ALGAE

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

DOI QR Code

Spatial-temporal distributions of the newly described mixotrophic dinoflagellate Gymnodinium smaydae in Korean coastal waters

  • Lee, Sung Yeon (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) ;
  • Ok, Jin Hee (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Kang, Hee Chang (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • You, Ji Hyun (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University)
  • Received : 2020.07.10
  • Accepted : 2020.08.25
  • Published : 2020.09.21
Download PDF
⟨ Previous Next ⟩

Abstract

Gymnodinium smaydae is a newly described mixotrophic dinoflagellate that feeds on only Heterocapsa spp. and Scrippsiella acuminata among 19 tested algal prey. It is one of the fastest growing dinoflagellates when feeding, but does not grow well without prey. To investigate its spatial-temporal distributions in Korean waters, we quantified its abundance in water samples that were seasonally collected from 28 stations along the Korean Peninsula from April 2015 to October 2018, using quantitative real-time polymerase chain reactions. This dinoflagellate had a wide distribution, as reflected by the detection of G. smaydae cells at 23 of the sampling stations. However, this distribution had a strong seasonality; it was detected at 21 stations in the summer and only one station in winter. The abundance of G. smaydae was significantly and positively correlated with chlorophyll a concentration as well as with water temperature. However, there were no significant correlations between the abundance of G. smaydae and salinity, concentrations of nutrients, or dissolved oxygen concentration. During the study period, G. smaydae was present when water temperatures were 7.6-28.0℃, salinities were 9.6-34.1, concentrations of NO3 were not detectable-106.0 μM, and concentrations of PO4 were not detectable-3.4 μM. The highest abundance of G. smaydae was 18.5 cells mL-1 in the coastal waters of Jinhae in July 2017 when the chlorophyll a concentration was 127 mg m-3 and water temperature was 23.8℃. Therefore, the spatial-temporal distribution of G. smaydae in Korean coastal waters may be affected by chlorophyll a concentration and water temperature.

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. Berge, T., Hansen, P. J. & Moestrup, O. 2008. Prey size spectrum and bioenergetics of the mixotrophic dinoflagellate Karlodinium armiger. Aquat. Microb. Ecol. 50:289-299. https://doi.org/10.3354/ame01166
  3. Bockstahler, K. R. & Coats, D. W. 1993. Grazing of the mixotrophic dinoflagellate Gymnodinium sanguineum on ciliate populations of Chesapeake Bay. Mar. Biol. 116:477-487. https://doi.org/10.1007/BF00350065
  4. Burkholder, J. M., Glasgow, H. B. Jr. & Hobbs, C. W. 1995. Fish kills linked to a toxic ambush-predator dinoflagellate: distribution and environmental conditions. Mar. Ecol. Prog. Ser. 124:43-61. https://doi.org/10.3354/meps124043
  5. Burkholder, J. M., Glibert, P. M. & Skelton, H. M. 2008. Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae 8:77-93. https://doi.org/10.1016/j.hal.2008.08.010
  6. Caron, D. A. 2016. Mixotrophy stirs up our understanding of marine food webs. Proc. Natl. Acad. Sci. U. S. A. 113:2806-2808. https://doi.org/10.1073/pnas.1600718113
  7. 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
  8. Flynn, K. J., Mitra, A., Anestis, K., Anschutz, A. A., Calbet, A., Ferreira, G. D., Gypens, N., Hansen, P. J., John, U., Martin, J. L., Mansour, J. S., Maselli, M., Medic, N., Norlin, A., Not, F., Pitta, P., Romano, F., Saiz, E., Schneider, L. K., Stolte, W. & Traboni, C. 2019. Mixotrophic protists and a new paradigm for marine ecology: where does plankton research go now? J. Plankton Res. 41:375-391. https://doi.org/10.1093/plankt/fbz026
  9. Flynn, K. J., Mitra, A., Glibert, P. M. & Burkholder, J. M. 2018. Mixotrophy in harmful algal blooms: by whom, on whom, when, why, and what next. In Gilbert, P. M., Berdalet, E., Burford, M. A., Picher, G. C. & Zhou, M. (Eds.) Global Ecology and Oceanography of Harmful Algal Blooms. Springer, Cham, pp. 113-132.
  10. Glasgow, H. B. Jr., Burkholder, J. M., Schmechel, D. E., Tester, P. A. & Rublee, P. A. 1995. Insidious effects of a toxic estuarine dinoflagellate on fish survival and human health. J. Toxicol. Environ. Health 46:501-522. https://doi.org/10.1080/15287399509532051
  11. Gomez, F. & Gast, R. J. 2018. Dinoflagellates Amyloodinium and Ichthyodinium (Dinophyceae), parasites of marine fishes in the South Atlantic Ocean. Dis. Aquat. Org. 131:29-37. https://doi.org/10.3354/dao03274
  12. Ha, K., Kim, H. -W. & Joo, G. -J. 1998. The phytoplankton succession in the lower part of hypertrophic Nakdong River (Mulgum), South Korea. Hydrobiologia 369-370:217-227. https://doi.org/10.1023/A:1017067809089
  13. Hand, W. G., Collard, P. A. & Davenport, D. 1965. The effects of temperature and salinity change on swimming rate in the dinoflagellates, Gonyaulax and Gyrodinium. Biol. Bull. 128:90-101. https://doi.org/10.2307/1539392
  14. 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
  15. 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
  16. Jacobson, D. M. & Anderson, D. M. 1996. Widespread phagocytosis of ciliates and other protists by marine mixotrophic and heterotrophic thecate dinoflagellates. J. Phycol. 32:279-285. https://doi.org/10.1111/j.0022-3646.1996.00279.x
  17. Jang, S. H. & Jeong, H. J. 2020. Spatio-temporal distributions of the newly described mixotrophic dinoflagellate Yihiella yeosuensis (Suessiaceae) in Korean coastal waters and its grazing impact on prey populations. Algae 35:45-59. https://doi.org/10.4490/algae.2020.35.2.24
  18. 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
  19. Jang, S. H., Jeong, H. J. & Yoo, Y. D. 2018. Gambierdiscus jejuensis sp. nov., an epiphytic dinoflagellate from the waters of Jeju Island, Korea, effect of temperature on the growth, and its global distribution. Harmful Algae 80:149-157. https://doi.org/10.1016/j.hal.2018.11.007
  20. 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
  21. 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
  22. 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
  23. 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. H., Shin, K., Jang, P. K., Ryu, J. -H., Kim, S. Y., Park, J. Y. & Kim, K. Y. 2017. 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
  24. Jeong, H. J., Ok, J. H., Lim, A. S., Kwon, J. E., Kim, S. J. & Lee, S. Y. 2016. Mixotrophy in the phototrophic dinoflagellate Takayama helix (family Kareniaceae): predator of diverse toxic and harmful dinoflagellates. Harmful Algae 60:92-106. https://doi.org/10.1016/j.hal.2016.10.008
  25. 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. H. & 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
  26. 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
  27. Jeong, H. J., You, J. H., Lee, K. H., Kim, S. J. & Lee, S. Y. 2018. 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
  28. Johnson, M. D. 2015. Inducible mixotrophy in the dinoflagellate Prorocentrum minimum. J. Eukaryot. Microbiol. 62:431-443. https://doi.org/10.1111/jeu.12198
  29. Kamykowski, D. & McCollum, S. A. 1986. The temperature acclimatized swimming speed of selected marine dinoflagellates. J. Plankton Res. 8:275-287. https://doi.org/10.1093/plankt/8.2.275
  30. Kang, H. C., Jeong, H. J., Jang, S. H. & Lee, K. H. 2019a. Feeding by common heterotrophic protists on the phototrophic dinoflagellate Biecheleriopsis adriatica (Suessiaceae) compared to that of other suessioid dinoflagellates. Algae 34:127-140. https://doi.org/10.4490/algae.2019.34.5.29
  31. 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. 2019b. 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
  32. Kang, N. S., Jeong, H. J., Moestrup, O., Lee, S. Y., Lim, A. S., Jang, T. Y., Lee, K. H., Lee, M. J., Jang, S. H., Potvin, E., Lee, S. K. & Noh, J. H. 2014. Gymnodinium smaydae n. sp., a new planktonic phototrophic dinoflagellate from the coastal waters of western Korea: morphology and molecular characterization. J. Eukaryot. Microbiol. 61:182-203. https://doi.org/10.1111/jeu.12098
  33. 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
  34. Kibbe, W. A. 2007. OligoCalc: an online oligonucleotide properties calculator. Nucleic Acids Res. 35(Suppl. 2):W43-W46. https://doi.org/10.1093/nar/gkm234
  35. Kim, H. -Y. & Park, K. -A. 2018. Comparison of sea surface temperature from oceanic buoys and satellite microwave measurements in the western coastal region of Korean Peninsula. J. Korean Earth Sci. Soc. 39:555-567. https://doi.org/10.5467/JKESS.2018.39.6.555
  36. 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. 55:868-881. https://doi.org/10.1111/jpy.12864
  37. Kudela, R. M. & Gobler, C. J. 2012. Harmful dinoflagellate blooms caused by Cochlodinium sp.: global expansion and ecological strategies facilitating bloom formation. Harmful Algae 14:71-86. https://doi.org/10.1016/j.hal.2011.10.015
  38. LaJeunesse, T. C., Parkinson, J. E., Gabrielson, P. W., Jeong, H. J., Reimer, J. D., Voolstra, C. R. & Santos, S. R. 2018. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 28:2570-2580. https://doi.org/10.1016/j.cub.2018.07.008
  39. Lee, H. -G., Kim, H. M., Min, J., Park, C., Jeong, H. J., Lee, K. & Kim, K. Y. 2020. Quantification of the paralytic shellfish poisoning dinoflagellate Alexandrium species using a digital PCR. Harmful Algae 92:101726. https://doi.org/10.1016/j.hal.2019.101726
  40. Lee, K. H., Jeong, H. J., Jang, T. Y., Lim, A. S., Kang, N. S., Kim, J. H., Kim, K. Y., Park, K. -T. & Lee, K. 2014a. 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
  41. Lee, S. K., Jeong, H. J., Jang, S. H., Lee, K. H., Kang, N. S., Lee, M. J. & Potvin, E. 2014b. Mixotrophy in the newly described dinoflagellate Ansanella granifera: feeding mechanism, prey species, and effect of prey concentration. Algae 29:137-152. https://doi.org/10.4490/algae.2014.29.2.137
  42. Lee, S. Y., Jeong, H. J., Kwon, J. E., You, J. H., Kim, S. J., Ok, J. H., Kang, H. C. & Park, J. Y. 2019. First report of the photosynthetic dinoflagellate Heterocapsa minima in the Pacific Ocean: morphological and genetic characterizations and the nationwide distribution in Korea. Algae 34:7-21. https://doi.org/10.4490/algae.2019.34.2.28
  43. Lee, S. Y., Jeong, H. J., Seong, K. A., Lim, A. S., Kim, J. H., Lee, K. H., Lee, M. J. & Jang, S. H. 2017. Improved real-time PCR method for quantification of the abundance of all known ribotypes of the ichthyotoxic dinoflagellate Cochlodinium polykrikoides by comparing 4 different preparation methods. Harmful Algae 63:23-31. https://doi.org/10.1016/j.hal.2017.01.006
  44. Lee, S. Y., Jeong, H. J., You, J. H. & Kim, S. J. 2018. Morphological and genetic characterization and the nationwide distribution of the phototrophic dinoflagellate Scrippsiella lachrymosa in the Korean waters. Algae 33:21-35. https://doi.org/10.4490/algae.2018.33.3.4
  45. Lim, A. S., Jeong, H. J., Kim, J. H., Jang, S. H., Lee, M. J. & Lee, K. 2015. Mixotrophy in the newly described dinoflagellate Alexandrium pohangense: a specialist for feeding on the fast-swimming ichthyotoxic dinoflagellate Cochlodinium polykrikoides. Harmful Algae 49:10-18. https://doi.org/10.1016/j.hal.2015.07.010
  46. Lim, A. S., Jeong, H. J. & Ok, J. H. 2019a. Five Alexandrium species lacking mixotrophic ability. Algae 34:289-301. https://doi.org/10.4490/algae.2019.34.11.21
  47. Lim, A. S., Jeong, H. J., Ok, J. H. & Kim, S. J. 2018. Feeding by the harmful phototrophic dinoflagellate Takayama tasmanica (Family Kareniaceae). Harmful Algae 74:19-29. https://doi.org/10.1016/j.hal.2018.03.009
  48. Lim, A. S., Jeong, H. J., Ok, J. H., You, J. H., Kang, H. C. & Kim, S. J. 2019b. Effects of light intensity and temperature on growth and ingestion rates of the mixotrophic dinoflagellate Alexandrium pohangense. Mar. Biol. 166:98. https://doi.org/10.1007/s00227-019-3546-9
  49. 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. 2017. 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
  50. Littaker, R. W., Vandersa, M. W., Kibler, S. R., Reece, K. S., Stokes, N. A., Steidinger, K. A., Millie, D. F., Bendis, B. J., Pigg, R. J. & Tester, P. A. 2003. Identification of Pfiesteria piscicida (Dinophyceae) and Pfiesteria-like organisms using internal transcribed spacer-specific PCR assays. J. Phycol. 39:754-761. https://doi.org/10.1046/j.1529-8817.2003.02112.x
  51. 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
  52. Millette, N. C., Pierson, J. J., Aceves, A. & Stoecker, D. K. 2017. Mixotrophy in Heterocapsa rotundata: a mechanism for dominating the winter phytoplankton. Limnol. Oceanogr. 62:836-845. https://doi.org/10.1002/lno.10470
  53. Morton, S. L., Norris, D. R. & Bomber, J. W. 1992. Effect of temperature, salinity and light intensity on the growth and seasonality of toxic dinoflagellates associated with ciguatera. J. Exp. Mar. Biol. Ecol. 157:79-90. https://doi.org/10.1016/0022-0981(92)90076-M
  54. National Institute of Biological Resources. 2020. Heterocapsa triquetra (Ehrenberg) Stein 1883. Available from: https://species.nibr.go.kr/geo/html/index.do?ktsn=120000012982. Accessed Jul 14, 2020.
  55. National Institute of Fisheries Science. 2020. Red-tide information system. Available from: http://www.nifs.go.kr/portal/external/environment/redtide/index.jsp. Accessed Jul 14, 2020.
  56. Nitschke, M. R., Davy, S. K., Cribb, T. H. & Ward, S. 2015. The effect of elevated temperature and substrate on freeliving Symbiodinium cultures. Coral Reefs 34:161-171. https://doi.org/10.1007/s00338-014-1220-8
  57. Ok, J. H., Jeong, H. J., Lim, A. S., You, J. H., Kang, H. C., Kim, S. J. & Lee, S. Y. 2019. Effects of light and temperature on the growth of Takayama helix (Dinophyceae): mixotrophy as a survival strategy against photoinhibition. J. Phycol. 55:1181-1195. https://doi.org/10.1111/jpy.12907
  58. Seo, H. -S., Jeong, Y. -H. & Kim, D. -S. 2020. A study on the characteristics of summer water temperature fluctuations by spectral analysis in coast of Korea in 2016. J. Korean Soc. Mar. Environ. Saf. 26:186-194. https://doi.org/10.7837/kosomes.2020.26.2.186
  59. Sherr, E. B. & Sherr, B. F. 2007. Heterotrophic dinoflagellates: a significant component of microzooplankton biomass and major grazers of diatoms in the sea. Mar. Ecol. Prog. Ser. 352:187-197. https://doi.org/10.3354/meps07161
  60. Shumway, S. E., Burkholder, J. M. & Morton, S. L. 2018. Harmful algal blooms: a compendium desk reference. John Wiley & Sons, Hoboken, NJ, 667 pp.
  61. Skovgaard, A. 1996. Mixotrophy in Fragilidium subglobosum (Dinophyceae): growth and grazing responses as functions of light intensity. Mar. Ecol. Prog. Ser. 143:247-253. https://doi.org/10.3354/meps143247
  62. Skovgaard, A., Karpov, S. A. & Guillou, L. 2012. The parasitic dinoflagellates Blastodinium spp. inhabiting the gut of marine, planktonic copepods: morphology, ecology, and unrecognized species diversity. Front. Microbiol. 3:305. https://doi.org/10.3389/fmicb.2012.00305
  63. 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
  64. Smith, K. F., Rhodes, L., Harwood, D. T., Adamson, J., Moisan, C., Munday, R. & Tillmann, U. 2016. Detection of Azadinium poporum in New Zealand: the use of molecular tools to assist with species isolations. J. Appl. Phycol. 28:1125-1132. https://doi.org/10.1007/s10811-015-0667-5
  65. Stoecker, D. K. 1999. Mixotrophy among Dinoflagellates. J. Eukaryot. Microbiol. 46:397-401. https://doi.org/10.1111/j.1550-7408.1999.tb04619.x
  66. 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
  67. 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
  68. Tamura, K., Dudley, J., Nei, M. & Kumar, S. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599. https://doi.org/10.1093/molbev/msm092
  69. 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
  70. Yokouchi, K., Onuma, R. & Horiguchi, T. 2018. Ultrastructure and phylogeny of a new species of mixotrophic dinoflagellate, Paragymnodinium stigmaticum sp. nov. (Gymnodiniales, Dinophyceae). Phycologia 57:539-554. https://doi.org/10.2216/17-140.1
  71. 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
  72. 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
  73. Yoo, Y. D., Seong, K. A., Kim, J. S., Nam, S. W., Jeong, H. J., Rho, J. -R., Yih, W. H. & Kim, H. S. 2018. Mixotrophy in the sand-dwelling dinoflagellate Thecadinium kofoidii. Mar. Biol. Res. 14:165-172. https://doi.org/10.1080/17451000.2017.1379604
  74. You, J. H., Jeong, H. J., Lim, A. S., Ok, J. H. & Kang, H. C. 2020. Effects of irradiance and temperature on the growth and feeding of the obligate mixotrophic dinoflagellate Gymnodinium smaydae. Mar. Biol. 167:1-13. https://doi.org/10.1007/s00227-019-3618-x

Cited by

  1. 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, 2020, https://doi.org/10.4490/algae.2021.36.3.4