44:263-278. https://doi.org/10.3354/ame044263
  21. Jeong, H. J., Kang, H., Shim, J. H., Park, J. K., Kim, J. S., Song, J. Y. & Choi, H. -J. 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. https://doi.org/10.3354/meps218077
  22. Jeong, H. J., Kang, H. C., You, J. H. & Jang, S. H. 2018a. Interactions between the newly described small‐ and fast‐swimming mixotrophic dinoflagellate Yihiella yeosuensis and common heterotrophic protists. J. Eukaryot. Microbiol. 65:612-626. https://doi.org/10.1111/jeu.12506
  23. Jeong, H. J., Kim, J. S., Lee, K. H., Seong, K. A., Yoo, Y. D., Kang, N. S., Kim, T. H., Song, J. Y. & Kwon, J. E. 2017a. Differential interactions between the nematocyst-bearing mixotrophic dinoflagellate Paragymnodinium shiwhaense and common heterotrophic protists and copepods: killer or prey. Harmful Algae 62:37-51. https://doi.org/10.1016/j.hal.2016.12.005
  24. Jeong, H. J., Kim, J. S., Song, J. Y., Kim, J. H., Kim, T. H., Kim, S. K. & Kang, N. S. 2007. Feeding by heterotrophic protists and copepods on the heterotrophic dinoflagellates Pfiesteria pisicicida, Stoeckeria algicida, and Luciella masanensis. Mar. Ecol. Prog. Ser. 349:199-211. https://doi.org/10.3354/meps07094
  25. Jeong, H. J., Kim, J. S., Yoo, Y. D., Kim, S. T., Kim, T. H., Park, M. G., Lee, C. H., Seong, K. A., Kang, N. S. & Shim, J. H. 2003. 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. Microbiol. 50:274-282. https://doi.org/10.1111/j.1550-7408.2003.tb00134.x
  26. Jeong, H. J., Kim, J. S., Yoo, Y. D., Kim, S. T., Song, J. Y., Kim, T. H., Seong, K. A., Kang, N. S., Kim, M. S., Kim, J. H., Kim, S., Ryu, J., Lee, H. M. & Yih, W. H. 2008a. Control of the harmful alga Cochlodinium polykrikoides by the naked ciliate Strombidinopsis jeokjo in mesocosm enclosures. Harmful Algae 7:368-377. https://doi.org/10.1016/j.hal.2007.12.004
  27. Jeong, H. J., Kim, S. K., Kim, J. S., Kim, S. T., Yoo, Y. D. & Yoon, J. Y. 2001b. Growth and grazing rates of the heterotrophic dinoflagellate Polykrikos kofoidii on red‐tide and toxic dinoflagellates. J. Eukaryot. Microbiol. 48:298-308. https://doi.org/10.1111/j.1550-7408.2001.tb00318.x
  28. Jeong, H. J., Kim, T. H., Yoo, Y. D., Yoon, E. Y., Kim, J. S., Seong, K. A., Kim, K. Y. & Park, J. Y. 2011. Grazing impact of heterotrophic dinoflagellates and ciliates on common redtide euglenophyte Eutreptiella gymnastica in Masan Bay, Korea. Harmful Algae 10:576-588. https://doi.org/10.1016/j.hal.2011.04.008
  29. Jeong, H. J., Lee, C. W., Yih, W. H. & Kim, J. S. 1997. 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. 151:299-305. https://doi.org/10.3354/meps151299
  30. Jeong, H. J., Lim, A. S., Franks, P. J. S., Lee, K. H., Kim, J. H., Kang, N. S., Lee, M. J., Jang, S. H., Lee, S. Y., Yoon, E. Y., Park, J. Y., Yoo, Y. D., Seong, K. A., Kwon, J. E. & Jang, T. Y. 2015. A hierarchy of conceptual models of red-tide generation: nutrition, behavior, and biological interactions. Harmful Algae 47:97-115. https://doi.org/10.1016/j.hal.2015.06.004
  31. Jeong, H. J., Lim, A. S., Lee, K., Lee, M. J., Seong, K. A., Kang, N. S., Jang, S. H., Lee, K. H., Lee, S. Y., Kim, M. O., Kim, J. H., Kwon, J. E., Kang, H. C., Kim, J. S., Yih, W., Shin, K., Jang, P. K., Ryu, J. -H., Kim, S. Y., Park, J. Y. & Kim, K. W. 2017b. Ichthyotoxic Cochlodinium polykrikoides red tides offshore in the South Sea, Korea in 2014: I. temporal variations in three-dimensional distributions of red-tide organisms and environmental factors. Algae 32:101-130. https://doi.org/10.4490/algae.2017.32.5.30
  32. Jeong, H. J., Lim, A. S., Yoo, Y. D., Lee, M. J., Lee, K. H., Jang, T. Y. & Lee, K. 2014. Feeding by heterotrophic dinoflagellates and ciliates on the free‐living dinoflagellate Symbiodinium sp.(Clade E). J. Eukaryot. Microb. 61:27-41. https://doi.org/10.1111/jeu.12083
  33. Jeong, H. J., Seong, K. A., Yoo, Y. D., Kim, T. H., Kang, N. S., Kim, S., Park, J. Y., Kim, J. S., Kim, G. H. & Song, J. Y. 2008b. Feeding and grazing impact by small marine heterotrophic dinoflagellates on hetertrophic bacteria. J. Eukaryot. Microbiol. 55:271-288. https://doi.org/10.1111/j.1550-7408.2008.00336.x
  34. Jeong, H. J., Shim, J. H., Lee, C. W., Kim, J. S. & Koh, S. M. 1999. Growth and grazing rates of the marine planktonic ciliate Strombidinopsis sp. on red‐tide and toxic dinoflagellates. J. Eukaryot. Microbiol.46:69-76. https://doi.org/10.1111/j.1550-7408.1999.tb04586.x
  35. Jeong, H. J., Yoo, Y. D. & Kim, J. S. 2002. Outbreak of red tides in the coastal waters off the Southern Saemankeum areas, Jeonbuk, Korea 2. Temporal variation in the heterotrophic dinoflagellates and ciliates in the summer-fall of 1999. J. Korean Soc. Oceanogr. 7:140-147. (in Korean with English abstract)
  36. Jeong, H. J., Yoo, Y. D., Kim, J. S., Seong, K. A., Kang, N. S. & Kim, T. H. 2010. Growth, feeding, and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci. J. 45:65-91. https://doi.org/10.1007/s12601-010-0007-2
  37. Jeong, H. J., You, J. H., Lee, K. H., Kim, S. J. & Lee, S. Y. 2018b. Feeding by common heterotrophic protists on the mixotrophic alga Gymnodinium smaydae (Dinophyceae), one of the fastest growing dinoflagellates. J. Phycol. 54:734-743. https://doi.org/10.1111/jpy.12775
  38. Johnson, M. D. 2015. Inducible mixotrophy in the dinoflagellate Prorocentrum minimum. J. Eukaryot. Microbiol. 62:431-443. https://doi.org/10.1111/jeu.12198
  39. Kang, H. C., Jeong, H. J., Kim, S. J., You, J. H. & Ok, J. H. 2018. Differential feeding by common heterotrophic protists on 12 different Alexandrium species. Harmful Algae 78:106-117. https://doi.org/10.1016/j.hal.2018.08.005
  40. Kang, H. C., Jeong, H. J., Ok, J. H., You, J. H., Jang, S. H., Lee, S. Y., Lee, K. H., Park, J. Y. & Rho, J-R. 2019. Spatial and seasonal distributions of the phototrophic dinoflagellate Biecheleriopsis adriatica (Suessiaceae) in Korea: quantification using qPCR. Algae 34:111-126. https://doi.org/10.4490/algae.2019.34.5.25
  41. Kang, N. S., Jeong, H. J., Yoo, Y. D., Yoon, E. Y., Lee, K. H., Lee, K. & Kim, G. 2011. Mixotrophy in the newly described phototrophic dinoflagellate Woloszynskia cincta from western Korean waters: feeding mechanism, prey species and effect of prey concentration. J. Eukaryot. Microbiol. 58:152-170. https://doi.org/10.1111/j.1550-7408.2011.00531.x
  42. Kang, N. S., Lee, K. H., Jeong, H. J., Yoo, Y. D., Seong, K. A., Potvin, E., Hwang, Y. J. & Yoon, E. Y. 2013. Red tides in Shiwha Bay, western Korea: a huge dike and tidal power plant established in a semi-enclosed embayment system. Harmful Algae 30(Suppl. 1):S114-S130. https://doi.org/10.1016/j.hal.2013.10.011
  43. Kim, J. S. & Jeong, H. J. 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. https://doi.org/10.3354/meps280085
  44. Kim, S. J., Jeong, H. J., Kang, H. C., You, J. H. & Ok, J. H. 2019. Differential feeding by common heterotrophic protists on four Scrippsiella species of similar size. J. Phycol. doi:10.1111/jpy.12864.
  45. Kim, Y. H. & Lee, J. B. 2003. Seasonal variations and species composition of planktonic ciliates in the southern coastal waters of Jeju Island, Korea. J. Korean Soc. Oceanogr. 8:59-69. (in Korean with English abstract)
  46. Kimmance, S. A., Atkinson, D. & Montagnes, D. J. S. 2006. Do temperature-food interactions matter? Responses of production and its components in the model heterotrophic flagellate Oxyrrhis marina. Aquat. Microb. Ecol. 42:63-73. https://doi.org/10.3354/ame042063
  47. Lessard, E. J. 1984. Oceanic heterotrophic dinoflagellates: distribution, abundance, and role as microzooplankton. Ph.D. dissertation, University of Rhode Island, Kingston, RI, 166 pp.
  48. Levinsen, H. & Nielsen, T. G. 2002. The trophic role of marine pelagic ciliates and heterotrophic dinoflagellates in arctic and temperate coastal ecosystems: a cross‐latitude comparison. Limnol. Oceanogr. 47:427-439. https://doi.org/10.4319/lo.2002.47.2.0427
  49. Lim, A. S., Jeong, H. J., Kim, J. H. & Lee, S. Y. 2017a. Control of ichthyotoxic Cochlodinium polykrikoides using the mixotrophic dinoflagellate Alexandrium pohangense: a potential effective sustainable method. Harmful Algae 63:109-118. https://doi.org/10.1016/j.hal.2017.02.001
  50. Lim, A. S., Jeong, H. J., Seong, K. A., Lee, M. J., Kang, N. S., Jang, S. H., Lee, K. H., Park, J. Y., Jang, T. Y. & Yoo, Y. D. 2017b. Ichthyotoxic Cochlodinium polykrikoides red tides offshore in the South Sea, Korea in 2014: II. Heterotrophic protists and their grazing impacts on redtide organisms. Algae 32:199-222. https://doi.org/10.4490/algae.2017.32.8.25
  51. Lindberg, K., Moestrup, O. & Daugbjerg, N. 2005. Studies on woloszynskioid dinoflagellates I: Woloszynskia coronata re-examined using light and electron microscopy and partial LSU rDNA sequences, with description of Tovellia gen. nov. and Jadwigia gen. nov. (Tovelliaceae fam. nov.). Phycologia 44:416-440. https://doi.org/10.2216/0031-8884(2005)44[416:SOWDIW]2.0.CO;2
  52. Mason, P. L., Litaker, R. W., Jeong, H. J., Ha, J. H., Reece, K. S., Stokes, N. A., Park, J. Y., Steidinger, K. A., Vandersea, M. W., Kibler, S., Tester, P. A. & Vogelbein, W. K. 2007. Description of a new genus 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. https://doi.org/10.1111/j.1529-8817.2007.00370.x
  53. Menden-Deuer, S. & Lessard, E. J. 2000. Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol. Oceanogr. 45:569-579. https://doi.org/10.4319/lo.2000.45.3.0569
  54. Menden-Deuer, S., Lessard, E. J., Satterberg, J. & Grunbaum, D. 2005. Growth rates and starvation survival of three species of the pallium-feeding, thecate dinoflagellate genus Protoperidinium. Aquat. Microb. Ecol. 41:145-152. https://doi.org/10.3354/ame041145
  55. Menden-Deuer, S. & Montalbano, A. L. 2015. Bloom formation potential in the harmful dinoflagellate Akashiwo sanguinea: clues from movement behaviors and growth characteristics. Harmful Algae 47:75-85. https://doi.org/10.1016/j.hal.2015.06.001
  56. Moestrup, O., Lindberg, K. & Daugbjerg, N. 2009. Studies on woloszynskioid dinoflagellates V. Ultrastructure of Biecheleriopsis gen. nov., with description of Biecheleriopsis adriatica sp. nov. Phycol. Res. 57:221-237. https://doi.org/10.1111/j.1440-1835.2009.00541.x
  57. Montagnes, D. J. S. & Lessard, E. J. 1999. Population dynamics of the marine planktonic ciliate Strombidinopsis multiauris: its potential to control phytoplankton blooms. Aquat. Microb. Ecol. 20:167-181. https://doi.org/10.3354/ame020167
  58. Ok, J. H., Jeong, H. J., Lim, A. S. & Lee, K. H. 2017. Interactions between the mixotrophic dinoflagellate Takayama helix and common heterotrophic protists. Harmful Algae 68:178-191. https://doi.org/10.1016/j.hal.2017.08.006
  59. Potvin, E., Hwang, Y. J., Yoo, Y. D., Kim, J. S. & Jeong, H. J. 2013. Feeding by heterotrophic protists and copepods on the photosynthetic dinoflagellate Azadinium cf. poporum from western Korean waters. Aquat. Microb. Ecol. 68:143-158. https://doi.org/10.3354/ame01603
  60. Sherr, E. B. & Sherr, B. F. 2002. Significance of predation by protists in aquatic microbial food webs. Antonie Van Leeuwenhoek 81:293-308. https://doi.org/10.1023/A:1020591307260
  61. Stoecker, D. K. 1999. Mixotrophy among dinoflagellates. J. Eukaryot. Microbiol. 46:397-401. https://doi.org/10.1111/j.1550-7408.1999.tb04619.x
  62. Stoecker, D. K., Hansen, P. J., Caron, D. A. & Mitra, A. 2017. Mixotrophy in the marine plankton. Annu. Rev. Mar. Sci. 9:311-335. https://doi.org/10.1146/annurev-marine-010816-060617
  63. Strom, S. L. & Buskey, E. J. 1993. Feeding, growth, and behavior of the thecate heterotrophic dinoflagellate Oblea rotunda. Limnol. Oceanogr. 38:965-977. https://doi.org/10.4319/lo.1993.38.5.0965
  64. Strom, S. L. & Morello, T. A. 1998. Comparative growth rates and yields of ciliates and heterotrophic dinoflagellates. J. Plankton Res. 20:571-584. https://doi.org/10.1093/plankt/20.3.571
  65. Strom, S., Wolfe, G., Holmes, J., Stecher, H., Shimeneck, C. & Sarah, L. 2003. Chemical defense in the microplankton I: feeding and growth rates of heterotrophic protists on the DMS‐producing phytoplankter Emiliania huxleyi. Limnol. Oceanogr. 48:217-229. https://doi.org/10.4319/lo.2003.48.1.0217
  66. Taylor, F. J. R., Hoppenrath, M. & Saldarriaga, J. F. 2008. Dinoflagellate diversity and distribution. Biodivers. Conserv. 17:407-418. https://doi.org/10.1007/s10531-007-9258-3
  67. Tillmann, U. 2004. Interactions between planktonic microalgae and protozoan grazers. J. Eukaryot. Microbiol. 51:156-168. https://doi.org/10.1111/j.1550-7408.2004.tb00540.x
  68. Tillmann, U. & Hoppenrath, M. 2013. Life cycle of the pseudocolonial dinoflagellate Polykrikos kofoidii (Gymnodiniales, Dinoflagellata). J. Phycol. 49:298-317. https://doi.org/10.1111/jpy.12037
  69. Tillmann, U. & Reckermann, M. 2002. Dinoflagellate grazing on the raphidophyte Fibrocapsa japonica. Aquat. Microb. Ecol. 26:247-257. https://doi.org/10.3354/ame026247
  70. Turner, J. T. & Borkman, D. G. 2005. Impact of zooplankton grazing on Alexandrium blooms in the offshore Gulf of Maine. Deep Sea Res. Part 2 Top. Stud. Oceanogr. 52:2801-2816.
  71. Watts, P. C., Martin, L. E., Kimmance, S. A., Montagnes, D. J. S. & Lowe, C. D. 2010. The distribution of Oxyrrhis marina: a global disperser or poorly characterized endemic? J. Plankton Res. 33:579-589.
  72. Yoo, Y. D., Jeong, H. J., Kang, N. S., Kim, J. S., Kim, T. H. & Yoon, E. Y. 2010. Ecology of Gymnodinium aureolum. II. predation by common heterotrophic dinoflagellates and a ciliate. Aquat. Microb. Ecol. 59:257-272. https://doi.org/10.3354/ame01401
  73. Yoo, Y. D., Jeong, H. J., Kim, J. S., Kim, T. H., Kim, J. H., Seong, K. A., Lee, S. H., Kang, N. S., Park, J. W., Park, J., Yoon, E. Y. & Yih, W. H. 2013a. Red tides in Masan Bay, Korea in 2004-2005: II. daily variations in the abundance of heterotrophic protists and their grazing impact on red-tide organisms. Harmful Algae 30(Suppl. 1):S89-S101. https://doi.org/10.1016/j.hal.2013.10.009
  74. Yoo, Y. D., Yoon, E. Y., Jeong, H. J., Lee, K. H., Hwang, Y. J., Seong, K. A., Kim, J. S. & Park, J. Y. 2013b. The newly de scribed heterotrophic dinoflagellate Gyrodinium moestrupii, an effective protistan grazer of toxic dinoflagellate. J. Eukaryot. Microbiol. 60:13-24. https://doi.org/10.1111/jeu.12002
  75. Yoo, Y. D., Yoon, E. Y., Lee, K. H., Kang, N. S. & Jeong, H. J. 2013c. Growth and ingestion rates of heterotrophic dinoflagellates and a ciliate on the mixotrophic dinoflagellate Biecheleria cincta. Algae 28:343-354. https://doi.org/10.4490/algae.2013.28.4.343
  76. Yoon, E. Y. 2018. The heterotrophic dinoflagellates Oxyrrhis marina and Oxyrrhis maritima in Korean waters: taxonomy, physiology, distribution, and production of useful materials. Ph.D. dissertation, Seoul National University, Seoul, 133 pp.
  77. Yoon, Y. H. 2017. Marine bio-environmental characteristics with the distributions of dinoflagellate cyst assemblages in the Ulsan coastal waters (UCW). Korean J. Environ. Biol. 35:361-372. (in Korean with English abstract) https://doi.org/10.11626/KJEB.2017.35.3.361

Cited by

  1. Spatio-temporal distributions of the newly described mixotrophic dinoflagellate Yihiella yeosuensis (Suessiaceae) in Korean coastal waters and its grazing impact on prey populations vol.35, pp.1, 2019, https://doi.org/10.4490/algae.2020.35.2.24
  2. Feeding by common heterotrophic protist predators on seven Prorocentrum species vol.35, pp.1, 2019, https://doi.org/10.4490/algae.2020.35.2.28
  3. Effects of irradiance and temperature on the growth and feeding of the obligate mixotrophic dinoflagellate Gymnodinium smaydae vol.167, pp.5, 2020, https://doi.org/10.1007/s00227-020-3678-y
  4. Effects of temperature on the growth and ingestion rates of the newly described mixotrophic dinoflagellate Yihiella yeosuensis and its two optimal prey species vol.35, pp.3, 2019, https://doi.org/10.4490/algae.2020.35.8.20
  5. Spatial-temporal distributions of the newly described mixotrophic dinoflagellate Gymnodinium smaydae in Korean coastal waters vol.35, pp.3, 2020, https://doi.org/10.4490/algae.2020.35.8.25
  6. Feeding by the newly described heterotrophic dinoflagellate Gyrodinium jinhaense: comparison with G. dominans and G. moestrupii vol.167, pp.10, 2019, https://doi.org/10.1007/s00227-020-03769-9
  7. Interactions Between the Kleptoplastidic Dinoflagellate Shimiella gracilenta and Several Common Heterotrophic Protists vol.8, 2019, https://doi.org/10.3389/fmars.2021.738547
  8. Comparative Transcriptome Analysis of the Phototrophic Dinoflagellate Biecheleriopsis adriatica Grown Under Optimal Temperature and Cold and Heat Stress vol.8, 2019, https://doi.org/10.3389/fmars.2021.761095
  9. Interactions between common heterotrophic protists and the dinoflagellate Tripos furca: implication on the long duration of its red tides in the South Sea of Korea in 2020 vol.36, pp.1, 2019, https://doi.org/10.4490/algae.2021.36.2.22
  10. Comparison of the spatial-temporal distributions of the heterotrophic dinoflagellates Gyrodinium dominans, G. jinhaense, and G. moestrupii in Korean coastal waters vol.36, pp.1, 2019, https://doi.org/10.4490/algae.2021.36.3.4