Microalgae fuel food webs and biogeochemical cycles of key elements in the ocean. What determines microalgal dominance in the ocean is a long-standing question. Red tide distribution data (spanning 1990 to 2019) show that mixotrophic dinoflagellates, capable of photosynthesis and predation together, were responsible for ~40% of the species forming red tides globally. Counterintuitively, the species with low or moderate growth rates but diverse prey including diatoms caused red tides globally. The ability of these dinoflagellates to trade off growth for prey diversity is another genetic factor critical to formation of red tides across diverse ocean conditions. This finding has profound implications for explaining the global dominance of particular microalgae, their key eco-evolutionary strategy, and prediction of harmful red tide outbreaks.

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The ichthyotoxic Cochlodinium polykrikoides red tides have caused great economic losses in the aquaculture industry in the waters of Korea and other countries. Predicting outbreak of C. polykrikoides red tides 1-2 weeks in advance is a critical step in minimizing losses. In the South Sea of Korea, large C. polykrikoides red tide patches have often been recorded offshore and transported to nearshore waters. To explore the processes of offshore C. polykrikoides red tides, temporal variations in 3-dimensional (3-D) distributions of red tide organisms and environmental parameters were investigated by analyzing 4,432 water samples collected from 2-5 depths of 60 stations in the South Sea, Korea 16 times from May to Nov, 2014. In the study area, the vegetative cells of C. polykrikoides were found as early as May 7, but C. polykrikoides red tide patches were observed from Aug 21 until Oct 9. Cochlodinium red tides occurred in both inner and outer stations. Prior to the occurrence of large C. polykrikoides red tides, the phototrophic dinoflagellates Prorocentrum donghaiense (Jun 12 to Jul 11), Ceratium furca (Jul 11 to Aug 21), and Alexandrium fraterculus (Aug 21) formed red tides in sequence, and diatom red tides formed 2-3 times without a certain distinct pattern. The temperature for the optimal growth of these four red tide dinoflagellates is known to be similar. Thus, the sequence of the maximum growth rates of P. donghaiense > C. furca > A. fraterculus > C. polykrikoides may be partially responsible for this sequence of red tides in the inner stations following high nutrients input in the surface waters because of heavy rains. Furthermore, Cochlodinium red tides formed and persisted at the outer stations when NO 3 concentrations of the surface waters were <2 µM and thermocline depths were >20 m with the retreat of deep cold waters, and the abundance of the competing red-tide species was relatively low. The sequence of the maximum swimming speeds and thus potential reachable depths of C. polykrikoides > A. fraterculus

The mixotroph Yihiella yeosuensis is a small-and fast-swimming dinoflagellate. To investigate its protistan predators, interactions between Y. yeosuensis and 11 heterotrophic protists were explored. No potential predators were able to feed on actively swimming Y. yeosuensis cells, which escaped via rapid jumps, whereas Aduncodinium glandula, Oxyrrhis marina, and Strombidinopsis sp. (approximately 150 lm in cell length) were able to feed on weakly swimming cells that could not jump. Furthermore, Gyrodinium dominans, Luciella masanensis, and Pfiesteria piscicida were able to feed on heat-killed Yihiella cells, whereas Gyrodinium moestrupii, Noctiluca scintillans, Oblea rotunda, Polykrikos kofoidii, and Strombidium sp. (20 lm) did not feed on them. Thus, the jumping behavior of Y. yeosuensis might be primarily responsible for the observed lack of predation. With increasing Yihiella concentration, the growth rate of O. marina decreased, whereas that of Strombidinopsis did not change. However, with increasing Yihiella concentration (up to 530 ng C/ml), the ingestion rate of Strombidinopsis on Yihiella increased linearly. The highest ingestion rate was 24.1 ng C per predator per d. The low daily carbon acquisition from Yihiella relative to the body carbon content of Strombidinopsis might be responsible for its negligible growth. Thus, Y. yeosuensis might have an advantage over its competitors due to its low mortality rate.

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