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The Korean Society of Phycology (한국조류학회(藻類))
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Effects of temperature on the growth and ingestion rates of the newly described mixotrophic dinoflagellate Yihiella yeosuensis and its two optimal prey species

  • 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) ;
  • Lim, An Suk (Division of Life Science, Gyeongsang National University) ;
  • Ok, Jin Hee (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) ;
  • Park, Sang Ah (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Lee, Sung Yeon (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Eom, Se Hee (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University)
  • Received : 2020.07.07
  • Accepted : 2020.08.20
  • Published : 2020.09.21
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Abstract

Water temperature is known to affect the growth and feeding of marine dinoflagellates. Each dinoflagellate species grows well at a certain optimal temperature but dies at very cold and hot temperatures. Thus, changes in water temperatures driven by global warming and extremely high or low temperatures can affect the distribution of dinoflagellates. Yihiella yeosuensis is a mixotrophic dinoflagellate that can feed on only the cryptophyte Teleaulax amphioxeia and the chlorophyte Pyramimonas sp. Furthermore, it grows fast mixotrophically but rarely grows photosynthetically. We explored the direct and indirect effects of water temperature on the growth and ingestion rates of Y. yeosuensis feeding on T. amphioxeia and the growth rates of T. amphioxeia and Pyramimonas sp. under 7 different water temperatures (5-35℃). Both the autotrophic and mixotrophic growth rates of Y. yeosuensis on T. amphioxeia were significantly affected by temperature. Under the mixotrophic and autotrophic conditions, Y. yeosuensis survived at 10-25℃, but died at 5℃ and ≥30℃. The maximum mixotrophic growth rate of Y. yeosuensis on T. amphioxeia (1.16 d-1) was achieved at 25℃, whereas the maximum autotrophic growth rate (0.16 d-1) was achieved at 15℃. The maximum ingestion rate of Y. yeosuensis on T. amphioxeia (0.24 ng C predator-1 d-1) was achieved at 25℃. The cells of T. amphioxeia survived at 10-25℃, but died at 5 and ≥30℃. The cells of Pyramimonas sp. survived at 5-25℃, but died at 30℃. The maximum growth rate of T. amphioxeia (0.72 d-1) and Pyramimonas sp. (0.75 d-1) was achieved at 25℃. The abundance of Y. yeosuensis is expected to be high at 25℃, at which its two prey species have their highest growth rates, whereas Y. yeosuensis is expected to be rare or absent at 5℃ or ≥30℃ at which its two prey species do not survive or grow. Therefore, temperature can directly or indirectly affect the population dynamics and distribution of Y. yeosuensis.

Keywords

References

  1. Anderson, S. R. & Menden-Deuer, S. 2017. Growth, grazing, and starvation survival in three heterotrophic dinoflagellate species. J. Eukaryot. Microbiol. 64:213-225. https://doi.org/10.1111/jeu.12353
  2. Baek, S. H., Shimode, S. & Kikuchi, T. 2008. Growth of dinoflagellates, Ceratium furca and Ceratium fusus in Sagami Bay, Japan: the role of temperature, light intensity and photoperiod. Harmful Algae 7:163-173. https://doi.org/10.1016/j.hal.2007.06.006
  3. Belkin, I. M. 2009. Rapid warming of large marine ecosystems. Prog. Oceanogr. 81:207-213. https://doi.org/10.1016/j.pocean.2009.04.011
  4. Diaz-Almeyda, E. M., Prada, C., Ohdera, A. H., Moran, H., Civitello, D. J., Iglesias-Prieto, R., Carlo, T. A., LaJeunesse, T. C. & Medina, M. 2017. Intraspecific and interspecific variation in thermotolerance and photoacclimation in Symbiodinium dinoflagellates. Proc. R. Soc. B Biol. Sci. 284:20171767. https://doi.org/10.1098/rspb.2017.1767
  5. 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
  6. 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
  7. Gregoire, V., Schmacka, F., Coffroth, M. A. & Karsten, U. 2017. Photophysiological and thermal tolerance of various genotypes of the coral endosymbiont Symbiodinium sp. (Dinophyceae). J. Appl. Phycol. 29:1893-1905. https://doi.org/10.1007/s10811-017-1127-1
  8. Hallegraeff, G. M. 1993. A review of harmful algal blooms and their apparent global increase. Phycologia 32:79-99. https://doi.org/10.2216/i0031-8884-32-2-79.1
  9. Hansen, J., Sato, M. & Ruedy, R. 2012. Perception of climate change. Proc. Natl. Acad. Sci. U. S. A. 109:E2415-E2423. https://doi.org/10.1073/pnas.1205276109
  10. Hansen, P. J. 1991. Quantitative importance and trophic role of heterotrophic dinoflagellates in a coastal pelagial food web. Mar. Ecol. Prog. Ser. 73:253-261. https://doi.org/10.3354/meps073253
  11. 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
  12. Heil, C. A., Glibert, P. M. & Fan, C. 2005. Prorocentrum minimum (Pavillard) Schiller: a review of a harmful algal bloom species of growing worldwide importance. Harmful Algae 4:449-470. https://doi.org/10.1016/j.hal.2004.08.003
  13. 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
  14. 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
  15. Jang, S. H., Jeong, H. J. & Chon, J. K. 2019. De novo transcriptome of the newly described phototrophic dinoflagellate Yihiella yeosuensis: comparison between vegetative cells and cysts. Mar. Biol. 166:104. https://doi.org/10.1007/s00227-019-3554-9
  16. Jang, S. H., Jeong, H. J., Kwon, J. E. & Lee, K. H. 2017a. 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., Moestrup, O., Kang, N. S., Lee, S. Y., Lee, K. H. & Seong, K. A. 2017b. Yihiella yeosuensis gen. et sp. nov. (Suessiaceae, Dinophyceae), a novel dinoflagellate isolated from the coastal waters of Korea. J. Phycol. 53:131-145. https://doi.org/10.1111/jpy.12486
  18. 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
  19. Jeong, H. J., Lee, K. H., Yoo, Y. D., Kang, N. S., Song, J. Y., Kim, T. H., Seong, K. A., Kim, J. S. & Potvin, E. 2018b. Effects of light intensity, temperature, and salinity on the growth and ingestion rates of the red-tide mixotrophic dinoflagellate Paragymnodinium shiwhaense. Harmful Algae 80:46-54. https://doi.org/10.1016/j.hal.2018.09.005
  20. 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. 2014. 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
  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. https://doi.org/10.1016/j.hal.2015.06.004
  22. 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. 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
  23. 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
  24. 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. 2005. 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
  25. 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
  26. 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
  27. 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
  28. Karim, W., Nakaema, S. & Hidaka, M. 2015. Temperature effects on the growth rates and photosynthetic activities of Symbiodinium cells. J. Mar. Sci. Eng. 3:368-381. https://doi.org/10.3390/jmse3020368
  29. Kibler, S. R., Litaker, R. W., Holland, W. C., Vandersea, M. W. & Tester, P. A. 2012. Growth of eight Gambierdiscus (Dinophyceae) species: effects of temperature, salinity and irradiance. Harmful Algae 19:1-14. https://doi.org/10.1016/j.hal.2012.04.007
  30. Kim, D. -I., Matsuyama, Y., Nagasoe, S., Yamaguchi, M., Yoon, Y. -H., Oshima, Y., Imada, N. & Honjo, T. 2004. Effects of temperature, salinity and irradiance on the growth of the harmful red tide dinoflagellate Cochlodinium polykrikoides Margalef (Dinophyceae). J. Plankton Res. 26:61-66. https://doi.org/10.1093/plankt/fbh001
  31. Klueter, A., Trapani, J., Archer, F. I., McIlroy, S. E. & Coffroth, M. A. 2017. Comparative growth rates of cultured marine dinoflagellates in the genus Symbiodinium and the effects of temperature and light. PLoS ONE 12:e0187707. https://doi.org/10.1371/journal.pone.0187707
  32. Korea Hydrographic and Oceanographic Agency (KHOA). 2020. Available from: http://www.khoa.go.kr. Accessed Jul 9, 2020.
  33. Laabir, M., Jauzein, C., Genovesi, B., Masseret, E., Grzebyk, D., Cecchi, P., Vaquer, A., Perrin, Y. & Collos, Y. 2011. Influence of temperature, salinity and irradiance on the growth and cell yield of the harmful red tide dinoflagellate Alexandrium catenella colonizing Mediterranean waters. J. Plankton Res. 33:1550-1563. https://doi.org/10.1093/plankt/fbr050
  34. 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
  35. Lee, C. -K., Park, T. -G., Park, Y. -T. & Lim, W. -A. 2013. Monitoring and trends in harmful algal blooms and red tides in Korean coastal waters, with emphasis on Cochlodinium polykrikoides. Harmful Algae 30(Suppl. 1):S3-S14. https://doi.org/10.1016/j.hal.2013.10.002
  36. Lee, K. H., Jeong, H. J., Kang, H. C., Ok, J. H., You, J. H. & Park, S. A. 2019a. Growth rates and nitrate uptake of cooccurring red-tide dinoflagellates Alexandrium affine and A. fraterculus as a function of nitrate concentration under light-dark and continuous light conditions. Algae 34:237-251. https://doi.org/10.4490/algae.2019.34.8.28
  37. Lee, S. K., Jeong, H. J., Jang, S. H., Lee, K. H., Kang, N. S., Lee, M. J. & Potvin, E. 2014. 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
  38. Lee, S. Y., Jeong, H. J., Kwon, J. E., You, J. H., Kim, S. J., Ok, J. H., Kang, H. C. & Park, J. Y. 2019b. 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
  39. 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
  40. Li, A., Stoecker, D. K. & Coats, D. W. 2000. Spatial and temporal aspects of Gyrodinium galatheanum in Chesapeake Bay: distribution and mixotrophy. J. Plankton Res. 22:2105-2124. https://doi.org/10.1093/plankt/22.11.2105
  41. 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
  42. Lim, A. S., Jeong, H. J., Ok, J. H., You, J. H., Kang, H. C. & Kim, S. J. 2019. 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
  43. Lopez-Cortes, D. J., Nunez Vazquez, E. J., Dorantes-Aranda, J. J., Band-Schmidt, C. J., Hernandez-Sandoval, F. E., Bustillos-Guzman, J. J., Leyva-Valencia, I. & Fernandez-Herrera, L. J. 2019. The state of knowledge of harmful algal blooms of Margalefidinium polykrikoides (a.k.a. Cochlodinium polykrikoides) in Latin America. Front. Mar. Sci. 6:463. https://doi.org/10.3389/fmars.2019.00463
  44. Matsubara, T., Nagasoe, S., Yamasaki, Y., Shikata, T., Shimasaki, Y., Oshima, Y. & Honjo, T. 2007. Effects of temperature, salinity, and irradiance on the growth of the dinoflagellate Akashiwo sanguinea. J. Exp. Mar. Biol. Ecol. 342:226-230. https://doi.org/10.1016/j.jembe.2006.09.013
  45. McBride, B. B., Muller-Parker, G. & Jakobsen, H. H. 2009. Low thermal limit of growth rate of Symbiodinium californium (Dinophyta) in culture may restrict the symbiont to southern populations of its host anemones (Anthopleura spp.; Anthozoa, Cnidaria). J. Phycol. 45:855-863. https://doi.org/10.1111/j.1529-8817.2009.00716.x
  46. McClanahan, T. R., Ateweberhan, M., Muhando, C. A., Maina, J. & Mohammed, M. S. 2007. Effects of climate and seawater temperature variation on coral bleaching and mortality. Ecol. Monogr. 77:503-525. https://doi.org/10.1890/06-1182.1
  47. Montero, P., Perez-Santos, I., Daneri, G., Gutierrez, M. H., Igor, G., Seguel, R., Purdie, D. & Crawford, D. W. 2017. A winter dinoflagellate bloom drives high rates of primary production in a Patagonian fjord ecosystem. Estuar. Coast. Shelf Sci. 199:105-116. https://doi.org/10.1016/j.ecss.2017.09.027
  48. 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
  49. 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
  50. 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
  51. Robison, J. D. & Warner, M. E. 2006. Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrhophyta). J. Phycol. 42:568-579. https://doi.org/10.1111/j.1529-8817.2006.00232.x
  52. Rogers, J. E. & Davis, R. H. 2006. Application of a new microculturing technique to assess the effects of temperature and salinity on specific growth rates of six Symbiodinium isolates. Bull. Mar. Sci. 79:113-126.
  53. Roselli, L., Vadrucci, M. R., Belmonte, M., Ciciriello, P., Rubino, F., Ungaro, N. & Caroppo, C. 2020. Two-stages bloom of Margalefidinium cf. polykrikoides in a Mediterranean shallow bay (Ionian Sea, Italy). Mar. Pollut. Bull. 151:110825. https://doi.org/10.1016/j.marpolbul.2019.110825
  54. Ruthrof, K. X., Breshears, D. D., Fontaine, J. B., Froend, R. H., Matusick, G., Kala, J., Miller, B. P., Mitchell, P. J., Wilson, S. K., van Keulen, M., Enright, N. J., Law, D. J., Wernberg, T. & Hardy, G. E. S. J. 2018. Subcontinental heat wave triggers terrestrial and marine, multi-taxa responses. Sci. Rep. 8:13094. https://doi.org/10.1038/s41598-018-31236-5
  55. Sakamoto, S., Lim, W. A., Lu, D., Dai, X., Orlova, T. & Iwataki, M. 2020. Harmful algal blooms and associated fisheries damage in East Asia: current status and trends in China, Japan, Korea and Russia. Harmful Algae. Advanced online publication. https://doi.org/10.1016/j.hal.2020.101787.
  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. Seong, K. -T., Choi, Y. -H., Koo, J. H. & Jeon, S. -B. 2014. Fluctuations and time series forecasting of sea surface temperature at Yeosu coast in Korea. J. Korean Soc. Mar. Environ. Energy 17:122-130. https://doi.org/10.7846/JKOSMEE.2014.17.2.122
  58. Skovgaard, A., Hansen, P. J. & Stoecker, D. K. 2000. Physiology of the mixotrophic dinoflagellate Fragilidium subglobosum. I. Effects of phagotrophy and irradiance on photosynthesis and carbon content. Mar. Ecol. Prog. Ser. 201:129-136. https://doi.org/10.3354/meps201129
  59. Spilling, K., Olli, K., Lehtoranta, J., Kremp, A., Tedesco, L., Tamelander, T., Klais, R., Peltonen, H. & Tamminen, T. 2018. Shifting diatom: dinoflagellate dominance during spring bloom in the Baltic Sea and its potential effects on biogeochemical cycling. Front. Mar. Sci. 5:327. https://doi.org/10.3389/fmars.2018.00327
  60. 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
  61. 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
  62. Wernberg, T., Smale, D. A., Tuya, F., Thomsen, M. S., Langlois, T. J., De Bettignies, T., Bennett, S. & Rousseaux, C. S. 2013. An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nat. Clim. Change 3:78-82. https://doi.org/10.1038/nclimate1627
  63. Yih, W., Kim, H. S., Jeong, H. J., Myung, G. & Kim, Y. G. 2004. Ingestion of cryptophyte cells by the marine photosynthetic ciliate Mesodinium rubrum. Aquat. Microb. Ecol. 36:165-170. https://doi.org/10.3354/ame036165
  64. You, J. H., Jeong, H. J., Kang, H. C., Ok, J. H., Park, S. A. & Lim, A. S. 2020a. Feeding by common heterotrophic protist predators on seven Prorocentrum species. Algae 35:61-78. https://doi.org/10.4490/algae.2020.35.2.28
  65. You, J. H., Jeong, H. J., Lim, A. S., Ok, J. H. & Kang, H. C. 2020b. Effects of irradiance and temperature on the growth and feeding of the obligate mixotrophic dinoflagellate Gymnodinium smaydae. Mar. Biol. 167:64. https://doi.org/10.1007/s00227-020-3678-y
  66. Zheng, S., Wang, G. & Lin, S. 2012. Heat shock effects and population survival in the polar dinoflagellate Polarella glacialis. J. Exp. Mar. Biol. Ecol. 438:100-108. https://doi.org/10.1016/j.jembe.2012.09.003

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