Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-22T06:57:19.106Z Has data issue: false hasContentIssue false
  • English
  • Français

Interactions between selected microalgae and microscopic propagules of Ulva prolifera

Published online by Cambridge University Press:  30 August 2017

Qing Liu ,
Tian Yan ,
Rencheng Yu ,
Qingchun Zhang  and
Mingjiang Zhou
Qing Liu
Affiliation:
College of Environmental Science and Engineering, Yangzhou University, Yangzhou 225100, China Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
Tian Yan*
Affiliation:
Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
Rencheng Yu
Affiliation:
Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
Qingchun Zhang
Affiliation:
Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
Mingjiang Zhou
Affiliation:
Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
*
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: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

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.

Keywords

Ulva proliferamicroscopic propagulesgreen tidemicroalgal bloominteraction
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 98 , Issue 7 , November 2018 , pp. 1571 - 1580
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

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, 2186–2192.Google Scholar
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, 713–720.Google Scholar
Amsler, C.D., Reed, D.C. and Neushul, M. (1992) The microclimate inhabited by macroalgal propagules. British Phycological Journal 27, 253–270.Google Scholar
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. 1–161.Google Scholar
China Marine Environmental Bulletin (2001–2012) http://www.coi.gov.cn/gongbao/huanjing/Google Scholar
Clayton, M.N. (1992) Propagules of marine macroalgae: structure and development. British Phycological Journal 27, 219–232.Google Scholar
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, 1182–1188.Google Scholar
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, 68–71.Google Scholar
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. 7–43.Google Scholar
Fletcher, R.L. and Callow, M.E. (1992) The settlement, attachment and establishment of marine algal spores. British Phycological Journal 27, 303–329.Google Scholar
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.Google Scholar
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. 26–60.Google Scholar
Guillard, R.R.L. and Hargraves, P.E. (1993) Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia 32, 234–236.Google Scholar
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, 275–284.Google Scholar
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, 185–194.Google Scholar
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, 79–89.Google Scholar
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, 496–508.Google Scholar
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. 329–344.Google Scholar
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, 41–55.Google Scholar
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, 1207–1207.Google Scholar
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, 727–733.Google Scholar
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, 1169–1182.Google Scholar
Leliaert, F., Zhang, X. and Ye, N.H. (2009) Research note: identity of the Qingdao algal bloom. Phycological Research 57, 147–151.Google Scholar
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, 40–47.Google Scholar
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, 2–10.Google Scholar
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, 56–63.Google Scholar
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, 1312–1320.Google Scholar
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, 82–88.Google Scholar
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, 46–54.Google Scholar
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, 259–268.Google Scholar
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, 394–397.Google Scholar
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, 547–555.Google Scholar
Schonbeck, M.W. and Norton, T.A. (1979) The effects of diatoms on the growth of Fucus spiralis germlings in culture. Botanica Marina 22, 233–236.Google Scholar
Schories, D. and Reise, K. (1993) Germination and anchorage of Enteromorpha spp. in sediments of the Wadden Sea. Helgoländer Meeresuntersuchungen 47, 275–285.Google Scholar
Schramm, W. (1999) Factors influencing seaweed responses to eutrophication: some results from EU-project EUMAC. Journal of Applied Phycology 11, 69–78.Google Scholar
Sfrifo, A. and Pavoni, B. (1994) Macroalgae and phytoplankton competition in the central Venice lagoon. Environmental Technology 15, 1–14.Google Scholar
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, 117–122.Google Scholar
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, 259–268.Google Scholar
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, 29–35.Google Scholar
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, 796–806.Google Scholar
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, 1792–1802.Google Scholar
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, 480–488.Google Scholar
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, 12–19.Google Scholar
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, 4389–4396.Google Scholar
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, 274–280.Google Scholar
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, 608–618.Google Scholar
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.Google Scholar
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, 600–606.Google Scholar
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, 112–119.Google Scholar
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, 24–31. [In Chinese, with English Abstract]Google Scholar
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, 173–180.Google Scholar
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, 96–102.Google Scholar