Log in

Morphological and molecular characterization of free-floating and attached green macroalgae Ulva spp. in the Yellow Sea of China

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

During the summer of 2008 and 2009, massive algal blooms repeatedly broke out in the Yellow Sea of China. These were undoubtedly caused by the accumulations of one or more species in the macroalgal genus Ulva. In previous reports, morphological observation indicated that the species involved in this phenomenon is Ulva prolifera but molecular analyses indicated that the species belongs to an Ulva linza–procera–prolifera (LPP) clade. Correct identification of the bloom species is required to understand and manage the blooms, but the taxonomic status of the bloom species remains unclear. In the current study, the taxonomic status of 22 selected specimens from the Yellow Sea was assessed by using both morphological and molecular (ITS and rbcL sequences) data. In addition, 5S rDNA analyses were performed for those samples clustering in the LPP clade, and phylogenetic tree and ribotype analyses were constructed for determining the possible origin of the bloom. Three free-floating and two attached Ulva species were distinguished and described: Ulva compressa Linnaeus and Ulva pertusa Kjellman were found in free-floating samples; U. linza Linnaeus was found on rocks; and U. prolifera O.F. Müller was found in both habitats. Diversity in free-floating Ulva of the Yellow Sea appears to be greater than previously thought. The dominant free-floating Ulva species, U. prolifera, was not closely related to local populations attached to rocks but was closely related to populations from Japan.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Blomster J, Back S, Fewer DP, Kiirikki M, Lehvo A, Maggs CA, Stanhope MJ (2002) Novel morphology in Enteromorpha (Ulvophyceae) forming green tides. Am J Bot 89(11):1756–1763

    Article  PubMed  Google Scholar 

  • Charlier RH, Morand P, Finkl CW (2008) How Brittany and Florida coasts cope with green tides. Int J Environ Res 65(2):191–208

    Google Scholar 

  • Chinese State Oceanic Administration (2009) 2008 China marine calamities bulletin

  • Chinese State Oceanic Administration (2010) 2009 China marine calamities bulletin

  • Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9(10):1657–1660

    Article  PubMed  CAS  Google Scholar 

  • Coat G, Dion P, Noailles MC, De Reviers B, Fontaine JM, Berger-Perrot Y, Loiseaux-de Goer S (1998) Ulva armoricana (Ulvales, Chlorophyta) from the coasts of Brittany (France). II. Nuclear rDNA ITS sequence analysis. Eur J Phycol 33(1):81–86

    Google Scholar 

  • Ding L, Luan R (2009) The taxonomy, habit and distribution of a green alga Enteromorpha prolifera (Ulvales, Chlorophyta). Oceanol Limnol Sin 40(1):68–71

    Google Scholar 

  • Dion P, de Reviers B, Coat G (1998) Ulva armoricana sp. nov. (Ulvales, Chlorophyta) from the coasts of Brittany (France). I. Morphological identification. Eur J Phycol 33(1):73–80

    Google Scholar 

  • Guiry MD, Guiry GM (2010) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. Available from:http://www.algaebase.org. Accessed on 19 July 2010

  • Hayden HS, Waaland JR (2004) A molecular systematic study of Ulva (Ulvaceae, Ulvales) from the northeast Pacific. Phycologia 43(4):364–382

    Article  Google Scholar 

  • Hayden H, Blomster J, Maggs C, Silva P, Stanhope M, Waaland R (2003) Linnaeus was right all along: Ulva and Enteromorpha are not distinct genera. Eur J Phycol 38(3):277–294

    Article  Google Scholar 

  • Heesch S, Broom JES, Neill KF, Farr TJ, Dalen JL, Nelson WA (2009) Ulva, Umbraulva and Gemina: genetic survey of New Zealand taxa reveals diversity and introduced species. Eur J Phycol 44(2):143–154

    Article  CAS  Google Scholar 

  • Hiraok M, Shimad S, Uenosono M, Masuda M (2003) A new green-tide-forming alga, Ulva ohnoi Hiraoka et Shimada sp. nov. (Ulvales, Ulvophyceae) from Japan. Phycol Res 52(1):17–29

    Article  Google Scholar 

  • Hiraoka M, Enomoto S (1998) The induction of reproductive cell formation of Ulva pertusa Kjellman (Ulvales, Ulvophyceae). Phycol Res 46(3):199–203

    Article  Google Scholar 

  • Jiang P, Wang JF, Cui YL, Li YX, Lin HZ, Qin S (2008) Molecular phylogenetic analysis of attached Ulvaceae species and free-floating Enteromorpha from Qingdao coasts in 2007. Chin J Oceanol Limnol 26(3):276–279

    Article  CAS  Google Scholar 

  • Koeman RPT, van den Hoek C (1981) The taxonomy of Ulva (Chlorophyceae) in the Netherlands. Bri Phycol J 16:9–53

    Article  Google Scholar 

  • Largo DB, Sembrano J, Hiraoka M, Ohno M (2004) Taxonomic and ecological profile of ‘green tide’ species of Ulva (Ulvales, Chlorophyta) in central Philippines. Hydrobiologia 512(1):247–253

    Article  Google Scholar 

  • Leliaert F, Malta EJ, Engelen AH, Mineur F, De Clerck O (2008) Quindao algal bloom culprit identified. Mar Pollut Bull 56(9):1516

    Google Scholar 

  • Leliaert F, Zhang X, Ye N, Malta EJ, Engelen AH, Mineur F, Verbruggen H, De Clerck O (2009) Identity of the Qingdao algal bloom. Phycol Res 57(2):147–151

    Article  Google Scholar 

  • Li J (2008) China Ocean News. Available from: http://epaper.oceanol.com/zghyb/20080822/index.htm. Accessed on 22 August 2008

  • Liu D, Keesing JK, **ng Q, Shi P (2009) World's largest macroalgal bloom caused by expansion of seaweed aquaculture in China. Mar Pollut Bull 58(6):888–895

    Article  PubMed  CAS  Google Scholar 

  • Liu D, Keesing JK, Dong Z, Zhen Y, Di B, Shi Y, Fearns P, Shi P (2010a) Recurrence of the world’s largest green-tide in 2009 in Yellow Sea, China: Porphyra yezoensis aquaculture rafts confirmed as nursery for macroalgal blooms. Mar Pollut Bull 60(9):1423–1432

    Article  PubMed  CAS  Google Scholar 

  • Liu F, Pang S, Chopin T, Xu N, Shan T, Gao S, Sun S (2010b) The dominant Ulva strain of the 2008 green algal bloom in the Yellow Sea was not detected in the coastal waters of Qingdao in the following winter. J Appl Phycol 22(5):531–540

    Article  Google Scholar 

  • Liu F, Pang SJ, Xu N, Shan TF, Sun S, Hu X, Yang JQ (2010c) Ulva diversity in the Yellow Sea during the large-scale green algal blooms in 2008–2009. Phycol Res 58(4):270–279

    Article  Google Scholar 

  • Loughnane CJ, McIvor LM, Rindi F, Stengel DB, Guiry MD (2008) Morphology, rbcL phylogeny and distribution of distromatic Ulva (Ulvophyceae, Chlorophyta) in Ireland and southern Britain. Phycologia 47(4):416–429

    Article  CAS  Google Scholar 

  • Malta EJ, Draisma S, Kamermans P (1999) Free-floating Ulva in the southwest Netherlands: species or morphotypes? a morphological, molecular and ecological comparison. Eur J Phycol 34(5):443–454

    Article  Google Scholar 

  • Pang S, Liu F, Shan T, Xu N, Zhang Z, Gao S, Chopin T, Sun S (2010) Tracking the algal origin of the Ulva bloom in the Yellow Sea by a combination of molecular, morphological and physiological analyses. Mar Environ Res 69(4):207–215

    Article  PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Bio Evol 4(4):406–425

    CAS  Google Scholar 

  • Shea R, Chopin T (2007) Effects of germanium dioxide, an inhibitor of diatom growth, on the microscopic laboratory cultivation stage of the kelp, Laminaria saccharina. J Appl Phycol 19(1):27–32

    Article  CAS  Google Scholar 

  • Shimada S, Hiraoka M, Nabata S, Iima M, Masuda M (2003) Molecular phylogenetic analyses of the Japanese Ulva and Enteromorpha (Ulvales, Ulvophyceae), with special reference to the free-floating Ulva. Phycol Res 51(2):99–108

    Article  CAS  Google Scholar 

  • Shimada S, Yokoyama N, Arai S, Hiraoka M (2008) Phylogeography of the genus Ulva (Ulvophyceae, Chlorophyta), with special reference to the Japanese freshwater and brackish taxa. J Appl Phycol 20(5):979–989

    Article  Google Scholar 

  • Sun S, Wang F, Li C, Qin S, Zhou M, Ding L, Pang S, Duan D, Wang G, Yin B (2008) Emerging challenges: massive green algae blooms in the Yellow Sea. Nature Proceedings. doi: hdl:10101/npre.2008.2266.1

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Bio Evol 24(8):1596–1599

    Article  CAS  Google Scholar 

  • Tan IH, Blomster J, Hansen G, Leskinen E, Maggs CA, Mann DG, Sluiman HJ, Stanhope MJ (1999) Molecular phylogenetic evidence for a reversible morphogenetic switch controlling the gross morphology of two common genera of green seaweeds, Ulva and Enteromorpha. Mol Bio Evol 16(8):1011–1018

    CAS  Google Scholar 

  • Tang S (2009) China Ocean News. Available from:http://epaper.oceanol.com/zghyb/20090724/index.htm. Accessed on 24 July 2009

  • Tanner CE (1986) Investigations of the taxonomy and morphological variation of Ulva (Chlorophyta): Ulva californica Wille. Phycologia 25(4):510–520

    Article  Google Scholar 

  • Wang Q, Tang S (2008) China Ocean News. Available from:http://epaper.oceanol.com/zghyb/20080704/index.htm. Accessed on 4 July 2008

  • Wang J, Jiang P, Cui Y, Li N, Wang M, Lin H, He P, Qin S (2010) Molecular analysis of green-tide-forming macroalgae in the Yellow Sea. Aquatic Bot 93(1):25–31

    Article  CAS  Google Scholar 

  • Yabe T, Ishii Y, Amano Y, Koga T, Hayashi S, Nohara S, Tatsumoto H (2009) Green tide formed by free-floating Ulva spp. at Yatsu tidal flat, Japan. Limnology 10(3):239–245

    Article  Google Scholar 

  • Ye N, Zhang X, Mao Y, Zhuang Z, Wang Q (2008a) Life history of Enteromorpha prolifera under laboratory conditions. J Fish Sci China 15(5):853–859

    Google Scholar 

  • Ye N, Zhuang Z, ** X, Wang Q, Zhang X, Li D, Wang H, Mao Y, Jiang Z, Li B, and Xue Z (2008b) China is on the track tackling Enteromorpha spp forming green tide. Nature Proceedings. doi: hdl.10101/npre.2008.2352.1

  • Yotsukura N, Kawai T, Kawashima S, Ebata H, Ichimura T (2006) Nucleotide sequence diversity of the 5S rDNA spacer in the simple blade kelp genera Laminaria, Cymathaere and Kjellmaniella (Laminariales, Phaeophyceae) from northern Japan. Phycol Res 54(4):269–279

    Article  CAS  Google Scholar 

  • Zhang X, Mao Y, Zhuang Z, Liu S, Wang Q, Ye N (2008) Morphological characteristics and molecular phylogenetic analysis of green tide Enteromorpha sp. occurred in the Yellow Sea. J Fish Sci China 15(5):822–829

    CAS  Google Scholar 

  • Zhang X, Wang H, Mao Y, Liang C, Zhuang Z, Wang Q, Ye N (2010) Somatic cells serve as a potential propagule bank of Enteromorpha prolifera forming a green tide in the Yellow Sea, China. J Appl Phycol 22(2):173–180

    Article  Google Scholar 

Download references

Acknowledgments

We thank Professor BA Jaffee of University of California–Davis for reviewing and editing the manuscript. We also thank three anonymous reviewers for the critical review of the manuscript. This research was jointly supported by the Chinese Academy of Inspection and Quarantine (2009JK002), the program of General Administration of Quality Supervision, Inspection and Quarantine of the People's Republic of China (2011IK181), and the Key Project in the National Science and Technology Pillar Program during the Eleventh Five-year Plan period of China (2006BAK10B06).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shuifang Zhu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Duan, W., Guo, L., Sun, D. et al. Morphological and molecular characterization of free-floating and attached green macroalgae Ulva spp. in the Yellow Sea of China. J Appl Phycol 24, 97–108 (2012). https://doi.org/10.1007/s10811-011-9654-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-011-9654-7

Keywords

Navigation