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http://dx.doi.org/10.4490/algae.2019.34.5.29

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)
Publication Information
ALGAE / v.34, no.2, 2019 , pp. 127-140 More about this Journal
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
ciliate; food web; heterotrophic dinoflagellate; predation; protist; Suessiales;
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1 Strom, S. L. & Buskey, E. J. 1993. Feeding, growth, and behavior of the thecate heterotrophic dinoflagellate Oblea rotunda. Limnol. Oceanogr. 38:965-977.   DOI
2 Strom, S. L. & Morello, T. A. 1998. Comparative growth rates and yields of ciliates and heterotrophic dinoflagellates. J. Plankton Res. 20:571-584.   DOI
3 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.   DOI
4 Taylor, F. J. R., Hoppenrath, M. & Saldarriaga, J. F. 2008. Dinoflagellate diversity and distribution. Biodivers. Conserv. 17:407-418.   DOI
5 Tillmann, U. 2004. Interactions between planktonic microalgae and protozoan grazers. J. Eukaryot. Microbiol. 51:156-168.   DOI
6 Tillmann, U. & Hoppenrath, M. 2013. Life cycle of the pseudocolonial dinoflagellate Polykrikos kofoidii (Gymnodiniales, Dinoflagellata). J. Phycol. 49:298-317.   DOI
7 Tillmann, U. & Reckermann, M. 2002. Dinoflagellate grazing on the raphidophyte Fibrocapsa japonica. Aquat. Microb. Ecol. 26:247-257.   DOI
8 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.
9 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.
10 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.   DOI
11 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.   DOI
12 Jeong, H. J. 1999. The ecological roles of heterotrophic dinoflagellates in marine planktonic community. J. Eukaryot. Microbiol. 46:390-396.   DOI
13 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.   DOI
14 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.   DOI
15 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.   DOI
16 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.
17 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.   DOI
18 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.   DOI
19 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.   DOI
20 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)   DOI
21 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.   DOI
22 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.   DOI
23 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.   DOI
24 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.   DOI
25 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.   DOI
26 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.   DOI
27 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.   DOI
28 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.   DOI
29 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.   DOI
30 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.   DOI
31 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.
32 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.   DOI
33 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.   DOI
34 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.   DOI
35 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.
36 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.   DOI
37 Calbet, A. & Landry, M. R. 2004. Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems. Limnol. Oceanogr. 49:51-57.   DOI
38 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.   DOI
39 Coats, D. W. 1999. Parasitic life styles of marine dinoflagellates. J. Eukaryot. Microbiol. 46:402-409.   DOI
40 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.   DOI
41 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.   DOI
42 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)
43 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.   DOI
44 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.   DOI
45 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.   DOI
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.   DOI
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.   DOI
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.   DOI
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.   DOI
51 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.   DOI
52 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.   DOI
53 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.   DOI
54 Menden-Deuer, S. & Lessard, E. J. 2000. Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol. Oceanogr. 45:569-579.   DOI
55 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.
56 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.   DOI
57 Hansen, P. J. 2011. The role of photosynthesis and food uptake for the growth of marine mixotrophic dinoflagellates. J. Eukaryot. Microbiol. 58:203-214.   DOI
58 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.   DOI
59 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.   DOI
60 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.   DOI
61 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.   DOI
62 Johnson, M. D. 2015. Inducible mixotrophy in the dinoflagellate Prorocentrum minimum. J. Eukaryot. Microbiol. 62:431-443.   DOI
63 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.   DOI
64 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.   DOI
65 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.   DOI
66 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.   DOI
67 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.   DOI
68 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.   DOI
69 Sherr, E. B. & Sherr, B. F. 2002. Significance of predation by protists in aquatic microbial food webs. Antonie Van Leeuwenhoek 81:293-308.   DOI
70 Stoecker, D. K. 1999. Mixotrophy among dinoflagellates. J. Eukaryot. Microbiol. 46:397-401.   DOI
71 Stoecker, D. K., Hansen, P. J., Caron, D. A. & Mitra, A. 2017. Mixotrophy in the marine plankton. Annu. Rev. Mar. Sci. 9:311-335.   DOI
72 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.   DOI
73 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.   DOI
74 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.   DOI
75 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.   DOI
76 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.   DOI
77 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)