Effects of tropical cyclones and biological interactions on red tide dynamics by the ichthyotoxic dinoflagellate Cochlodinium polykrikoides in the Korean coastal waters

Abstract

Red tides are discoloration of the sea surface due to microalgal blooms. The mixotrophic dinoflagellate <i>Cochlodinium polykrikoides</i> often forms red tide patches in the coastal waters of many countries and has sometimes caused large-scaled mortality of fish in both cages and natural environments. This dinoflagellate has caused losses of USD $1-60 million to Korean aquaculture industry every year. The mechanism of the outbreak, persistence, and decline of <i><i>Cochlodinium</i></i> red tides have not been fully understood yet, although, ecophysiological characteristics of <i>C. polykrikoides</i> have been well documented.

Here, I explored effects of some critical physical and biological factors such as tropical cyclones, competing diatoms, and novel mixotrophic dinoflagellate grazers on the red tide dynamics of <i>C. polykrikoides</i>.

Korea usually experiences several tropical cyclones (typhoons) in <i>C. polykrikoides</i> red tide period every year. Tropical cyclones are generally accompanied by strong winds and heavy rains and thus can change some critical factors affecting red tide dynamics. Strong winds often generate intensive turbulence which can inhibit growth of red tide organisms. Several studies reported that after the passage of tropical cyclones, the dominant red tide species in the water column were switched from flagellates to diatoms. Thus, tropical cyclones are likely to physically and biologically affect on the red tide dynamics of <i>C. polykrikoides</i>. However, effects of tropical cyclones on <i>Cochlodinium</i> red tides have not been well documented yet. Therefore, I explored the effects of tropical cyclones on the outbreak, persistence, and decline of <i>Cochlodinium</i> red tides by analyzing the daily maximum wind speed and daily maximum <i>Cochlodinium</i> cell abundance during the 14 tropical cyclone cases in South Sea of Korea in 2012-2014. I found that <i>Cochlodinium</i> red tides disappeared when daily maximum wind speeds exceeded 14 m s-1, but were not markedly affected when daily maximum wind speeds were less than 5 m s-1. Thus, this study suggests that daily maximum wind speeds of tropical cyclones may differentially affect the outbreak and persistence of <i>Cochlodinium</i> red tides.

I explored the effects of competing diatoms on dynamics of <i>Cochlodinium</i> and found that some competing diatoms reduced the growth and swimming speed of <i>Cochlodinium</i> through both physical contact and chemical stress when the concentration of the diatoms exceeds certain levels. This evidence suggests that the outbreak of <i>Cochlodinium</i> red tides can be prevented or delayed when the concentration of diatoms is high.

No effective mixotrophic dinoflagellate grazer on <i>C. polykrikoides</i> has been found yet, whereas several ciliates and heterotrophic protistan grazers have been reported. During <i>Cochlodinium</i> red tides in the coastal waters of eastern Korea, in 2014, I isolated a <i>Alexandrium </i>cell and established a clonal culture. This <i>Alexandrium </i>was revealed to be a mixotrophic dinoflagellate that exclusively feeds on <i>C. polykrikoides</i>. Based on the results from morphological and genetic analyses, the <i>Alexandrium </i>strain was revealed to be a new species, to be named as <i>Alexandrium pohangense</i> n. sp.

To explore the roles of <i>Alexandrium pohangense</i> in marine ecosystems, I measured the growth and ingestion rates of <i>A. pohangense</i> as a function of the concentration of only prey <i>C. polykrikoides</i> in the laboratory. The maximum ingestion rate of <i>A. pohangense</i> on <i>C. polykrikoides</i> was 7 cells predator-1 d-1, and the maximum mixotrophic growth rate reached 0.5 d-1, while the autotrophic growth rate was 0.1-1. Furthermore, by combining the results from the feeding experiments and abundance data obtained in field, I estimated grazing impact of <i>A. pohangense</i> on populations of <i>C. polykrikoides</i> in the natural environments. The grazing coefficients attributable to <i>A. pohangense</i> on co-occurring <i>C. polykrikoides</i> were up to 1.57 d-1. Thus, up to 79 % of the <i>C. polykrikoides</i> populations could be removed by <i>A. pohangense</i> population in a day.

Conclusively, through field observation, diverse feeding experiments in the laboratory, and morphological and molecular analyses, I found that tropical cyclones, competing diatoms, and a new mixotrophic dinoflagellate <i>A. pohangense</i> can significantly affect the red tide dynamics by <i>C. polykrikoides</i>.