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Botanica Marina

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Temporal succession of community structure and biphase ratio in a natural population of Ulva spp. (Chlorophyta) attached to Pyropia rafts in the Yellow Sea, China

Yu Du
  • Department of Cell Biology, School of Biology and Basic Medical, Soochow University, No. 199 Renai Road, Suzhou 215123, China
  • College of Aqua-life Sciences and Technology, Shanghai Ocean University, Shanghai 201306, China
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/ Yuan Ao
  • Department of Cell Biology, School of Biology and Basic Medical, Soochow University, No. 199 Renai Road, Suzhou 215123, China
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/ Yuan He
  • Department of Cell Biology, School of Biology and Basic Medical, Soochow University, No. 199 Renai Road, Suzhou 215123, China
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/ Yi Yin
  • Department of Cell Biology, School of Biology and Basic Medical, Soochow University, No. 199 Renai Road, Suzhou 215123, China
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/ Yafeng Ma
  • Department of Cell Biology, School of Biology and Basic Medical, Soochow University, No. 199 Renai Road, Suzhou 215123, China
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/ Anxiang Yuan
  • Department of Cell Biology, School of Biology and Basic Medical, Soochow University, No. 199 Renai Road, Suzhou 215123, China
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/ Songdong Shen
  • Corresponding author
  • Department of Cell Biology, School of Biology and Basic Medical, Soochow University, No. 199 Renai Road, Suzhou 215123, China
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Published Online: 2019-08-21 | DOI: https://doi.org/10.1515/bot-2018-0115

Abstract

Green tide algal blooms occur worldwide, especially in China’s Yellow Sea, and have caused serious damage to local ecological environments and economies. As a dominant agent of green tides, the green macroalga Ulva has caused widespread concern. In this study, phylogenetic clades were constructed among related Ulva species isolated from Pyropia rafts at six sites over 1.5 years based on internal transcribed spacer (ITS) and tufA sequences. In addition, traditional observation ploidy methods and flow cytometry methods were used to analyse continuous change in the biphase and sex ratios of Ulva species and to assess the changes in phase advantages over time. The results showed that the perennial Ulva populations on rafts mainly consisted of Ulva flexuosa and Ulva prolifera, and the biphasic dominance of the attached Ulva populations changed with the seasons: sporophytes were predominant mainly in winter and spring, and gametophytes were predominant mainly in summer and autumn. At the same time, there were some differences in gametophyte and sporophyte frequencies (mainly sporophyte biased) compared to the null model prediction of a √2:1 ratio, while the sex ratio of male and female gametophytes remained 1:1 throughout the year. Our results indicate the presence of both phases of bloom-forming species of Ulva in green tides year round, and that multiple generations coexist and grow continuously.

This article offers supplementary material which is provided at the end of the article.

Keywords: flow cytometry; generative cell size; molecular identification; the null prediction; Ulva population

References

  • Alström-Rapaport, C., E. Leskinen and P. Pamilo. 2010. Seasonal variation in the mode of reproduction of Ulva intestinalis in a brackish water environment. Aquatic. Bot. 93: 244–249.CrossrefGoogle Scholar

  • Brodie, J., C.A. Maggs and D.M. John. 2007. The green seaweeds of Britain and Ireland. British Phycological Society, London. pp. 1–242.Google Scholar

  • Bull, J.J. 1981. Coevolution of haplo-diploidy and sex determination in the Hymenoptera. Evolution 35: 568–580.CrossrefGoogle Scholar

  • Couceiro, L., G.M. Le, H.M. Hunsperger, S. Mauger, C. Destombe, J.M. Cock, S. Ahmed, S.M. Coelho, M. Valero and A.F. Peters. 2015. Evolution and maintenance of haploid-diploid life cycles in natural populations: the case of the marine brown alga Ectocarpus. Evolution 69: 1808–1822.CrossrefGoogle Scholar

  • Cui, J., J. Zhang, Y. Huo, L. Zhou, Q. Wu, L. Chen, K. Yu and P. He. 2015. Adaptability of free-floating green tide algae in the Yellow Sea to variable temperature and light intensity. Mar. Pollut. Bull. 101: 660–666.CrossrefGoogle Scholar

  • Czerwik-Marcinkowska, J., E. Tomal, A. Malinowska-Gniewosz, U. Majewska and A. Kubala-Kukuś. 2017. Morphological and molecular charcteristics of Ulva flexuosa subsp. pilifera (Ulvales, Chlorophyta) from Montenegro. Phycologia, Journal of the International Phycological Society.Google Scholar

  • Destombe, C., M. Valero, P. Vernet and D. Couvet. 1989. What controls haploid-diploid ratio in the red alga, Gracilaria verrucosa? J. Evol. Biol. 2: 317–338.CrossrefGoogle Scholar

  • Ding, L.P. and R.X. Luan. 2004. Flora algarum marinarum sinicarum Tomus IV Chlorophyta No. I Ulotrichales, Chaetophorales, Phaeophilales, Ulvales, Prasiolales, Cladophorales, Acrosiphoniales. Science Press, Beijing. pp. 40–60 (in Chinese).Google Scholar

  • Doležel, J., J. Greilhuber and J. Suda. 2007. Estimation of nuclear DNA content in plants using flow cytometry. Nat. Protoc. 2: 2233–2244.CrossrefGoogle Scholar

  • Famà, P., B. Wysor, W.H.C.F. Kooistra and G.C. Zuccarello. 2002. Molecular phylogeny of the genus Caulerpa (Caulerpales, Chlorophyta) inferred from Chloroplast tufA gene. J. Phycol. 38: 1040–1050.CrossrefGoogle Scholar

  • Gao, S., X.Y. Chen, Q.Q. Yi, G.C. Wang, G.H. Pan, A.P. Lin and G. Peng. 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.CrossrefGoogle Scholar

  • Gao, G., A.S. Clare, C. Rose and G.S. Caldwell. 2016. Eutrophication and warming-driven green tides (Ulva rigida) are predicted to increase under future climate change scenarios. Mar. Pollut. Bull. 114: 439–447.Google Scholar

  • Graham, L.E. and L. Wilcox. 2000. Algae (vol 36, pg 788, 2000). J. Phycol. 36: 1029–1036.Google Scholar

  • Guillemin, M.L., S. Faugeron, C. Destombe, F. Viard, J.A. Correa and M. Valero. 2008. Genetic variation in wild and cultivated populations of the haploid-diploid red alga Gracilaria chilensis: how farming practices favor asexual reproduction and heterozygosity. Evolution 62: 1500–1519.CrossrefGoogle Scholar

  • Han, W., L.P. Chen, J.H. Zhang, X.L. Tian, L. Hua, Q. He, Y.Z. Huo, K.F. Yu, D.J. Shi, J.H. Ma and P.M. He. 2013. Seasonal variation of dominant free-floating and attached Ulva species in Rudong coastal area, China. Harmful Algae 28: 46–54.CrossrefGoogle Scholar

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

  • Hiraoka, M. and G. Yoshida. 2010. Temporal variation in isomorphic phase and sex ratios of a natural population of Ulva pertusa (Chlorophyta). J. Phycol. 46: 882–888.CrossrefGoogle Scholar

  • Hiraoka, M., K. Ichihara, W. Zhu, S. Shimada, N. Oka, J. Cui, S. Tsubaki and P. He. 2017. Examination of species delimitation of ambiguous DNA-based Ulva (Ulvophyceae, Chlorophyta) clades by culturing and hybridisation. Phycologia 56: 517–532.CrossrefGoogle Scholar

  • Huo, Y., H. Han, H. Shi, H. Wu, J. Zhang, K. Yu, R. Xu, C. Liu, Z. Zhang, K. Liu, P. He and D. Ding. 2015. Changes to the biomass and species composition of Ulva sp. on Porphyra aquaculture rafts, along the coastal radial sandbank of the Southern Yellow Sea. Mar. Pollut. Bull. 93: 210–216.CrossrefGoogle Scholar

  • Kain, J.M. and C. Destombe. 1995. A review of the life history, reproduction and phenology of Gracilaria. J. Appl. Phycol. 7: 269–281.CrossrefGoogle Scholar

  • Kapraun, D.F. 1970. Field and cultural studies of Ulva and Enteromorpha in the vicinity of Port Aransas, Texas. Contrib. Mar. Sci. 15: 205–285.Google Scholar

  • Keesing, J.K., D.Y. Liu, P. Fearns and R. Garcia. 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. Mar. Pollut. Bull. 62: 1169–1182.CrossrefGoogle Scholar

  • Klinger, T. 1993. The persistence of haplodiploidy in algae. Trends Ecol Evol 8: 256–258.CrossrefGoogle Scholar

  • Kuwano, K., R. Sakurai, Y. Motozu, Y. Kitade and N. Saga. 2010. Diurnal cell division regulated by gating the G1(1)/S transition in Enteromorpha compressa (Chlorophyta). J. Phycol. 44: 364–373.Google Scholar

  • Leliaert, F., X.W. Zhang, N.H. Ye, E. Malta, A.H. Engelen, F. Mineur, H. Verbruggen and O. De Clerck. 2009. Research note: Identity of the Qingdao algal bloom. Phycol. Res. 57: 147–151.CrossrefGoogle Scholar

  • Lewis, W.M. 1985. Nutrient scarcity as an evolutionary cause of haploidy. Am. Nat. 125: 692–701.CrossrefGoogle Scholar

  • Li, Y., J. Xiao, L. Ding, Z. Wang, W. Song and S. Fan. 2015. Community structure and controlled factor of attached green algae on the Porphyra yezoensis aquaculture rafts in the Subei Shoal, China. Acta Oceanol. Sin. 34: 93–99.CrossrefGoogle Scholar

  • Lin, Z.H., S.D. Shen, W.Z. Chen and H.H. Li. 2013. Phylogenetic analyses of four species of Ulva and Monostroma grevillei using ITS, rbcL and 18S rDNA sequence data. Chin. J. Oceanol. Limnol. 31: 97–105.CrossrefGoogle Scholar

  • Liu, D., J.K. Keesing, Z. Dong, Y. Zhen, B. Di, Y. Shi, P. Fearns and P. Shi. 2010. 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: 1423–1432.CrossrefGoogle Scholar

  • Liu, Q., R.C. Yu, T. Yan, Q.C. Zhang and M.J. Zhou. 2015. Laboratory study on the life history of bloom-forming Ulva prolifera in the Yellow Sea. Estuar. Coast. Shelf Sci. 163: 82–88.CrossrefGoogle Scholar

  • Lyons, P., C. Thornber, J. Portnoy and E. Gwilliam. 2009. Dynamics of macroalgal blooms along the cape cod national seashore. Northeastern Nat. 16: 53–66.CrossrefGoogle Scholar

  • Merchant, S.S., S.E. Prochnik, O. Vallon, E.H. Harris, S.J. Karpowicz, G.B. Witman, A. Terry, A. Salamov, L.K. Fritz-Laylin, L. Marechal-Drouard, W.F. Marshall, L.H. Qu, D.R. Nelson, A.A. Sanderfoot, M.H. Spalding, V.V. Kapitonov, Q.H. Ren, P. Ferris, E. Lindquist, H. Shapiro, S.M. Lucas, J. Grimwood, J. Schmutz, P. Cardol, H. Cerutti, G. Chanfreau, C.L. Chen, V. Cognat, M.T. Croft, R. Dent, S. Dutcher, E. Fernandez, H. Fukuzawa, D. Gonzalez-Ballester, D. Gonzalez-Halphen, A. Hallmann, M. Hanikenne, M. Hippler, W. Inwood, K. Jabbari, M. Kalanon, R. Kuras, P.A. Lefebvre, S.D. Lemaire, A.V. Lobanov, M. Lohr, A. Manuell, I. Meir, L. Mets, M. Mittag, T. Mittelmeier, J.V. Moroney, J. Moseley, C. Napoli, A.M. Nedelcu, K. Niyogi, S.V. Novoselov, I.T. Paulsen, G. Pazour, S. Purton, J.P. Ral, D.M. Riano-Pachon, W. Riekhof, L. Rymarquis, M. Schroda, D. Stern, J. Umen, R. Willows, N. Wilson, S.L. Zimmer, J. Allmer, J. Balk, K. Bisova, C.J. Chen, M. Elias, K. Gendler, C. Hauser, M.R. Lamb, H. Ledford, J.C. Long, J. Minagawa, M.D. Page, J.M. Pan, W. Pootakham, S. Roje, A. Rose, E. Stahlberg, A.M. Terauchi, P.F. Yang, S. Ball, C. Bowler, C.L. Dieckmann, V.N. Gladyshev, P. Green, R. Jorgensen, S. Mayfield, B. Mueller-Roeber, S. Rajamani, R.T. Sayre, P. Brokstein, I. Dubchak, D. Goodstein, L. Hornick, Y.W. Huang, J. Jhaveri, Y.G. Luo, D. Martinez, W.C.A. Ngau, B. Otillar, A. Poliakov, A. Porter, L. Szajkowski, G. Werner, K.M. Zhou, I.V. Grigoriev, D.S. Rokhsar and A.R. Grossman. 2007. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245–250.CrossrefGoogle Scholar

  • Miao, X., J. Xiao, M. Pang, X. Zhang, Z. Wang, J. Miao and Y. Li. 2017. Effect of the large-scale green tide on the species succession of green macroalgal micro-propagules in the coastal waters of Qingdao, China. Mar. Pollut. Bull. 126: 549–556.Google Scholar

  • Nilsen, G. and Ø. Nordby. 1975. A sporulation-inhibiting substance from vegetative thalli of the green alga Ulva mutabilis, føyn. Planta 125: 127–139.Google Scholar

  • Nordby, Ø. and R.C. Hoxmark. 1972. Changes in cellular parameters during synchronous meiosis in Ulva mutabilis føyn. Exp. Cell. Res. 75: 321–328.CrossrefGoogle Scholar

  • Otto, S.P. and A.C. Gerstein. 2008. The evolution of haploidy and diploidy. Curr. Biol. 18: R1121–R1124.CrossrefGoogle Scholar

  • Pang, S.J., F. Liu, T.F. Shan, N. Xu, Z.H. Zhang, S.Q. Gao, T. Chopin and S. Sun. 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: 207–215.CrossrefGoogle Scholar

  • Paquin, C. and J. Adams. 1983. Frequency of fixation of adaptive mutations is higher in evolving diploid than haploid yeast populations. Nature 302: 495–500.CrossrefGoogle Scholar

  • Potter, E.E., C.S. Thornber, J.D. Swanson and M. McFarland. 2016. Ploidy distribution of the harmful bloom forming macroalgae Ulva spp. in Narragansett Bay, Rhode Island, USA, using flow cytometry methods. PLoS One 11: e0149182.CrossrefGoogle Scholar

  • Pringle, J.D. 1986. Structure of certain north-American government fishery agencies and effective resource-management. Ocean Manage. 10: 11–20.CrossrefGoogle Scholar

  • Santelices, B. 1990. Patterns of reproduction, dispersal and recruitment in seaweeds. Oceanogr. Mar. Biol. Annu. Rev. 28: 177–276.Google Scholar

  • Schoschina, E.V., V.N. Makarov, G.M. Voskoboinikov and C.V.D. Hoek. 1996. Growth and reproductive phenology of nine intertidal algae on the murman coast of the Barents Sea. Bot. Mar. 39: 83–94.Google Scholar

  • Smith, J.E., J.W. Runcie and C.M. Smith. 2005. Characterization of a large-scale ephemeral bloom of the green alga Cladophora sericea on the coral reefs of West Maui, Hawai’i. Mar. Ecol. Prog. Ser. 302: 77–91.CrossrefGoogle Scholar

  • Stratmann, J., G. Paputsoglu and W. Oertel. 1996. Differentiation of Ulva mutabilis (Chlorophyta) gametangia and gamete release are controlled by extracellular inhibitors. J. Phycol. 32: 1009–1021.CrossrefGoogle Scholar

  • Thornber, C.S. 2006. Functional properties of the isomorphic biphasic algal life cycle. Integr. Comp. Biol. 46: 605–614.CrossrefGoogle Scholar

  • Thornber, C.S. and S.D. Gaines. 2004. Population demographics in species with biphasic life cycles. Ecology 85: 1661–1674.CrossrefGoogle Scholar

  • Tian, X.L., Y.Z. Huo, L.P. Chen, J.H. He, J.J. Zhang, R. Jia, H. Liu, J.H. Wang, R. Xu, J.Q. Yang, X. Hu, J.M. Fang, J.H. Ma and P.M. He. 2011. Molecular detection and analysis of green seaweeds from Rudong coasts in Jiangsu Province. Chinese Sci Bull 56: 309−317 (in Chinese language, with English abstract).Google Scholar

  • Togashi, T. and P.A. Cox. 2001. Tidal-linked synchrony of gamete release in the marine green alga, Monostroma angicava Kjellman. J. Exp. Mar. Biol. Ecol. 264: 117–131.CrossrefGoogle Scholar

  • Tokuyasu, K.T. 1973. A technique for ultracryotomy of cell suspensions and tissues. J. Cell. Biol. 57: 551–565.CrossrefGoogle Scholar

  • Vesty, E.F., R.W. Kessler, T. Wichard and J.C. Coates. 2015. Regulation of gametogenesis and zoosporogenesis in Ulva linza (Chlorophyta): comparison with Ulva mutabilis and potential for laboratory culture. Front. Plant Sci. 6: 15.Google Scholar

  • Wang, J.F., J. Peng, Y.L. Cui, L. Nan, M.Q. Wang, H.Z. Lin, P.M. He and S. Qin. 2010. Molecular analysis of green-tide-forming macroalgae in the Yellow Sea. Aquatic. Bot. 93: 25–31.CrossrefGoogle Scholar

  • Wang, Z.L., J. Xiao, S.L. Fan, Y. Li, X.Q. Liu and D.Y. Liu. 2015. Who made the world’s largest green tide in China?—an integrated study on the initiation and early development of the green tide in Yellow Sea. Limnol. Oceanogr. 60: 1105–1117.CrossrefGoogle Scholar

  • Wichard, T. and W. Oertel. 2010. Gametogenesis and gamete release of Ulva mutabilis and Ulva lactuca (Chlorophyta): regulatory effects and chemical characterization of the “swarming inhibitor”. J. Phycol. 46: 248–259.CrossrefGoogle Scholar

  • Xiao, J., Y. Li, W. Song, Z. Wang, M. Fu, R. Li, X. Zhang and M. Zhu. 2013. Discrimination of the common macroalgae (Ulva, and Blidingia) in coastal waters of Yellow Sea, northern China, based on restriction fragment-length polymorphism (RFLP) analysis. Harmful Algae 27: 130–137.CrossrefGoogle Scholar

  • Zhang, X.W., H.X. Wang and Y. Mao. 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: 173–180.CrossrefGoogle Scholar

  • Zhang, J., Y. Huo, K. Yu, Q. Chen, Q. He, W. Han, L. Chen, J. Cao, D. Shi and P. He. 2013. Growth characteristics and reproductive capability of green tide algae in Rudong coast, China. J. Appl. Phycol. 25: 795–803.CrossrefGoogle Scholar

About the article

Yu Du

Yu Du is a graduate student which has been working in the lab of Professor Songdong Shen since 2016. His main research interests are species succession of green algae, the outbreak mechanism and prevention of green tide, and functional metabolism of Porphyra spp. in China.

Yuan Ao

Yuan Ao is a graduate student working in the lab of Professor Songdong Shen. His research subjects are identification of Ulva in molecular biology and genetic breeding of Pyropia vietnamensis.

Yuan He

Yuan He received a Master of Science degree from Soochow University, Jiangsu China in 2016. Since 2016, he has been studying for his doctorate in the lab of Professor Songdong Shen. He is mainly engaged in the study of molecular biology and taxonomy algae.

Songdong Shen

Songdong Shen is a phycology researcher mainly focusing on cell and molecular biology of Pyropia and of Ulva prolifera, which caused the largest green tides recently in China. He has studied reproductive diversity, growth factors, species identification and phylogeny in order to find the source and the cause.


aYu Du and Yuan Ao: These authors contributed equally to this work.


Received: 2018-12-18

Accepted: 2019-07-30

Published Online: 2019-08-21


Funding Source: National Key R & D Program of China

Award identifier / Grant number: 2016YFC1402102

Funding Source: Priority Academic Program Development of Jiangsu Higher Education Institutions and National Natural Science Foundation of China

Award identifier / Grant number: 41276134

This work was funded by National Key R & D Program of China (2016YFC1402102), Priority Academic Program Development of Jiangsu Higher Education Institutions and National Natural Science Foundation of China (Funder Id: http://dx.doi.org/10.13039/501100001809, project no. 41276134). We also thank Bohong Gu, the manager of Jiangsu Oriental Seaweed Processing Factory for providing attached Ulva spp. every once or twice a month.


Citation Information: Botanica Marina, 20180115, ISSN (Online) 1437-4323, ISSN (Print) 0006-8055, DOI: https://doi.org/10.1515/bot-2018-0115.

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