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Differential responses of the dinoflagellate Cochlodinium polykrikoides bloom to episodic typhoon events

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Abstract

To better understand the effect of typhoons on the harmful alga Cochlodinium polykrikoides, we investigated cell population dynamics in relation to hydrographic conditions in Korean coastal waters before and after the passage of typhoons. After typhoon Lingling passed through the Yellow Sea, significant accumulation of C. polykrikoides on the southern coast of Namhae Island was associated with southerly winds on September 8, 2019. Similar to field observations of red tide, a particle transport model simulation showed that the virtual particles were greatly influenced by wind-driven currents associated with typhoons, particularly when diel vertical migration was included in the model. However, a bloom of C. polykrikoides disappeared immediately after the passage of typhoon Tapah on September 23, 2019. Because of the different patterns of bloom behavior after the passage of these typhoons, characteristics of other typhoons that affected the Korean peninsula during previous C. polykrikoides blooms were investigated. Analysis of typhoon properties including wind direction, precipitation, and wave height and energy suggested that high wave energy during the passage of a typhoon plays a critical role in the termination of C. polykrikoides blooms, because of its generation of high turbulence relative to other factors. In our study, the wave energy associated with typhoon Tapah (753.6 kJ m−2 over 48 h) was much higher than that associated with typhoon Lingling (441.7 kJ m−2 over 48 h). The results indicate that typhoons have an important role in determining the accumulation and termination of C. polykrikoides blooms through the physical effects of wind direction and wave energy.

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References

  • Agrawal Y, Terray E, Donelan M, Hwang P, Williams A, Drennan WM, Kahma K, Krtaigorodskii S (1992) Enhanced dissipation of kinetic energy beneath surface waves. Nature 359:219–220

    Article  Google Scholar 

  • Aoki K, Kuroda H, Setou T, Okazaki M, Yamatogi T, Hirae S, Ishida N, Yoshida K, Mitoya Y (2019) Exceptional red-tide of fish-killing dinoflagellate Karenia mikimotoi promoted by typhoon-induced upwelling. Estuar Coast Shelf Sci 219:14–23

    Article  Google Scholar 

  • Bae S-W, Kim D-S (2012) Understanding the flow properties by a numerical modeling in the South Sea of Korea. J Korean Soc Mar Environ Saf 18:295–307

    Article  Google Scholar 

  • Baek SH, Lee M, Kim Y-B (2018) Spring phytoplankton community response to an episodic windstorm event in oligotrophic waters offshore from the Ulleungdo and Dokdo islands, Korea. J Sea Res 132:1–14

    Article  Google Scholar 

  • Bauerfeind S (1985) Degradation of phytoplankton detritus by bacteria: estimation of bacterial consumption and respiration in an oxygen chamber. Mar Ecol Prog Ser 21:27–36

    Article  CAS  Google Scholar 

  • Chen Y-lL, Chen H-Y, Jan S, S-h T (2009) Phytoplankton productivity enhancement and assemblage change in the upstream Kuroshio after typhoons. Mar Ecol Prog Ser 385:111–126

    Article  CAS  Google Scholar 

  • Cho H-Y, Park K-S, Kim S (2016) Global parameter estimation of the Cochlodinium polykrikoides model using bioassay data. Acta Oceanol Sin 35:39–45

    Article  CAS  Google Scholar 

  • Choo H-S (2019) Acoustic Doppler current profiler bottom tracking survey of flow structures around Geumo Archipelago in the southern waters of Korea. J Korean Soc Mar Environ Saf 25:589–600

    Article  Google Scholar 

  • Chung C-C, Gong G-C, Hung C-C (2012) Effect of Typhoon Morakot on microphytoplankton population dynamics in the subtropical Northwest Pacific. Mar Ecol Prog Ser 448:39–49

    Article  Google Scholar 

  • Elsner JB, Kossin JP, Jagger TH (2008) The increasing intensity of the strongest tropical cyclones. Nature 455:92–95

    Article  CAS  PubMed  Google Scholar 

  • Falnes J (2007) A review of wave-energy extraction. Mar Struct 20:185–201

    Article  Google Scholar 

  • Gargett AE (1989) Ocean turbulence. Annu Rev Fluid Mech 21:419–451

    Article  Google Scholar 

  • Gibson CH, Thomas WH (1995) Effects of turbulence intermittency on growth inhibition of a red tide dinoflagellate, Gonyaulax polyedra Stein. J Geophys Res Oceans 100:24841–24846

    Article  Google Scholar 

  • Gobler CJ, Berry DL, Anderson OR, Burson A, Koch F, Rodgers BS, Moore LK, Goleski JA, Allam B, Bowser P (2008) Characterization, dynamics, and ecological impacts of harmful Cochlodinium polykrikoides blooms on eastern Long Island, NY, USA. Harmful Algae 7:293–307

    Article  CAS  Google Scholar 

  • Green T, Houk D (1979) The mixing of rain with near-surface water. J Fluid Mech 90:569–588

    Article  Google Scholar 

  • Hall NS, Paerl HW (2011) Vertical migration patterns of phytoflagellates in relation to light and nutrient availability in a shallow microtidal estuary. Mar Ecol Prog Ser 425:1–19

    Article  CAS  Google Scholar 

  • Hallegraeff GM (1993) A review of harmful algal blooms and their apparent global increase. Phycologia 32:79–99

    Article  Google Scholar 

  • Hung C-C, Chung C-C, Gong G-C, Jan S, Tsai Y, Chen K-S, Chou WC, Lee M-A, Chang Y, Chen M-H (2013) Nutrient supply in the southern East China Sea after typhoon Morakot. J Mar Res 71:133–149

    Article  CAS  Google Scholar 

  • Jeong HJ, Shim JH, Kim JS, Park JY, Lee CW, Lee Y (1999) Feeding by the mixotrophic thecate dinoflagellate Fragilidium cf. mexicanum on red-tide and toxic dinoflagellates. Mar Ecol Prog Ser 176:263–277

    Article  Google Scholar 

  • Jeong HJ, Yoo YD, Kim JS, Kim TH, Kim JH, Kang NS, Yih W (2004) Mixotrophy in the phototrophic harmful alga Cochlodinium polykrikoides (Dinophycean): prey species, the effects of prey concentration, and grazing impact. J Eukaryot Microbiol 51:563–569

    Article  PubMed  Google Scholar 

  • Jeong HJ, Lim AS, Franks PJ, Lee KH, Kim JH, Kang NS, Lee MJ, Jang SH, Lee SY, Yoon EY (2015) A hierarchy of conceptual models of red-tide generation: nutrition, behavior, and biological interactions. Harmful Algae 47:97–115

    Article  Google Scholar 

  • Kim CS, Lee SG, Lee CK, Kim HG, Jung J (1999) Reactive oxygen species as causative agents in the ichthyotoxicity of the red tide dinoflagellate Cochlodinium polykrikoides. J Plankton Res 21:2105–2115

    Article  CAS  Google Scholar 

  • Kim CS, Lee SG, Kim HG (2000) Biochemical responses of fish exposed to a harmful dinoflagellate Cochlodinium polykrikoides. J Exp Mar Biol Ecol 254:131–141

    Article  CAS  PubMed  Google Scholar 

  • Kirkwood D (1992) Stability of solutions of nutrient salts during storage. Mar Chem 38:151–164

    Article  CAS  Google Scholar 

  • Kitaigorodskii S, Donelan M, Lumley J, Terray E (1983) Wave-turbulence interactions in the upper ocean. part ii. statistical characteristics of wave and turbulent components of the random velocity field in the marine surface layer. J Phys Oceanogr 13:1988–1999

    Article  Google Scholar 

  • Kudela RM, Gobler CJ (2012) Harmful dinoflagellate blooms caused by Cochlodinium sp.: global expansion and ecological strategies facilitating bloom formation. Harmful Algae 14:71–86

    Article  Google Scholar 

  • Lange PA, Graaf G, Gade M (2000) Rain-induced subsurface turbulence measured using image processing methods, Proc. IGARSS 7:3175–3177

    Google Scholar 

  • 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:S3–S14

    Article  Google Scholar 

  • Lie H-J, Cho C-H, Lee J-H, Lee S, Tang Y (2000) Seasonal variation of the Cheju warm current in the northern East China Sea. J Oceanogr 56:197–211

    Article  Google Scholar 

  • Lim AS, Jeong HJ, Jang TY, Kang NS, Jang SH, Lee MJ (2015) Differential effects of typhoons on ichthyotoxic Cochlodinium polykrikoides red tides in the South Sea of Korea during 2012–2014. Harmful Algae 45:26–32

    Article  Google Scholar 

  • Lin I, Liu WT, Wu CC, Wong GT, Hu C, Chen Z, Liang WD, Yang Y, Liu KK (2003) New evidence for enhanced ocean primary production triggered by tropical cyclone. Geophys Res Lett 30:1718

    Article  Google Scholar 

  • Losa SN, Kivman GA, Ryabchenko VA (2004) Weak constraint parameter estimation for a simple ocean ecosystem model: what can we learn about the model and data? J Mar Syst 45:1–20

    Article  Google Scholar 

  • Marcinko CL, Martin AP, Allen JT (2014) Modelling dinoflagellates as an approach to the seasonal forecasting of bioluminescence in the North Atlantic. J Mar Syst 139:261–275

    Article  Google Scholar 

  • MOF, Ministry of Oceans and Fisheries, 2021, `21 National Safety Management Execution Plan in the Maritime and Fisheries Field (https://www.mof.go.kr/article/view.do?menuKey=427&boardKey=2&articleKey=38639)

  • Park TG, Lim WA, Park YT, Lee CK, Jeong HJ (2013) Economic impact, management and mitigation of red tides in Korea. Harmful Algae 30:S131–S143

    Article  Google Scholar 

  • Park K-S, Heo K-Y, Jun K, Kwon J-I, Kim J, Choi J-Y, Cho K-H, Choi B-J, Seo S-N, Kim YH (2015) Development of the operational oceanographic system of Korea. Ocean Sci J 50:353–369

    Article  CAS  Google Scholar 

  • Parsons TR, Maita Y, Lalli CM (1984) A manual of biological and chemical methods for seawater analysis. Oxford 15:475–490

    Google Scholar 

  • Smayda TJ (1997) Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol Oceanogr 42:1137–1153

    Article  Google Scholar 

  • Smayda TJ (2010) Adaptations and selection of harmful and other dinoflagellate species in upwelling systems. 2. Motility and migratory behaviour. Prog Oceanogr 85:71–91

    Article  Google Scholar 

  • Sournia A (1978) Phytoplankton: manual. Unesco, United Nations Educational, Scientific and Cultural Organization, Paris

    Google Scholar 

  • Stumpf RP, Litaker RW, Lanerolle L, Tester PA (2008) Hydrodynamic accumulation of Karenia off the west coast of Florida. Cont Shelf Res 28:189–213

    Article  Google Scholar 

  • Tang YZ, Gobler CJ (2009) Cochlodinium polykrikoides blooms and clonal isolates from the northwest Atlantic coast cause rapid mortality in larvae of multiple bivalve species. Mar Biol 156:2601–2611

    Article  CAS  Google Scholar 

  • Teague W, Jacobs G, Ko D, Tang T, Chang K-I, Suk M-S (2003) Connectivity of the Taiwan, Cheju, and Korea straits. Cont Shelf Res 23:63–77

    Article  Google Scholar 

  • Thimijan RW, Heins RD (1983) Photometric, radiometric, and quantum light units of measure: a review of procedures for interconversion. HortScience 18:818–822

    Article  Google Scholar 

  • Thomas WH, Gibson CH (1990a) Effects of small-scale turbulence on microalgae. J Appl Phycol 2:71–77

    Article  Google Scholar 

  • Thomas WH, Gibson CH (1990b) Quantified small-scale turbulence inhibits a red tide dinoflagellate, Gonyaulax polyedra Stein. Deep Sea Res Part I Oceanogr Res Pap 37:1583–1593

    Article  Google Scholar 

  • Thomas WH, Vernet M, Gibson CH (1995) Effects of small-scale turbulence on photosynthesis, pigmentation, cell division, and cell size in the marine dinoflagellate Gonyaulax polyedra (Dinophyceae). J Phycol 3:50–59

    Article  Google Scholar 

  • Tsuchiya K, Kuwahara VS, Yoshiki T, Nakajima R, Miyaguchi H, Kumekawa N, Kikuchi T, Toda T (2014) Phytoplankton community response and succession in relation to typhoon passages in the coastal waters of Japan. J Plankton Res 36:424–438

    Article  CAS  Google Scholar 

  • Tynan CT (1994) The effects of small-scale turbulence on dinoflagellates. Ph.D. Thesis, University of California

  • White A (1976) Growth inhibition caused by turbulence in the toxic marine dinoflagellate Gonyaulax excavata. J Fish Board Canada 33:2598–2602

  • Zappa CJ, Ho DT, McGillis WR, Banner ML, Dacey JW, Bliven LF, Ma B, Nystuen J (2009) Rain-induced turbulence and air-sea gas transfer. J Geophys Res Oceans 114

  • Zheng GM, Tang D (2007) Offshore and nearshore chlorophyll increases induced by typhoon winds and subsequent terrestrial rainwater runoff. Mar Ecol Prog Ser 333:61–74

    Article  CAS  Google Scholar 

Download references

Funding

This research was supported by the Basic Core Technology Development Program for the Oceans and the Polar Regions of the National Research Foundation (NRF) funded by the Ministry of Science, ICT & Future Planning [grant number NRF-2016M1A5A1027456] and was also supported by the KIOST (Korea Institute of Ocean Science and Technology) project (PE99912).

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Authors and Affiliations

  1. Risk Assessment Research Center, KIOST (Korea Institute of Ocean Science and Technology), Geoje, 53201, Republic of Korea

    Young Kyun Lim & Seung Ho Baek

  2. Department of Ocean Science, University of Science and Technology, Daejeon, 34113, Republic of Korea

    Young Kyun Lim, Giseop Lee, Hong-Yeon Cho & Seung Ho Baek

  3. Marine Bigdata Center, KIOST (Korea Institute of Ocean Science and Technology), Busan, 49111, Republic of Korea

    Giseop Lee & Hong-Yeon Cho

  4. Marine Ecosystem Research Center, KIOST (Korea Institute of Ocean Science and Technology), Busan, 49111, Republic of Korea

    Bum Soo Park

  5. Marine Disaster Research Center, KIOST (Korea Institute of Ocean Science and Technology), Busan, 49111, Republic of Korea

    Jin-Yong Choi

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  1. Young Kyun Lim
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Correspondence to Seung Ho Baek.

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Lim, Y.K., Lee, G., Park, B.S. et al. Differential responses of the dinoflagellate Cochlodinium polykrikoides bloom to episodic typhoon events. J Appl Phycol 33, 2299–2311 (2021). https://doi.org/10.1007/s10811-021-02392-5

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