Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 662 No. 1: 6 Aug. 2024
Type: Article
Published: 2024-08-06
DOI: 10.11646/phytotaxa.662.1.5
Page range: 67-79
Abstract views: 160
PDF downloaded: 132

Species diversity and phylogeny of the green macroalga Ulva (Ulvophyceae, Chlorophyta) in Singapore

Department of Biological Sciences, National University of Singapore, Singapore 117558, Singapore
Department of Biological Sciences, National University of Singapore, Singapore 117558, Singapore, Lee Kong Chian Natural History Museum, National University of Singapore, Singapore 117377, Singapore, Tropical Marine Science Institute, National University of Singapore, Singapore 119227, Singapore, Centre for Nature-based Climate Solutions, National University of Singapore, Singapore 117558, Singapore
Algae Blue carbon DNA barcoding Green seaweed Marine Morphology Southeast Asia

Abstract

The green macroalgal genus Ulva (Ulvaceae, Ulvophyceae, Chlorophyta) is commonly found in coastal ecosystems and confers many important marine ecological services. Despite prior research interest and recent advancements in Ulva taxonomy, in many parts of the world, its species diversity remains unresolved due to a high degree of morphological variation and phenotypic plasticity. DNA barcoding and phylogenetic approaches can potentially assist in identifying Ulva species precisely. Here, we analysed chloroplast tufA, rbcL and nuclear ITS from 49 Ulva specimens from Singapore. Gross and microscopic morphological examinations were also performed to characterise the morphological range of each species. Our results confirm the presence of three Ulva species in Singapore, all of which are new local records: U. meridionalis, U. ohnoi, and U. tepida. Although 10 Ulva species have been historically recorded in Singapore, none of them were found in the present study, likely due to prior misidentification, limited seasonal sampling, or local extirpations. Ulva ohnoi shows high morphological variation with five morphotypes. This study demonstrates that molecular analyses combined with morphological examinations are useful for characterising Ulva diversity.

References

  1. Agardh, C.A. (1811) Dispositio algarum Sueciae. Litteris Berlingianis, Lundae, pp. 17–26.
  2. Agardh, C.A. (1823) Species algarum rite cognitae, cum synonymis, differentiis specificis et descriptionibus succinctis. Sumtibus Ernesti Mauritii, Gryphiswaldiae, pp. 399–531.
  3. Areschoug, J.E. (1854) Phyceae novae et minus cognitae in maribus extraeuropaeis collectae. Nova Acta Regiae Societatis Scientiarum Upsaliensis 3: 329–372.
  4. Bast, F., John, A.A. & Bhushan, S. (2014) Strong endemism of bloom-forming tubular Ulva in Indian West Coast, with description of Ulva paschima sp. nov. (Ulvales, Chlorophyta). PLOS ONE 9: e109295. https://doi.org/10.1371/journal.pone.0109295
  5. Charoensiddhi, S., Conlon, M., Methacanon, P., Thayanukul, P., Hongsprabhas, P. & Zhang, W. (2022) Gut microbiome modulation and gastrointestinal digestibility in vitro of polysaccharide-enriched extracts and seaweeds from Ulva rigida and Gracilaria fisheri. Journal of Functional Foods 96: 105204. https://doi.org/10.1016/j.jff.2022.105204
  6. Chou, L.M., Huang, D., Tan, K.S., Toh, T.C., Goh, B.P.L. & Tun, K. (2019) Singapore. In: Sheppard, A. (Ed.) World Seas: An Environmental Evaluation (Second Edition). Academic Press, Singapore, pp. 539–558. https://doi.org/10.1016/B978-0-08-100853-9.00031-2
  7. Chuang, S.H. (1961) On Malayan Shores. Muwu Shosa, Singapore, 225 pp.
  8. Clark, K., Karsch-Mizrachi, I., Lipman, D.J., Ostell, J. & Sayers, E.W. (2016) GenBank. Nucleic Acids Research 44: D67–D72. https://doi.org/10.1093/nar/gkv1276
  9. Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772. https://doi.org/10.1038/nmeth.2109
  10. Doyle, J.J. & Doyle, J.L. (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19: 11–15.
  11. Egan, S., Thomas, T., Holmström, C. & Kjelleberg, S. (2000) Phylogenetic relationship and antifouling activity of bacterial epiphytes from the marine alga Ulva lactuca. Environmental Microbiology 2: 343–347. https://doi.org/10.1046/j.1462-2920.2000.00107.x
  12. Forsskål, P. (1775) Flora Aegyptiaca-Arabica sive descriptiones plantarum, quas per Aegyptum inferiorem et Arabium delicem detexit. 32 pp.
  13. Gao, G., Zhong, Z., Zhou, X. & Xu, J. (2016) Changes in morphological plasticity of Ulva prolifera under different environmental conditions: A laboratory experiment. Harmful Algae 59: 51–58. https://doi.org/10.1016/j.hal.2016.09.004
  14. Green-Gavrielidis, L.A. & Thornber, C.S. (2022) Will climate change enhance algal blooms? The individual and interactive effects of temperature and rain on the macroalgae Ulva. Estuaries and Coasts 45: 1688–1700. https://doi.org/10.1007/s12237-022-01048-y
  15. Guindon, S. & Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52: 696–704. https://doi.org/10.1080/10635150390235520
  16. Hayden, H.S., Blomster, J., Maggs, C.A., Silva, P.C., Stanhope, M.J. & Waaland, J.R. (2003) Linnaeus was right all along: Ulva and Enteromorpha are not distinct genera. European Journal of Phycology 38: 277–294. https://doi.org/10.1080/1364253031000136321
  17. Hiraoka, M., Shimada, S., Uenosono, M. & Masuda, M. (2004) A new green-tide-forming alga, Ulva ohnoi Hiraoka et Shimada sp. nov. (Ulvales, Ulvophyceae) from Japan. Phycological Research 52: 17–29. https://doi.org/10.1111/j.1440-1835.2003.00321.x
  18. Horimoto, R., Masakiyo, Y., Ichihara, K. & Shimada, S. (2011) Enteromorpha-like 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 Science Museum Series B (Botany) 37: 155–167.
  19. Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755. https://doi.org/10.1093/bioinformatics/17.8.754
  20. Kang, J.H., Jang, J.E., Kim, J.H., Byeon, S.Y., Kim, S., Choi, S.K., Kang, Y.H., Park, S.R. & Lee, H.J. (2019) Species composition, diversity, and distribution of the genus Ulva along the coast of Jeju Island, Korea based on molecular phylogenetic analysis. PLOS ONE 14: e0219958. https://doi.org/10.1371/journal.pone.0219958
  21. Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. https://doi.org/10.1093/molbev/mst010
  22. Kidgell, J.T., Magnusson, M., de Nys, R. & Glasson, C.R.K. (2019) Ulvan: A systematic review of extraction, composition and function. Algal Research 39: 101422. https://doi.org/10.1016/j.algal.2019.101422
  23. Kumar, A.S. & Palanisamy, M. (2021) A new combination of endemic species in Ulva from India. Nelumbo 63: 218–219.
  24. Kwan, V., Fong, J., Ng, C.S.L. & Huang, D. (2022) Temporal and spatial dynamics of tropical macroalgal contributions to blue carbon. Science of the Total Environment 828: 154369. https://doi.org/10.1016/j.scitotenv.2022.154369
  25. Kwan, V., Yip, Z.T., Fong, J. & Huang, D. (2021) Diversity and phylogeny of the brown alga Lobophora (Dictyotales, Phaeophyceae) in Singapore. Phytotaxa 496 (3): 215–227. https://doi.org/10.11646/phytotaxa.496.3.1
  26. Kwon, H.K., Kang, H., Oh, Y.H., Park, S.R. & Kim, G. (2017) Green tide development associated with submarine groundwater discharge in a coastal harbor, Jeju, Korea. Scientific Reports 7: 6325. https://doi.org/10.1038/s41598-017-06711-0
  27. Lagourgue, L., Gobin, S., Brisset, M., Vandenberghe, S., Bonneville, C., Jauffrais, T., Van Wynsberge, S. & Payri, C.E. (2022) Ten new species of Ulva (Ulvophyceae, Chlorophyta) discovered in New Caledonia: Genetic and morphological diversity, and bloom potential. European Journal of Phycology 57: 1–21. https://doi.org/10.1080/09670262.2022.2027023
  28. Lee, A.C., Liao, L.M. & Tan, K.S. (2009) New records of marine algae on artificial structures and intertidal flats in coastal waters of Singapore. Raffles Bulletin of Zoology 22: 5–40.
  29. Lee, H.W., Kang, J.C. & Kim, M.S. (2019) Taxonomy of Ulva causing blooms from Jeju Island, Korea with new species, U. pseudo-ohnoi sp. nov. (Ulvales, Chlorophyta). Algae 34: 253–266. https://doi.org/10.4490/algae.2019.34.12.9
  30. Lee, S.K. (1966) The natural history of the shore flora and fauna off Tanjong Teritip, Singapore. Malayan Nature Journal 19: 259–274.
  31. Levine, I.A. (2018) Algae: A way of life and health. In: Levine, I.A. & Fleurence, J. (Eds.) Microalgae in Health and Disease Prevention. Academic Press, pp. 1–5. https://doi.org/10.1016/B978-0-12-802772-1.00001-4
  32. Linnaeus, C. (1753) Species plantarum, exhibentes plantas rite cognitas, ad genera relatas, cum differentiis specificis, nominibus trivialibus, synonymis selectis, locis natalibus, secundum systema sexuale digestas. Vol. 2 pp. Holmiae [Stockholm]: Impensis Laurentii Salvii, [i], 561–1200, [1–30, index], [i, err.].
  33. Liu, S., Trevathan-Tackett, S.M., Ewers Lewis, C.J., Huang, X. & Macreadie, P.I. (2020) Macroalgal blooms trigger the breakdown of seagrass blue carbon. Environmental Science & Technology 54: 14750–14760. https://doi.org/10.1021/acs.est.0c03720
  34. Macreadie, P.I., Jarvis, J., Trevathan-Tackett, S.M. & Bellgrove, A. (2017) Seagrasses and macroalgae: Importance, vulnerability and impacts. In: Phillips, B.F. & Pérez-Ramírez, M. (Eds.) Climate Change Impacts on Fisheries and Aquaculture. John Wiley & Sons Ltd, pp. 729–770. https://doi.org/10.1002/9781119154051.ch22
  35. Maddison, W.P. & Maddison, D.R. (2021) Mesquite: a modular system for evolutionary analysis. Version 3.70. [http://www.mesquiteproject.org]
  36. Masakiyo, Y. & Shimada, S. (2014) Species diversity of the genus Ulva (Ulvophyceae, Chlorophyta) in Japanese waters, with special reference to Ulva tepida Masakiyo et S. Shimada sp. nov. Bulletin of the National Science Museum Series B (Botany) 40: 1–13.
  37. Melton III, J.T. & Lopez-Bautista, J.M. (2021) Diversity of the green macroalgal genus Ulva (Ulvophyceae, Chlorophyta) from the east and Gulf Coast of the United States based on molecular data. Journal of Phycology 57: 551–568. https://doi.org/10.1111/jpy.13120
  38. Müller, O.F. (1778) Flora Danica. Havniae, Copenhagen, 8 pp.
  39. Nakamura, M., Kumagai, N.H., Tamaoki, M., Arita, K., Ishii, Y., Nakajima, N. & Yabe, T. (2020) Photosynthesis and growth of Ulva ohnoi and Ulva pertusa (Ulvophyceae) under high light and high temperature conditions, and implications for green tide in Japan. Phycological Research 68: 152–160. https://doi.org/10.1111/pre.12410
  40. Noiraksar, T., Lewmanomont, K., Tan, K.S. & Ong, J.J.L. (2012) Diversity of seaweeds and seagrasses St. John’s Island, Singapore. Contributions to Marine Science: 33–47.
  41. O’Kelly, C.J., Kurihara, A., Shipley, T.C. & Sherwood, A.R. (2010) Molecular assessment of Ulva spp. (Ulvophyceae, Chlorophyta) in the Hawaiian Islands. Journal of Phycology 46: 728–735. https://doi.org/10.1111/j.1529-8817.2010.00860.x
  42. Pham, M.N., Tan, H.T.W., Mitrovic, S. & Yeo, H.H.T. (2011) A Checklist of the Algae of Singapore, 2nd Edition. Raffles Museum of Biodiversity Research, National University of Singapore, Singapore, 99 pp.
  43. Poquita-Du, R.C., Quek, Z.B.R., Jain, S.S., Schmidt-Roach, S., Tun, K., Heery, E.C., Chou, L.M., Todd, P.A. & Huang, D. (2019) Last species standing: loss of Pocilloporidae corals associated with coastal urbanization in a tropical city state. Marine Biodiversity 49: 1727–1741. https://doi.org/10.1007/s12526-019-00939-x
  44. Rambaut, A., Drummond, A.J., Xie, D., Baele, G. & Suchard, M.A. (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67: 901–904. https://doi.org/10.1093/sysbio/syy032
  45. Roberts, C.M., McClean, C.J., Veron, J.E.N., Hawkins, J.P., Allen, G.R., McAllister, D.E., Mittermeier, C.G., Schueler, F.W., Spalding, M., Wells, F., Vynne, C. & Werner, T.B. (2002) Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 295: 1280–1284. https://doi.org/10.1126/science.1067728
  46. Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574. https://doi.org/10.1093/bioinformatics/btg180
  47. 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: 487–528.
  48. Sayers, E.W., Cavanaugh, M., Clark, K., Ostell, J., Pruitt, K.D. & Karsch-Mizrachi, I. (2019) GenBank. Nucleic Acids Research 47: D94–D99. https://doi.org/10.1093/nar/gky989
  49. Setchell, W.A. & Gardner, N.L. (1920) Phycological contributions. University of California Publications in Botany 7: 286–287.
  50. Sin, T.M., Ang, H.P., Buurman, J., Lee, A.C., Leong, Y.L., Ooi, S.K., Steinberg, P. & Teo, S.L.M. (2016) The urban marine environment of Singapore. Regional Studies in Marine Science 8: 331–339. https://doi.org/10.1016/j.rsma.2016.01.011
  51. Stamatakis, A. (2014) RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
  52. Tang, Y.Z. & Gobler, C.J. (2011) The green macroalga, Ulva lactuca, inhibits the growth of seven common harmful algal bloom species via allelopathy. Harmful Algae 10: 480–488. https://doi.org/10.1016/j.hal.2011.03.003
  53. Tay, J.Y.L., Wong, S.K.M., Chou, L.M. & Todd, P.A. (2018) Land reclamation and the consequent loss of marine habitats around the Ayer Islands, Singapore. Nature in Singapore 11: 1–5.
  54. Teo, L.W. & Wee, Y.C. (1983) Seaweeds of Singapore. Singapore University Press, Singapore, 123 pp.
  55. Thivy, F. & Sharma, H.C. (1966) Ulva beytensis sp. nov. from Gujarat, India. Current Science (Bangalore) 35: 150–151.
  56. Tran, L.A.T., Leliaert, F., Vieira, C., Tran, T.V., Nguyen, T.V., Dam, T.D. & De Clerck, O. (2023) Molecular assessment of Ulva (Ulvales, Chlorophyta) diversity in Vietnam including the new species U. vietnamensis. Phycological Research 71: 13–24. https://doi.org/10.1111/pre.12507
  57. Tran, L.A.T., Vieira, C., Steinhagen, S., Maggs, C.A., Hiraoka, M., Shimada, S., Van Nguyen, T., De Clerck, O. & Leliaert, F. (2022) An appraisal of Ulva (Ulvophyceae, Chlorophyta) taxonomy. Journal of Applied Phycology 34: 2689–2703. https://doi.org/10.1007/s10811-022-02815-x
  58. Wang, Y., Wang, Y., Zhu, L., Zhou, B. & Tang, X. (2012) Comparative studies on the ecophysiological differences of two green tide macroalgae under controlled laboratory conditions. PLOS ONE 7: e38245. https://doi.org/10.1371/journal.pone.0038245
  59. Wulfen, F.X. (1803) Cryptogama aquatica. Archives de Botanique 3: 1–64.
  60. Xie, W.F., Wu, C.H., Zhao, J., Lin, X.Y. & 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. European Journal of Phycology 55: 412–425. https://doi.org/10.1080/09670262.2020.1740946
  61. Ye, N., Zhang, X., Mao, Y., Liang, C., Xu, D., Zou, J., Zhuang, Z. & Wang, Q. (2011) ‘Green tides’ are overwhelming the coastline of our blue planet: Taking the world’s largest example. Ecological Research 26: 477–485. https://doi.org/10.1007/s11284-011-0821-8
  62. Yip, Z.T., Quek, R.Z.B., Low, J.K.Y., Wilson, B., Bauman, A.G., Chou, L.M., Todd, P.A. & Huang, D. (2018) Diversity and phylogeny of Sargassum (Fucales, Phaeophyceae) in Singapore. Phytotaxa 369 (3): 200–210. https://doi.org/10.11646/phytotaxa.369.3.3
  63. Yoshida, G., Uchimura, M. & Hiraoka, M. (2015) Persistent occurrence of floating Ulva green tide in Hiroshima Bay, Japan: Seasonal succession and growth patterns of Ulva pertusa and Ulva spp. (Chlorophyta, Ulvales). Hydrobiologia 758: 223–233. https://doi.org/10.1007/s10750-015-2292-3
  64. Zeroual, S., El Bakkal, S.E., Mansori, M., Lhernould, S., Faugeron-Girard, C., El Kaoua, M. & Zehhar, N. (2020) Cell wall thickening in two Ulva species in response to heavy metal marine pollution. Regional Studies in Marine Science 35: 101125. https://doi.org/10.1016/j.rsma.2020.101125
  65. Zhang, Y., He, P., Li, H., Li, G., Liu, J., Jiao, F., Zhang, J., Huo, Y., Shi, X., Su, R., Ye, N., Liu, D., Yu, R., Wang, Z., Zhou, M. & Jiao, N. (2019) Ulva prolifera green-tide outbreaks and their environmental impact in the Yellow Sea, China. National Science Review 6: 825–838. https://doi.org/10.1093/nsr/nwz026