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Journal of Applied Phycology

, Volume 30, Issue 6, pp 3455–3469 | Cite as

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

  • Li-Chia Liu
  • Showe-Mei LinEmail author
  • Annalisa Caragnano
  • Claude Payri
8th Asian Pacific Phycological Forum

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.

Keywords

Crustaphytum pacificum gen. and sp. nov. Harveylithon rosea sp. nov. Phymatolithon margoundulatus sp. nov. psbRed algae SSU Taiwan 

Notes

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 information

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.

Supplementary material

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Table S1 (DOC 211 kb)

References

  1. Adey WH (1964) The genus Phymatolithon in the Gulf of Maine. Hydrobiologia 24:377–420CrossRefGoogle Scholar
  2. Adey WH (1965) The genus Clathromorphum in the Gulf of Maine. Hydrobiologia 26:539–573Google Scholar
  3. Adey WH (1966) The genera Lithothamnium, Leptophytum (nov. gen.) and Phymatolithonin the Gulf of Maine. Hydrobiologia 28:321–370Google Scholar
  4. Adey WH (1973) Temperature control of reproduction and productivity in a subarctic coralline alga. Phycologia 12:111–118CrossRefGoogle Scholar
  5. Adey WH (1975) The algal ridges and coral reefs of St. Croix: their structure and Holocene development. Atoll Res Bull 187:1–67CrossRefGoogle Scholar
  6. Adey WH (1998) Coral reefs: algal structured and mediated ecosystems in shallow, turbulent, alkaline waters. J Phycol 34:393–406CrossRefGoogle Scholar
  7. 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 13:100–106CrossRefGoogle Scholar
  8. Adey WH, Johansen HW (1972) Morphology and taxonomy of Corallinaceae with special reference to Clathromorphum, Mesophyllum, and Neopolyporolithon gen. nov. (Rhodophyceae, Cryptonemiales). Phycologia 1:159–180Google Scholar
  9. 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 36:191–204Google Scholar
  10. 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 51:189–203Google Scholar
  11. 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 36:519–533CrossRefGoogle Scholar
  12. 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 33:399–410CrossRefGoogle Scholar
  13. 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 12:551–558Google Scholar
  14. Athanasiadis A, Adey WH (2006) The genus Leptophytum (Melobesioideae, Corallinales, Rhodophyta) on the Pacific coast of North America. Phycologia 45:71–115Google Scholar
  15. Bosence DW (1983a) Coralline algal reef frameworks. J Geol Soc 140:365–376CrossRefGoogle Scholar
  16. Bosence DW (1983b) The occurrence and ecology of recent rhodoliths. A review. In: Tadensz MP (ed) Coated grains. Springer, Berlin, pp 225–242CrossRefGoogle Scholar
  17. Cabioch J (1970) Le maërl des côtes de Bretagne et le problème de sa survie. Penn Ar Bed (Brest) 7:421–429Google Scholar
  18. 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 268:91–105CrossRefGoogle Scholar
  19. 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 26:219–233CrossRefGoogle Scholar
  20. 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)Google Scholar
  21. Foster MS (2001) Rhodoliths: between rocks and soft places. J Phycol 37:659–667CrossRefGoogle Scholar
  22. Freiwald A, Henrich R (1994) Reefal coralline algal build-ups within the Arctic Circle: morphology and sedimentary dynamics under extreme environmental seasonality. Sedimentology 41:963–984CrossRefGoogle Scholar
  23. Guiry MD, Guiry GM (2018) AlgaeBase. World-wide electronic publication. National University of Ireland, Galway http://www.algaebase.org; searched on 30 January 2018Google Scholar
  24. 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 39:988–998CrossRefGoogle Scholar
  25. 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 145Google Scholar
  26. Kaleb S, Falace A, Woelkerling W (2012) Phymatolithon lamii (Hapalidiaceae, Corallinales, Rhodophyta): a first report for the Mediterranean Sea. Bot Mar 55:377–385CrossRefGoogle Scholar
  27. Lebednik PA (1977) Postfertilization development in Clathromorphum, Melobesia and Mesophyllum with comments on the evolution of the Corallinaceae and the Cryptonemiales (Rhodophyta). Phycologia 16:379406Google Scholar
  28. Le Gall L, Payri CE, Bittner L, Saunders GW (2010) Multigene phylogenetic analyses support recognition of the Sporolithales ord. nov. Mol Phylogenet Evol 54:302–305CrossRefGoogle Scholar
  29. Lewis JE, Norris JN (1987) A history and annotated account of the benthic marine algae of Taiwan. Smithson Contrib Mar Sci 29:1–38CrossRefGoogle Scholar
  30. 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 37:881–899CrossRefGoogle Scholar
  31. 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 40:962–976CrossRefGoogle Scholar
  32. Lin HJ, Hsu HF, Liao WS, Lee CL, Liu PJ, Lin SM (2013) Biodiversity of the algal reefs in Taoyuan. J Wetl 2:1–24Google Scholar
  33. Liou C-Y, Yang S-Y, Chen CA (2017) Unprecedented calcareous algal reefs in northern Taiwan merit high conservation priority. Coral Reefs 36:1253CrossRefGoogle Scholar
  34. 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 116:25–44CrossRefGoogle Scholar
  35. 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 74:13–34CrossRefGoogle Scholar
  36. 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 74:555–566CrossRefGoogle Scholar
  37. 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 149:367–380CrossRefGoogle Scholar
  38. 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 51:454–468CrossRefGoogle Scholar
  39. 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 36:31–54CrossRefGoogle Scholar
  40. 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 36:429–459CrossRefGoogle Scholar
  41. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefGoogle Scholar
  42. Rösler A, Perfectti F, Peña V, Braga JC (2016) Phylogenetic relationships of corallinaceae (Corallinales, Rhodophyta): taxonomic implications for reef-building corallines. J Phycol 52:412–431CrossRefGoogle Scholar
  43. 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 74:694–707CrossRefGoogle Scholar
  44. Steneck RS (1986) The ecology of coralline algal crusts: convergent patterns and adaptive strategies. Annu Rev Ecol Syst 17:273–303CrossRefGoogle Scholar
  45. Steneck RS, Adey WH (1976) The role of environment in control of morphology in Lithophyllum congestum, a Caribbean algal ridge builder. Bot Mar 19:197–235CrossRefGoogle Scholar
  46. Steneck RS, Dethier M (1994) A functional group approach to the structure of algal-dominated communities. Oikos 69:476–498CrossRefGoogle Scholar
  47. Swofford DL (2003) PAUP*: Phylogentic analysis using parsimony (* and other methods). Version 4.0b10. Sinauer Associates, SunderlandGoogle Scholar
  48. Tamura T, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefGoogle Scholar
  49. 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 90:170–192CrossRefGoogle Scholar
  50. 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)
  51. 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)
  52. Wilks KM, Woelkerling WJ (1994) An account of southern Australian species of Phymatolithon (Corallinaceae, Rhodophyta) with comments on Leptophytum. Aust Syst Bot 7:183–223CrossRefGoogle Scholar
  53. 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 268Google Scholar
  54. Woelkerling WJ, Irvine LM (1986) The typification and status of Phymatolithon (Corallinaceae, Rhodophyta). Br Phycol J 21:55–80CrossRefGoogle Scholar
  55. 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 32:323–331CrossRefGoogle Scholar
  56. 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 134:75–81CrossRefGoogle Scholar
  57. 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 AustinGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.National Taiwan Ocean UniversityInstitute of Marine BiologyKeelungRepublic of China
  2. 2.Institute de Recherche pour le DéveloppementNouméa CedexNew Caledonia

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