Abstract
In Taiwan the algal reefs in Taoyuan County are the largest, composed of recent and fossil non-geniculate coralline algae. However, their diversity and phylogenetics in the region have never been documented. In this study, we analyzed the phylogenetic relationships of the non-geniculate coralline algae species collected from Taoyuan algal reefs and related non-geniculate species from other places in Taiwan and around the world based on psbA and SSU sequences. The molecular analyses revealed that at least 12 non-geniculate coralline species belonging in six evolutionary clades (Harveylithon, Lithophyllum, Pneophyllum, Crustaphytum gen. nov., and Phymatolithon, Sporolithon) occur in Taoyuan algal reefs. Eleven of these species do not match any described species and one (Lithophyllum margaritae) is a new record for the marine flora of Taiwan. We also describe a new genus (Crustaphytum gen. nov.) and three new non-geniculate coralline species (Crustaphytum pacificum sp. nov., Harveylithon rosea sp. nov., and Phymatolithon margoundulatus sp. nov.) for the most dominant and commonly seen species revealed by the molecular analyses. Among the latter three species, P. margoundulatus is only found in Taoyuan County and is the most dominant species there, comprising over 30% of the total cover, whereas C. pacificum has the widest distribution in the western Pacific Ocean (Taiwan and New Caledonia). Harveylithon rosea is a common species occurring in both algal reefs and rocky shores in the northern Taiwan. The other undescribed CCA species will be published when more specimens with reproductive structures are collected.
Similar content being viewed by others
References
Adey WH (1964) The genus Phymatolithon in the Gulf of Maine. Hydrobiologia 24:377–420
Adey WH (1965) The genus Clathromorphum in the Gulf of Maine. Hydrobiologia 26:539–573
Adey WH (1966) The genera Lithothamnium, Leptophytum (nov. gen.) and Phymatolithonin the Gulf of Maine. Hydrobiologia 28:321–370
Adey WH (1973) Temperature control of reproduction and productivity in a subarctic coralline alga. Phycologia 12:111–118
Adey WH (1975) The algal ridges and coral reefs of St. Croix: their structure and Holocene development. Atoll Res Bull 187:1–67
Adey WH (1998) Coral reefs: algal structured and mediated ecosystems in shallow, turbulent, alkaline waters. J Phycol 34:393–406
Adey WH, McKibbin DL (1970) Studies on the maerl species Phymatolithon calcareum (Pallas) nov. comb. and Lithothamnium coralloides Crouan in the Ria de Vigo. Bot Mar 13:100–106
Adey WH, Johansen HW (1972) Morphology and taxonomy of Corallinaceae with special reference to Clathromorphum, Mesophyllum, and Neopolyporolithon gen. nov. (Rhodophyceae, Cryptonemiales). Phycologia 1:159–180
Adey WH, Athanasiadis A, Lebednik PA (2001) Re-instatement of Leptophytum and its type Leptophytum laeve: taxonomy and biogeography of the genera Leptophytum and Phymatolithon (Corallinales, Rhodophyta). Eur J Phycol 36:191–204
Adey WH, Hernández-Kantún JJ, Johnson G, Gabrielson PW (2015) DNA sequencing, anatomy, and calcification patterns support a monophyletic, subarctic, carbonate reef-forming Clathromorphum (Hapalidiaceae, Corallinales, Rhodophyta). J Phycol 51:189–203
Aguirre J, Perfectti F, Braga JC (2010) Integrating phylogeny, molecular clocks, and the fossil record in the evolution of coralline algae (Corallinales and Sporolithales, Rhodophyta). Paleobiology 36:519–533
Amado-Filho GM, Maneveldt G, Marins BV, Manso RCC, Pacheco MR, Guimares SPB (2007) Structure of rhodolith beds from 4 to 55 meters deep along the southern coast of Espírito Santo State, Brazil. Cienc Mar 33:399–410
Athanasiadis, A. (2016) Leptophytum flavescens comb. nov. (Corallinales, Rhodophyta), an Arctic endemic from the sublittoral of NW Spitsbergen, North Norway, and western Novaya Zemlya, with epitypification of L. laeve. Mar Biol Res 12:551–558
Athanasiadis A, Adey WH (2006) The genus Leptophytum (Melobesioideae, Corallinales, Rhodophyta) on the Pacific coast of North America. Phycologia 45:71–115
Bosence DW (1983a) Coralline algal reef frameworks. J Geol Soc 140:365–376
Bosence DW (1983b) The occurrence and ecology of recent rhodoliths. A review. In: Tadensz MP (ed) Coated grains. Springer, Berlin, pp 225–242
Cabioch J (1970) Le maërl des côtes de Bretagne et le problème de sa survie. Penn Ar Bed (Brest) 7:421–429
Cabioch G, Montaggioni L, Thouveny N, Frank N, Sato T, Chazottes V, Dalamasso H, Payri C, Pichon M, Sémah AM (2008) The chronology and structure of the western New Caledonian barrier reef tracts. Palaeogeogr Palaeoclimatol Palaeoecol 268:91–105
Chamberlain YM (1991) Observations on Phymatolithon lamii (Lemonine) Y. Chamberlain comb. nov. (Rhodophyta, Corallinales) in the British Isles with an assessment of its relationship to P. rugulosum, Lithophyllum lamii and L. melobesioides. Br Phycol J 26:219–233
Dai CF, SW W, Chang JS (2009) Taoyuan Guanyin algal reef ecological guide manual (A). Liquefied Natural Gas Engineering Office, CPC Corporation, Taiwan 98 pp. (in Chinese)
Foster MS (2001) Rhodoliths: between rocks and soft places. J Phycol 37:659–667
Freiwald A, Henrich R (1994) Reefal coralline algal build-ups within the Arctic Circle: morphology and sedimentary dynamics under extreme environmental seasonality. Sedimentology 41:963–984
Guiry MD, Guiry GM (2018) AlgaeBase. World-wide electronic publication. National University of Ireland, Galway http://www.algaebase.org; searched on 30 January 2018
Harvey AS, Broadwater ST, Woelkerling WJ, Mitrovski PJ (2003) Choreonema (Corallinales, Rhodophyta): 18S rDNA phylogeny and resurrection of the Hapalidiaceae for the subfamilies Choreonematoideae, Australithoideae, and Melobesioideae. J Phycol 39:988–998
Harvey AS, Woelkerling WJ, Farr T, Neill K, Nelson W (2005) Coralline algae of central New Zealand. An identification guide to common crustose species. NIWA Press, Wellington, p 145
Kaleb S, Falace A, Woelkerling W (2012) Phymatolithon lamii (Hapalidiaceae, Corallinales, Rhodophyta): a first report for the Mediterranean Sea. Bot Mar 55:377–385
Lebednik PA (1977) Postfertilization development in Clathromorphum, Melobesia and Mesophyllum with comments on the evolution of the Corallinaceae and the Cryptonemiales (Rhodophyta). Phycologia 16:379406
Le Gall L, Payri CE, Bittner L, Saunders GW (2010) Multigene phylogenetic analyses support recognition of the Sporolithales ord. nov. Mol Phylogenet Evol 54:302–305
Lewis JE, Norris JN (1987) A history and annotated account of the benthic marine algae of Taiwan. Smithson Contrib Mar Sci 29:1–38
Lin SM, Fredericq S, Hommersand MH (2001) Systematics of the Delesseriaceae (Ceramiales, Rhodophyta) based on large subunit rDNA and rbcL sequences, including the Phycodryoideae, subfam. nov. J Phycol 37:881–899
Lin SM, Fredericq S, Hommersand MH (2004) Augophyllum, a new genus of the Delesseriaceae (Rhodophyta) based on rbcL sequence analysis and cystocarp development. J Phycol 40:962–976
Lin HJ, Hsu HF, Liao WS, Lee CL, Liu PJ, Lin SM (2013) Biodiversity of the algal reefs in Taoyuan. J Wetl 2:1–24
Liou C-Y, Yang S-Y, Chen CA (2017) Unprecedented calcareous algal reefs in northern Taiwan merit high conservation priority. Coral Reefs 36:1253
Littler MM, Littler DS (1980) The evolution of thallus form and survival strategies in benthic marine macroalgae: field and laboratory tests of a functional form model. Am Nat 116:25–44
Littler MM, Littler DS (1984) Relationships between macroalgal functional form groups and substrata stability in a subtropical rocky-intertidal system. J Exp Mar Biol Ecol 74:13–34
Maneveldt GW, Chamberlain YM, Keats DW (2008) A catalogue with keys to the non-geniculate coralline algae (Corallinales, Rhodophyta) of South Africa. S Afr J Bot 74:555–566
Nakayama T, Marin B, Kranz HD, Surek B, Huss VA, Inouye I, Melkonian M (1998) The basal position of scaly green flagellates among the green algae (Chlorophyta) is revealed by analyses of nuclear-encoded SSU rRNA sequences. Protist 149:367–380
Nelson WA, Sutherland JE, Farr TJ, Hart DR, Neill KF, Kim HJ, Yoon HS (2015) Multi-gene phylogenetic analyses of New Zealand coralline algae: Corallinapetra novaezelandiae gen. et sp. nov. and recognition of the Hapalidiales ord. nov. J Phycol 51:454–468
Pardo C, Peña V, Barreiro R, Bárbara I (2015) A molecular and morphological study of Corallina sensu lato (Corallinales, Rhodophyta) in the Atlantic Iberian Peninsula. Cryptogam Algol 36:31–54
Peña V, Pardo C, López L, Carro B, Hernandez-Kantun J, Adey WH, Bárbara I, Barreiro R, Le Gall L (2015) Phymatolithon lusitanicum sp. nov. (Hapalidiales, Rhodophyta): the third most abundant maerl-forming species in the Atlantic Iberian Peninsula. Cryptogam Algol 36:429–459
Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Rösler A, Perfectti F, Peña V, Braga JC (2016) Phylogenetic relationships of corallinaceae (Corallinales, Rhodophyta): taxonomic implications for reef-building corallines. J Phycol 52:412–431
Saunders GW, Kraft GT (1996) Small-subunit rRNA gene sequences from representatives of selected families of the Gigartinales and Rhodymeniales (Rhodophyta). II. Recognition of the Halymeniales Ord. Nov. Can J Bot 74:694–707
Steneck RS (1986) The ecology of coralline algal crusts: convergent patterns and adaptive strategies. Annu Rev Ecol Syst 17:273–303
Steneck RS, Adey WH (1976) The role of environment in control of morphology in Lithophyllum congestum, a Caribbean algal ridge builder. Bot Mar 19:197–235
Steneck RS, Dethier M (1994) A functional group approach to the structure of algal-dominated communities. Oikos 69:476–498
Swofford DL (2003) PAUP*: Phylogentic analysis using parsimony (* and other methods). Version 4.0b10. Sinauer Associates, Sunderland
Tamura T, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Van der Merwe E, Maneveldt GW (2014) The genus Phymatolithon (Hapalidiaceae, Corallinales, Rhodophyta) in South Africa, including species previously ascribed to Leptophytum. S Afr J Bot 90:170–192
Wang SW (2008) Reef. Newsletter, National Museum of Natural Science, vol 251, ver 5. Retrieved from http://web2.nmns.edu.tw/PubLib/NewsLetter/97/251/5.pdf on 30 January 2018 (in Chinese)
Wang SW (2010) Reef and algal reefs. Newsletter, National Museum of Natural Science, vol 275. Retrieved from http://web2.nmns.edu.tw/PubLib/NewsLetter/99/275/a-6.pdf on 30 January 2018 (in Chinese)
Wilks KM, Woelkerling WJ (1994) An account of southern Australian species of Phymatolithon (Corallinaceae, Rhodophyta) with comments on Leptophytum. Aust Syst Bot 7:183–223
Woelkerling WJ (1988) The coralline red algae. An analysis of the genera and subfamilies of non-geniculate Corallinaceae. British Museum (Natural History), London and Oxford University Press, Oxford, p 268
Woelkerling WJ, Irvine LM (1986) The typification and status of Phymatolithon (Corallinaceae, Rhodophyta). Br Phycol J 21:55–80
Woelkerling WJ, Penrose D, Chamberlain YM (1993) A reassessment of type collections of non-geniculate Corallinaceae (Corallinales, Rhodophyta) described by C. Montagne and L. Dufour, and of Melobesia brassica-florida Harvey. Phycologia 32:323–331
Wolf MA, Falace A, Kaleb S, Moro I (2016) Molecular data confirm the existence of attached crustose tetrasporangial thalli in Phymatolithon calcareum (Melobesioideae, Hapalidiaceae, Rhodophyta) from the Mediterranean Sea. Aquat Bot 134:75–81
Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D. dissertation, University of Texas at Austin
Acknowledgements
SEM imaging was assisted by the Instrumentation Center at National Taiwan Ocean University. We thank Dr. Mark J. Grygier in the Center of Excellence for the Ocean at National Taiwan Ocean University for helping with English writing. We also thank the seaweed lab members Y.-S. Chiou and Y.-C. Wang for assisting with field collecting and specimen sorting.
Funding
Financial support for this study was mainly provided by the MOST research grants (103-2923-B-019-001-MY3, 103-2621-B-019-001, and 104-2621-B-019-001) and the Haiken Foundation Algal Research Fund (104G32401) to SML.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Liu, LC., Lin, SM., Caragnano, A. et al. 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. J Appl Phycol 30, 3455–3469 (2018). https://doi.org/10.1007/s10811-018-1620-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-018-1620-1