Skip to main content

Interactions between selected microalgae and microscopic propagules of Ulva prolifera

  • Qing Liu (a1) (a2), Tian Yan (a2), Rencheng Yu (a2), Qingchun Zhang (a2) and Mingjiang Zhou (a2)...

Large-scale green tides of Ulva prolifera occur repeatedly in the Yellow Sea, and the microscopic propagules of U. prolifera play a critical role during the development of green tides. Ulva prolifera propagules and microalgae are both present in seawater and share similar niches, but their potential interactions are poorly understood. Nine species of microalgae were selected to study their interactions with the propagules of U. prolifera (gametes) in laboratory. The results showed that settlement of gametes could be inhibited by some microalgae, such as Alexandrium tamarense, Prorocentrum lima and Karenia mikimotoi, at the cell density of blooming (102–103 cells ml–1). Inversely, the germlings germinated from U. prolifera gametes had negative effects on the microalgae, the inhibition rate ranged from 28 to 66%. Our results demonstrated the complex interactions between microalgae and propagules of green algae, which may influence the formation of green tides and their ecological consequences in the Yellow Sea.

Corresponding author
Correspondence should be addressed to: T. Yan, Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China email:
Hide All
Alamsjah, M.A., Hirao, S., Ishibashi, F. and Fujita, Y. (2005) Isolation and structure determination of algicidal compounds from Ulva fasciata . Bioscience, Biotechnology, and Biochemistry 69, 21862192.
Alamsjah, M.A., Hirao, S., Ishibashi, F., Oda, T. and Fujita, Y. (2008) Algicidal activity of polyunsaturated fatty acids derived from Ulva fasciata and U. pertusa (Ulvaceae, Chlorophyta) on phytoplankton. Journal of Applied Phycology 20, 713720.
Amsler, C.D., Reed, D.C. and Neushul, M. (1992) The microclimate inhabited by macroalgal propagules. British Phycological Journal 27, 253270.
Chapman, A.R.O. (1986) Population and community ecology of seaweeds. In Blaxter, J.H.S. and Southwood, A.J. (eds) Advances in marine biology. London: Academic Press, pp. 1161.
China Marine Environmental Bulletin (2001–2012)
Clayton, M.N. (1992) Propagules of marine macroalgae: structure and development. British Phycological Journal 27, 219232.
Dan, A., Hiraoka, M., Ohno, M. and Critchley, A.T. (2002) Observations on the effect of salinity and photon fluence rate on the induction of sporulation and rhizoid formation in the green alga Enteromorpha prolifera (Müller) J. Agardh (Chlorophyta, Ulvales). Fisheries Science 68, 11821188.
Ding, L.P. and Luan, R.X. (2009) The taxonomy, habit and distribution of a green alga Enteromorpha prolifera (Ulvales, Chlorophyta). Oceanologia et Limnologia Sinica 40, 6871.
Fletcher, R.L. (1996) The occurrence of ‘green tide’. In Schramm, W. and Nienhuis, P.H. (eds) Marine benthic vegetation – recent changes and the effects of eutrophication. Berlin: Springer Verlag, pp. 743.
Fletcher, R.L. and Callow, M.E. (1992) The settlement, attachment and establishment of marine algal spores. British Phycological Journal 27, 303329.
Gao, S., Chen, X.Y., Yi, Q.Q., Wang, G.C., Pan, G.H., Lin, A.P. and Peng, G. (2010) A strategy for the proliferation of Ulva prolifera, main causative species of green tides, with formation of sporangia by fragmentation. PLoS ONE 5, e8571.
Guillard, R.R.L. (1975) Culture of phytoplankton for feeding marine invertebrates. In Smith, W.L. and Chanley, M.H. (eds) Culture of marine invertebrate animals. New York, NY: Plenum Press, pp. 2660.
Guillard, R.R.L. and Hargraves, P.E. (1993) Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia 32, 234236.
Hiraoka, M., Dan, A., Shimada, S., Hagihira, M., Migita, M. and Ohno, M. (2003) Different life histories of Enteromorpha prolifera (Ulvales, Chlorophyta) from four rivers on Shikoku Island, Japan. Phycologia 42, 275284.
Hoffmann, A.J. and Santelices, B. (1991) Banks of algal microscopic forms: hypotheses on their functioning and comparisons with seed banks. Marine Ecology Progress Series 79, 185194.
Huang, R. and Boney, A.D. (1983) Effects of diatom mucilage on the growth and morphology of marine algae. Journal of Experimental Marine Biology and Ecology 67, 7989.
Huo, Y.Z., Tian, Q.T., Xu, S.N., Wang, Y.Y., Feng, Z.H., Fang, Y. and He, P.M. (2010) Allelopathic effects of Ulva prolifera on growth of Karenia mikimotoi . Marine Environmental Science 29, 496508.
Jensen, A. (1977) Chemical conditioning of seawater by algal growth and development. In Faulkner, D.J. and Fenical, W.H. (eds) Marine natural products chemistry. New York, NY: Plenum Press, pp. 329344.
Jin, Q. and Dong, S.L. (2003) Comparative studies on the allelopathic effects of two different strains of Ulva pertusa on Heterosigma akashiwo and Alexandrium tamarense . Journal of Experimental Marine Biology and Ecology 293, 4155.
Joint, I., Tait, K., Callow, M.E., Callow, J.A., Milton, D., Williams, P. and Cámara, M. (2002) Cell-to-cell communication across the prokaryote-eukaryote boundary. Science 298, 12071207.
Kang, W., Sun, Y., Sun, L.F., Xu, Z.L. and Que, J.L. (2013) Distribution of phytoplankton in radial sand ridge area in north Jiangsu Shoal. Chinese Journal of Applied Environmental Biology 19, 727733.
Keesing, J.K., Liu, D.Y., Fearns, P. and Garcia, R. (2011) Inter-and intra-annual patterns of Ulva prolifera green tides in the Yellow Sea during 2007–2009, their origin and relationship to the expansion of coastal seaweed aquaculture in China. Marine Pollution Bulletin 62, 11691182.
Leliaert, F., Zhang, X. and Ye, N.H. (2009) Research note: identity of the Qingdao algal bloom. Phycological Research 57, 147151.
Li, Y., Song, W., Xiao, J., Wang, Z.L., Fu, M.Z., Zhu, M.Y., Li, R.X., Zhang, X.L. and Wang, X.N. (2014) Tempo-spatial distribution and species diversity of green algae micro-propagules in the Yellow Sea during the large-scale green tide development. Harmful Algae 39, 4047.
Liu, D.Y., Keesing, J.K., He, P.M., Wang, Z.L., Shi, Y.J. and Wang, Y.J. (2013) The world's largest macroalgal bloom in the Yellow Sea, China: formation and implications. Estuarine, Coastal and Shelf Science 129, 210.
Liu, F., Pang, S.J., Zhao, X.B. and Hu, C.M. (2012) Quantitative, molecular and growth analyses of Ulva microscopic propagules in the coastal sediment of Jiangsu province where green tides initially occurred. Mainer Environmental Research 74, 5663.
Liu, Q., Yan, T., Zhou, M.J., Zhang, Q.C. and Lin, J.N. (2015a) Interactions between microscopic propagules of Ulva prolifera and Alexandrium. Oceanologia et Limnologia Sinica 46, 13121320.
Liu, Q., Yu, R.C., Yan, T., Zhang, Q.C. and Zhou, M.J. (2015b) Laboratory study on the life history of bloom-forming Ulva prolifera in the Yellow Sea. Estuarine, Coastal and Shelf Science 163, 8288.
Lotze, H.K., Schramm, W., Schories, D. and Worm, B. (1999) Control of macroalgal blooms at early developmental stages: Pilayella littoralis vs Enteromorpha spp. Oecologia 119, 4654.
Nan, C.R., Zhang, H. and Zhao, G. (2004) Allelopathic interactions between the macroalga Ulva pertusa and eight microalgal species. Journal of Sea Research 52, 259268.
Qin, Y.T., Ji, H.H., Song, C.Y. and Xu, R. (2011) Phytoplankton ecological characteristics in green tide area of Southern Yellow Sea. Marine Environmental Science 30, 394397.
Santelices, B., Aedo, D. and Hoffmann, A. (2002) Banks of microscopic forms and survival to darkness of propagules and microscopic stages of macroalgae. Revista Chilena de Historia Natural 75, 547555.
Schonbeck, M.W. and Norton, T.A. (1979) The effects of diatoms on the growth of Fucus spiralis germlings in culture. Botanica Marina 22, 233236.
Schories, D. and Reise, K. (1993) Germination and anchorage of Enteromorpha spp. in sediments of the Wadden Sea. Helgoländer Meeresuntersuchungen 47, 275285.
Schramm, W. (1999) Factors influencing seaweed responses to eutrophication: some results from EU-project EUMAC. Journal of Applied Phycology 11, 6978.
Sfrifo, A. and Pavoni, B. (1994) Macroalgae and phytoplankton competition in the central Venice lagoon. Environmental Technology 15, 114.
Shimada, S., Nagano, M., Hiraoka, M., Ichihara, K., Mineur, F. and Zhu, W. (2010) Phylogeographic analysis of the genus Ulva (Ulvales, Chlorophyta), including bloom sample in Qingdao, China. Coastal Marine Science 34, 117122.
Smith, D.W. and Horne, A.J. (1988) Experimental measurement of resource competition between planktonic microalgae and macroalgae (seaweeds) in mesocosms simulating the San Francisco Bay-Estuary, California. Hydrobiologia 159, 259268.
Song, W., Li, Y. and Fang, S.L. (2015) Temporal and spatial distributions of green algae micro-propagules in the coastal waters of the Subei Shoal, China. Estuarine, Coastal and Shelf Sciences 163, 2935.
Sun, Y.Y., Liu, X.X., Yan, B.L. and Ma, J.H. (2010) The growth inhibition of the four species of red tide microalgae by the extracts from Porphyra yezoensis . Journal of Fisheries of China 34, 796806.
Tait, K., Williamson, H., Atkinson, S., Williams, P., Cámara, M. and Joint, I. (2009) Turnover of quorum sensing signal molecules modulates cross-kingdom signalling. Environmental Microbiology 11, 17921802.
Tang, Y.Z. and Gobler, C.J. (2011) The green macroalga, Ulva lactuca, inhibits the growth of seven common harmful algal bloom species via allelopathy. Harmful Algae 10, 480488.
Wang, C., Yu, R.C. and Zhou, M.J. (2012) Effects of the decomposing green macroalga Ulva (Enteromorpha) prolifera on the growth of four red-tide species. Harmful Algae 16, 1219.
Wang, R.J., Wang, Y., Zhou, J., Sun, J.H. and Tang, X.X. (2013) Algicidal activity of Ulva pertusa and Ulva prolifera on Prorocentrum donghaiense under laboratory conditions. African Journal of Microbiology Research 7, 43894396.
Wang, Y., Yu, Z.M., Song, X. X. and Zhang, S.D. (2006) Effects of macroalgae on growth of 2 species of bloom microalgae and interactions between these microalgae in laboratory culture. Environmental Science 27, 274280.
Wheeler, G.L., Tait, K., Taylor, A., Brownlee, C. and Joint, I. (2006) Acyl-homoserine lactones modulate the settlement rate of zoospores of the marine alga Ulva intestinalis via a novel chemokinetic mechanism. Plant, Cell and Environment 29, 608618.
Xu, J.F., Fan, X. and Zhang, X.W. (2012) Evidence of coexistence of C3 and C4 photosynthetic pathways in a green-tide-forming alga, Ulva prolifera . PLoS ONE 7, e37438.
Zhang, H.W., Ma, J.H. and Hu, X. (2011) Reproductive characteristics of the floating algae in green tide. Journal of Shanghai Ocean University 20, 600606.
Zhang, Q.C., Liu, Q. and Yu, R.C. (2015) Application of a fluorescence in situ hybridization (FISH) method to study green tides in the Yellow Sea. Estuarine, Coastal and Shelf Science 163, 112119.
Zhang, X., Luan, Q.S., Sun, J.Q. and Wang, J. (2013) Influence of Enteromorpha prolifera (Chlorophyta) on the phytoplankton community structure. Marine Science 37, 2431. [In Chinese, with English Abstract]
Zhang, X.W., Wang, H.X., Mao, Y.Z., Liang, C.W., Zhuang, Z.M., Wang, Q.Y. and Ye, N.H. (2010) Somatic cells serve as a potential propagules bank of Enteromorpha prolifera forming a green tide in the Yellow Sea, China. Journal of Applied Phycology 22, 173180.
Zhao, J., Jiang, P. and Qin, S. (2015) Genetic analyses of floating Ulva prolifera in the Yellow Sea suggest a unique ecotype. Estuarine, Coastal and Shelf Science 163, 96102.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Journal of the Marine Biological Association of the United Kingdom
  • ISSN: 0025-3154
  • EISSN: 1469-7769
  • URL: /core/journals/journal-of-the-marine-biological-association-of-the-united-kingdom
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 1
Total number of PDF views: 19 *
Loading metrics...

Abstract views

Total abstract views: 131 *
Loading metrics...

* Views captured on Cambridge Core between 30th August 2017 - 17th March 2018. This data will be updated every 24 hours.