Cite this paper:
Xiaoqian LÜ, Hao XU, Sheng ZHAO, Fanzhou KONG, Tian YAN, Peng JIANG. The green tide in Yingkou, China in summer 2021 was caused by a subtropical alga—Ulva meridionalis (Ulvophyceae, Chlorophyta)[J]. Journal of Oceanology and Limnology, 2022, 40(6): 2354-2363

The green tide in Yingkou, China in summer 2021 was caused by a subtropical alga—Ulva meridionalis (Ulvophyceae, Chlorophyta)

Xiaoqian LÜ1,2,3, Hao XU1,2,3, Sheng ZHAO4, Fanzhou KONG5,6, Tian YAN5,6, Peng JIANG1,2
1 CAS and Shandong Province Key Laboratory of Experimental Marine Biology, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
2 Laboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology(Qingdao), Qingdao 266237, China;
3 University of Chinese Academy of Sciences, Beijing 100049, China;
4 North China Sea Environmental Monitoring Center, State Oceanic Administration, Qingdao 266033, China;
5 CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
6 Laboratory for Marine Ecology and Environmental Science, Pilot National Laboratory for Marine Science and Technology(Qingdao), Qingdao 266237, China
Abstract:
The large-scale green tide caused by Ulva has occurred successively in the Yellow Sea since 2007, and new events of green tide also continued to appear in nearby sea areas, indicating an undergoing rapid development of occurrence patterns for harmful macroalgal blooms (HMBs) along coastal China. In August 2021, a green tide occurred for the first time in Bayuquan sea area of Yingkou city, Liaoning Province in the Bohai Sea. In this study, morphological and molecular approaches were used to identify the causative species as U. meridionalis, an alien subtropical alga previously found to dominate green tides in the South China Sea. According to the hydrological data of Bayuquan in summer 2021, combined with morphological and developmental observations for this alga, we hypothesized that the disturbance caused by the typhoon In-Fa might have detached the local U. meridionalis from substrates, especially for those thalli with poorly developed holdfasts, and the ensuing wave-free period with unusually high temperature, which fell in the reported optimum growth temperature for U. meridionalis, might have provided the favorable conditions for the final bloom of the floating seaweeds. This is the first report on the bloom of subtropical U. meridionalis in the north temperate sea zone, indicating that the ecological risk of causing green tides in the future by this rapidly spreading species deserves high attention.
Key words:    Bohai Sea|green tide|holdfast|alien species|Ulva meridionalis|Yingkou   
Received: 2022-01-11   Revised:
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References:
Cui J J, Monotilla A P, Zhu W R et al. 2018. Taxonomic reassessment of Ulva prolifera (Ulvophyceae, Chlorophyta) based on specimens from the type locality and Yellow Sea green tides. Phycologia, 57(6): 692-704, https://doi.org/10.2216/17-139.1.
Department of Natural Resources of Liaoning Provincial. 2021a. The Department of Natural Resources of Liaoning Provincial issued a marine ecological warning to Bayuquan Sea for green tide. http://zrzy.ln.gov.cn/ywbb/gtkx/202108/t20210817_4231700.html. Accessed on 2021-10-30. (in Chinese)
Department of Natural Resources of Liaoning Provincial. 2021b. The green tide has basically subsided in Yingkou Bayuquan. http://zrzy.ln.gov.cn/ywbb/gtkx/202108/t20210823_4233587.html. Accessed on 2021-10-30.
Dong Z J, Liu D Y, Keesing J K. 2010. Jellyfish blooms in China: dominant species, causes and consequences.Marine Pollution Bulletin, 60(7): 954-963, https://doi.org/10.1016/j.marpolbul.2010.04.022.
Dou Y, Shang J P, Shao P et al. 2020. Frequency of red tides in Bohai Sea and the influence of environmental factors(2000-2016). Journal of Hydroecology, 41(6): 141-148, https://doi.org/10.15928/j.1674-3075.2020.06.017. (in Chinese with English abstract)
Duan L Q, Song J M, Li X G et al. 2010. Distribution of selenium and its relationship to the eco-environment in Bohai Bay seawater. Marine Chemistry, 121(1-4): 87-99, https://doi.org/10.1016/j.marchem.2010.03.007.
Fletcher R L. 1996. The occurrence of “Green tides” — a review. In: Schramm W, Nienhuis P H eds. Marine Benthic Vegetation: Recent Changes and the Effects of Eutrophication. Springer, Berlin Heidelberg. p.7-43, https://doi.org/10.1007/978-3-642-61398-2_2.
Geng H X, Yu R C, Zhang Q C et al. 2019. Tracing the settlement region of massive floating green algae in the Yellow Sea.Journal of Oceanology and Limnology, 37(5): 1555-1565, https://doi.org/10.1007/s00343-019-8348-x.
Hiraoka M, Enomoto S. 1998. The induction of reproductive cell formation of Ulva pertusa Kjellman (Ulvales, Ulvophyceae). Phycological Research, 46(3): 199-203, https://doi.org/10.1111/j.1440-1835.1998.tb00114.x.
Hiraoka M, Kinoshita Y, Higa M et al. 2020a. Fourfold daily growth rate in multicellular marine alga Ulva meridionalis. Scientific Reports, 10(1): 12606, https://doi.org/10.1038/s41598-020-69536-4.
Hiraoka M, Tanaka K, Yamasaki T et al. 2020b. Replacement of Ulva ohnoi in the type locality under rapid ocean warming in southwestern Japan. Journal of Applied Phycology, 32(4): 2489-2494, https://doi.org/10.1007/s10811-019-01974-8.
Hiraoka M. 2012. Intensive biomass production by green seaweed Ulva. Journal of the Japan Institute of Energy, 91: 1154-1160.
Hiraoka M. 2021. Massive Ulva green tides caused by inhibition of biomass allocation to sporulation. Plants, 10(11): 2482, https://doi.org/10.3390/plants10112482.
Horimoto R, Masakiyo Y, Ichihara K et al. 2011. Enteromorphalike Ulva (Ulvophyceae, Chlorophyta) growing in the Todoroki River, Ishigaki Island, Japan, with special reference to Ulva meridionalis Horimoto et Shimada, sp. nov. Bulletin of the National Museum of Nature and Science, 37(4): 155-167.
Jiang P, Wang J F, Cui Y L et al. 2008. Molecular phylogenetic analysis of attached Ulvaceae species and free-floating Enteromorpha from Qingdao coasts in 2007. Chinese Journal of Oceanology and Limnology, 26(3): 276-279, https://doi.org/10.1007/s00343-008-0276-0.
Jiang P, Zhao J. 2018. Identification of floating ecotype of Ulva prolifera: implication for the green tide in the Yellow Sea. Oceanologia et Limnologia Sinica, 49(5): 959-966, https://doi.org/10.11693/hyhz20180800199. (in Chinese with English abstract)
Leskinen E, Pamilo P. 1997. Evolution of the ITS sequences of ribosomal DNA in Enteromorpha (Chlorophyceae).Hereditas, 126(1): 17-23, https://doi.org/10.1111/j.1601-5223.1997.00017.x.
Li D X, Gao Z Q, Zheng X Y et al. 2020. Analysis of the interannual variation characteristics of the northernmost drift position of the green tide in the Yellow Sea. Environmental Science and Pollution Research, 27(28): 35137-35147, https://doi.org/10.1007/s11356-020-09730-z.
Liu D Y, Keesing J K, Xing Q G et al. 2009. World’s largest macroalgal bloom caused by expansion of seaweed aquaculture in China. Marine Pollution Bulletin, 58(6):888-895, https://doi.org/10.1016/j.marpolbul.2009.01.013.
Liu J L, Yang X Q, Cui J J et al. 2020. Complete chloroplast genome of Ulva meridionalis (Ulvales: Ulvaceae): an extremely fast-growing green macroalgae. Mitochondrial DNA Part B, 5(2): 1390-1392, https://doi.org/10.1080/23 802359.2020.1735967.
Liu Z Y, Liu H Y, Zhao Y S et al. 2011. Investigation on Enteromorpha in Bohai Sea. Journal of Biology, 28(5):27-29, https://doi.org/10.3724/SP.J.1011.2011.00187. (in Chinese with English abstract)
Ma Y Y, Zhao J, Xie W F et al. 2020. Branching phenotype and plasticity in floating ecotype of Ulva prolifera(Ulvophyceae, Chlorophyta). Marine Sciences, 44(8): 98-105. (in Chinese with English abstract)
Manhart J R. 1994. Phylogenetic analysis of green plant rbcL sequences. Molecular Phylogenetics and Evolution, 3(2):114-127, https://doi.org/10.1006/mpev.1994.1014.
Miao X X, Xiao J, Pang M 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, https://doi.org/10.1016/j.marpolbul.2017.09.060.
National Meteorological Center. 2021. The path of In-Fa.http://typhoon.nmc.cn/web.html. Accessed on 2021-11-22. (in Chinese)
Saunders G W, Kucera H. 2010. An evaluation of rbcL, tufA, UPA, LSU and ITS as DNA barcode markers for the marine green macroalgae. Cryptogamie, Algologie, 31(4):487-528.
Shimada S, Yokoyama N, Arai S et al. 2008. Phylogeography of the genus Ulva (Ulvophyceae, Chlorophyta), with special reference to the Japanese freshwater and brackish taxa. Journal of Applied Phycology, 20(5): 979-989, https://doi.org/10.1007/s10811-007-9296-y.
Smetacek V, Zingone A. 2013. Green and golden seaweed tides on the rise. Nature, 504(7478): 84-88, https://doi.org/10.1038/nature12860.
Song D B, Gao Z Q, Xu F X et al. 2017. Assessment of ecosystem health in the Bohai Sea and coun-termeasures study.Marine Sciences, 41(5): 17-26, https://doi.org/10.11759/hykx20160922003. (in Chinese with English abstract)
Song W, Han H B, Wang Z L et al. 2019a. Molecular identification of the macroalgae that cause green tides in the Bohai Sea, China. Aquatic Botany, 156: 38-46, https://doi.org/10.1016/j.aquabot.2019.04.004.
Song W, Wang Z L, Li Y et al. 2019b. Tracking the original source of the green tides in the Bohai Sea, China.Estuarine, Coastal and Shelf Science, 219: 354-362, https://doi.org/10.1016/j.ecss.2019.02.036.
Tamura K, Stecher G, Peterson D et al. 2013. MEGA6:molecular evolutionary genetics analysis version 6.0.Molecular Biology and Evolution, 30(12): 2725-2729, https://doi.org/10.1093/molbev/mst197.
Tsubaki S, Nishimura H, Imai T et al. 2020. Probing rapid carbon fixation in fast-growing seaweed Ulva meridionalis using stable isotope 13C-labelling. Scientific Reports, 10(1): 20399, https://doi.org/10.1038/s41598-020-77237-1.
Tsubaki S, Onda A, Ueda T et al. 2017. Microwave-assisted hydrothermal processing of seaweed biomass. In: Ruiz H A, Hedegaard Thomsen M, Trajano H L eds. Hydrothermal Processing in Biorefineries. Springer, International Publishing. p.443-445, https://doi.org/10.1007/978-3-319-56457-9_19.
Valiela I, McClelland J, Hauxwell J et al. 1997.Macroalgal blooms in shallow estuaries: controls and ecophysiological and ecosystem consequences.Limnology and Oceanography, 42(5): 1105-1118, https://doi.org/10.4319/lo.1997.42.5_part_2.1105.
Wang C, Yu R C, Zhou M J. 2011. Acute toxicity of live and decomposing green alga Ulva (Enteromorpha) prolifera to abalone Haliotis discus hannai. Chinese Journal of Oceanology and Limnology, 29(3): 541-546, https://doi.org/10.1007/s00343-011-0126-3.
Wang H, Wang H W. 2009. Investigation and study on Enteromorpha in Liaoning province. Journal of Anhui Agricultural Sciences, 37(6): 2676-2678, https://doi.org/10.3969/j.issn.0517-6611.2009.06.138. (in Chinese with English abstract)
Wang X L, Cui Z G, Guo Q et al. 2009. Distribution of nutrients and eutrophication assessment in the Bohai Sea of China.Chinese Journal of Oceanology and Limnology, 27(1):177-183, https://doi.org/10.1007/s00343-009-0177-x.
Wei X, Liu W Z, Lin X Y et al. 2022. First record of Ulva californica in mainland China: a single alien parthenogenetic population with discontinuous distribution. Journal of Oceanology and Limnology.https://doi.org/10.1007/s00343-022-1392-y.
Xie W F, Wu C H, Zhao J et al. 2020. New records of Ulva spp. (Ulvophyceae, Chlorophyta) in China, with special reference to an unusual morphology of U. meridionalis forming green tides. European Journal of Phycology, 55(4): 412-425, https://doi.org/10.1080/09670262.2020. 1740946.
Xing Q G, Braga F, Tosi L et al. 2016. Detection of low salinity groundwater seeping into the Eastern Laizhou Bay (China) with the aid of landsat thermal data. Journal of Coastal Research, 74(sp1): 149-156, https://doi.org/10.2112/SI74-014.1.
Xu M, Zhou Y, Song X J et al. 2019. The distribution of large floating seagrass (Zostera marina) aggregations in northern temperate zones of Bohai Bay in the Bohai Sea, China. PLoS One, 14(3): e0201574, https://doi.org/10.1371/journal.pone.0201574.
Yu Q R, Yang G, Liu Z Y. 2017. Morphological observation and molecular biology identification of Ulva sp. in Huanghai and Bohai Sea islands. Ecological Science, 36(1): 102-110, https://doi.org/10.14108/j.cnki.1008-8873.2017.01.014. (in Chinese with English abstract)
Yu R C, Sun S, Yan T et al. 2018. Progresses and perspectives on green-tide studies in the Yellow Sea. Oceanologia et Limnologia Sinica, 49(5): 942-949, https://doi.org/10.11693/hyhz20180700158. (in Chinese with English abstract)
Zhang J H, Liu C C, Yang L L et al. 2015. The source of the Ulva blooms in the East China Sea by the combination of morphological, molecular and numerical analysis.Estuarine, Coastal and Shelf Science, 164: 418-424, https://doi.org/10.1016/j.ecss.2015.08.007.
Zhang Q C, Qiu L M, Yu R C et al. 2012. Emergence of brown tides caused by Aureococcus anophagefferens Hargraves et Sieburth in China. Harmful Algae, 19: 117-124, https://doi.org/10.1016/j.hal.2012.06.007.
Zhang Q C, Yu R C, Chen Z F 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.
Zhao D Z, Zhao L, Zhang F S et al. 2004. Temporal occurrence and spatial distribution of red tide events in China’s coastal waters. Human and Ecological Risk Assessment:An International Journal, 10(5): 945-957, https://doi.org/10.1080/10807030490889030.
Zhao J H, Geng H X, Zhang Q C et al. 2022. Green tides in the Yellow Sea promoted the proliferation of pelagophyte Aureococcus anophagefferens. Environmental Science & Technology, 56(5): 3056-3064, https://doi.org/10.1021/acs.est.1c06502.
Zhao J, Jiang P, Liu Z Y et al. 2013. The Yellow Sea green tides were dominated by one species, Ulva (Enteromorpha) prolifera, from 2007 to 2011. Chinese Science Bulletin, 58(19): 2298-2302.
Zhao J, Jiang P, Qin S et al. 2015. Genetic analyses of floating Ulva prolifera in the Yellow Sea suggest a unique ecotype. Estuarine, Coastal and Shelf Science, 163: 96-102, https://doi.org/10.1016/j.ecss.2015.05.027.
Zhao J, Jiang P, Qiu R et al. 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.
Zhao J, Kong F Z, Liu Q C et al. 2022. Tempo-spatial distribution of the Ulva spp. micro-propagules in the Yellow Sea during and after the green tide in 2019. Journal of Oceanology and Limnology, https://10.1007/s00343-022-1365-1.
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