Marine Biodiversity

, Volume 48, Issue 4, pp 1961–1967 | Cite as

Rare zooxanthellate Nanipora octocoral (Helioporacea) in the Gulf of Thailand

  • Pau Urgell Plaza
  • Rahul MehrotraEmail author
  • Chad M. Scott
  • James Davis Reimer
Original Paper


The octocoral Nanipora kamurai is the fifth species of octocoral described with an aragonite skeleton. So far, it has only been known from a single location in Okinawa, Japan. Here, we report on the second recorded location of the genus Nanipora, in the Gulf of Thailand, where its colonies were found in relatively high densities. A total of 143 separate Nanipora colonies were counted in transects on a coral reef at Koh Tao, Thailand. They were found living on dead coral skeletons and on the shell of a living Tridacna squamosa clam. Phylogenetic analyses of cytochrome oxidase subunit 1 (COI) and mitochondrial mismatch repair protein (mtMutS) sequences showed that they belong to N. kamurai or to a close relative of this species. Additionally, a symbiotic relationship with Symbiodinium was observed for the first time in Nanipora, confirmed by sequences of the internal transcribed spacer region of ribosomal DNA (ITS-rDNA) of the dinoflagellate.


Aragonite skeleton Symbiodinium Koh Tao, Thailand Rarity COI mtMutS 



The authors would like to thank Dr. Yehuda Benayahu, Dr. Leen van Ofwegen, Dr. Catherine McFadden, and Dr. Juan Armando Sánchez Muñoz for their input and advice, and Dr. Caterina Carbonell for invaluable assistance in the field and lab. This research was partially funded by the Ratchadaphiseksomphot Endowment Fund (CU-56-921-CC) and by King Chulalongkorn University, Thailand (RES560530213 CC). Comments from the three anonymous reviewers greatly improved an earlier version of the manuscript.


  1. Arrigoni R, Kitano YF, Stolarski J, Hoeksema BW, Fukami H, Stefani F, Galli P, Montano S, Castoldi E, Benzoni F (2014) A phylogeny reconstruction of the Dendrophylliidae (Cnidaria, Scleractinia) based on molecular and micromorphological criteria, and its ecological implications. Zool Scr 43:661–688. doi: 10.1111/zsc.12072 CrossRefGoogle Scholar
  2. Bayer FM (1992) The Helioporacean octocoral Epiphaxum, recent and fossil: a monographic iconography. Stud Trop Occeanogr Miami 15:1–76Google Scholar
  3. Bayer FM, Muzik KM (1977) An Atlantic Helioporan coral (Coelenterata; Octocorallia). Proc Biol Soc Wash 90:975–984Google Scholar
  4. Brockman SA, McFadden CS (2012) The mitochondrial genome of paraminabea aldersladei (Cnidaria: Anthozoa: Octocorallia) supports intramolecular recombination as the primary mechanism of gene rearrangement in octocoral mitochondrial genomes. Genome Biol Evol 4(9):994–1006Google Scholar
  5. Chen CA, Willis BL, Miller DJ (1996) Systematic relationships between tropical corallimorpharians (Cnidaria: Anthozoa: Corallimorpharia): utility of the 5.8 S and internal transcribed spacer (ITS) regions of the rRNA transcription unit. Bull Mar Sci 59:196–208Google Scholar
  6. Dolan E, Tyler PA, Yesson C, Rogers AD (2013) Phylogeny and systematics of deep-sea sea pens (Anthozoa: Octocorallia: Pennatulacea). Mol Phylogenet Evol 69(3):610–618Google Scholar
  7. France SC, Hoover LL (2002) DNA sequences of the mitochondrial COI gene have low levels of divergence among deep-sea octocorals (Cnidaria: Anthozoa). Hydrobiologia 471:149–155. doi: 10.1023/A:1016517724749 CrossRefGoogle Scholar
  8. Gori A (2011) The ecology of deep sublittoral populations of Mediterranean gorgonians. Doctoral thesis, Universitat de Barcelona, CataloniaGoogle Scholar
  9. Goulet TL, Simmons C, Goulet D (2008) Worldwide biogeography of Symbiodinium in tropical octocorals. Mar Ecol Prog Ser 355:45–58. doi: 10.3354/meps07214 CrossRefGoogle Scholar
  10. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  11. Hoeksema BW (2012) Forever in the dark: the cave-dwelling azooxanthellate reef coral Leptoseris troglodyta sp. n. (Scleractinia, Agariciidae). ZooKeys 228:21–37. doi: 10.3897/zookeys.228.3798 CrossRefGoogle Scholar
  12. Irei Y, Sinniger F, Reimer JD (2015) Descriptions of two azooxanthellate Palythoa species (subclass Hexacorallia, order Zoantharia) from the Ryukyu archipelago, southern Japan. ZooKeys 478:1–26. doi: 10.3897/zookeys.478.8512 CrossRefGoogle Scholar
  13. Jell J, Sorauf JE (1999) Tubipora musica Linnaeus, its calcitic skeleton and palaeontological significance. In: Proceedings of the 8th International Symposium on Fossil Cnidaria and Porifera, Tohoku University, Sendai, Japan, September 1999, p 42Google Scholar
  14. Jeng MS, Huang HD, Dai CF, Hsiao YC, Benayahu Y (2011) Sclerite calcification and reef-building in the fleshy octocoral genus Sinularia (Octocorallia: Alcyonacea). Coral Reefs 30:925–933. doi: 10.1007/s00338-011-0765-z CrossRefGoogle Scholar
  15. Kimball JB, Dunbar RB, Guilderson TP (2014) Oxygen and carbon isotope fractionation in calcitic deep-sea corals: implications for paleotemperature reconstruction. Chem Geol 381:223–233. doi: 10.1016/j.chemgeo.2014.05.008 CrossRefGoogle Scholar
  16. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. doi: 10.1093/molbev/msw054 CrossRefGoogle Scholar
  17. LaJeunesse TC, Pettay DT, Sampayo EM, Phongsuwan N, Brown B, Obura DO, Hoegh-Guldberg O, Fitt WK (2010) Long-standing environmental conditions, geographic isolation and host–symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. J Biogeogr 37:785–800. doi: 10.1111/j.1365-2699.2010.02273.x CrossRefGoogle Scholar
  18. LaJeunesse TC, Wham DC, Pettay DT, Parkinson JE, Keshavmurthy S, Chen CA (2014) Ecologically differentiated stress-tolerant endosymbionts in the dinoflagellate genus (Dinophyceae) Clade D are different species. Phycologia 53(4):305–319Google Scholar
  19. McFadden CS, van Ofwegen LP (2012) Stoloniferous octocorals (Anthozoa, Octocorallia) from South Africa, with descriptions of a new family of Alcyonacea, a new genus of Clavulariidae, and a new species of Cornularia (Cornulariidae). Invertebr Syst 26:331-356Google Scholar
  20. McFadden CS, Tullis ID, Hutchinson MB, Winner K, Sohm JA (2004) Variation in coding (NADH dehydrogenase subunits 2, 3, and 6) and noncoding intergenic spacer regions of the mitochondrial genome in Octocorallia (Cnidaria: Anthozoa). Mar Biotechnol 6:516–526. doi: 10.1007/s10126-002-0102-1 CrossRefPubMedGoogle Scholar
  21. McFadden CS, France SC, Sánchez JA, Alderslade P (2006) A molecular phylogenetic analysis of the Octocorallia (Cnidaria: Anthozoa) based on mitochondrial protein-coding sequences. Mol Phylogenet Evol 41(3):513–527Google Scholar
  22. McFadden CS, Benayahu Y, Pante E, Thoma JN, Nevarez PA, France SC (2011) Limitations of mitochondrial gene barcoding in Octocorallia. Mol Ecol Resour 11:19–31. doi: 10.1111/j.1755-0998.2010.02875.x CrossRefPubMedGoogle Scholar
  23. McFadden CS, Brown AS, Brayton C, Hunt CB, van Ofwegen LP (2014) Application of DNA barcoding in biodiversity studies of shallow-water octocorals: molecular proxies agree with morphological estimates of species richness in Palau. Coral Reefs 33:275–286. doi: 10.1007/s00338-013-1123-0 CrossRefGoogle Scholar
  24. Miyazaki Y, Reimer JD (2015) A new genus and species of octocoral with aragonite calcium-carbonate skeleton (Octocorallia, Helioporacea) from Okinawa, Japan. ZooKeys 511:1–23. doi: 10.3897/zookeys.511.9432 CrossRefGoogle Scholar
  25. Miyazaki Y, Santos MEA, Kunihiro S, Weinstein DK, Reimer JD (2016) Rarity of Nanipora kamurai (Anthozoa: Octocorallia: Helioporacea) at its type locality. Mar Biodivers 46:917–921. doi: 10.1007/s12526-015-0435-4 CrossRefGoogle Scholar
  26. Neo ML, Eckman W, Vicentuan K, Teo SLM, Todd PA (2015) The ecological significance of giant clams in coral reef ecosystems. Biol Conserv 181:111–123. doi: 10.1016/j.biocon.2014.11.004 CrossRefGoogle Scholar
  27. Perrin J, Vielzeuf D, Ricolleau A, Dallaporta H, Valton S, Floquet N (2015) Block-by-block and layer-by-layer growth modes in coral skeletons. Am Mineral 100:681–695. doi: 10.2138/am-2015-4990 CrossRefGoogle Scholar
  28. Sánchez JA (2016) Diversity and evolution of octocoral animal forests at both sides of tropical America. In: Rossi S, Bramanti L, Gori A, Orejas C (eds) Marine animal forests. Springer International, pp 1–33. doi: 10.1007/978-3-319-17001-5_39-1
  29. Sánchez JA, McFadden CS, France SC, Lasker HR (2003) Molecular phylogenetic analyses of shallow-water Caribbean octocorals. Mar Biol 142:975–987. doi: 10.1007/s00227-003-1018-7 CrossRefGoogle Scholar
  30. Santiago-Vázquez LZ, Ranzer LK, Kerr RG (2006) Comparison of two total RNA extraction protocols using the marine gorgonian coral Pseudopterogorgia elisabethae and its symbiont Symbiodinium sp. Electron J Biotechnol 9:598–603. doi: 10.2225/vol9-issue5-fulltext-15 CrossRefGoogle Scholar
  31. Santodomingo N, Reyes J, Gracia A, Martínez A, Ojeda G, García C (2007) Azooxanthellate Madracis coral communities off San Bernardo and Rosario Islands (Colombian Caribbean). Bull Mar Sci 81:273–287Google Scholar
  32. Spiro BF (1971) Ultrastructure and chemistry of the skeleton of Tubipora musica Linné. Bull Geol Soc Den 20:279–284Google Scholar
  33. Tamura K (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+ C-content biases. Mol Biol Evol 9:678–687PubMedGoogle Scholar
  34. van der Schoot R, Scott CM, ten Hove HA, Hoeksema BW (2016) Christmas tree worms as epibionts of giant clams at Koh Tao, Gulf of Thailand. Mar Biodivers 46:751–752. doi: 10.1007/s12526-015-0439-0 CrossRefGoogle Scholar
  35. van Ofwegen L (2016) Octocorallia. Accessed through: World Register of Marine Species at on 2016-12-16
  36. van Oppen MJ, Palstra FP, Piquet AMT, Miller DJ (2001) Patterns of coral–dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host–symbiont selectivity. Proc R Soc Lond B 268:1759–1767. doi: 10.1098/rspb.2001.1733 CrossRefGoogle Scholar
  37. van Oppen MJ, Mieog JC, Sanchez CA, Fabricius KE (2005) Diversity of algal endosymbionts (zooxanthellae) in octocorals: the roles of geography and host relationships. Mol Ecol 14:2403–2417. doi: 10.1111/j.1365-294X.2005.02545.x CrossRefPubMedGoogle Scholar
  38. Vicentuan-Cabaitan K, Neo ML, Eckman W, Teo SLM, Todd PA (2014) Giant clam shells host a multitude of epibionts. Bull Mar Sci 90:795–796. doi: 10.5343/bms.2014.1010 CrossRefGoogle Scholar
  39. Williams GC, Delbeek JC, Shepherd B, Wolters S (2010) Zooxanthellae in ellisellid gorgonians of the Philippines. Proc Calif Acad Sci 61:647–648Google Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.New Heaven Reef Conservation ProgramSurat ThaniThailand
  2. 2.Reef Biology Research Group, Department of Marine Science, Faculty of ScienceChulalongkorn UniversityBangkokThailand
  3. 3.Molecular Invertebrate and Systematics Ecology Laboratory, Department of Biology, Chemistry and Marine Sciences, Faculty of ScienceUniversity of the RyukyusNishiharaJapan
  4. 4.Tropical Biosphere Research CenterUniversity of the RyukyusNishiharaJapan

Personalised recommendations