Two-stage reproduction derived from cells of thallus could directly contribute to seeds for green tidal algal Enteromorpha(Ulva) prolifera/clathrata bloom, with disclosure of their ephemeral trait

Bingxin Huang Lanping Ding Yao Zhang Youxuan Guo Junxia Liang Yanqi Xie Yue Chu

Bingxin Huang, Lanping Ding, Yao Zhang, Youxuan Guo, Junxia Liang, Yanqi Xie, Yue Chu. Two-stage reproduction derived from cells of thallus could directly contribute to seeds for green tidal algal Enteromorpha(Ulva) prolifera/clathrata bloom, with disclosure of their ephemeral trait[J]. Acta Oceanologica Sinica, 2023, 42(9): 101-112. doi: 10.1007/s13131-023-2158-x
Citation: Bingxin Huang, Lanping Ding, Yao Zhang, Youxuan Guo, Junxia Liang, Yanqi Xie, Yue Chu. Two-stage reproduction derived from cells of thallus could directly contribute to seeds for green tidal algal Enteromorpha(Ulva) prolifera/clathrata bloom, with disclosure of their ephemeral trait[J]. Acta Oceanologica Sinica, 2023, 42(9): 101-112. doi: 10.1007/s13131-023-2158-x

doi: 10.1007/s13131-023-2158-x

Two-stage reproduction derived from cells of thallus could directly contribute to seeds for green tidal algal Enteromorpha(Ulva) prolifera/clathrata bloom, with disclosure of their ephemeral trait

Funds: The National Natural Science Foundation of China under contract Nos 31970216 and 31670199.
More Information
    Corresponding author: E-mail:
  • 11Ding Lanping, International Symposium of Advanced Research on Green Tides, May 09–11, 2014, Shanghai, China.
    • 关键词:
    •  / 
    •  / 
    •  / 
    •  / 
    •  / 
    •  / 
    11Ding Lanping, International Symposium of Advanced Research on Green Tides, May 09–11, 2014, Shanghai, China.
  • Figure  1.  The somatic cells development process of Enteromorpha clathrata shows the juvenile to maturity in turn.

    Figure  2.  Reproductive cells born and germinate into the seawater under the semi-drying condition (a); the reproductive cells germinated in the adult parent thalli or their remnant (b).

    Figure  3.  Cell reproduction of infantile Enteromorpha prolifera under room temperature. a. The indoor culture tank of infantile E. prolifera. b. The seedlings of E. prolifera (the thallus, short arrow shows the basal rhizoid). c. The part of the seedling unformed reproductive cells, and the reproductive cells formed near the base of the seedlings and remnants of cell walls after released.

    Figure  4.  Adolescent Enteromorpha prolifera with reproductive cells formed and released at 22℃. a. Adolescent thalli (short arrow show the formation and release of reproductive cells at first-order branches); b. Base of the adolescent thalli (short arrows show the holdfast);c. Near the base of the adolescent thalli; d1–2. Branch cells of the adolescent thalli (d2 shows magnification image); e1–7. Formation of branches and their type and morphology released reproductive cells; f1–6. Reproductive cells released by the branched of adolescent thalli (magnification image, short arrows showed the ostiole releasing the reproductive cells) (scale bar: a. 1 mm; b. 100 μm; c. 100 μm; d1. 50 μm; d2. 20 μm; e1–7. 50 μm; f1–6. 20 μm) .

    Figure  5.  Reproductive cells formed and released by the filamentous thallus of adolescent Enteromorpha prolifera at 25℃. a. Reproductive cells formed from the upper cells of the filamentous thallus and their remnants after released. b. Reproductive cells are releasing from some branches.

    Figure  6.  Seasonal variation of water temperature in the western part of the South Yellow Sea (Hu, 2013).

    Figure  7.  Juvenile Enteromorpha prolifera at the intertidal mudflat of Xiangshan County, Ningbo City, Zhejiang Province.

  • Clayton M N. 1992. Propagules of marine macroalgae: structure and development. British Phycological Journal, 27(3): 219–232. doi: 10.1080/00071619200650231
    Cui Jianjun, Zhang Jianheng, Huo Yuanzi, et al. 2015. Adaptability of free-floating green tide algae in the Yellow Sea to variable temperature and light intensity. Marine Pollution Bulletin, 101(2): 660–666. doi: 10.1016/j.marpolbul.2015.10.033
    Deng Yunyan, Tang Xiaorong, Huang Bingxin, et al. 2011. The temperature character of marine green alga, Chaetomorpha valida, with analysis of its diffusion potential in marine algal flora of China. Oceanologia et Limnologia Sinica (in Chinese), 42(3): 404–408
    Ding Lanping. 2013. Flora Algarum Marinarum Sinicarum: Tomus IV Chlorophyta: No. I Ulotrichales, Chaetophorales, Phaeophilales, Ulvales, Prasiolales, Cladophorales, Acrosiphoniales (in Chinese). Beijing: Science Press
    Ding Lanping. 2022. Species diversity of genus Entermorpha in coastal China with the legitimacy evaluation on the scientific name of E. prolifera as the main origin ones of green tides in the Yellow Sea (in Chinese). Life World, (3): 30–33
    Ding Lanping, Fei Xiugeng, Lu Qinqin, et al. 2009. The Possibility analysis of habitats, origin and reappearance of bloom green alga (Enteromorpha prolifera) on inshore of western Yellow Sea. Chinese Journal of Oceanology and Limnology, 27(3): 421–424. doi: 10.1007/s00343-009-9277-x
    Ding Lanping, Luan Rixiao. 2009. The taxonomy, habit, and distribution of a green alga Enteromorpha prolifera (Ulvales, Chlorophyta). Oceanologia et Limnologia Sinica (in Chinese), 40(1): 68–71
    Ding Lanping, Teng Linhong, Lu Qinqin, et al. 2014. The morphological comparison, variation and molecular analysis between two green tidal algae Enteromorpha prolifera and E. clathrata from China. Algological Studies, 145–146: 27–38
    Fang Song, Wang Zongling, Li Yan, et al. 2012. The dynamics of micro-propagules before the green tide (Ulva prolifera) outbreak in the Southern Huanghai Sea and Changjiang (Yangtze) River Estuary area. Haiyang Xuebao (in Chinese), 34(4): 147–154
    Feng Zihui, Meng Yang, Lu Wei, et al. 2012. Studies on photosynthesis carbon fixation and ocean acidification prevention in Ulva prolifera I. Rate of photosynthesis carbon fixation and seawater pH increase. Haiyang Xuebao (in Chinese), 34(2): 162–168
    Gao Shan, Chen Xiaoyuan, Yi Qianqian, et al. 2010. A strategy for the proliferation of Ulva prolifera, main causative species of green tides, with formation of sporangia by fragmentation. PLoS ONE, 5(1): e8571. doi: 10.1371/journal.pone.0008571
    Gordon R, Brawley S H. 2004. Effects of water motion on propagule release from algae with complex life histories. Marine Biology, 145(1): 21–29
    Han Hongbin, Li Yan, Ma Xiaojun, et al. 2022. Factors influencing the spatial and temporal distributions of green algae micro-propagules in the coastal waters of Jinmenghaiwan, Qinhuangdao, China. Marine Pollution Bulletin, 175: 113328. doi: 10.1016/j.marpolbul.2022.113328
    Han Hongbin, Song Wei, Wang Zongling, et al. 2019. Distribution of green algae micro-propagules and their function in the formation of the green tides in the coast of Qinhuangdao, the Bohai Sea, China. Acta Oceanologica Sinica, 38(8): 72–77. doi: 10.1007/s13131-018-1278-1
    Han Hongbin, Wei Zhangliang, Huo Yuanzi, et al. 2015. Effects of temperature and light intensity on the release and germination of Ulva prolifera spores/gametes. Marine Fisheries (in Chinese), 37(6): 517–524
    Hayden H S, Blomster J, Maggs C A, et al. 2003. Linnaeus was right all along: Ulva and Enteromorpha are not distinct genera. European Journal of Phycology, 38(3): 277–294. doi: 10.1080/1364253031000136321
    He Peimin, Zhang Jianheng, Huo Yuanzi, et al. 2019. Green Tides of China (in Chinese). Beijing: Science Press
    Hiraoka M, Dan A, Shimada S, et al. 2003. Different life histories of Enteromorpha prolifera (Ulvales, Chlorophyta) from four rivers on Shikoku Island, Japan. Phycologia, 42(3): 275–284. doi: 10.2216/i0031-8884-42-3-275.1
    Hoffmann A J. 1987. The arrival of seaweed propagules at the shore: a review. Botanica Marina, 30(2): 151–166. doi: 10.1515/botm.1987.30.2.151
    Hu Yingying. 2013. Seasonal and interannual variations of the water temperature in the Yellow Sea and East China Sea (in Chinese)[dissertation]. Qingdao: Ocean University of China
    Huang Zhiyuan, Zhong Zheke, Zhang Xiaoping, et al. 2021. Formation mechanism and regulation measures of on-year and off-year of Moso Bamboo forest: a review. World Forestry Research (in Chinese), 34(5): 20–25
    Huo Yuanzi, Han Hongbin, Hua Liang, et al. 2016. Tracing the origin of green macroalgal blooms based on the large scale spatio-temporal distribution of Ulva microscopic propagules and settled mature Ulva vegetative thalli in coastal regions of the Yellow Sea, China. Harmful Algae, 59: 91–99. doi: 10.1016/j.hal.2016.09.005
    Jiang Hongxia, Ni Xue, Hu Baoyun, et al. 2015. Physiological characteristics of floating Enteromorpha prolifera in the Yellow Sea. Jiangsu Agricultural Sciences (in Chinese), 43(2): 355–357
    Kamermans P, Malta E, Verschuure J M, et al. 1998. Role of cold resistance and burial for winter survival and spring initiation of an Ulva spp. (Chlorophyta) bloom in a eutrophic lagoon (Veerse Meer Lagoon, The Netherlands). Marine Biology, 131(1): 45–51. doi: 10.1007/s002270050295
    Li Xinshu, Xu Juntian, Yao Dongrui, et al. 2013. Effects of nitrogen and phosphorus on the growth, photosynthesis and pigments of Ulva prolifera. Journal of Fisheries of China (in Chinese), 37(8): 1206–1212. doi: 10.3724/SP.J.1231.2013.38319
    Lin Apeng, Wang Chao, Qiao Hongjin, et al. 2009. Study on the photosynthetic performances of Enteromorpha prolifera collected from the surface and bottom of the sea of Qingdao sea area. Chinese Science Bulletin, 54(3): 399–404
    Liu Feng, Pang Shaojun, Chopin T, et al. 2013. Understanding the recurrent large-scale green tide in the Yellow Sea: temporal and spatial correlations between multiple geographical, aquacultural and biological factors. Marine Environmental Research, 83: 38–47. doi: 10.1016/j.marenvres.2012.10.007
    Liu Feng, Pang Shaojun, Shan Tifeng, et al. 2010. A novel method to quantify the microscopic stages of Ulva species in seawater and its applications in forcasting green tides of the Yellow Sea. Chinese Science Bulletin (in Chinese), 55(6): 468–473
    Liu Feng, Pang Shaojun, Zhao Xiaobo, et al. 2012. Quantitative, molecular and growth analyses of Ulva microscopic propagules in the coastal sediment of Jiangsu Province where green tides initially occurred. Marine Environmental Research, 74: 56–63. doi: 10.1016/j.marenvres.2011.12.004
    Liu Xiangqing, Wang Zongling, Li Yan, et al. 2015. Effects of temperature on the germination of green algal micro-propagules in the sediment. Advances in Marine Science (in Chinese), 33(2): 219–226
    Lotze H K, Schramm W, Schories D, et al. 1999. Control of macroalgal blooms at early developmental stages: Pilayella littoralis versus Enteromorpha spp. Oecologia, 119(1): 46–54. doi: 10.1007/s004420050759
    Ma Wenfei, Li Jingyu. 2022. Analysis of the underlying mechanisms of green tide with a perspective of algae ecophysiology. Chinese Journal of Applied Ecology (in Chinese), 33(5): 1420–1428
    Ma Jiahai, Zhang Liming, Ji Chuanli, et al. 1998. On the refrigerated nets of Porphyra yezoensis and quality analysis of produce. Journal of Fisheries of China (in Chinese), 22(S1): 65–71
    Miao Xiaoxiang, Xiao Jie, Pang Min, et al. 2018. Effect of the large-scale green tide on the species succession of green macroalgal micro-propagules in the coastal waters of Qingdao, China. Marine Pollution Bulletin, 126: 549–556. doi: 10.1016/j.marpolbul.2017.09.060
    Miao Xiaoxiang, Xiao Jie, Wang Zongling, et al. 2020. Study on the tempo-spatial distribution of green macroalgal micro-propagules along the coasts of Jiangsu and Shandong Provinces. Haiyang Xuebao (in Chinese), 42(2): 115–123
    Santelices B, Hoffmann A J, Aedo D, et al. 1995. A bank of microscopic forms on disturbed boulders and stones in tide pools. Marine Ecology Progress Series, 129(1–3): 215–228
    Shen Songdong. 2022. Brief introduction of micropropagule. Oceanologia et Limnologia Sinica (in Chinese), 53(1): 1–7
    Song Wei, Peng Keqin, Xiao Jie, et al. 2015. Effects of temperature on the germination of green algae micro-propagules in coastal waters of the Subei Shoal, China. Estuarine, Coastal and Shelf Science, 163: 63–68
    Taiz L, Zeiger E, Møller I M, et al. 2015. Plant Physiology and Development. 6th ed. Sunderland: Sinauer Associates
    Togashi T, Cox P A. 2001. Tidal-linked synchrony of gamete release in the marine green alga, Monostroma angicava Kjellman. Journal of Experimental Marine Biology and Ecology, 264(2): 117–131
    Wang Hui. 2017. Photosynthetic changes and response towards signaling molecule nitric oxide during the sporulation of Ulva prolifera (in Chinese)[dissertation]. Qingdao: Institute of Oceanology, Chinese Academy of Sciences
    Wang Hui, Lin Apeng, Gu Wenhui, et al. 2016. The sporulation of the green alga Ulva prolifera is controlled by changes in photosynthetic electron transport chain. Scientific Reports, 6: 24923. doi: 10.1038/srep24923
    Wang Xiaokun, Ma Jiahai, Ye Daocai, et al. 2007a. Preliminary study on the life history of Enteromorpha prolifera. Marine Science Bulletin (in Chinese), 26(5): 112–116
    Wang Guangce, Wang Hui, Gao Shan, et al. 2020. Study on the biological mechanism of green tide. Oceanologia et Limnologia Sinica (in Chinese), 51(4): 789–808
    Wang Xiangyu, Wu Haiyi. 2015. Nutrient uptaking and growth performance of Ulva prolifera. Journal of Guangxi Academy of Sciences (in Chinese), 31(4): 243–246, 252
    Wang Jianwei, Yan Binlun, Lin Apeng, et al. 2007b. Ecological factor research on the growth and induction of spores release in Enteromorpha prolifera (chlorophyta). Marine Science Bulletin (in Chinese), 26(2): 60–65
    Worm B, Lotze H K, Sommer U. 2001. Algal propagule banks modify competition, consumer and resource control on Baltic rocky shores. Oecologia, 128(2): 281–293. doi: 10.1007/s004420100648
    Wu Hailong, Gao Guang, Zhong Zhihai, et al. 2018. Physiological acclimation of the green tidal alga Ulva prolifera to a fast-changing environment. Marine Environmental Research, 137: 1–7. doi: 10.1016/j.marenvres.2018.02.018
    Xia Bin, Ma Shaosai, Cui Yi, et al. 2009. Distribution of temperature, salinity, dissolved oxygen, nutrients and their relationships with green tide in Enteromorpha prolifera outbreak area of the Yellow Sea. Progress in Fishery Sciences (in Chinese), 30(5): 94–101
    Xie Yanqi. 2013. The bioecological mechanism on green tidal blooming of Enteromorpha species (in Chinese)[dissertation]. Shantou: Shantou University
    Yang Jing, Zhang Si, Liu Guimei. 2017. Variability analysis of the Green Tide based on satellite remote sensing monitoring data from 2011 to 2016 in the Yellow Sea. Marine Forecasts (in Chinese), 34(3): 56–61
    Ye Naihao, Zhang Xiaowen, Mao Yuze, et al. 2008. Life history of Enteromorpha prolifera under laboratory conditions. Journal of Fishery Sciences of China (in Chinese), 15(5): 853–859
    Zhang Xiaowen, Wang Hongxia, Mao Yuze, et al. 2010. Somatic cells serve as a potential propagule bank of Enteromorpha prolifera forming a green tide in the Yellow Sea, China. Journal of Applied Phycology, 22(2): 173–180. doi: 10.1007/s10811-009-9437-6
    Zhang Xiaowen, Xu Dong, Mao Yuze, et al. 2011. Settlement of vegetative fragments of Ulva prolifera confirmed as an important seed source for succession of a large-scale green tide bloom. Limnology and Oceanography, 56(1): 233–242. doi: 10.4319/lo.2011.56.1.0233
    Zhang Yao, Yan Jing, Huang Bingxin, et al. 2023. The epiphytic macroalgae on red alga Gelidium amansii from Qinhuangdao area, Bohai Sea in autumn based on thermostatic incubation experiments. Oceanologia et Limnologia Sinica (in Chinese), 54(2): 493–451
    Zhao Xiaohui, Cui Jianjun, Zhang Jianheng, et al. 2019. Reproductive strategy of the floating alga Ulva prolifera in blooms in the Yellow Sea based on a combination of zoid and chromosome analysis. Marine Pollution Bulletin, 146: 584–590. doi: 10.1016/j.marpolbul.2019.07.018
    Zou Dinghui, Xia Jianrong. 2004. Studies progresses of sexual reproductive ecology in seaweeds. Acta Ecologica Sinica (in Chinese), 24(12): 2870–2877
  • 加载中
  • 文章访问数:  103
  • HTML全文浏览量:  49
  • PDF下载量:  7
  • 被引次数: 0
  • 收稿日期:  2022-07-05
  • 录用日期:  2022-11-02
  • 网络出版日期:  2023-09-13
  • 刊出日期:  2023-09-01