, Volume 651, Issue 1, pp 225–238 | Cite as

Effects of nutrients on growth of the red-tide dinoflagellate Gyrodinium instriatum Freudenthal et Lee and a possible link to blooms of this species

  • Sou NagasoeEmail author
  • Tomoyuki Shikata
  • Yasuhiro Yamasaki
  • Tadashi Matsubara
  • Yohei Shimasaki
  • Yuji Oshima
  • Tsuneo Honjo
Primary research paper


We investigated the impact of different nitrogen (N) and phosphorus (P) compounds and concentrations on the growth of Gyrodinium instriatum Freudenthal et Lee in laboratory experiments, and possible links to blooms of this species at Hakozaki Fishing Port, Fukuoka, Japan. G. instriatum utilized only inorganic N compounds as N sources for growth. In contrast, G. instriatum utilized many inorganic and organic phosphorus compounds. We used the Monod equation to describe the growth rate of G. instriatum in N- or P-limited batch cultures as a function of ambient nutrient concentrations. Kinetic growth parameters for maximum specific growth rate (μmax) and half-saturation nutrient concentration (K S) were 0.57 divisions d−1 and 14.2 μmol l−1, respectively, under N-limitation and 0.65 divisions d−1 and 1.75 μmol l−1, respectively, under P-limitation. Compared with these K S values, all in situ average dissolved inorganic nitrogen (DIN) concentrations in Hakozaki Fishing Port were higher than K S for N, but all in situ average dissolved inorganic phosphorus (DIP) concentrations were lower than K S for P, whether a red tide occurred or not bloom. Moreover, average DIP concentration in April (a month critical to red-tide genesis) of 2004 (a non-red-tide year) was less than half those in 2002 and 2003 (red-tide years). Thus, differences in DIP concentrations may be an important factor controlling blooms of G. instriatum in Hakozaki Fishing Port.


Harmful algae Monod equation Nitrogen Phosphorus Dynamics 



The authors thank the staff of Fukuoka Fisheries and Marine Technology Research Center (FFMTRC), especially C. Yamamoto, for permitting us to use the autoanalyzer and other FFMTRC facilities. We also thank Dr. Y. Matsuyama for providing helpful insights on the manuscript.


  1. Bonin, D. J. & S. Y. Maestrini, 1981. Importance of organic nutrients for phytoplankton growth in natural environments: implications for algal species succession. Canadian Bulletin of Fisheries and Aquatic Sciences 210: 279–291.Google Scholar
  2. Campbell, P. H., 1973. Studies on brackish water phytoplankton. Sea Grant Publication UNC-SG-73-07, University of North Carolina. Chapel Hill, North Carolina.Google Scholar
  3. Droop, M. R., 1968. Vitamin B12 and marine ecology. IV. The kinetics of uptake growth and inhibition in Monochrysis lutheri. Journal of the Marine Biological Association of the United Kingdom 48: 689–733.CrossRefGoogle Scholar
  4. Flynn, K. J. & I. Butler, 1986. Nitrogen sources for the growth of marine microalgae: role of dissolved free amino acids. Marine Ecology Progress Series 34: 281–304.CrossRefGoogle Scholar
  5. Guillard, R. R. L., 1973. Division rate. In Stein, J. R. (ed.), Handbook of Phycological Methods: Culture Methods and Growth Measurements. Cambridge University Press, Cambridge: 289–311.Google Scholar
  6. Hulburt, E. M., 1957. The taxonomy of unarmored Dinophyceae of shallow embayments on Cape-Cod, Massachusetts. The Biological Bulletin 112: 196–219.CrossRefGoogle Scholar
  7. Imai, I. & M. Yamaguchi, 1994. A simple technique for establishing axenic cultures of phytoflagellates. Bulletin of the Japanese Society of Microbial Ecology 9: 15–17.Google Scholar
  8. Iwasaki, H., 1979. Physiological ecology of red tide flagellates. In Levandovsky, M. & S. H. Hunter (eds), Biochemistry and Physiology of Protozoa, Vol. 1, 2nd ed. Academic Press, New York: 357–393.Google Scholar
  9. Jimenéz, R., 1993. Ecological factors related to Gyrodinium instriatum bloom in the inner estuary of the Gulf of Guayaquil. In Smayda, T. J. & Y. Shimizu (Eds), Toxic Phytoplankton Blooms in the Sea. Proceedings of the 5th International Conference on Toxic Marine Phytoplankton, Newport, Rhode Island, U.S.A., 28 October–1 November 1991. Elsevier, Amsterdam: 257–262.Google Scholar
  10. Kim, D. I., 2003. Physiological and ecological studies on harmful red tide dinoflagellate Cochlodinium polykrikoides (Margalef). Ph.D. dissertation, Kyushu University, Fukuoka (in Japanese).Google Scholar
  11. Kofoid, C. A. & O. Swezy, 1921. The free-living unarmored Dinoflagellata. Memoirs University of California, Vol. 5. California Press, Berkeley.Google Scholar
  12. Lee, Y. S., 2008. Utilization of various nitrogen, phosphorus, and selenium compounds by Cochlodinium polykrikoides. Journal of Environmental Biology 29: 799–804.PubMedGoogle Scholar
  13. Mahoney, J. B. & J. J. A. McLaughlin, 1977. Association of phytoflagellate blooms in Lower New York Bay with hypertrophication. Journal of Experimental Marine Biology and Ecology 28: 53–65.CrossRefGoogle Scholar
  14. McLachlan, J., 1973. Growth media-marine. In Stein, J. R. (ed.), Handbook of Phycological Methods. Culture Methods and Growth Mesurements. Cambridge University Press, Cambridge: 25–51.Google Scholar
  15. Monod, J., 1949. The growth of bacterial cultures. Annual Review of Microbiology 3: 371–394.CrossRefGoogle Scholar
  16. Nagasoe, S., D. I. Kim, Y. Shimasaki, Y. Oshima, M. Yamaguchi & T. Honjo, 2006a. Effects of temperature, salinity and irradiance on the growth of the red tide dinoflagellate Gyrodinium instriatum Freudenthal et Lee. Harmful Algae 5: 20–25.CrossRefGoogle Scholar
  17. Nagasoe, S., S. Toda, Y. Shimasaki, Y. Oshima, T. Uchida & T. Honjo, 2006b. Growth inhibition of Gyrodinium instriatum (Dinophyceae) by Skeletonema costatum (Bacillariophyceae). African Journal of Marine Science 28: 325–329.Google Scholar
  18. Nakamura, Y. & M. M. Watanabe, 1983. Growth characteristics of Chattonella antiqua Part 2. Effects of nutrients on growth. Journal of the Oceanographical Society of Japan 39: 151–155.CrossRefGoogle Scholar
  19. Norris, L. & K. K. Chew, 1975. Effect of environmental factors on growth of Gonyaulax catenella. In LoCicero, V. R. (ed.), Proceedings of the first international conference on Toxic Dinoflagellate Blooms, November, 1974, Boston, Massachusetts. Massachusetts Science and Technology Foundation, Massachusetts: 143–152.Google Scholar
  20. Porter, K. G. & Y. S. Feig, 1980. The use of DAPI for identifying and counting aquatic microflora. Limnology and Oceanography 25: 943–948.CrossRefGoogle Scholar
  21. Sharp, J. H., 1983. The distributions of inorganic nitrogen and dissolved and particulate organic nitrogen in the sea. In Carpenter, E. J. & D. G. Capone (eds), Nitrogen in the Marine Environment. Academic Press, New York: 1–35.Google Scholar
  22. Shikata, T., S. Nagasoe, T. Matsubara, Y. Yamasaki, Y. Shimasaki, Y. Oshima, T. Uchida, I. R. Jenkinson & T. Honjo, 2008. Encystment and excystment of Gyrodinium instriatum Freudenthal et Lee. Journal of Oceanography 64: 355–365.CrossRefGoogle Scholar
  23. Strickland, J. D. H. & T. R. Parsons, 1972. A Practical Handbook of Seawater Analysis, Vol. 167, 2nd ed. Bulletin of the Fiseries Research Board of Canada, Ottawa.Google Scholar
  24. Takahashi, M. & N. Fukazawa, 1982. A mechanism of “red-tide” formation. II. Effect of selective nutrient stimulation on the growth of different phytoplankton species in natural water. Marine Biology 70: 267–273.CrossRefGoogle Scholar
  25. Tatewaki, M. & L. Provasoli, 1964. Vitamin requirements of three species of Antithamnion. Botanica Marina 6: 193–203.CrossRefGoogle Scholar
  26. Tilman, D., 1976. Ecological competition between algae—experimental confirmation of resource-based competition theory. Science 192: 463–465.CrossRefGoogle Scholar
  27. Toriumi, S., 1980. Synopsis of red tide organisms. Fish Agency, Japan Government, Tokyo (in Japanese).Google Scholar
  28. Uchida, T., Y. Matsuyama, M. Yamaguchi & T. Honjo, 1996. The life cycle of Gyrodinium instriatum (Dinophyceae) in culture. Phycological Research 44: 119–123.CrossRefGoogle Scholar
  29. van Boekel, W. H. M., 1991. Ability of Phaeocystis sp. to grow on organic phosphates: direct measurement and prediction with the use of an inhibition constant. Journal of Plankton Research 13: 959–970.CrossRefGoogle Scholar
  30. Wang, H. K., L. M. Huang, X. P. Huang, X. Y. Song, H. J. Wang, N. J. Wu & C. Li, 2003. A red tide caused by Gyrodinium instriatum and its environmental characters in Zhujiang River estuary. Redai Haiyang Xuebao 22: 55–62. (in Chinese with English abstract).Google Scholar
  31. Watanabe, M. M., Y. Nakamura, S. Mori & S. Yamochi, 1982. Effects of physico-chemical factors and nutrients on the growth of Heterosigma akashiwo Hada from Osaka Bay, Japan. Japanese Journal of Phycology 30: 279–288.Google Scholar
  32. Yamaguchi, M., 1994. Physiological ecology of the red tide flagellate Gymnodinium nagasakiense (Dinophyceae). Mechanism of the red tide occurrence and its prediction. Bulletin of Nansei National Fisheries Research Institute 27: 251–394. (in Japanese with English abstract).Google Scholar
  33. Yamaguchi, M., 1996. Keisou-rui no eiyouen-riyou-tokusei oyobi Chattonella tono eiyouen-kyougou. In Agriculture, Forestry and Fisheries Research Council, Ministry of Agriculture, Forestry and Fisheries of Japan (ed.), Yūgai-Akashio no Seitaigakuteki-Seigyo ni yoru Higai-Boujyo-Gijyutsu no Kaihatsu ni kansuru Kenkyu. Nourinkousai-kai, Tokyo: 44–59 (in Japanese).Google Scholar
  34. Yamaguchi, M., S. Itakura & T. Uchida, 2001. Nutrition and growth kinetics in nitrogen- or phosphorus-limited cultures of the ‘novel red tide’ dinoflagellate Heterocapsa circularisquama (Dinophyceae). Phycologia 40: 313–318.CrossRefGoogle Scholar
  35. Yamasaki, Y., S. Nagasoe, T. Matsubara, T. Shikata, Y. Shimasaki, Y. Oshima & T. Honjo, 2007. Allelopathic interactions between the bacillariophyte Skeletonema costatum and the raphidophyte Heterosigma akashiwo. Marine Ecology Progress Series 339: 83–92.CrossRefGoogle Scholar
  36. Yanagi, T., 1999. Seasonal variations in nutrient budgets of Hakata Bay, Japan. Journal of Oceanography 55: 439–448.CrossRefGoogle Scholar
  37. Yanagi, T. & G. Onitsuka, 2000. Seasonal Variation in lower trophic level ecosystem of Hakata Bay, Japan. Journal of Oceanography 56: 233–243.CrossRefGoogle Scholar
  38. Zhang, Y., F. Fu, E. Whereat, K. J. Coyne & D. A. Hutchins, 2006. Bottom-up controls on a mixed-species HAB assemblage: A comparison of sympatric Chattonella subsalsa and Heterosigma akashiwo (Raphidophyceae) isolates from the Delaware Inland Bays, USA. Harmful Algae 5: 310–320.CrossRefGoogle Scholar
  39. Zhu, X. S., B. Yi, Y. H. Dong & L. F. Yang, 2004. A primary study on one of the “bilateral” red tide at Chi Bay of Pearl River Estuary. Haiyang Huanjing Kexue 23: 41–44. (in Chinese with English abstract).Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Sou Nagasoe
    • 1
    Email author
  • Tomoyuki Shikata
    • 2
  • Yasuhiro Yamasaki
    • 3
  • Tadashi Matsubara
    • 4
  • Yohei Shimasaki
    • 4
  • Yuji Oshima
    • 4
  • Tsuneo Honjo
    • 5
  1. 1.Seikai National Fisheries Research InstituteFisheries Research Agency NagasakiJapan
  2. 2.The Graduate University for Advanced Studies (SOKENDAI)HayamaJapan
  3. 3.Division of Biochemistry, Faculty of FisheriesNagasaki UniversityNagasakiJapan
  4. 4.Laboratory of Marine Environmental Science, Faculty of AgricultureKyushu UniversityFukuokaJapan
  5. 5.Seto Inland Sea Regional Research CenterKagawa UniversityTakamatsuJapan

Personalised recommendations