Morphological discrimination of fouling Ulva and Blidingia species on Pyropia rafts in Rudong, China: an in-field protocol for early monitoring of algae forming the Yellow Sea green tide

Yingying Ma; Jin Zhao; Fanzhou Kong; Tian Yan; Peng Jiang

doi:10.1515/bot-2023-0077

Article

Morphological discrimination of fouling Ulva and Blidingia species on Pyropia rafts in Rudong, China: an in-field protocol for early monitoring of algae forming the Yellow Sea green tide

Yingying Ma

Yingying Ma was a graduate student in the Institute of Oceanology, Chinese Academy of Sciences. Her research interest is morphological and molecular identification of the Ulva species.
, Jin Zhao

Jin Zhao is an associate professor in the Institute of Oceanology, Chinese Academy of Sciences. She is engaged in studying the genetic composition, formation mechanism and dynamic process of macroalgal blooms, including green tides and golden tides, in China.
, Fanzhou Kong

Fanzhou Kong acquired his PhD in Environmental Science from Institute of Oceanography, Chinese Academy of Sciences, and now is an associate professor. His interests are in phytoplankton pigments, harmful algal bloom species and community ecology, macroalgal bloom biomass and distribution.
, Tian Yan

Tian Yan is a senior scientist at Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences. She is engaged in studying harmful algal blooms including red tides, green tides and golden tides in China, and especially in the ecotoxicology field.
and Peng Jiang

Peng Jiang is a professor in the Institute of Oceanology, Chinese Academy of Sciences. His research interests are in biological mechanisms of harmful macroalgal blooms, genetics and metabolic engineering of marine algae.

Published/Copyright: September 17, 2024

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From the journal Botanica Marina Volume 68 Issue 1

Abstract

Fouling seaweeds on nori cultivation rafts in Subei radial sand ridges (Jiangsu, China) are believed to be the source of the Yellow Sea green tide (YSGT). Although major species are consistent across years, their biomass and proportions undergo significant annual changes, which was speculated to be related to the size of YSGT. Therefore, early detection and biomass assessment of the bloom-forming algae are crucial, increasing the need to develop a morphological identification method suitable for large sample sizes in the field. In this study, fouling seaweeds were collected from this area in spring 2017. Five major species, Ulva aragoënsis, Ulva compressa, Ulva linza, Ulva prolifera, and Blidingia sp. were molecularly identified, and confirmed as the predominant fouling seaweeds on nori rafts over the past decade. In this unique ecological niche, the morphological features of species changed significantly yet stably. Based on morphological observations, an identification key for these five species was established. Furthermore, a simplified version containing only two indices was developed for practical field use, with an average accuracy of 81 % (δ² = 0.003) in empirical accuracy assessments. This method can be used to monitor the community structure and succession of fouling seaweeds at the geographical source of YSGT.

Keywords: green tide; morphological identification; Pyropia raft; the Yellow Sea; Ulva

Corresponding author: Peng Jiang, CAS and Shandong Province Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China; and Laboratory for Marine Biology and Biotechnology, Qingdao Marine Science and Technology Center, Qingdao, China, E-mail: jiangpeng@qdio.ac.cn

Yingying Ma and Jin Zhao contributed equally to this work.

Funding source: Natural Science Foundation of Qingdao City

Award Identifier / Grant number: 23-2-1-172-zyyd-jch

Funding source: Science & Technology Basic Resources Investigation Program of China

Award Identifier / Grant number: 2018FY100205

Funding source: National Natural Science Foundation of China

Award Identifier / Grant number: 41776153

Funding source: Strategic Priority Research Program of the Chinese Academy of Sciences

Award Identifier / Grant number: XDB42030302

Funding source: Nantong Municipal Science and Technology Project

Award Identifier / Grant number: MS2023011

About the authors

Yingying Ma

Yingying Ma was a graduate student in the Institute of Oceanology, Chinese Academy of Sciences. Her research interest is morphological and molecular identification of the Ulva species.

Jin Zhao

Jin Zhao is an associate professor in the Institute of Oceanology, Chinese Academy of Sciences. She is engaged in studying the genetic composition, formation mechanism and dynamic process of macroalgal blooms, including green tides and golden tides, in China.

Fanzhou Kong

Fanzhou Kong acquired his PhD in Environmental Science from Institute of Oceanography, Chinese Academy of Sciences, and now is an associate professor. His interests are in phytoplankton pigments, harmful algal bloom species and community ecology, macroalgal bloom biomass and distribution.

Tian Yan

Tian Yan is a senior scientist at Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences. She is engaged in studying harmful algal blooms including red tides, green tides and golden tides in China, and especially in the ecotoxicology field.

Peng Jiang

Peng Jiang is a professor in the Institute of Oceanology, Chinese Academy of Sciences. His research interests are in biological mechanisms of harmful macroalgal blooms, genetics and metabolic engineering of marine algae.

Research ethics: Not applicable.
Author contributions: The authors have accepted responsibility for the entire content of this manuscript and approved its submission.
Competing interests: The authors state no conflict of interest.
Research funding: This work was supported by the Natural Science Foundation of Qingdao City (23-2-1-172-zyyd-jch), Strategic Priority Research Program of the Chinese Academy of Sciences (XDB42030302), Nantong Municipal Science and Technology Project (MS2023011), Science & Technology Basic Resources Investigation Program of China (2018FY100205), and National Natural Science Foundation of China (41776153).
Data availability: The raw data can be obtained on request from the corresponding author.

References

Blomster, J., Maggs, C.A., and Stanhope, M.J. (1998). Molecular and morphological analysis of Enteromorpha intestinalis and E. compressa (Chlorophyta) in the British iIsles. J. Phycol. 34: 319–340, https://doi.org/10.1046/j.1529-8817.1998.340319.x.Search in Google Scholar

Blomster, J., Bäck, S., Fewer, D.P., Kiirikki, M., Lehvo, A., Maggs, C.A., and Stanhope, M. (2002). Novel morphology in Enteromorpha (Ulvophyceae) forming green tides. Am. J. Bot. 89: 1756–1763, https://doi.org/10.3732/ajb.89.11.1756.Search in Google Scholar PubMed

Du, Y., Ao, Y., He, Y., Yin, Y., Ma, Y.F., Yuan, A.X., and Shen, S.D. (2019). 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. Bot. Marina 62: 549–561, https://doi.org/10.1515/bot-2018-0115.Search in Google Scholar

Duan, W.J., Guo, L.X., Sun, D., Zhu, S.F., Chen, X.F., Zhu, W.R., Xu, T., and Chen, C.F. (2012). 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, https://doi.org/10.1007/s10811-011-9654-7.Search in Google Scholar

Fan, S.L., Fu, M.Z., Wang, Z.L., Zhang, X.L., Song, W., Li, Y., Liu, G.X., Shi, X.Y., Wang, X.M., and Zhu, M.Y. (2015). Temporal variation of green macroalgal assemblage on Porphyra aquaculture rafts in the Subei Shoal, China. Estuar. Coast. Shelf Sci. 163: 23–28, https://doi.org/10.1016/j.ecss.2015.03.016.Search in Google Scholar

Fletcher, R.L. (1996). The occurrence of “green tides”- a review. In: Schramm, W., and Nienhuis, P.H. (Eds.), Marine benthic vegetation: recent changes and the effects of eutrophication. Springer, Berlin, pp. 7–43.Search in Google Scholar

Han, W., Chen, L.P., Zhang, J.H., Tian, X.L., Hua, L., He, Q., Huo, Y.Z., Yu, K.F., Shi, D.J., Ma, J.H., et al.. (2013). Seasonal variation of dominant free-floating and attached Ulva species in Rudong coastal area, China. Harmful Algae 28: 46–54, https://doi.org/10.1016/j.hal.2013.05.018.Search in Google Scholar

Hiraoka, M., Ichihara, K., Zhu, W.R., Shimada, S., Oka, N., Cui, J.J., Tsubaki, S., and He, P.M. (2017). Examination of species delimitation of ambiguous DNA-based Ulva (Ulvophyceae, Chlorophyta) clades by culturing and hybridisation. Phycologia 56: 517–532, https://doi.org/10.2216/16-109.1.Search in Google Scholar

Hu, C.M., Li, D.Q., Chen, C.S., Ge, J.Z., Muller-Karger, F.E., Liu, J.P., Yu, F., and He, M.X. (2010). On the recurrent Ulva prolifera blooms in the Yellow Sea and East China Sea. J. Geophys. Res. 115: C05017, https://doi.org/10.1029/2009jc005561.Search in Google Scholar

Hughey, J.R., Millerb, K.A., and Gabrielson, P.W. (2018). Mitogenome analysis of a green tide forming Ulva from California, USA confirms its identity as Ulva expansa (Ulvaceae, Chlorophyta). Mitochondrial DNA Part B 3: 1302–1303, https://doi.org/10.1080/23802359.2018.1535859.Search in Google Scholar PubMed PubMed Central

Hughey, J.R., Maggs, C.A., Mineur, F., Jarvis, C., Miller, K.A., Shabaka, S.H., and Gabrielson, P.W. (2019). Genetic analysis of the Linnaean Ulva lactuca (Ulvales, Chlorophyta) holotype and related type specimens reveals name misapplications, unexpected origins, and new synonymies. J. Phycol. 55: 503–508, https://doi.org/10.1111/jpy.12860.Search in Google Scholar PubMed

Huo, Y.Z., Zhang, J.H., Chen, L.P., Hu, M., Yu, K.F., Chen, Q.F., He, Q., and He, P.M. (2013). Green algae blooms caused by Ulva prolifera in the southern Yellow Sea: iIdentification of the original bloom location and evaluation of biological processes occurring during the early northward floating period. Limnol. Oceanogr. 58: 2206–2218, https://doi.org/10.4319/lo.2013.58.6.2206.Search in Google Scholar

Huo, Y.Z., Hua, L., Wu, H.L., Zhang, J.H., Cui, J.J., Huang, X.W., Yu, K.F., Shi, H.H., He, P.M., and Ding, D.W. (2014). Abundance and distribution of Ulva microscopic propagules associated with a green tide in the southern coast of the Yellow Sea. Harmful Algae 39: 357–364, https://doi.org/10.1016/j.hal.2014.09.008.Search in Google Scholar

Huo, Y.Z., Han, H.B., Shi, H.H., Wu, H.L., Zhang, J.H., Yu, K.F., Xu, R., Liu, C.C., Zhang, Z.L., Liu, K.F., et al.. (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, https://doi.org/10.1016/j.marpolbul.2015.01.014.Search in Google Scholar PubMed

Huo, Y.Z., Han, H.B., Hua, L., Wei, Z.L., Yu, K.F., Shi, H.H., Kim, J.K., Yarish, C., and He, P.M. (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, https://doi.org/10.1016/j.hal.2016.09.005.Search in Google Scholar PubMed

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. Mar. Pollut. Bull. 62: 1169–1182, https://doi.org/10.1016/j.marpolbul.2011.03.040.Search in Google Scholar PubMed

Kirkendale, L., Saunders, G.W., and Winberg, P. (2013). A molecular survey of Ulva (Chlorophyta) in temperate Australia reveals enhanced levels of cosmopolitanism. J. Phycol. 49: 69–81, https://doi.org/10.1111/jpy.12016.Search in Google Scholar PubMed

Koeman, R.P.T. and Vandenhoek, C. (1981). The taxonomy of Ulva (Chlorophyceae) in Tthe Netherlands. British Phycol. J. 16: 9–53, https://doi.org/10.1080/00071618100650031.Search in Google Scholar

Krupnik, N., Rinkevich, B., Paz, G., Douek, J., Lewinsohn, E., Israel, A., Carmel, N., Mineur, F., and Maggs, C.A. (2018). Native, invasive and cryptogenic Ulva species from the Israeli Mediterranean Sea: risk and potential. Mediterr. Mar. Sci. 19: 132–146, https://doi.org/10.12681/mms.2104.Search in Google Scholar

Lee, J.H., Pang, I.C., Moon, I.J., and Ryu, J.H. (2011). On physical factors that controlled the massive green tide occurrence along the southern coast of the Shandong Peninsula in 2008: a numerical study using a particle-tracking experiment. J. Geophys. Res. 116: C12036, https://doi.org/10.1029/2011jc007512.Search in Google Scholar

Lee, S.H., Kang, P.J., and Nam, K.W. (2014). New record of two marine Ulvalean species (Chlorophyta) in Korea. J. Ecol. Environ. 37: 379–385, https://doi.org/10.5141/ecoenv.2014.039.Search in Google Scholar

Leskinen, E. and Pamilo, P. (1997). Evolution of the ITS sequences of ribosomal DNA in Enteromorpha (Chlorophyceae). Hereditas 126: 17–23, https://doi.org/10.1111/j.1601-5223.1997.00017.x.Search in Google Scholar PubMed

Li, Y., Xiao, J., Ding, L.P., Wang, Z.L., Song, W., Fang, S., Fan, S.L., Li, R.X., and Zhang, X.L. (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, https://doi.org/10.1007/s13131-015-0677-9.Search in Google Scholar

Lin, X.Y., Liu, W.Z., Wei, X., and Jiang, P. (2022). Complete chloroplast genome of an invasive marine macroalga Ulva californica (Ulvophyceae, Chlorophyta). Mitochondrial DNA Part B 7: 1337–1339, https://doi.org/10.1080/23802359.2022.2098854.Search in Google Scholar PubMed PubMed Central

Liu, D.Y., Keesing, J.K., Xing, Q.U., and Shi, P. (2009). World’s largest macroalgal bloom caused by expansion of seaweed aquaculture in China. Mar. Pollut. Bull. 58: 888–895, https://doi.org/10.1016/j.marpolbul.2009.01.013.Search in Google Scholar PubMed

Liu, D.Y., Keesing, J.K., Dong, Z.J., Zhen, Y., Di, B.P., Shi, Y.J., Fearns, P., and Shi, P. (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, https://doi.org/10.1016/j.marpolbul.2010.05.015.Search in Google Scholar PubMed

Liu, F., Pang, S.J., Chopin, T., Gao, S.Q., Shan, T.F., Zhao, X.B., and Li, J. (2013). Understanding the recurrent large-scale green tide in the Yellow Sea: temporal and spatial correlations between multiple geographical, aquacultural and biological factors. Mar. Environ. Res. 83: 38–47, https://doi.org/10.1016/j.marenvres.2012.10.007.Search in Google Scholar PubMed

Liu, X.Q., Wang, Z.L., Fan, S.L., Xiao, J., Li, Y., Zhang, X.L., Li, R.X., and Wang, X.N. (2016). The current situations of green macroalgae and micro-propagules in Pyropia aquaculture of the Subei Shoal in spring of 2013. Acta Oceanol. Sin. 35: 94–100, https://doi.org/10.1007/s13131-016-0879-9.Search in Google Scholar

Liu, F., Melton, J.T., Lopez-Bautista, J.M., and Chen, N.S. (2020). Multiple intraspecific variations of mitochondrial genomes in the green-tide forming alga, Ulva compressa Linnaeus (Ulvophyceae, Chlorophyta). Front. Mar. Sci. 7: 714, https://doi.org/10.3389/fmars.2020.00714.Search in Google Scholar

Loughnane, C.J., McIvor, L.M., Rindi, F., Stengel, D.B., and Guiry, M.D. (2008). Morphology, rbcL phylogeny and distribution of distromatic Ulva (Ulvophyceae, Chlorophyta) in Ireland and southern Britain. Phycologia 47: 416–429, https://doi.org/10.2216/ph07-61.1.Search in Google Scholar

Ma, Y.Y., Zhao, J., Xie, W.F., and Jiang, P. (2020). Branching phenotype and plasticity in floating ecotype of Ulva prolifera (Ulvophyceae, Chlorophyta). Mar. Sci. 44: 98–105, (In Chinese with English abstract).Search in Google Scholar

Miao, X.X., Xiao, J., Pang, M., Zhang, X.L., Wang, Z.L., Miao, J.W., and Li, Y. (2018). 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, https://doi.org/10.1016/j.marpolbul.2017.09.060.Search in Google Scholar PubMed

Phillips, J.A. and Clayton, M.N. (1983). Morphology and development in culture of Enteromorpha linza (L.) J. Agardh, (Ulvaceae, Chlorophyta), a common marine alga of southern Australia. Aust. J. Bot. 31: 11–18, https://doi.org/10.1071/bt9830011.Search in Google Scholar

Shen, Q., Li, H.Y., Li, Y., Wang, Z.L., Liu, J.S., and Yang, W.D. (2012). Molecular identification of green algae from the rafts based infrastructure of Porphyra yezoensis. Mar. Pollut. Bull. 64: 2077–2082, https://doi.org/10.1016/j.marpolbul.2012.07.021.Search in Google Scholar PubMed

Shimada, S., Hiraoka, M., Nabata, S., Iima, M., and 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: 99–108, https://doi.org/10.1046/j.1440-1835.2003.00296.x.Search in Google Scholar

Shimada, S., Yokoyama, N., Arai, S., and Hiraoka, M. (2008). Phylogeography of the genus Ulva (Ulvophyceae, Chlorophyta), with special reference to the Japanese freshwater and brackish taxa. J. Appl. Phycol. 20: 979–989, https://doi.org/10.1007/s10811-007-9296-y.Search in Google Scholar

Smetacek, V. and Zingone, A. (2013). Green and golden seaweed tides on the rise. Nature 504: 84–88, https://doi.org/10.1038/nature12860.Search in Google Scholar PubMed

Song, W., Jiang, M.J., Wang, Z.L., Wang, H.P., Zhang, X.L., and Fu, M.Z. (2018). Source of propagules of the fouling green macroalgae in the Subei Shoal, China. Acta Oceanol. Sin. 37: 102–108, https://doi.org/10.1007/s13131-018-1169-5.Search in Google Scholar

Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis Version 6.0. Mol. Biol. Evol. 30: 2725–2729, https://doi.org/10.1093/molbev/mst197.Search in Google Scholar PubMed PubMed Central

Tanner, C.E. (1986). Investigations of the taxonomy and morphological variation of Ulva (Chlorophyta): Ulva californica. Phycologia 25: 510–520, https://doi.org/10.2216/i0031-8884-25-4-510.1.Search in Google Scholar

Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25: 4876–4882, https://doi.org/10.1093/nar/25.24.4876.Search in Google Scholar PubMed PubMed Central

Tian, X.L., Huo, Y.Z., Chen, L.P., He, J.H., Zhang, J.H., Jia, R., Liu, H., Wang, J.H., Xu, R., Yang, J.Q., et al.. (2011). Molecular detection and analysis of green seaweeds from Rudong coasts in Jiangsu Province. Chin. Sci. Bull. 56: 309–317, (In Chinese with English Abstract), https://doi.org/10.1360/972010-2124.Search in Google Scholar

Tong, Y.C., Xia, L.H., Liu, J.L., Zhao, S., Sun, Y.Q., Wu, T.J., Xia, Z.Y., Li, S., Cao, J.X., and Zhang, J.H. (2022). Distribution and identification of Ulva aragoënsis (Ulvaceae, Chlorophyta), a constituent species of green tides in the Southern Yellow Sea, based on molecular data. J. Mar. Sci. Eng. 10: 1767, https://doi.org/10.3390/jmse10111767.Search in Google Scholar

Wang, Z.L., Xiao, J., Fan, S.L., Li, Y., Liu, X.Q., and Liu, D.Y. (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, https://doi.org/10.1002/lno.10083.Search in Google Scholar

Wei, X., Liu, W., Liu, W.Z., Lin, X.Y., Liu, Q.C., and Jiang, P. (2022). First record of Ulva californica in mainland China: a single alien parthenogenetic population with discontinuous distribution. J. Oceanol. Limnol. 40: 2343–2353, https://doi.org/10.1007/s00343-022-1392-y.Search in Google Scholar

Xiao, J., Li, Y., Song, W., Wang, Z.L., Fu, M.Z., Li, R.X., Zhang, X.L., and Zhu, M.Y. (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, https://doi.org/10.1016/j.hal.2013.05.003.Search in Google Scholar

Xiao, J., Wang, Z.L., Liu, D.Y., Fu, M.Z., Yuan, C., and Yan, T. (2021). Harmful macroalgal blooms (HMBs) in China’s coastal water: green and golden tides. Harmful Algae 107, https://doi.org/10.1016/j.hal.2021.102061.Search in Google Scholar PubMed

Xie, W.F., Wu, C.H., Zhao, J., Lin, X.Y., and Jiang, P. (2020). New records of Ulva spp. (Ulvophyceae, Chlorophyta) in China, with special reference to an unusual morphology of U. meridionalis forming green tides. Eur. J. Phycol. 55: 412–425, https://doi.org/10.1080/09670262.2020.1740946.Search in Google Scholar

Xing, Q.G., An, D.Y., Zheng, X.Y., Wen, Z.N., Wang, X.H., Li, L., Tian, L.Q., and Chen, J. (2019). Monitoring seaweed aquaculture in the Yellow Sea with multiple sensors for managing the disaster of macroalgal blooms. Remote Sens. Environ. 231: 111279, https://doi.org/10.1016/j.rse.2019.111279.Search in Google Scholar

Zhang, X.W., Xu, D., Mao, Y.Z., Li, Y.X., Xue, S.Y., Zou, J., Lian, W., Liang, C.W., Zhuang, Z.M., Wang, Q.Y., 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. Limnol. Oceanogr. 56: 233–242, https://doi.org/10.4319/lo.2011.56.1.0233.Search in Google Scholar

Zhang, J.H., Huo, Y.Z., Zhang, Z.L., Yu, K.F., He, Q., Zhang, L.H., Yang, L.L., Xu, R., and He, P.M. (2013). Variations of morphology and photosynthetic performances of Ulva prolifera during the whole green tide blooming process in the Yellow Sea. Mar. Environ. Res. 92: 35–42, https://doi.org/10.1016/j.marenvres.2013.08.009.Search in Google Scholar PubMed

Zhang, J.H., Huo, Y.Z., Wu, H.L., Yu, K.F., Kim, J.K., Yarish, C., Qin, Y.T., Liu, C.C., Xu, R., and He, P.M. (2014). The origin of the Ulva macroalgal blooms in the Yellow Sea in 2013. Mar. Pollut. Bull. 89: 276–283, https://doi.org/10.1016/j.marpolbul.2014.09.049.Search in Google Scholar PubMed

Zhang, J.H., Zhao, P., Huo, Y.Z., Yu, K.F., and He, P.M. (2017). The fast expansion of Pyropia aquaculture in “Sansha” regions should be mainly responsible for the Ulva blooms in Yellow Sea. Estuar. Coast. Shelf Sci. 189: 58–65, https://doi.org/10.1016/j.ecss.2017.03.011.Search in Google Scholar

Zhang, Q.C., Yu, R.C., Chen, Z.F., Qiu, L.M., Wang, Y.F., Kong, F.Z., Geng, H.X., Zhao, Y., Jiang, P., Yan, T., et al.. (2018). Genetic evidence in tracking the origin of Ulva prolifera blooms in the Yellow Sea, China. Harmful Algae 78: 86–94, https://doi.org/10.1016/j.hal.2018.08.002.Search in Google Scholar PubMed

Zhang, J.H., Shi, J.T., Gao, S., Huo, Y.Z., Cui, J.J., Shen, H., Liu, G.Y., and He, P.M. (2019). Annual patterns of macroalgal blooms in the Yellow Sea during 2007-2017. PLoS ONE 14: e0210460, https://doi.org/10.1371/journal.pone.0210460.Search in Google Scholar PubMed PubMed Central

Zhao, J., Jiang, P., Liu, Z.Y., Wei, W., Lin, H.Z., Li, F.C., Wang, J.F., and Qin, S. (2013). The Yellow Sea green tides from 2007 to 2011 were dominated by one species - Ulva (Enteromorpha) prolifera. Chin. Sci. Bull. 58: 2298–2302, https://doi.org/10.1007/s11434-012-5441-3.Search in Google Scholar

Zhao, J., Jiang, P., Qin, S., Liu, X.J., Liu, Z.Y., Lin, H.Z., Li, F.C., Chen, H.X., and Wu, C.H. (2015). Genetic analyses of floating Ulva prolifera in the Yellow Sea suggest a unique ecotype. Estuar. Coast. Shelf Sci. 163: 96–102, https://doi.org/10.1016/j.ecss.2015.05.027.Search in Google Scholar

Zhao, J., Jiang, P., Qiu, R., Ma, Y.Y., Wu, C.H., Fu, H.H., Chen, H., and Li, F. (2018). The Yellow Sea green tide: a risk of macroalgae invasion. Harmful Algae 77: 11–17, https://doi.org/10.1016/j.hal.2018.05.007.Search in Google Scholar PubMed

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This article contains supplementary material (https://doi.org/10.1515/bot-2023-0077).

Received: 2023-08-31

Accepted: 2024-08-20

Published Online: 2024-09-17

Published in Print: 2025-02-25

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Keywords for this article

green tide; morphological identification; Pyropia raft; the Yellow Sea; Ulva