Journal of Applied Phycology

, Volume 29, Issue 1, pp 285–296 | Cite as

Response of Chattonella marina (Raphidophyceae) and marine plankton to yellow clay and thiazolidinedione derivative TD49 in a mesocosm enclosure

  • Seung Ho Baek
  • Moonho Son
  • Young Ok Kim
  • Hoon Cho
  • Minji Lee
  • Dong Hee Na
  • Si Wouk Kim


We examined the effects of the algicide thiazolidinedione (TD49) and yellow clay on Chattonella marina and assessed their ecological risk for the entire planktonic community. Mesocosm (1000 L) exposure experiments were employed to investigate time-course responses over 9 days. The growth of C. marina was controlled at ≥0.4 μM TD49 but not inhibited in yellow clay treatments. Although the algicidal activity of the 0.4-μM TD49 + 0.4 kg t−1 yellow clay treatment for C. marina was high (72.5 % at 24 h), target alga regrowth occurred. In all treatments, inorganic nutrients such as nitrate + nitrite and phosphate decreased following commencement of the experiment but were >1 μM (limitation concentration) at days 5 and 6, even though consumption pattern of those nutrients was influenced by the TD49 concentration. Depletion of silicate in initial stages played an important role in controlling the shift from diatoms including Chaetoceros and Skeletonema spp. to cryptophytes. Zooplankton were not affected by even the highest the yellow clay treatments and TD concentration of <0.8 μM, but their abundance significantly reduced after day 1 at 0.8 μM TD49. Zooplankton nauplii gradually increased to the end of the experimental period, implying that TD49 may have a limited effect on zooplankton communities. The initial dosing concentration of each substance and the fate of nutrients following algicide application were critical in determining the timing of shifts in the phytoplankton and zooplankton species composition, as well as the algicidal effect on the target alga.


Algicidal effects Yellow clay Chemical algicide Mesocosm Chattonella marina 



This research was supported by the Pioneer Research Center Program through the National Research Program of Korea (grant no. M1071118001-08M1118-00110) and 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 and Future Planning (grant number NRF-2016M1A5A1027456), and KIOST projects (PE99432).

Supplementary material

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ESM 1 (DOC 50 kb)
10811_2016_965_MOESM2_ESM.doc (51 kb)
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  1. Anderson DM (2009) Approaches to monitoring, control and management of harmful algal blooms (HABs). Ocean Coast Manage 52:342–347CrossRefGoogle Scholar
  2. Baek SH, Shimode S, Han M-S, Kikuchi T (2008) Growth of dinoflagellates, Ceratium furca and Ceratium fusus in Sagami Bay, Japan: The role of nutrients. Harmful Algae 7:729–739CrossRefGoogle Scholar
  3. Baek SH, Hong SS, Song SY, Lee HO, Nakano SI, Han MS (2009) Grazing effects on toxic and non-toxic Microcystis aeruginosa by the mixotrophic flagellate Ochromonas sp. J Freshw Ecol 24:367–373CrossRefGoogle Scholar
  4. Baek SH, Jang MC, Son MH, Joo HM, Cho H, Kim YO (2012) Algicidal effects of a newly developed thiazolidinedione derivative TD49, on dinoflagellate Akashiwo sanguinea. Ocean Polar Res 34:1–11 (In Korean)Google Scholar
  5. Baek SH, Jang MC, Son M, Kim SW, Cho H, Kim YO (2013a) Algicidal effects on Heterosigma akashiwo and Chattonella marina (Raphidophyceae), and toxic effects on natural plankton assemblages by a thiazolidinedione derivative TD49 in a microcosm. J Appl Phycol 25:1055–1064CrossRefGoogle Scholar
  6. Baek SH, Son M, Bae SW, Shin K, Na DH, Cho H, Yamaguchi M, Kim YO, Kim SW (2013b) Algicidal activity of the thiazolidinedione derivative TD49 against the harmful dinoflagellate Heterocapsa circularisquama in a mesocosm enclosure. J Appl Phycol 25:1555–1565CrossRefGoogle Scholar
  7. Baek SH, Son M, Jung SW, Na DH, Cho H, Yamaguchi M, Kim SW, Kim YO (2014a) Enhanced species-specific chemical control of harmful and non-harmful algal bloom species by the thiazolidinedione derivative TD49. J Appl Phycol 26:311–321CrossRefGoogle Scholar
  8. Baek SH, Shin K, Son M, Bae SW, Cho H, Na DH, Kim YO, Kim SW (2014b) Algicidal effects of yellow clay and the thiazolidinedione derivative TD49 on the fish-killing dinoflagellate Cochlodinium polykrikoides in microcosm experiments. J Appl Phycol 26:2367–2378CrossRefGoogle Scholar
  9. Burson A, Matthijs HCP, Bruijne WD, Talens R, Hoogenboom R, Gerssen A, Visser PM, Stomp M, Steur K, Scheppingen YV, Huisman J (2014) Termination of a toxic Alexandrium bloom with hydrogen peroxide. Harmful Algae 31:125–135CrossRefPubMedGoogle Scholar
  10. Coats DW (1999) Parasitic life styles of marine dinoflagellates. J Eukaryot Microbiol 46:402–409CrossRefGoogle Scholar
  11. Deeds JR, Terlizzi DE, Adolf JE, Stoecker DK, Place AR (2002) Toxic activity from cultures of Karlodinium micrum (Dinophyceae)—a dinoflagellate associated with fish mortalities in an estuarine aquaculture facility. Harmful Algae 1:169–189CrossRefGoogle Scholar
  12. Dortch Q, Whitledge TE (1992) Does nitrogen or silicon limit phytoplankton production in the Mississippi River plume and nearby regions? Cont Shelf Res 12:1293–1309CrossRefGoogle Scholar
  13. Doucette GJ, McGovern ER, Babinchak JA (1999) Algicidal bacteria active against Gymnodinium breve (Dinophyceae). I. Bacteria isolation and characterization of killing activity. J Phycol 35:1447–1454CrossRefGoogle Scholar
  14. Imai I, Yamaguchi M (2012) Life cycle, physiology, ecology and red tide occurrences of the fishkilling raphidophyte Chattonella. Harmful Algae 14:46–70CrossRefGoogle Scholar
  15. Imai I, Ishida Y, Hata Y (1993) Killing of marine phytoplankton by gliding bacterium Cytophaga sp., isolated from the coastal sea of Japan. Mar Biol 116:527–532CrossRefGoogle Scholar
  16. Imai I, Hatano M, Naito K (2004) Development of a chemically defined artificial medium for marine red tide-causing raphidophycean flagellates. Plankton Biol Ecol 51:95–102Google Scholar
  17. Invidia M, Sei S, Gorbi G (2004) Survival of the copepod Acartia tonsa following egg exposure to near anoxia and to sulfide at different pH values. Mar Ecol Prog Ser 276:187–196CrossRefGoogle Scholar
  18. Jeong JH, Jin HJ, Sohn CH, Suh KH, Hong YK (2000) Algicidal activity of the seaweed Corallina pilulifera against red tide microalgae. J Appl Phycol 12:37–43CrossRefGoogle Scholar
  19. Jeong HJ, Kim JS, Yoo YD, Kim ST, Song JY, Kim TH, Seong KA, Kang NS, Kim MS, Kim JH, Kim S, Ryu J, Lee HM, Yih WH (2008) Control of the harmful alga Cochlodinium polykrikoides by the naked ciliate Strombidinopsis jeokjo in mesocosm enclosures. Harmful Algae 7:368–377CrossRefGoogle Scholar
  20. Jeong HJ, Yoo YD, Kim JS, Seong KA, Kang NS, Kim TH (2010) Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci J 45:65–91CrossRefGoogle Scholar
  21. Jeong HJ, Yoo YD, Lim AS, Kim TW, Lee K, Kang CK (2014) Raphidophyte red tides in Korean waters. Harmful Algae 30:S41–S52CrossRefGoogle Scholar
  22. Kim HG (2006) Mitigation and controls of HABs. In: Granéli E, Turner JT (eds) Ecology of harmful algae. Springer, Berlin, pp 327–338CrossRefGoogle Scholar
  23. Kim D, Nakamura A, Okamoto T, Komatsu N, Oda T, Iida T, Ishimatsu A, Muramatsu T (2000) Mechanism of superoxide anion generation in the toxic red tide phytoplankton Chattonella marina: possible involvement of NAD(P)H oxidase. Biochim Biophys Acta 1524:220–227CrossRefPubMedGoogle Scholar
  24. Kim D, Okamoto T, Oda T, Tachibana K, Lee KS, Ishimatsu A, Matsuyama Y, Honjo T, Muramatsu T (2001) Possible involvement of the glycocalyx in the ichthyotoxicity of Chattonella marina (Raphidophyceae): immunological approach using antiserum against cell surface structures of the flagellate. Mar Biol 139:625–632CrossRefGoogle Scholar
  25. Kim YM, Wu Y, Duong TU, Ghodake GS, Kim SW, Jin ES, Cho H (2010) Thiazolidinediones as a novel class of algicides against red tide harmful algal species. Appl Biochem Biotechnol 162:2273–2283CrossRefPubMedGoogle Scholar
  26. Kim YM, Wu Y, Duong TU, Jung SG, Kim SW, Cho H, Jin ES (2012) Algicidal activity of thiazolidinediones derivatives against harmful algal blooming species. Mar Biotech 14:312–322CrossRefGoogle Scholar
  27. Klaveness D (1989) Biology and ecology of the crytophyceae: status and challenges. Biol Oceanogr 6:257–270Google Scholar
  28. Lam AKY, Prepas EE, Spink D, Hrudey SE (1995) Chemical control of hepatotoxic phytoplankton: implications for human health. Water Res 29:1845–1854CrossRefGoogle Scholar
  29. Lehman JM, Moore LB, Smith-Oliver TA, Wilkinson WO, Willson TM, Kliewer SA (1995) An antidiabetic thiazolidinedione is a high affinity ligand for peroxisome proliferator-activated receptor (PPAR). J Biol Chem 270:12953–12956CrossRefGoogle Scholar
  30. Li FM, Hu HY (2005) Isolation and characterization of a novel antialgal allelochemical from Phragmites communis. Appl Environ Microb 71:6545–6553CrossRefGoogle Scholar
  31. Liu J, Zhang H, Yang W, Gao J, Ke Q (2004) Studies on biquaternary ammonium salt algaecide for removing red tide. Mar Sci Bull 6:60–65CrossRefGoogle Scholar
  32. Marcus NH, Richmond C, Sedlacek C, Miller GA, Oppert C (2004) Impact of hypoxia on the survival, egg production and population dynamics of Acartia tonsa Dana. J Exp Mar Biol Ecol 301:111–128CrossRefGoogle Scholar
  33. Marshall JA, Nichols PD, Hamilton B, Lewis RJ, Hallegraeff GM (2003) Ichthyotoxicity of Chattonella marine (Raphidophyceae) to damselfish (Acanthochromis polycanthus): the synergistic role of reactive oxygen species and free fatty acids. Harmful Algae 2:273–281CrossRefGoogle Scholar
  34. Moon SY, Soh HY, Choi SD, Jung CS, Kim SY, Lee YS (2006) Effect of a low-oxygen layer on the vertical distribution of zooplankton in Gamak Bay. Kor J Environ Biol 24:240–247Google Scholar
  35. Na GH, Choi WJ, Chun YY (1996) A study on red tide control with loess suspension. Kor J Aquacult 9:239–245Google Scholar
  36. Nagasaki K, Yamaguchi M (1998) Intra-species host specificity of HaV (Heterosigma akashiwo virus) clones. Aquat Microbiol Ecol 14:109–112CrossRefGoogle Scholar
  37. Nagasaki K, Tomaru Y, Tarutani K, Katanozaka N, Yamanaka S, Tanabe H, Yamaguchi M (2003) Growth characteristics and intraspecies host specificity of a large virus infecting the dinoflagellate Heterocapsa circularisquama. Appl Environ Microbiol 69:2580–2586CrossRefPubMedPubMedCentralGoogle Scholar
  38. Officer CB, Ryther JH (1980) The possible importance of silicon in marine eutrophication. Mar Ecol Prog Ser 3:383–391CrossRefGoogle Scholar
  39. Park JS, Kim HG, Lee SG (1989) Studies on red tide phenomena in Korea coastal water. In: Okaichi T, Anderson DM, Nemoto T (eds) Red tides: biology, environmental science and toxicology. Elsevier, New York, pp 37–40Google Scholar
  40. Park TG, Lim WA, Park YT, Lee CK, Jeong HJ (2014) Economic impact, management and mitigation of red tides in Korea. Harmful Algae 30S:S131–S143Google Scholar
  41. Porsbring T, Blanck H, Tjellstrom H, Backhaus T (2009) Toxicity of the pharmaceutical clotrimazole to marine microalgal communities. Aquat Toxicol 91:203–211CrossRefPubMedGoogle Scholar
  42. Prakash A, Rashid MA (1968) Influence of humic substances on the growth of marine phytoplankton: dinoflagellates. Limnol Oceanogr 13:598–606CrossRefGoogle Scholar
  43. Preston BL (2002) Indirect effects in aquatic exotoxicology: implications for ecological risk assessment. Environ Manag 29:311–323CrossRefGoogle Scholar
  44. Sengco MR (2004) Prevention and control of Karenia brevis blooms. Harmful Algae 8:623–628CrossRefGoogle Scholar
  45. Sengco MR, Anderson DM (2004) Controlling harmful algal blooms through clay flocculation. J Eukaryot Microbiol 51:169–172CrossRefPubMedGoogle Scholar
  46. Shimada M, Murakami TH, Imahayashi T, Ozaki HS, Toyoshima T, Okaichi T (1983) Effects of sea bloom, Chattonella antiqua, on gill primary lamellae of the young yellowtail, Seriola quinqueradiata. Acta Histochem Cytochem 16:232–244CrossRefGoogle Scholar
  47. Shirota A (1989a) Red tide problem and countermeasures. Int J Aquacult Fish Technol 1:195–293Google Scholar
  48. Shirota A (1989b) Red tide problem and countermeasures. Int J Aquat Fish Technol 1:195–293Google Scholar
  49. Shumway SE, Frank DM, Ewart LM, Ward JE (2003) Effect of yellow loess on clearance rate in seven species of benthic, filter-feeding invertebrates. Aquacult Res 34:1391–1402CrossRefGoogle Scholar
  50. Smayda TJ (1997) Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol Oceanog 42:1137–1153CrossRefGoogle Scholar
  51. Son M, Baek SH, Shin K, Bae SW, Choi KH, Cho H, Na DH, Chung IK, Kim YO, Kim SW (2015) Effects of algicide, thiazolidinedione derivative TD49, on microbial communities in a mesocosm experiment. Environ Monitor Assess 187:163–172CrossRefGoogle Scholar
  52. Subrahmanyan R (1954) On the life-history and ecology of Hornellia marina gen. et sp. nov., (Chloromonadineae), causing green discoloration of the sea and mortality among marine organisms off the Malabar Coast. Indian J Fish 1:182–203Google Scholar
  53. Tillmann U (2004) Interactions between planktonic microalgae and protozoan grazers. J Eukaryot Microbiol 51:156–168CrossRefPubMedGoogle Scholar
  54. Yu ZM, Zou JZ, Ma X (1994) Application of clays to removal of red tide organisms 1. Coagulation of red tide organisms with clays. Chinese J Oceanol Limnol 12:193–200CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Korea Institute of Ocean Science and Technology (KIOST)/South Sea Environment Research CenterGeojeSouth Korea
  2. 2.National Institute of Fisheries Science (NIFS)/South Sea Fisheries Research InstituteYeosuSouth Korea
  3. 3.Department of Polymer Science and EngineeringChosun UniversityGwangjuSouth Korea
  4. 4.College of PharmacyKyungpook National UniversityDaeguSouth Korea
  5. 5.Department of Environmental EngineeringPioneer Research Center for Controlling of Harmful Algal Bloom, Chosun UniversityGwangjuSouth Korea

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