, Volume 641, Issue 1, pp 33–44 | Cite as

The role of interactions between Prorocentrum minimum and Heterosigma akashiwo in bloom formation

  • Y. YamasakiEmail author
  • S. Nagasoe
  • M. Tameishi
  • T. Shikata
  • Y. Zou
  • Z. Jiang
  • T. Matsubara
  • Y. Shimasaki
  • K. Yamaguchi
  • Y. Oshima
  • T. Oda
  • T. Honjo
Primary research paper


We examined the growth and interactions between the bloom-forming flagellates Prorocentrum minimum and Heterosigma akashiwo using bi-algal culture experiments. When both species were inoculated at high cell densities, growth of H. akashiwo was inhibited by P. minimum. In other combinations of inoculation densities, the species first reaching the stationary phase substantially suppressed maximum cell densities of the other species, but the growth inhibition effect of P. minimum was stronger than that of H. akashiwo. We used a mathematical model to simulate growth and interactions of P. minimum and H. akashiwo in bi-algal cultures. The model indicated that P. minimum always out-competed H. akashiwo over time. Additional experiments showed that crude extracts from P. minimum and H. akashiwo cultures did not affect the growth of either species, but both strongly inhibited the growth of the bloom-forming diatom Skeletonema costatum. Further experiments showed that it was unlikely that reactive oxygen species produced by H. akashiwo were responsible for the inhibition of P. minimum growth.


Allelopathy Growth and interaction Heterosigma akashiwo Prorocentrum minimum Reactive oxygen species Skeletonema costatum 



We are grateful to anonymous reviewers and the editor for thoughtful comments. This work was supported by the Grant-in-Aid for the Japan Society for the Promotion of Science (JSPS) Fellows (20-5980).


  1. Andersen, R. J., M. J. Leblanc & F. W. Sum, 1980. 1(2,6,6-Trimethyl-4-hydroxycyclo-hexenyl)-1,3-butanedione, extracellular metabolite from the dinoflagellate Prorocentrum minimum. Journal of Organic Chemistry 45: 1169–1170.CrossRefGoogle Scholar
  2. Anderson, D. M., 1997. Turning back the harmful red tide. Nature 388: 513–514.CrossRefGoogle Scholar
  3. Bodeanu, N. & M. Usurelu, 1979. Dinoflagellate blooms in the Romanian Black Sea coastal waters. In Taylor, D. L. & H. H. Seliger (eds), Toxic Dinoflagellate Blooms. Elsevier, New York: 151–154.Google Scholar
  4. Bruggeman, J. & S. A. L. M. Kooijman, 2007. A biodiversity-inspired approach to aquatic ecosystem modeling. Limnology and Oceanography 52: 1533–1544.Google Scholar
  5. Cembella, A. D., 2003. Chemical ecology of eukaryotic microalgae in marine ecosystems. Phycologia 42: 420–447.Google Scholar
  6. Cembella, A. D., N. I. Antia & P. J. Harrison, 1982. The utilization of inorganic and organic phosphorous compounds as nutrients by eukaryotic microalgae: a multidisciplinary perspective: Part 1. Critical Reviews Microbiology 10: 317–391.CrossRefGoogle Scholar
  7. Denardou, A., Y.-F. Pouchus, J.-F. Verbist, B. Berland & D. Grzebyk, 1995. Toxicity of different strains of the dinoflagellate Prorocentrum minimum. Toxicon 33: 1121–1122.CrossRefGoogle Scholar
  8. Denardou-Queneherve, A., D. Grzebyk, Y. F. Pouchus, M. P. Sauviat, E. Alliot, J. F. Biard, B. Berland & J. F. Verbist, 1999. Toxicity of French strains of the dinoflagellate Prorocentrum minimum experimental and natural contaminations of mussels. Toxicon 37: 1711–1719.CrossRefPubMedGoogle Scholar
  9. Diehl, S., S. Berger, R. Ptacnik & A. Wild, 2002. Phytoplankton, light, and nutrients in a gradient of mixing depths: field experiments. Ecology 83: 399–411.Google Scholar
  10. Eppley, R. W., J. N. Rogers & J. J. McCarthy, 1969. Half-saturation constants for uptake of nitrate and ammonium by marine phytoplankton. Limnology and Oceanography 12: 685–695.Google Scholar
  11. Granéli, E. & P. J. Hansen, 2006. Allelopathy in harmful algae: a mechanism to compete for resources? In Granéli, E. & T. J. Turner (eds), Ecology of Harmful Algae. Springer-Verlag, Berlin: 189–201.CrossRefGoogle Scholar
  12. Grzebyk, D., A. Denardou, B. Berland & Y. F. Pouchus, 1997. Evidence of a new toxin in the red-tide dinoflagellate Prorocentrum minimum. Journal of Plankton Research 19: 1111–1124.CrossRefGoogle Scholar
  13. Haigh, R., F. J. R. Taylor & T. F. Sutherland, 1992. Phytoplankton ecology of Sechelt Inlet, a fjord system on the British Columbia coast. I. General features of the nano- and microplankton. Marine Ecology Progress Series 89: 117–134.CrossRefGoogle Scholar
  14. Haque, S. M. & Y. Onoue, 2002. Effects of salinity on growth and toxin production of a noxious phytoflagellate, Heterosigma akashiwo (Raphidophyceae). Botanica Marina 45: 356–363.CrossRefGoogle Scholar
  15. Heil, C. A., P. M. Glibert & C. Fan, 2005. Prorocentrum minimum (Pavillard) Schiller: a review of a harmful algal bloom species of growing worldwide importance. Harmful Algae 4: 449–470.CrossRefGoogle Scholar
  16. Herndon, J. & W. P. Cochlan, 2007. Nitrogen utilization by the raphidophyte Heterosigma akashiwo: growth and uptake kinetics in laboratory cultures. Harmful Algae 6: 260–270.CrossRefGoogle Scholar
  17. Honjo, T. & K. Tabata, 1985. Growth dynamics of Olisthodiscus luteus in outdoor tanks with flowing coastal water and in small vessels. Limnology and Oceanography 30: 653–664.CrossRefGoogle Scholar
  18. Honjo, T., T. Shimouse & T. Hanaoka, 1978. A red tide occurred at the Hakozaki fishing port, Hakata Bay, in 1973. The growth process and the chlorophyll content. Bulletin of the Plankton Society of Japan 25: 7–12.Google Scholar
  19. Imada, I., E. F. Sato, M. Miyamoto, Y. Ichimori, Y. Minamiyama, R. Konaka & M. Inoue, 1999. Analysis of reactive oxygen species generated by neutrophils using a chemiluminescence probe L-012. Analytical Biochemistry 271: 53–58.CrossRefPubMedGoogle Scholar
  20. Iwasa, Y. (ed.), 1998. Suri-seibutugaku nyuumon, 2nd ed. Kyoritu Syuppan, Tokyo (in Japanese).Google Scholar
  21. Kadomura, K., T. Nakashima, M. Kurachi, K. Yamaguchi & T. Oda, 2006. Production of reactive oxygen species (ROS) by devil stinger (Inimicus japonicus) during embryogenesis. Fish & Shellfish Immunology 21: 209–214.CrossRefGoogle Scholar
  22. Karentz, D. & T. J. Smayda, 1984. Temperature and seasonal occurrence pattern of 30 dominant phytoplankton species in Narragansett Bay over a 22-year period (1959–1980). Marine Ecology Progress Series 18: 277–293.CrossRefGoogle Scholar
  23. Khan, S., O. Arakawa & Y. Onoue, 1997. Neurotoxins in a toxic red tide of Heterosigma akashiwo (Raphidophyceae) in Kagoshima Bay, Japan. Aquaculture Research 28: 9–14.CrossRefGoogle Scholar
  24. Kim, D., A. Nakamura, T. Okamoto, N. Komatsu, T. Oda, A. Ishimatsu & T. Muramatsu, 1999. Toxic potential of the raphidophyte Olisthodiscus luteus: mediation by reactive oxygen species. Journal of Plankton Research 21: 1017–1027.CrossRefGoogle Scholar
  25. Kim, D., M. Watanabe, Y. Nakayasu & K. Kohata, 2004. Production of superoxide anion and hydrogen peroxide associated with cell growth of Chattonella antiqua. Aquatic Microbial Ecology 35: 57–64.CrossRefGoogle Scholar
  26. Kim, D., M. Watanabe, Y. Nakayasu & K. Kohata, 2005. Changes in O2 and H2O2 production by Chattonella antiqua during diel vertical migration under nutrient stratification. Aquatic Microbial Ecology 39: 183–191.CrossRefGoogle Scholar
  27. Kondo, K., Y. S. Seike & Y. Date, 1990. Red tides in the brackish Lake Nakanoumi. 1. The frequency and causative species of red tides. Bulletin of the Plankton Society of Japan 36: 103–110.Google Scholar
  28. Legrand, C., K. Rengefors, G. O. Fistarol & E. Granéli, 2003. Allelopathy in phytoplankton – biochemical, ecological and evolutionary aspects. Phycologia 42: 406–419.CrossRefGoogle Scholar
  29. Marquardt, D. W., 1963. An algorithm for least-squares estimation of nonlinear inequalities. SIAM Journal on Applied Mathematics 11: 431–441.CrossRefGoogle Scholar
  30. Marshall, J. A., M. de Salas, T. Oda & G. Hallegraeff, 2005. Superoxide production by marine microalgae. Marine Biology 147: 533–540.CrossRefGoogle Scholar
  31. Matsuyama, Y., U. Takuji & Y. Kotani, 2000. Effect of culture filtrate of raphidophytes Heterosigma akashiwo and Chattonella antiqua on the growth of diatom Skeletonema costatum. Bulletin of Fisheries and Environment of Inland Sea 2: 57–66.Google Scholar
  32. Nagasoe, S., S. Toda, Y. Shimasaki, Y. Oshima, T. Uchida & T. Honjo, 2006. Growth inhibition of Gyrodinium instriatum (Dinophyceae) by Skeletonema costatum (Bacillariophyceae). African Journal of Marine Science 28: 325–329.Google Scholar
  33. Oda, T., A. Nakamura, M. Shikayama, I. Kawano, A. Ishimatsu & T. Muramatsu, 1997. Generation of reactive oxygen species by Raphidophycean phytoplankton. Bioscience, Biotechnology and Biochemistry 61: 1658–1662.CrossRefGoogle Scholar
  34. 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
  35. Pratt, D. M., 1966. Competition between Skeletonema costatum and Olisthodiscus luteus in Narragansett Bay and in culture. Limnology and Oceanography 11: 447–455.CrossRefGoogle Scholar
  36. Rice, E. L., 1984. Allelopathy, 2nd ed. Academic Press, London.Google Scholar
  37. Sciandra, A., 1991. Coupling and uncoupling between nitrate uptake and growth rate in Prorocentrum minimum (Dinophyceae) under different frequencies of pulsed nitrate supply. Marine Ecology Progress Series 72: 261–269.CrossRefGoogle Scholar
  38. Shikata, T., 2009. Studies on the mechanisms of bloom development in the raphidophyte Heterosigma akashiwo. Doctoral thesis, Kyushu University.Google Scholar
  39. Shikata, T., S. Nagasoe, M. Matsubara, S. Yoshikawa, Y. Yamasaki, Y. Shimasaki, Y. Oshima, I. R. Jenkinson & T. Honjo, 2008. Factors influencing the initiation of blooms of the raphidophyte Heterosigma akashiwo and the diatom Skeletonema costatum in a port in Japan. Limnology and Oceanography 53: 2503–2518.Google Scholar
  40. Silva, E. S., 1985. Ecological factors related to Prorocentrum minimum blooms in Obidos Lagoon (Portugal). In Anderson, D. M., A. White & D. Baden (eds), Toxic Dinoflagellates. Elsevier, New York: 251–256.Google Scholar
  41. Smayda, T. J., 1998. Ecophysiology and bloom dynamics of Heterosigma akashiwo (Raphidophyceae). In Anderson, D. M., A. D. Cembella & G. F. Hallegraeff (eds), Physiological Ecology of Harmful Algal Blooms. Springer-Verlag, Heidelberg: 113–131.Google Scholar
  42. Smayda T. J. & D. Borkman, 2003. Long-term bloom behavior of Prorocentrum species in Narragansett Bay. Second Symposium on Harmful Marine Algae in the U.S., Woods Hole, MA, USA, (abstract at .
  43. Tameishi, M., Y. Yamasaki, S. Nagasoe, Y. Shimasaki, Y. Oshima & T. Honjo, 2009. Allelopathic effects of the dinophyte Prorocentrum minimum on the growth of the bacillariophyte Skeletonema costatum. Harmful Algae 8: 421–429.CrossRefGoogle Scholar
  44. Tarutani, K. & T. Yamamoto, 1994. Phosphate uptake and growth kinetics of Skeletonema costatum isolated from Hiroshima Bay. Journal of Faculty of Applied Biological Science, Hiroshima University 33: 59–64.Google Scholar
  45. Tomas, C. R., 1979. Olisthodiscus luteus (Chrysophyceae). III. Uptake and utilization of nitrogen and phosphorus. Journal of Phycology 15: 5–12.CrossRefGoogle Scholar
  46. Trick, C. G., R. J. Andersen & P. J. Harrison, 1984. Environmental factors influencing the production of an antibacterial metabolite from a marine dinoflagellate, Prorocentrum minimum. Canadian Journal of Fisheries and Aquatic Sciences 41: 423–432.CrossRefGoogle Scholar
  47. Twiner, M. J., S. J. Dixon & C. G. Trick, 2001. Toxic effects of Heterosigma akashiwo do not appear to be mediated by hydrogen peroxide. Limnology and Oceanography 46: 1400–1405.CrossRefGoogle Scholar
  48. Uchida, T., 2001. The role of cell contact in the life cycle of some dinoflagellate species. Journal of Plankton Research 23: 889–891.CrossRefGoogle Scholar
  49. Uchida, T., S. Toda, Y. Matsuyama, M. Yamaguchi, Y. Kotani & T. Honjo, 1999. Interactions between the red tide dinoflagellates Heterocapsa circularisquama and Gymnodinium mikimotoi in laboratory culture. Journal of Experimental Marine Biology and Ecology 241: 285–299.CrossRefGoogle Scholar
  50. Van Rijssel, M., M. K. De Boer, M. R. Tyl & W. W. C. Gieskes, 2008. Evidence for inhibition of bacterial luminescence by allelochemicals from Fibrocapsa japonica (Raphidophyceae), and the role of light and microalgal growth rate. Hydrobiologia 596: 289–299.CrossRefGoogle Scholar
  51. Yamasaki, Y., S. Nagasoe, T. Matsubara, T. Shikata, Y. Shimasaki, Y. Oshima & T. Honjo, 2007a. Allelopathic interactions between the bacillariophyte Skeletonema costatum and the raphidophyte Heterosigma akashiwo. Marine Ecology Progress Series 339: 83–92.CrossRefGoogle Scholar
  52. Yamasaki, Y., S. Nagasoe, T. Matsubara, T. Shikata, Y. Shimasaki, Y. Oshima & T. Honjo, 2007b. Growth inhibition and formation of morphologically abnormal cells of Akashiwo sanguinea (Hirasaka) G. Hansen et Moestrup by cell contact with Cochlodinium polykrikoides Margalef. Marine Biology 152: 157–163.CrossRefGoogle Scholar
  53. Yamasaki, Y., T. Shikata, A. Nukata, S. Ichiki, S. Nagasoe, T. Matsubara, Y. Shimasaki, M. Nakao, K. Yamaguchi, Y. Oshima, T. Oda, M. Ito, I. R. Jenkinson, M. Asakawa & T. Honjo, 2009. Extracellular polysaccharide-protein complexes of a harmful alga mediate the allelopathic control it exerts within the phytoplankton community. International Society for Microbial Ecology Journal 3: 808–817.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Y. Yamasaki
    • 1
    Email author
  • S. Nagasoe
    • 2
  • M. Tameishi
    • 3
  • T. Shikata
    • 3
  • Y. Zou
    • 1
  • Z. Jiang
    • 1
  • T. Matsubara
    • 3
  • Y. Shimasaki
    • 3
  • K. Yamaguchi
    • 1
  • Y. Oshima
    • 3
  • T. Oda
    • 1
  • T. Honjo
    • 3
  1. 1.Division of Biochemistry, Faculty of FisheriesNagasaki UniversityNagasakiJapan
  2. 2.Seikai National Fisheries Research InstituteNagasakiJapan
  3. 3.Laboratory of Marine Environmental Science, Division of Marine Biological Chemistry, Department of Bioscience and Biotechnology, Faculty of AgricultureKyushu UniversityHakozaki, FukuokaJapan

Personalised recommendations