Journal of Oceanology and Limnology

, Volume 36, Issue 4, pp 1280–1293 | Cite as

Seasonal phenology of the heterotrophic dinoflagellate Noctiluca scintillans (Macartney) in Jiaozhou Bay and adjacent coastal Yellow Sea, China

  • Weicheng Wang (王卫成)
  • Song Sun (孙松)Email author
  • Xiaoxia Sun (孙晓霞)
  • Fang Zhang (张芳)
  • Guangtao Zhang (张光涛)
  • Mingliang Zhu (朱明亮)


Seasonal variations in numerical abundance, cell diameter and population carbon biomass of the heterotrophic dinoflagellate Noctiluca scintillans were studied for 10 years from 2004 to 2013 in Jiaozhou Bay and adjacent coastal Yellow Sea, China, and their ecological functions were evaluated. In both areas, N. scintillans occurred throughout the year and demonstrated an essentially similar seasonality; the cell abundance increased rapidly from the winter minimum to an annual peak in late spring and early summer, and decreased gradually toward the autumn-winter minimum. The peak abundance differed by years, and there was no consistent trend in long-term numerical variations. The cell diameter also showed a seasonal fluctuation, being larger in spring and early summer than the other seasons. Estimated carbon biomass of N. scintillans population reached to a peak as high as 90.3 mg C/m3, and occasionally exceed over phytoplankton and copepod biomass. Our results demonstrate that N. scintillans in northwestern Yellow Sea displays the seasonal phenology almost identical to the populations in other temperate regions, and play important trophic roles as a heterotroph to interact with sympatric phytoplankton and copepods.


cell size biomass copepods phytoplankton ZooScan 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.



We sincerely thank Prof. S. Uye, Hiroshima University, for investing his time and effort in revising this manuscript. We are grateful for all the staff of Jiaozhou Bay Marine Ecosystem Research Station for their valuable helps with field work and collecting the samples. Thanks are due also to the anonymous reviewers for their valuable comments and suggestions on the manuscript.


  1. Al-Azri A, Al-Hashmi K, Goes J, Gomes H, Rushdi A I, Al-Habsi H, Al-Khusaibi S, Al-Kindi R, Al-Azri N. 2007. Seasonality of the bloom-forming heterotrophic dinoflagellate Noctiluca scintillans in the Gulf of Oman in relation to environmental condition. International Journal of Oceans and Oceanography, 2 (1): 51–60.Google Scholar
  2. Alcaraz M, Saiz E, Calbet A, Trepat I, Broglio E. 2003. Estimating zooplankton biomass through image analysis. Marine Biology, 143 (2): 307–315.CrossRefGoogle Scholar
  3. Anderson D M. 1997. Turning back the harmful red tide. Nature, 388 (6642): 513–514.CrossRefGoogle Scholar
  4. Anderson D M. 2009. Approaches to monitoring, control and management of harmful algal blooms (HABs). Ocean & Coastal Management, 52 (7): 342–347.CrossRefGoogle Scholar
  5. Ara K, Nakamura S, Takahashi R, Shiomoto A, Hiromi J. 2013. Seasonal variability of the red tide-forming heterotrophic dinoflagellate Noctiluca scintillans in the neritic area of Sagami Bay, Japan: its role in the nutrientenvironment and aquatic ecosystem. Plankton and Benthos Research, 8 (1): 9–30.CrossRefGoogle Scholar
  6. Buskey E J. 1995. Growth and bioluminescence of Noctiluca scintillans on varying algal diets. Journal of Plankton Research, 17: 29–40.CrossRefGoogle Scholar
  7. Daan R. 1987. Impact of egg predation by Noctiluca miliaris on the summer development of copepod populations in the southern North Sea. Marine Ecology Progress Series, 37: 9–17.CrossRefGoogle Scholar
  8. Dela-Cruz J, Ajani P, Lee R, Pritchard T, Suthers I. 2002. Temporal abundance patterns of the red tide dinoflagellate Noctiluca scintillans along the southeast coast of Australia. Marine Ecology Progress Series, 236: 75–88.CrossRefGoogle Scholar
  9. Dela-Cruz J, Middleton J H, Suthers I M. 2003. Population growth and transport of the red tide dinoflagellate, Noctiluca scintillans, in the coastal waters offSydney Australia, using cell diameter as a tracer. Limnology and Oceanology, 48 (2): 656–674.CrossRefGoogle Scholar
  10. Dela-Cruz J, Middleton J H, Suthers I M. 2008. The influence of upwelling, coastal currents and water temperature on the distribution of the red tide dinoflagellate, Noctiluca scintillans, along the east coast of Australia. Hydrobiologia, 598 (1): 59–75.CrossRefGoogle Scholar
  11. Drits A V, Nikishina A B, Sergeeva V M, Solov’ev K A. 2013. Feeding, respiration, and excretion of the Black Sea Noctiluca scintillans MacCartney in summer. Oceanology, 53 (4): 442–450.CrossRefGoogle Scholar
  12. Elbrächter M, Qi Y Z. 1998. Aspects of Noctiluca (Dinophyceae) population dynamics. In: Anderson D M, Cembella A D, HallegraeffG M eds. Physiological Ecology of Harmful Algal Blooms. Springer Verlag, Berlin. p.315–335.Google Scholar
  13. Frangópulos M, Spyrakos E, Guisande C. 2011. Ingestion and clearance rates of the red Noctiluca scintillans fed on the toxic dinoflagellate Alexandrium minutum (Halim). Harmful Algae, 10 (3): 304–309.CrossRefGoogle Scholar
  14. Gai J J, Jiao X M, Ni J D, Zou H H. 2012. The characteristics of spatial distribution of Noctiluca in the Haizhou Bay. Journal of Aquacuture, 33 (10): 13–16. (in Chinese with English abstract)Google Scholar
  15. Glibert P M, Anderson D M, Gentien P, Granéli E, Sellner K G. 2005. The global, complex phenomena of harmful algal blooms. Oceanography, 18 (2): 136–147.CrossRefGoogle Scholar
  16. Grosjean P, Picheral M, Warembourg C, Gorsky G. 2004. Enumeration, measurement, and identification of net zooplankton samples using the ZOOSCAN digital imaging system. ICES Journal of Marine Science, 61 (4): 518–525.CrossRefGoogle Scholar
  17. HallegraeffG M. 1993. A review of harmful algal blooms and their apparent global increase. Phycologia, 32 (2): 79–99.CrossRefGoogle Scholar
  18. Harrison P J, Furuya K, Glibert P M, Xu J, Liu H B, Yin K, Lee J H W, Anderson D M, Gowen R, Al-Azri A R, Ho A Y T. 2011. Geographical distribution of red and green Noctiluca scintillans. Chinese Journal of Oceanology and Limnology, 29 (4): 807–831.CrossRefGoogle Scholar
  19. Huang C, Qi Y. 1997. The abundance cycle and influence factors on red tide phenomena of Noctiluca scintillans (Dinophyceae) in Dapeng Bay, the South China Sea. Journal of Plankton Research, 19 (3): 303–318.CrossRefGoogle Scholar
  20. Isinibilir M, Hubareva E, Svetlichny L. 2014. Interpopulation dynamics between Acartia clausi (Copepoda) and Noctiluca scintillan s (Dinoflagellata) in the Bosphorus area of the Black and the Marmara Seas. Italian Journal of Zoology, 81 (3): 451–456.CrossRefGoogle Scholar
  21. Jin X S, Zhang B, Xue Y. 2010. The response of the diets of four carnivorous fishes to variations in the Yellow Sea ecosystem. Deep Sea Research Part II: Topical Studies in Oceanography, 57 (11–12): 996–1 000.CrossRefGoogle Scholar
  22. Kirchner M, Sahling G, Uhlig G, Gunkel W, Klings K W. 1996. Does the red tide-forming dinoflagellate Noctiluca scintillans feed on bacteria? Sarsia, 81 (1): 45–55.CrossRefGoogle Scholar
  23. Liu D Y, Keesing J K, Xing Q G, Shi P. 2009. World’s largest macroalgal bloom caused by expansion of seaweed aquaculture in China. Marine Pollution Bulletin, 58 (6): 888–895.CrossRefGoogle Scholar
  24. Liu M T, Li C L, Sun S. 2011. Seasonal variation in fatty acid composition of seston and the copepod Calanus sinicus (Brodsky, 1962) in Jiaozhou Bay and its trophic implications. Chinese Journal of Oceanology and Limnology, 29 (6): 1 164–1 173.CrossRefGoogle Scholar
  25. Mikaelyan A S, Malej A, Shiganova T A, Turk V, Sivkovitch A E, Musaeva E I, Kogovšek T, Lukasheva T A. 2014. Populations of the red tide forming dinoflagellate Noctiluca scintillans (Macartney): a comparison between the Black Sea and the northern Adriatic Sea. Harmful Algae, 33: 29–40.CrossRefGoogle Scholar
  26. Miyaguchi H, Fujiki T, Kikuchi T, Kuwahara V S, Toda T. 2006. Relationship between the bloom of Noctiluca scintillans and environmental factors in the coastal waters of Sagami Bay, Japan. Journal of Plankton Research, 28 (3): 313–324.CrossRefGoogle Scholar
  27. Mohamed Z A, Mesaad I. 2007. First report on Noctiluca scintillans blooms in the Red Sea offthe coasts of Saudi Arabia: consequences of eutrophication. Oceanologia, 49 (3): 337–351.Google Scholar
  28. Mohanty A K, Satpathy K K, Sahu G, Sasmal S K, Sahu B K, Panigrahy R C. 2007. Red tide of Noctiluca scintillans and its impact on the coastal water quality of the nearshore waters, offthe Rushikulya River, Bay of Bengal. Current Science, 93 (5): 616–618.Google Scholar
  29. Nakamura Y. 1998. Growth and grazing of a large heterotrophic dinoflagellate, Noctiluca scintillans, in laboratory cultures. Journal of Plankton Research, 20 (9): 1711–1720.CrossRefGoogle Scholar
  30. Parsons T R, Maita Y, Lalli C M. 1984. A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press, New York. p.3–122.Google Scholar
  31. Qi Y Z, Zhang Z, Hong Y. 1993. Occurrence of red tides on the coasts of China. In: Smayda T J, Shimizu Y eds. Toxic Phytoplankton Bloom in the Sea. Elsevier Science Pulishers, the Netherlands. p.43–46.Google Scholar
  32. Quevedo M, Gonzalez-Quiros R, Anadon R. 1999. Evidence of heavy predation by Noctiluca scintillans on Acartia clausi (Copepoda) eggs offthe central Cantabrian coast (NW Spain). Oceanologica Acta, 22 (1): 127–131.CrossRefGoogle Scholar
  33. Sato N E, Hernández D, Viñas M D. 2010. Feeding habits of Noctiluca scintillans in coastal waters offBuenos Aires Province, Argentina. Latin American Journal of Aquatic Research, 38 (3): 403–412.Google Scholar
  34. Schultes S, Lopes R M. 2009. Laser optical plankton counter and zooscan intercomparison in tropical and subtropical marine ecosystems. Limnology and Oceanography: Methods, 7 (11): 771–784.Google Scholar
  35. Sekiguchi H, Kato T. 1976. Influence of Noctiluca 's predation on the Acartia population in Ise Bay, Central Japan. Journal of the Oceanographical Society of Japan, 32 (5): 195–198.CrossRefGoogle Scholar
  36. Shen Z L. 2001. Historical Changes in Nutrient Structure and its Influences on Phytoplantkon Composition in Jiaozhou Bay. Estuarine, Coastal and Shelf Science, 52 (2): 211–224.CrossRefGoogle Scholar
  37. Song N Q, Wang N, Lu Y, Zhang J R. 2016. Temporal and spatial characteristics of harmful algal blooms in the Bohai Sea during 1952–2014. Continental Shelf Research, 122: 77–84.CrossRefGoogle Scholar
  38. Sulochanan B, Dineshbabu A P, Saravanan R, Bhat G S, Lavanya S. 2014. Occurrence of Noctiluca scintillans bloom offMangalore in the Arabian Sea. Indian Journal of Fisheries, 61 (1): 42–48.Google Scholar
  39. Sun S, Tao Z C, Li C L, Liu H L. 2011a. Spatial distribution and population structure of Euphausia pacifica in the Yellow Sea (2006–2007). Journal of Plankton Research, 33 (6): 873–889.CrossRefGoogle Scholar
  40. Sun X H, Sun S, Li C L, Zhang G T. 2011b. Seasonal and spatial variability in egg production, abundance and production of small copepods in and near Jiaozhou Bay, China. Journal of Plankton Research, 33 (5): 741–750.CrossRefGoogle Scholar
  41. Sun X X, Sun S, Wu Y L, Zhang Y S, Zheng S. 2011c. Longterm changes of phytoplankton community structure in the Jiaozhou Bay. Oceanologia et Limnologia Sinica, 42 (5): 639–646. (in Chinese with English abstract)Google Scholar
  42. Tada K, Morishita M. 1997. The changes of environmental chemical conditions and biomass on lower tropic levels in a coastal bay. Tech. Bull. Fac. Agric. Kagawa Univ., 49 (1): 35–47.Google Scholar
  43. Tada K, Pithakpol S, Montani S. 2004. Seasonal variation in the abundance of Noctiluca scintillans in the Seto Inland Sea, Japan. Plankton Biology and Ecology, 51 (1): 7–14.Google Scholar
  44. Tang D L, Di B P, Wei G F, Ni I H, Oh I, Wang S F. 2006. Spatial, seasonal and species variations of harmful algal blooms in the South Yellow Sea and East China Sea. Hydrobiologia, 568 (1): 245–253.CrossRefGoogle Scholar
  45. Tang Q S, Ying Y P, Wu Q. 2016. The biomass yields and management challenges for the Yellow sea large marine ecosystem. Environmental Development, 17 (S1): 175–181.CrossRefGoogle Scholar
  46. Tiselius P, Kiørboe T. 1998. Colonization of diatom aggregates by the dinoflagellate Noctiluca scintillans. Limnology and Oceanography, 43 (1): 154–159.CrossRefGoogle Scholar
  47. Tseng L C, Kumar R, Chen Q C, Hwang J S. 2011. Summer distribution of Noctiluca scintillans and mesozooplankton in the Western and Southern East China Sea prior to the Three Gorges Dam operation. Hydrobiologia, 666 (1): 239–256.CrossRefGoogle Scholar
  48. Turkoglu M. 2013. Red tides of the dinoflagellate Noctiluca scintillans associated with eutrophication in the Sea of Marmara (the Dardanelles, Turkey). Oceanologia, 55 (3): 709–732.CrossRefGoogle Scholar
  49. Turner J T, Granéli E. 1992. Zooplankton feeding ecology: grazing during enclosure studies of phytoplankton blooms from the west coast of sweden. Journal of Experimental Marine Biology and Ecology, 157 (1): 19–31.CrossRefGoogle Scholar
  50. Umani S F, Beran A, Parlato S, Virgilio D, Zollet T, De Olazabal A, Lazzarini B, Cabrini M. 2004. Noctiluca scintillans MACARTNEY in the Northern Adriatic Sea: long-term dynamics, relationships with temperature and eutrophication, and role in the food web. Journal of Plankton Research, 26 (5): 545–561.CrossRefGoogle Scholar
  51. Wu Y L, Sun S, Zhang Y S. 2005. Long-term change of environment and it’s influence on phytoplankton community structure in Jiaozhou Bay. Oceanologia et Limnologia Sinica, 36 (6): 487–498. (in Chinese with English abstract)Google Scholar
  52. Wu Z X, Yu Z M, Song X X, Yuan Y Q, Cao X H, Liang Y B. 2013. The spatial and temporal characteristics of harmful algal blooms in the southwest Bohai sea. Continental Shelf Research, 59: 10–17.CrossRefGoogle Scholar
  53. Yılmaz I N, Okus E, Yüksek A. 2005. Evidences for influence of a heterotrophic dinoflagellate (Noctiluca scintillans) on zooplankton community structure in a highly stratified basin. Estuarine, Coastal and Shelf Science, 64 (2–3): 475–485.CrossRefGoogle Scholar
  54. Yin K D. 2003. Influence of monsoons and oceanographic processes on red tides in Hong Kong waters. Marine Ecology Progress Series, 262: 27–41.CrossRefGoogle Scholar
  55. Yuan Y, Song D H, Wu W, Liang S K, Wang Y, Ren Z P. 2016. The impact of anthropogenic activities on marine environment in Jiaozhou Bay, Qingdao, China: a review and a case study. Regional Studies in Marine Science, 8: 287–296.CrossRefGoogle Scholar
  56. Zhang W C, Zhang C X, Xiao T. 2009. Role of microzooplankton in marine planktonic ecosystem. Advances in Earth Science, 24 (11): 1 195–1 201.Google Scholar
  57. Zhou M J, Shen Z L, Yu R C. 2008. Responses of a coastal phytoplankton community to increased nutrient input from the Changjiang (Yangtze) River. Continental Shelf Research, 28 (12): 1 483–1 489.CrossRefGoogle Scholar

Copyright information

© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Weicheng Wang (王卫成)
    • 1
    • 3
  • Song Sun (孙松)
    • 1
    • 2
    • 3
    • 4
    Email author
  • Xiaoxia Sun (孙晓霞)
    • 2
    • 3
    • 4
  • Fang Zhang (张芳)
    • 1
    • 3
  • Guangtao Zhang (张光涛)
    • 2
    • 3
    • 4
  • Mingliang Zhu (朱明亮)
    • 2
  1. 1.Key Laboratory of Marine Ecology and Environmental Sciences, Institute of OceanologyChinese Academy of SciencesQingdaoChina
  2. 2.Jiaozhou Bay Marine Ecosystem Research Station, Institute of OceanologyChinese Academy of SciencesQingdaoChina
  3. 3.University of Chinese Academy of SciencesBeijingChina
  4. 4.Laboratory for Marine Ecology and Environmental ScienceQingdao National Laboratory for Marine Science and TechnologyQingdaoChina

Personalised recommendations