Six Thallus Surface Types of Coralline Algae with Descriptions of Two New Records of Amphiroa beauvoisii and Neogoniolithon setchellii in Sanya reef, China

Source:
By:Xinming Lei, Lei Jiang, Youfang Sun, Yuyang Zhang, Guowei Zhou, Jianhui Yang, Jiansheng Lian, Hui Huang

DOI: https://doi.org/10.30564/jms.v2i2.1822

Abstract:

Coralline algae are globally distributed calcifying species and play critical ecological roles to marine ecosystems by contributing significantly to their structural complexity and diversity. Thallus surface types of historical samples in Sanya coral reef reserve were studied based on the scanning electron microscope (SEM) method. Our results show six thallus surface types within the study area: Corallina-type, Jania-type, Leptophytum-type, Phymatolithon-type, Pneophyllum-type, and Spongites-type. The Phymatolithon-type is the dominant surface type in Sanya reefs. Two new record species in the region are described: Amphiroa beauvoisii and Neogoniolithon setchellii. Although thallus surface types provide useful diagnostics characters for distinguishing coralline algae at tribe or subfamily level, species identification needs to refer to the reproductive features. This is the first surface study of coralline algae in the South China Sea. This result provides the baseline data needed for the monitoring and management of reef-building organisms of coral reef in China.

References:

Adey, W.H. (1970) The Effects of Light and Temperature on Growth Rates in Boreal-Subarctic Crustose Corallines. Journal of Phycology 6: 269-276. https://doi.org/10.1111/j.1529-8817.1970.tb02392.x Adey, W.H. (1998) Coral reefs: Algal structured and mediated ecosystems in shallow, turbulent, alkaline waters. Journal of Phycology 34: 393-406. https://doi.org/10.1046/j.1529-8817.1998.340393.x Adey, W.H., Chamberlain, Y.M. & Irvine, L.M. (2005) An Sem-Based Analysis of the Morphology, Anatomy, and Reproduction of Lithothamnion Tophiforme (Esper) Unger (Corallinales, Rhodophyta), with a Comparative Study of Associated North Atlantic Arctic/Subarctic Melobesioideae. Journal of Phycology 41: 1010-1024. https://doi.org/10.1111/j.1529-8817.2005.00123.x Adey, W.H., Townsend, R. & Boykins, W. (1982) The Crustose Coralline Algae (Rhodophyta: Corallinaceae) of the Hawaiian Islands. Smithsonian Contributions to the Marine Sciences 15: 1-74. https://doi.org/10.5479/si.01960768.15.1 Bosence, D.W.J. (1983) Coralline Algal Reef Frameworks. Journal of the Geological Society 140: 365-376. https://doi.org/10.1144/gsjgs.140.3.0365 Caragnano, A., Foetisch, A., Maneveldt, G.W., Millet, L., Liu, L.C., Lin, S.M., Rodondi, G. & Payri, C.E. (2018) Revision of Corallinaceae (Corallinales, Rhodophyta): recognizing Dawsoniolithon gen. nov., Parvicellularium gen. nov. and Chamberlainoideae subfam. nov. containing Chamberlainium gen. nov. and Pneophyllum. Journal of Phycology 54: 391-409. https://doi.org/10.1111/jpy.12644 Chamberlain, Y.M. (1990) The genus Leptophytum (Rhodophyta, Corallinaceae) in the British Isles with descriptions of Leptophytum bornetii, L. elatum sp. nov. and L. laeve. British Phycological Journal 25: 179-199. https://doi.org/10.1080/00071619000650171 Choi, D.S. & Lee, I.K. (1988) On Surface Structures of Amphiroa (Corallinaceae, Rhodophyta). Algae 3: 111-117. https://www.e-algae.org/upload/pdf/ALGAE3-2_03.pdf Ding, L.P., Huang, B.X. & Wang, H.W. (2015) New clsssification system of marine red algae of China. Guangxi Sciences, 22(2): 164–188. (in Chinese with English abstract) Foster, M.S. (2001) Rhodoliths: Between rocks and soft places. Journal of Phycology 37: 659-667. https://doi.org/10.1046/j.1529-8817.2001.00195.x Gabrielson, P.W., Miller, K.A. & Martone, P.T. (2011) Morphometric and molecular analyses confirm two distinct species of Calliarthron (Corallinales, Rhodophyta), a genus endemic to the northeast Pacific. Phycologia 50: 298-316. https://doi.org/10.2216/10-42.1 Garbary, D.J. & Johansen, H.W. (1982) Scanning electron microscopy of Corallina and Haliptilon (Corallinaceae, Rhodophyta): surface features and their taxonomic implication. Journal of Phycology 18: 211-219. https://doi.org/10.1111/j.1529-8817.1982.tb03176.x Guiry, M.D. & Guiry, G.M. (2019) AlgaeBase Worldwide electronic publication, Nat. Univ. Ireland, Galway. Available from: http://www.algaebase.org (accessed 5 April 2019) Harvey, A.S. & Woelkerling, W.J. (2007) A guide to nongeniculate coralline red algal (Corallinales, Rhodophyta) rhodolith identification. Ciencias Marinas 33: 411-426. https://doi.org/10.7773/cm.v33i4.1210 Harvey, A.S., Woelkerling, W.J., Huisman, J.M. & Gurgel, C.F.D. (2013) A monographic account of Australian species of Amphiroa (Corallinaceae, Rhodophyta). Australian Systematic Botany 26: 81-144. https://doi.org/10.1071/Sb13010 Harvey, A.S., Woelkerling, W.J. & Millar, A.J.K. (2009) The Genus Amphiroa (Lithophylloideae, Corallinaceae, Rhodophyta) from the Temperate Coasts of the Australian Continent, Including the Newly Described A. klochkovana. Phycologia 48: 258-290. https://doi.org/10.2216/08-84.1 Heyward, A.J. & Negri, A.P. (1999) Natural inducers for coral larval metamorphosis. Coral Reefs 18: 273-279. https://doi.org/10.1007/s003380050193 Huggett, M.J., Williamson, J.E., de Nys, R., Kjelleberg, S. & Steinberg, P.D. (2006) Larval settlement of the common Australian sea urchin Heliocidaris erythrogramma in response to bacteria from the surface of coralline algae. Oecologia 149: 604-619. https://doi.org/10.1007/s00442-006-0470-8 Johansen, H.W. (1981) Coralline Algae, A First Synthesis. CRC Press, Boca Raton, Florida, 239 pp. Johnson, C.R., Sutton, D.C., Olson, R.R. & Giddins, R. (1991) Settlement of Crown-of-Thorns Starfish - Role of Bacteria on Surfaces of Coralline Algae and a Hypothesis for Deep-Water Recruitment. Marine Ecology Progress Series 71: 143-162. https://doi.org/10.3354/meps071143 Lamouroux, J.V.F. (1816) Histoire des polypiers coralligènes flexibles, vulgairement nomme´s zoophytes. F. Poisson, Caen. 559 pp. Lei, X.M., Huang, H., Lian, J.S., Zhou, G.W. & Jiang, L. (2018) Community structure of coralline algae and its relationship with environment in Sanya reefs, China. Aquatic Ecosystem Health & Management 21: 19-29. https://doi.org/10.1080/14634988.2018.1432954 Littler, M.M. (1972) The crustose corallinaceae. Oceanography and Marine Biology: An Annual Review 10: 311-347. Liu, L.C., Lin, S.M., Caragnano, A. & Payri, C. (2018) Species diversity and molecular phylogeny of non-geniculate coralline algae (Corallinophycidae, Rhodophyta) from Taoyuan algal reefs in northern Taiwan, including Crustaphytum gen. nov. and three new species. Journal of Applied Phycology 30: 3455-3469. https://doi.org/10.1007/s10811-018-1620-1 Maneveldt, G.W., Chamberlain, Y.M. & Keats, D.W. (2008) A catalogue with keys to the non-geniculate coralline algae (Corallinales, Rhodophyta) of South Africa. South African Journal of Botany 74: 555-566. https://doi.org/10.1016/j.sajb.2008.02.002 Martin, S., Cohu, S., Vignot, C., Zimmerman, G. & Gattuso, J.P. (2013) One-year experiment on the physiological response of the Mediterranean crustose coralline alga, Lithophyllum cabiochae, to elevated pCO2 and temperature. Ecology and Evolution 3: 676-693. https://doi.org/10.1002/ece3.475 Martin, S. & Gattuso, J.-P. (2009) Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Global Change Biology 15: 2089-2100. https://doi.org/10.1111/j.1365-2486.2009.01874.x Masaki, T., Fujita, D. & Hagen, N.T. (1984) The surface ultrastructure and epithallium shedding of crustose coralline algae in an 'Isoyake' area of southwestern Hokkaido, Japan. Hydrobiologia 116/117: 218-223. https://doi.org/10.1007/bf00027669 Mateo-Cid, L.E., Mendoza-Gonzalez, A.C. & Gabrielson, P.W. (2014) Neogoniolithon (Corallinales, Rhodophyta) on the Atlantic coast of Mexico, including N. siankanensis sp nov. Phytotaxa 190: 64-93. https://doi.org/10.11646/phytotaxa.190.1.7 Muñoz, P.T., Sáez, C.A., Martínez-Callejas, M.B., Flores-Molina, M.R., Bastos, E., Fonseca, A., Gurgel, C.F.D., Barufi, J.B., Rörig, L., Hall-Spencer, J.M. & Horta, P.A. (2018) Short-term interactive effects of increased temperatures and acidification on the calcifying macroalgae Lithothamnion crispatum and Sonderophycus capensis. Aquatic Botany 148: 46-52. https://doi.org/10.1016/j.aquabot.2018.04.008 Nelson, W.A. (2009) Calcified macroalgae - critical to coastal ecosystems and vulnerable to change: a review. Marine and Freshwater Research 60: 787-801. https://doi.org/10.1071/Mf08335 Norris, J.N. & Johansen, H.W. (1981) Articulated coralline algae of the Gulf of California, Mexico, I: Amphiroa Lamouroux. Smithsonian Contributions to the Marine Sciences 9: 1-40. https://doi.org/10.5479/si.01960768.9.iii Penrose, D. (1992) Neogoniolithon fosliei (Corallinaceae, Rhodophyta), the type species of Neogoniolithon, in Southern Australia. Phycologia 31: 338-350. https://doi.org/10.2216/i0031-8884-31-3-4-338.1 Pueschel, C.M., Judson, B.L., Esken, J.E. & Beiter, E.L. (2002) A developmental explanation for the Corallina- and Jania-types of surfaces in articulated coralline red algae (Corallinales, Rhodophyta). Phycologia 41: 79-86.https://doi.org/10.2216/i0031-8884-41-1-79.1 Pueschel, C.M. & Keats, D.W. (1997) Fine structure of deep-layer sloughing and epithallial regeneration in Lithophyllum neoatalayense (Corallinales, Rhodophyta). Phycological Research 45: 1-8.https://doi.org/10.1111/j.1440-1835.1997.tb00056.x Scherner, F., Pereira, C.M., Duarte, G., Horta, P.A., CB, E.C., Barufi, J.B. & Pereira, S.M. (2016) Effects of Ocean Acidification and Temperature Increases on the Photosynthesis of Tropical Reef Calcified Macroalgae. PLoS One 11: e0154844. https://doi.org/10.1371/journal.pone.0154844 Sneed, J.M., Ritson-Williams, R. & Paul, V.J. (2015) Crustose coralline algal species host distinct bacterial assemblages on their surfaces. The ISME Journal 9: 2527-2536. https://doi.org/10.1038/ismej.2015.67 Steneck, R.S. (1986) The ecology of coralline algal crusts: convergent patterns and adaptative strategies. Annual Review of Ecology and Systematics 17: 273-303. https://doi.org/10.1146/annurev.es.17.110186.001421 TÂMega, F.T.S., Riosmena-Rodriguez, R., Mariath, R. & Figueiredo, M. (2014) Nongeniculate coralline red algae (Rhodophyta: Corallinales) in coral reefs from Northeastern Brazil and a description of Neogoniolithon atlanticum sp. nov. Phytotaxa 190: 277-298.https://doi.org/10.11646/phytotaxa.190.1.17 Titlyanov, E.A., Titlyanova, T.V., Li, X. & Huang, H. (2017) Coral Reef Marine Plants of Hainan Island. Science Press, Beijing, 254 pp. Tseng, C.K. (1983) Common Seaweeds of China. Science Press, Beijing, 316 pp. Vasquez-Elizondo, R.M. & Enriquez, S. (2016) Coralline algal physiology is more adversely affected by elevated temperature than reduced pH. Scientific Reports 6: 19030. https://doi.org/10.1038/srep19030 Vidal, R., Meneses, I. & Smith, M. (2003) Molecular genetic identification of crustose representatives of the order Corallinales (Rhodophyta) in Chile. Molecular Phylogenetics and Evolution 28: 404-419.https://doi.org/10.1016/s1055-7903(03)00123-4 Wang, W.L. (1996) The morphological studies of crustose coralline red algae (Corallinales, Rhodophyta) from Taiwan. PhD thesis, National Taiwan University, p175. (in Chinese with English abstract) Woelkerling, W.J. (1988) The Coralline Red Algae: An Analysis of the Genera and Subfamilies of Nongeniculate Corallinaceae. British Museum (Natural History) and Oxford University Press, London and Oxford, 268 pp. Woelkerling, W.J., Gustavsen, G., Myklebost, H.E., Prestø, T. & Såstad, S.M. (2005) The coralline red algal herbarium of Mikael Foslie: revised catalogue with analyses. Gunneria 77: 1-625. http://hdl.handle.net/11250/273026 Woelkerling, W.J., Irvine, L.M. & Harvey, A.S. (1993) Growth-forms in Non-geniculate Coralline Red Algae (Coralliinales, Rhodophyta). Australian Systematic Botany 6: 277-293. https://doi.org/10.1071/sb9930277 Xia, B.M. (2013) Flora algarum marinarum sinicarum: TomusⅡ Rhodophyta No. Ⅳ Corallinales. Science Press, Beijing, 147pp. (in Chinese with English index) Zhou, J.H., Zhang, D.R. (1987) Study on the crustose coralline algae of the Hainan Island and its vicinity Ⅰ. Studia Marina Sinica 28: 115-124. (in Chinese with English abstract)