ALGAE

The Korean Society of Phycology (한국조류학회(藻類))
권호 표지
DOI QR코드

DOI QR Code

Mixotrophy in the newly described dinoflagellate Ansanella granifera: feeding mechanism, prey species, and effect of prey concentration

  • Lee, Sook Kyung (KHNP-Central Research Institute, Korea Hydro & Nuclear Power Corporation) ;
  • 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) ;
  • Kang, Nam Seon (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Lee, Moo Joon (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Potvin, Eric (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University)
  • Received : 2014.04.10
  • Accepted : 2014.05.20
  • Published : 2014.06.15
Download PDF
⟨ Previous Next ⟩

Abstract

Mixotrophic protists play diverse roles in marine food webs as predators and prey. Thus, exploring mixotrophy in phototrophic protists has emerged as a critical step in understanding marine food webs and cycling of materials in marine ecosystem. To investigate the feeding of newly described mixotrophic dinoflagellate Ansanella granifera, we explored the feeding mechanism and the different types of species that A. granifera was able to feed on. In addition, we measured the growth and ingestion rates of A. granifera feeding on the prasinophyte Pyramimonas sp., the only algal prey, as a function of prey concentration. A. granifera was able to feed on heterotrophic bacteria and the cyanobacterium Synechococcus sp. However, among the 12 species of algal prey offered, A. granifera ingested only Pyramimonas sp. A. granifera ingested the algal prey cell by engulfment. With increasing mean prey concentration, the growth rate of A. granifera feeding on Pyramimonas sp. increased rapidly, but became saturated at a concentration of $434ngCmL^{-1}$ (10,845 cells $mL^{-1}$). The maximum specific growth rate (i.e., mixotrophic growth) of A. granifera feeding on Pyramimonas sp. was $1.426d^{-1}$, at $20^{\circ}C$ under a 14 : 10 h light-dark cycle of $20{\mu}Em^{-2}s^{-1}$, while the growth rate (i.e., phototrophic growth) under similar light conditions without added prey was $0.391d^{-1}$. With increasing mean prey concentration, the ingestion rate of A. granifera feeding on Pyramimonas sp. increased rapidly, but slightly at the concentrations ${\geq}306ngCmL^{-1}$ (7,649 cells $mL^{-1}$). The maximum ingestion rate of A. granifera feeding on Pyramimonas sp. was 0.97 ng C $predator^{-1}d^{-1}$ (24.3 cells $grazer^{-1}d^{-1}$). The calculated grazing coefficients for A. granifera feeding on co-occurring Pyramimonas sp. were up to $2.78d^{-1}$. The results of the present study suggest that A. granifera can sometimes have a considerable grazing impact on the population of Pyramimonas spp.

Keywords

References

  1. Adolf, J. E., Stoecker, D. K. & Harding, L. W. Jr. 2006. The balance of autotrophy and heterotrophy during mixotrophic growth of Karlodinium micrum (Dinophyceae). J. Plankton Res. 28:737-751. https://doi.org/10.1093/plankt/fbl007
  2. Alonso-Rodriguez, R., Paez-Osuna, F. & Cortes-Altamirano, R. 2000. Trophic conditions and stoichiometric nutrient balance in subtropical waters influenced by municipal sewage effluents in Mazatlan Bay (SE Gulf of California). Mar. Pollut. Bull. 40:331-339. https://doi.org/10.1016/S0025-326X(99)00225-8
  3. Berge, T., Hansen, P. J. & Moestrup, O. 2008a. Feeding mechanism, prey specificity and growth in light and dark of the plastidic dinoflagellate Karlodinium armiger. Aquat. Microb. Ecol. 50:279-288. https://doi.org/10.3354/ame01165
  4. Berge, T., Hansen, P. J. & Moestrup, O. 2008b. Prey size spectrum and bioenergetics of the mixotrophic dinoflagellate Karlodinium armiger. Aquat. Microb. Ecol. 50:289-299. https://doi.org/10.3354/ame01166
  5. Bird, D. F. & Karl, D. M. 1991. Massive prasinophyte bloom in northern Gerlache Strait. Antarct. J. U. S. 26:152-154.
  6. Burkholder, J. M., Glibert, P. M. & Skelton, H. M. 2008. Mixotrophy, a major mode of nutrition for harmful algal speeies in eutrophic waters. Harmful Algae 8:77-93. https://doi.org/10.1016/j.hal.2008.08.010
  7. Burkholder, J. M., Noga, E. J., Hobbs, C. H., Glasgow, H. B. Jr. & Smith, S. A. 1992. New "phantom" dinoflagellate is the causative agent of major estuarine fish kills. Nature 358:407-410. https://doi.org/10.1038/358407a0
  8. Daugbjerg, N., Marchant, H. J. & Thomsen, H. A. 2000. Life history stages of Pyramimonas tychotreta (Prasinophyceae, Chlorophyta), a marine flagellate from the Ross Sea, Antarctica. Phycol. Res. 48:199-209. https://doi.org/10.1111/j.1440-1835.2000.tb00216.x
  9. Eppley, R. W. & Harrison, W. G. 1975. Physiological ecology of Gonyaulax polyedra, a red water dinoflagellate of southern California. In Locicero, V. R. (Ed.) Proc. 1st Int. Conf. Toxic Dinoflagellate Blooms, Massachusetts Science and Technology Foundation, Wakefield, MA, pp. 11-22.
  10. 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
  11. Glibert, P. M., Burkholder, J. M., Kana, T. M., Alexander, J., Skelton, H. & Shilling, C. 2009. Grazing by Karenia brevis on Synechococcus enhances its growth rate and may help to sustain blooms. Aquat. Microb. Ecol. 55:17-30. https://doi.org/10.3354/ame01279
  12. Gradinger, R. 1996. Occurrence of an algal bloom under Arctic pack ice. Mar. Ecol. Prog. Ser. 131:301-305. https://doi.org/10.3354/meps131301
  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., Bjornsen, P. K. & Hansen, B. W. 1997. Zooplankton grazing and growth: scaling within the 2-2,000-$\mu{m}$ body size range. Limnol. Oceanogr. 42:687-704. https://doi.org/10.4319/lo.1997.42.4.0687
  15. Hansen, P. J. & Nielsen, T. G. 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. https://doi.org/10.3354/meps147187
  16. 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
  17. Horiguchi, T. & Pienaar, R. N. 1994a. Gymnodinium natalense sp. nov. (Dinophyceae), a new tide pool dinoflagellate from South Africa. Jpn. J. Phycol. 42:21-28.
  18. Horiguchi, T. & Pienaar, R. N. 1994b. Ultrastructure and ontogeny of a new type of eyespot in dinoflagellates. Protoplasma 179:142-150. https://doi.org/10.1007/BF01403952
  19. Jacobson, D. M. & Anderson, D. M. 1986. Thecate heterotrophic dinoflagellates: feeding behavior and mechanisms. J. Phycol. 22:249-258. https://doi.org/10.1111/j.1529-8817.1986.tb00021.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., Ha, J. H., Yoo, Y. D., Park, J. Y., Kim, J. H., Kang, N. S., Kim, T. H., Kim, H. S. & Yih, W. H. 2007. Feeding by the Pfiesteria-like heterotrophic dinoflagellate Luciella masanensis. J. Eukaryot. Microbiol. 54:231-241. https://doi.org/10.1111/j.1550-7408.2007.00259.x
  22. Jeong, H. J., Jang, S. H., Moestrup, O., Kang, N. S., Lee, S. Y., Potvin, E. & Noh, J. H. 2014a. Ansanella granifera gen. et sp. nov. (dinophyceae), a new dinoflagellate from the coastal waters of Korea. Algae 29:75-99. https://doi.org/10.4490/algae.2014.29.2.075
  23. Jeong, H. J., Kim, J. S., Kim, J. H., Kim, S. T., Seong, K. A., Kim, T. H., Song, J. Y. & Kim, S. K. 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. https://doi.org/10.3354/meps295069
  24. Jeong, H. J., Lee, K. H., Yoo, Y. D., Kang, N. S. & Lee, K. 2011. Feeding by the newly described, nematocyst-bearing heterotrophic dinoflagellate Gyrodiniellum shiwhaense. J. Eukaryot. Microbiol. 58:511-524. https://doi.org/10.1111/j.1550-7408.2011.00580.x
  25. Jeong, H. J., Lee, S. Y., Kang, N. S., Yoo, Y. D., Lim, A. S., Lee, M. J., Kim, H. S., Yih, W., Yamashita, H. & LaJeunesse, T. C. 2014b. Genetics and morphology characterize the dinoflagellate Symbiodinium voratum, n. sp., (Dinophyceae) as the sole representative of Symbiodinium clade E. J. Eukaryot. Microbiol. 61:75-94. https://doi.org/10.1111/jeu.12088
  26. Jeong, H. J., Park, J. Y., Nho, J. H., Park, M. O., Ha, J. H., Seong, K. A., Jeng, C., Seong, C. N., Lee, K. Y. & Yih, W. H. 2005b. Feeding by the red-tide dinoflagellates on the cyanobacterium Synechococcus. Aquat. Microb. Ecol. 41:131-143. https://doi.org/10.3354/ame041131
  27. Jeong, H. J., Shim, J. H., Kim, J. S., Park, J. Y., Lee, C. W. & Lee, Y. 1999. Feeding by the mixotrophic thecate dinoflagellate Fragilidium cf. mexicanum on red-tide and toxic dinoflagellates. Mar. Ecol. Prog. Ser. 176:263-277. https://doi.org/10.3354/meps176263
  28. Jeong, H. J., Yoo, Y. D., Kang, N. S., Lim, A. S., Seong, K. A., Lee, S. Y., Lee, M. J., Lee, K. H., Kim, H. S., Shin, W., Nam, S. W., Yih, W. & Lee, K. 2012. Heterotrophic feeding as a newly identified survival strategy of the dinoflagellate Symbiodinium. Proc. Natl. Acad. Sci. U. S. A. 109:12604-12609. https://doi.org/10.1073/pnas.1204302109
  29. Jeong, H. J., Yoo, Y. D., Kang, N. S., Rho, J. R., Seong, K. A., Park, J. W., Nam, G. S. & Yih, W. 2010a. Ecology of Gymnodinium aureolum. I. Feeding in western Korean waters. Aquat. Microb. Ecol. 59:239-255. https://doi.org/10.3354/ame01394
  30. Jeong, H. J., Yoo, Y. D., Kim, J. S., Kim, T. H., Kim, J. H., Kang, N. S. & Yih, W. 2004. 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. https://doi.org/10.1111/j.1550-7408.2004.tb00292.x
  31. Jeong, H. J., Yoo, Y. D., Kim, J. S., Seong, K. A., Kang, N. S. & Kim, T. H. 2010b. 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
  32. Jeong, H. J., Yoo, Y. D., Lee, K. H., Kim, T. H., Seong, K. A., Kang, N. S., Lee, S. Y., Kim, J. S., Kim, S. & Yih, W. H. 2013a. Red tides in Masan Bay, Korea in 2004-2005: I. Daily variations in the abundance of red-tide organisms and environmental factors. Harmful Algae 30(Suppl. 1):S75-S88. https://doi.org/10.1016/j.hal.2013.10.008
  33. Jeong, H. J., Yoo, Y. D., Lim, A. S., Kim, T. -W., Lee, K. & Kang, C. K. 2013b. Raphidophyte red tides in Korean waters. Harmful Algae 30(Suppl. 1):S41-S52. https://doi.org/10.1016/j.hal.2013.10.005
  34. Jeong, H. J., Yoo, Y. D., Park, J. Y., Song, J. Y., Kim, S. T., Lee, S. H., Kim, K. Y. & Yih, W. H. 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. https://doi.org/10.3354/ame040133
  35. Jeong, H. J., Yoo, Y. D., Seong, K. A., Kim, J. H., Park, J. Y., Kim, S., Lee, S. H., Ha, J. H. & Yih, W. H. 2005d. Feeding by the mixotrophic red-tide dinoflagellate Gonyaulax polygramma: mechanisms, prey species, effects of prey concentration, and grazing impact. Aquat. Microb. Ecol. 38:249-257. https://doi.org/10.3354/ame038249
  36. Kang, N. S., Jeong, H. J., Moestrup, O., Shin, W., Nam, S. W., Park, J. Y., de Salas, M. F., Kim, K. W. & Noh, J. H. 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. https://doi.org/10.1111/j.1550-7408.2009.00462.x
  37. 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
  38. 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
  39. Kim, S., Kang, Y. G., Kim, H. S., Yih, W., Coats, D. W. & Park, M. G. 2008. Growth and grazing responses of the mixotrophic dinoflagellate Dinophysis acuminata as functions of light intensity and prey concentration. Aquat. Microb. Ecol. 51:301-310. https://doi.org/10.3354/ame01203
  40. Kremp, A., Elbrachter, M., Schweikert, M., Wolny, J. L. & Gottschling, M. 2005. Woloszynskia halophila (Biecheler) comb. nov.: a bloom-forming cold-water dinoflagellate co-occurring with Scrippsiella hangoei (Dinophyceae) in the Baltic Sea. J. Phycol. 41:629-642. https://doi.org/10.1111/j.1529-8817.2005.00070.x
  41. Lee, K. H., Jeong, H. J., Jang, T. Y., Lim, A. S., Kang, N. S., Kim, J. H., Kim, K. Y., Park, K. & Lee, K. 2014. Feeding by the newly described mixotrophic dinoflagellate Gymnodinium smaydae: feeding mechanism, prey species, and effect of prey concentration. J. Exp. Mar. Biol. Ecol. 459:114-125. https://doi.org/10.1016/j.jembe.2014.05.011
  42. Li, A., Stoecker, D. K. & Adolf, J. E. 1999. Feeding, pigmentation, photosynthesis and growth of the mixotrophic dinoflagellate Gyrodinium galatheanum. Aquat. Microb. Ecol. 19:163-176. https://doi.org/10.3354/ame019163
  43. Lim, A. S., Jeong, H. J., Jang, T. Y., Yoo, Y. D., Kang, N. S., Yoon, E. Y. & Kim, G. H. 2014. Feeding by the newly described heterotrophic dinoflagellate Stoeckeria changwonensis: a comparison with other species in the family Pfiesteriaceae. Harmful Algae 36:11-21. https://doi.org/10.1016/j.hal.2014.04.001
  44. Luo, Z., Yang, W., Xu, B. & Gu, H. 2013. First record of Biecheleria cincta (Dinophyceae) from Chinese coasts, with morphological and molecular characterization of the strains. Chin. J. Oceanol. Limnol. 31:835-845. https://doi.org/10.1007/s00343-013-2315-8
  45. Moestrup, O., Hansen, G. & Daugbjerg, N. 2008. Studies on woloszynskioid dinoflagellates III: on the ultrastructure and phylogeny of Borghiella dodgei gen. et sp. nov., a cold-water species from Lake Tovel, N. Italy, and on B. tenuissima comb. nov. (syn. Woloszynskia tenuissima). Phycologia 47:54-78. https://doi.org/10.2216/07-32.1
  46. Moestrup, O., Lindberg, K. & Daugbjerg, N. 2009a. Studies on woloszynskioid dinoflagellates IV: The genus Biecheleria gen. nov. Phycol. Res. 57:203-220. https://doi.org/10.1111/j.1440-1835.2009.00540.x
  47. Moestrup, O., Lindberg, K. & Daugbjerg, N. 2009b. 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
  48. Montresor, M., Procaccini, G. & Stoecker, D. K. 1999. Polarella glacialis, gen. nov., sp. nov. (Dinophyceae): Suessiaceae are still alive!. J. Phycol. 35:186-197. https://doi.org/10.1046/j.1529-8817.1999.3510186.x
  49. Nakamura, Y., Suzuki, S. & Hiromi, J. 1995. Growth and grazing of a naked heterotrophic dinoflagellate, Gyrodinium dominans. Aquat. Microb. Ecol. 9:157-164. https://doi.org/10.3354/ame009157
  50. Park, J. G., Jeong, M. K., Lee, J. A., Cho, K. J. & Kwon, O. S. 2001. Diurnal vertical migration of a harmful dinoflagellate, Cochlodinium polykrikoides (Dinophyceae), during a red tide in coastal waters of Namhae Island, Korea. Phycologia 40:292-297. https://doi.org/10.2216/i0031-8884-40-3-292.1
  51. Park, J., Jeong, H. J., Yoo, Y. D. & Yoon, E. Y. 2013a. Mixotrophic dinoflagellate red tides in Korean waters: distribution and ecophysiology. Harmful Algae 30(Suppl. 1):S28-S40. https://doi.org/10.1016/j.hal.2013.10.004
  52. Park, M. G., Kim, M. & Kang, M. 2013b. A dinoflagellate Amylax triacantha with plastids of the cryptophyte origin: phylogeny, feeding mechanism, and growth and grazing responses. J. Eukaryot. Microbiol. 60:363-376. https://doi.org/10.1111/jeu.12041
  53. Park, M. G., Kim, S., Kim, H. S., Myung, G., Kang, Y. G. & Yih, W. 2006. First successful culture of the marine dinoflagellate Dinophysis acuminata. Aquat. Microb. Ecol. 45:101-106. https://doi.org/10.3354/ame045101
  54. Putt, M. 1991. Development and evaluation of tracer particles for use in microzooplankton herbivory studies. Mar. Ecol. Prog. Ser. 77:27-37. https://doi.org/10.3354/meps077027
  55. Rodriguez, F., Varela, M. & Zapata, M. 2002. Phytoplankton assemblages in the Gerlache and Bransfield Straits (Antarctic Peninsula) determined by light microscopy and CHEMTAX analysis of HPLC pigment data. Deep Sea Res. Part II Top. Stud. Oceanogr. 49:723-747. https://doi.org/10.1016/S0967-0645(01)00121-7
  56. Seong, K. A., Jeong, H. J., Kim, S., Kim, G. H. & Kang, J. H. 2006. Bacterivory by co-occurring red-tide algae, heterotrophic nanoflagellates, and ciliates. Mar. Ecol. Prog. Ser. 322:85-97. https://doi.org/10.3354/meps322085
  57. Sherr, B. F., Sherr, E. B. & Fallon, R. D. 1987. Use of monodispersed, fluorescently labeled bacteria to estimate in situ protozoan bacterivory. Appl. Environ. Microbiol. 53:958-965.
  58. Siano, R., Kooistra, W. H. C. F., Montresor, M. & Zingone, A. 2009. Unarmoured and thin-walled dinoflagellates from the Gulf of Naples, with the description of Woloszynskia cincta sp. nov. (Dinophyceae, Suessiales). Phycologia 48:44-65. https://doi.org/10.2216/08-61.1
  59. Siano, R., Montresor, M., Probert, I., Not, F. & de Vargas, C. 2010. Pelagodinium gen. nov. and P. beii comb. nov., a dinoflagellate symbiont of planktonic foraminifera. Protist 161:385-399. https://doi.org/10.1016/j.protis.2010.01.002
  60. Smayda, T. J. 1997. Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol. Oceanogr. 42:1137-1153. https://doi.org/10.4319/lo.1997.42.5_part_2.1137
  61. Spurr, A. R. 1969. A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26:31-43. https://doi.org/10.1016/S0022-5320(69)90033-1
  62. Stoecker, D. K. 1999. Mixotrophy among dinoflagellates. J. Eukaryot. Microbiol. 46:397-401. https://doi.org/10.1111/j.1550-7408.1999.tb04619.x
  63. Stoecker, D. K., Li, A., Coats, D. W., Gustafson, D. E. & Nannen, M. K. 1997. Mixotrophy in the dinoflagellate Prorocentrum minimum. Mar. Ecol. Prog. Ser. 152:1-12. https://doi.org/10.3354/meps152001
  64. Stoecker, D. K., Silver, M. W., Michaels, A. E. & Davis, L. H. 1988. Obligate mixotrophy in Laboea strobila, a ciliate which retains chloroplasts. Mar. Biol. 99:415-423. https://doi.org/10.1007/BF02112135
  65. Takahashi, K., Sarai, C. & Iwataki, M. 2014. Morphology of two marine woloszynskioid dinoflagellates, Biecheleria brevisulcata sp. nov. and Biecheleriopsis adriatica (Suessiaceae, Dinophyceae), from Japanese coasts. Phycologia 53:52-65. https://doi.org/10.2216/13-192.1
  66. Turner, J. T. 2006. Harmful algae interactions with marine planktonic grazers. In Graneli, E. & Turner, J. T. (Eds.) Ecology of Harmful Algae. Springer-Verlag, Berlin, pp. 259-270.
  67. Yoo, Y. D., Jeong, H. J., Kang, N. S., Song, J. Y., Kim, K. Y., Lee, G. & Kim, J. 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. https://doi.org/10.1111/j.1550-7408.2009.00448.x
  68. Yoo, Y. D., Jeong, H. J., Kim, M. S., Kang, N. S., Song, J. Y., Shin, W., Kim, K. Y. & Lee, K. 2009. Feeding by phototrophic red-tide dinoflagellates on the ubiquitous marine diatom Skeletonema costatum. J. Eukaryot. Microbiol. 56:413-420. https://doi.org/10.1111/j.1550-7408.2009.00421.x

Cited by

  1. A hierarchy of conceptual models of red-tide generation: Nutrition, behavior, and biological interactions vol.47, 2015, https://doi.org/10.1016/j.hal.2015.06.004
  2. Heterokont Predator Develorapax marinus gen. et sp. nov. – A Model of the Ochrophyte Ancestor vol.7, 2016, https://doi.org/10.3389/fmicb.2016.01194
  3. Reduction in CO2 uptake rates of red tide dinoflagellates due to mixotrophy vol.31, pp.4, 2016, https://doi.org/10.4490/algae.2016.31.11.17
  4. Easy and rapid quantification of lipid contents of marine dinoflagellates using the sulpho-phospho-vanillin method vol.31, pp.4, 2016, https://doi.org/10.4490/algae.2016.31.12.7
  5. Differential interactions between the nematocyst-bearing mixotrophic dinoflagellate Paragymnodinium shiwhaense and common heterotrophic protists and copepods: Killer or prey vol.62, 2017, https://doi.org/10.1016/j.hal.2016.12.005
  6. Mixotrophy in the nematocyst–taeniocyst complex-bearing phototrophic dinoflagellate Polykrikos hartmannii vol.49, 2015, https://doi.org/10.1016/j.hal.2015.08.006
  7. Mixotrophy in the newly described dinoflagellate Yihiella yeosuensis: A small, fast dinoflagellate predator that grows mixotrophically, but not autotrophically vol.62, 2017, https://doi.org/10.1016/j.hal.2016.12.007
  8. Mixotrophy in the phototrophic dinoflagellate Takayama helix (family Kareniaceae): Predator of diverse toxic and harmful dinoflagellates vol.60, 2016, https://doi.org/10.1016/j.hal.2016.10.008
  9. Mixotrophy in Heterocapsa rotundata : A mechanism for dominating the winter phytoplankton vol.62, pp.2, 2017, https://doi.org/10.1002/lno.10470
  10. De novo assembly and characterization of the transcriptome of the newly described dinoflagellate Ansanella granifera : Spotlight on flagellum-associated genes vol.33, 2017, https://doi.org/10.1016/j.margen.2017.01.003
  11. Morphology, molecular phylogeny, and pigment characterization of an isolate of the dinoflagellate Pelagodinium bei from Korean waters vol.30, pp.3, 2015, https://doi.org/10.4490/algae.2015.30.3.183
  12. Mixotrophic ability of the phototrophic dinoflagellates Alexandrium andersonii, A. affine, and A. fraterculus vol.59, 2016, https://doi.org/10.1016/j.hal.2016.09.008
  13. Mixotrophy in the newly described dinoflagellate Alexandrium pohangense: A specialist for feeding on the fast-swimming ichthyotoxic dinoflagellate Cochlodinium polykrikoides vol.49, 2015, https://doi.org/10.1016/j.hal.2015.07.010
  14. Interactions between the mixotrophic dinoflagellate Takayama helix and common heterotrophic protists vol.68, 2017, https://doi.org/10.1016/j.hal.2017.08.006
  15. Interactions between the voracious heterotrophic nanoflagellate Katablepharis japonica and common heterotrophic protists vol.32, pp.4, 2017, https://doi.org/10.4490/algae.2017.32.11.27
  16. vol.14, pp.2, 2018, https://doi.org/10.1080/17451000.2017.1379604
  17. Amino acids profiles of six dinoflagellate species belonging to diverse families: possible use as animal feeds in aquaculture vol.33, pp.3, 2018, https://doi.org/10.4490/algae.2018.33.9.10
  18. and Common Heterotrophic Protists vol.65, pp.5, 2018, https://doi.org/10.1111/jeu.12506
  19. Feeding and grazing impact by the bloom-forming euglenophyte Eutreptiella eupharyngea on marine eubacteria and cyanobacteria vol.73, pp.None, 2014, https://doi.org/10.1016/j.hal.2018.02.003
  20. De novo transcriptome of the newly described phototrophic dinoflagellate Yihiella yeosuensis: comparison between vegetative cells and cysts vol.166, pp.8, 2019, https://doi.org/10.1007/s00227-019-3554-9
  21. Dactylodinium arachnoides sp. nov. (Borghiellaceae, Dinophyceae): a new marine dinoflagellate with a loop-shaped apical structure complex and tubular membranous extrusomes vol.58, pp.6, 2014, https://doi.org/10.1080/00318884.2019.1658399
  22. 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, 2014, https://doi.org/10.4490/algae.2020.35.2.24
  23. 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, 2014, https://doi.org/10.4490/algae.2020.35.8.20
  24. 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
  25. Feeding by the newly described heterotrophic dinoflagellate Gyrodinium jinhaense: comparison with G. dominans and G. moestrupii vol.167, pp.10, 2014, https://doi.org/10.1007/s00227-020-03769-9