Marine Biodiversity

, Volume 47, Issue 4, pp 1079–1091 | Cite as

Zooxanthellate zoantharians (Anthozoa: Hexacorallia: Zoantharia: Brachycnemina) in the northern Red Sea

  • James Davis Reimer
  • Javier Montenegro
  • Maria E. A. Santos
  • Martyn E. Y. Low
  • Marcela Herrera
  • Remy Gatins
  • May B. Roberts
  • Michael L. Berumen
Red Sea Biodiversity
  • 86 Downloads

Abstract

The Red Sea was one of the first areas of the Indo-Pacific to be investigated by marine taxonomists, and the literature on suborder Brachycnemina (Anthozoa: Hexacorallia: Zoantharia) for this region dates from the early nineteenth century. However, in the last 100 years there has been only one focused study on this group in the Red Sea. In the present study, specimens collected from the Saudi Arabian coast of the northern half of the Red Sea were phylogenetically analyzed by sequencing nuclear internal transcribed spacer regions of ribosomal DNA (ITS-rDNA), mitochondrial cytochrome oxidase subunit I (COI), and 16S ribosomal DNA (16S–rDNA). The new results were compared with historical data in the literature and recent results from the Persian Gulf and the southeastern coast of Africa. Results show the presence of six to seven potential Brachycnemina species in the Red Sea; five to six Palythoa species (Palythoa mutuki, P. tuberculosa, P. cf. heliodiscus, P. aff. heliodiscus, and one to two species within the P. sp. “sakurajimensis” group) together with Zoanthus sansibaricus. While P. mutuki, P. tuberculosa, and Z. sansibaricus are known to be widely distributed in the Indo-Pacific, P. cf. heliodiscus and P. sp. “sakurajimensis” have not been reported from the Persian Gulf or the southeastern coast of Africa, and the current results represent large range extensions for these two species. Only one of the observed species, P. aff. heliodiscus, is potentially endemic to the Red Sea, further demonstrating the generally wide distributions of most zooxanthellate Brachycnemina species.

Keywords

Saudi Arabia Taxonomy Zoogeography Cnidaria Species diversity 

Supplementary material

12526_2017_706_MOESM1_ESM.pdf (480 kb)
Supplementary Figure S1Maximum likelihood (ML) tree of mitochondrial 16S ribosomal DNA (16S–rDNA) sequences of Brachycnemina. Sequences from previous studies with GenBank accession numbers, location, and species name. Sequences from specimens in this study in bold. Values at nodes represent ML and neighbor-joining (NJ) values. (PDF 480 kb)
12526_2017_706_MOESM2_ESM.pdf (177 kb)
Supplementary Figure S2Maximum likelihood (ML) tree of mitochondrial cytochrome oxidase subunit 1 (COI) sequences of Brachycnemina. Sequences from previous studies with GenBank accession numbers, location, and species name. Sequences from specimens in this study in bold. Values at nodes represent ML and neighbor-joining (NJ) values. (PDF 176 kb)
12526_2017_706_MOESM3_ESM.xlsx (17 kb)
Supplementary Table S1Some taxonomic historical notes of Brachycnemina species-group names in the Red Sea. (XLSX 17 kb)
12526_2017_706_MOESM4_ESM.xlsx (20 kb)
Supplementary Table S2Brachycnemina specimens from the northern Red Sea collected in this study, their collection information, GenBank Accession Numbers, and identification. (XLSX 19.7 kb)

References

  1. Acosta A (2001) Asexual reproduction in a zoanthid by fragmentation: the role of exogenous factors. Bull Mar Sci 68:363–381Google Scholar
  2. Acosta A, González AM (2007) Fission in the Zoantharia Palythoa caribaeorum (Duchassaing and Michelotii, 1860) populations: a latitudinal comparison. Bol Invest Mar Cost 36:151–166Google Scholar
  3. Acosta A, Sammarco PW, Duarte LF (2005) New fission processes in the zoanthid Palythoa caribaeorum: description and quantitative aspects. Bull Mar Sci 76:1–26Google Scholar
  4. Aguilar C, Reimer JD (2010) Molecular phylogenetic hypotheses of Zoanthus species (Anthozoa: Hexacorallia) using RNA secondary structure of the internal transcribed spacer 2 (ITS2). Mar Biodivers 40:195–204CrossRefGoogle Scholar
  5. Audouin JV (1826) Explication sommaire des planches de polypes de l’Égypte et de la Syrie, publiées par Jules-César Savigny, membre de l’Institut; offrant un exposé des caractères naturels des genres, avec la distinction des espèces. pp. 225–244. In: Description de l’Égypte ou Recueil des observations et des recherches qui on été faites en Égypte pendant l’expédition de l’armee française, publié par les ordres de Sa Majesté l’empereur Napoléon le Grand. Histoire naturelle. Tome premier. Quatrième partie [Text]. Imprimerie Impériale, ParisGoogle Scholar
  6. Bastidas C, Bone D (1996) Competitive strategies between Palythoa caribaeorum and Zoanthus sociatus (Cnidaria: Anthozoa) at a reef flat environment in Venezuela. Bull Mar Sci 59:543–555Google Scholar
  7. Briggs JC (2003) Marine centres of origin as evolutionary engines. J Biogeogr 30:1–18CrossRefGoogle Scholar
  8. Briggs JC, Bowen BW (2012) A realignment of marine biogeographic provinces with particular reference to fish distributions. J Biogeogr 39:12–30CrossRefGoogle Scholar
  9. Briggs JC, Bowen BW (2013) Marine shelf habitat: biogeography and evolution. J Biogeogr 40:1023–1035CrossRefGoogle Scholar
  10. Burnett WJ (2002) Longitudinal variation in algal symbionts (zooxanthellae) from the Indian Ocean zoanthid Palythoa caesia. Mar Ecol Prog Ser 234:105–109CrossRefGoogle Scholar
  11. Burnett WJ, Ryland JS (1997) Order Zoanthidea. In: Richmond MD (ed) A guide to the seashores of eastern Africa and the Western Indian Ocean Islands. Sida/Department for Research Cooperation, SAREC, Stockholm, pp 138–139Google Scholar
  12. Burnett WJ, Benzie JAH, Beardmore JA, Ryland JS (1994) High genetic variability and patchiness in a common Great Barrier Reef zoanthid (Palythoa caesia). Mar Biol 121:153–160CrossRefGoogle Scholar
  13. Burnett WJ, Benzie JAH, Beardmore J, Ryland JS (1995) Patterns of genetic subdivision in populations of a clonal cnidarian, Zoanthus coppingeri, from the Great Barrier Reef. Mar Biol 122:665–673CrossRefGoogle Scholar
  14. Burnett WJ, Benzie JAH, Beardmore JA, Ryland JS (1997) Zoanthids (Anthozoa, Hexacorallia) from the Great Barrier Reef and Torres Strait, Australia: systematics, evolution and a key to species. Coral Reefs 16:55–68CrossRefGoogle Scholar
  15. Carlgren O (1900) Ostafrikanische Actinien, gesammelt von Herrn Dr. F. Stuhlmann 1898 und 1899. Mitt aus dem Naturhist Mus Hambg 17(Supplement 2):21–144 pls. 1–7Google Scholar
  16. Carlgren O (1939) South African Actiniaria and Zoantharia. Kungliga Svenska Vetenskapsakademiens Handlingar, ser. 3, 17(3):1–148, pls. 1–3Google Scholar
  17. Chimetto LA, Brocchi M, Gondo M, Thompson CC, Gomez-Gil B, Thompson FL (2009) Genomic diversity of vibrios associated with the Brazilian coral Mussismilia hispida and its sympatric zoanthids (Palythoa caribaeorum, Palythoa variabilis and Zoanthus solanderi). J Appl Microbiol 106:1818–1826CrossRefPubMedGoogle Scholar
  18. Costa OS Jr, Nimmo M, Attrill MJ (2008) Coastal nutrification in Brazil: a review of the role of nutrient excess on coral reef demise. J S Am Earth Sci 25:257–270CrossRefGoogle Scholar
  19. Cruz ICS, Loiola M, Albuquerque T, Reis R, Nunes JACC, Reimer JD, Mizuyama M, Kikuchi RKP, Creed JC (2015) Effect of phase shift from corals to Zoantharia on reef fish assemblages. PLoS One 10:e0116944CrossRefPubMedPubMedCentralGoogle Scholar
  20. Cruz ICS, Henschen VM, Kikuchi RK, Creed JC (2016) The role of competition in the phase shift to dominance of the zoanthid Palythoa cf. variabilis on coral reefs. Mar Environ Res 115:28–35CrossRefPubMedGoogle Scholar
  21. DiBattista JD, Roberts MB, Bouwmeester J, Bowen BW, Coker DJ, Lozano-Cortes DF, Choat JH, Gaither MR, Hobbs JPA, Khalil MT, Kochzius M, Myers R, Paulay G, Robitzch VSN, Saenz-Agudelo P, Salas E, Sinclair-Taylor TH, Toonen RJ, Westneat MW, Williams ST, Berumen ML (2016) A review of contemporary patterns of endemism for shallow water reef Fauna in the Red Sea. J Biogeogr 43:423–439CrossRefGoogle Scholar
  22. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32:1792–1797CrossRefPubMedPubMedCentralGoogle Scholar
  23. Ehrenberg CG (1834) Beiträge zur physiologischen Kenntniss der Corallenthiere im allgemeinen, und besonders des rother Meeres, nebst einem Versuche zur physiologischen Systematik derselbe. Abhandlungen der Königlichen Akademie der Wissenschaften zu Berlin 1832(1):225–380 1 tableGoogle Scholar
  24. Ekman S (1953) Zoogeography of the sea. Sigwick and Jackson, LondonGoogle Scholar
  25. Esper EJC (1805) Die Pflanzenthiere in Abbildungen nach der Natur mit Farben erleuchtet nebst Beschreibungen. Raspe, Nürnberg. Theilen 1–3, Lieferungen 13Google Scholar
  26. Fautin DG Buddemeier RW (2008) Biogeoinformatics of the Hexacorals: http://www.kgs.ku.edu/Hexacoral/
  27. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299PubMedGoogle Scholar
  28. Fujii T, Reimer JD (2013) A new family of diminutive zooxanthellate zoanthids (Hexacorallia: Zoantharia). Zool J Linnean Soc 169:509–522CrossRefGoogle Scholar
  29. Goreau T (1959) The ecology of Jamaican coral reefs I. Species composition and zonation. Ecology 40:67–90CrossRefGoogle Scholar
  30. Gray JE (1828) Radiata. In: Spicilegia zoologica; or Original Figures and Short Systematic Descriptions of New and Unfigured Animals. Treüttel, Würtz and Co., London, vol. 1, p. 8, pl. 6Google Scholar
  31. Gray JE (1832) [T]he Animal Flowers, or Zoantharia, and the stellated corals. In: Synopsis of the Contents of the British Museum, Twenty-Sixth edn. G. Woodfall and Son, London, pp 94–106Google Scholar
  32. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321. doi:10.1093/sysbio/syq010 CrossRefPubMedGoogle Scholar
  33. Haddon AC, Shackleton AM (1891a) The Zoantheae. A revision of the British Actiniae. Part II. Reports on the zoological collections made in the Torres Straits by AC Haddon, 1888–1889. Sci Trans R Dublin Soc ser. 2, 4(12):609–672, pls. 58–60Google Scholar
  34. Haddon AC, Shackleton AM (1891b) Reports on the zoological collections made in Torres Straits by Professor A.C. Haddon, 1888–1889. Actiniae: I. Zoantheae. Sci Trans R Dublin Soc 4:673–701Google Scholar
  35. Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174CrossRefPubMedGoogle Scholar
  36. Herberts C (1972) Etude systématique de quelques zoanthaires tempérés et tropicaux. Tethys Supplement 3:69–156Google Scholar
  37. Hertwig R (1882) Report on the Actiniaria dredged by H.M.S. Challenger during the years 1873–1876. In: Report of the Scientific Results of the Voyage of H.M.S. Challenger During the Years 1873–76, Under the Command of Captain George S. Nares, R.N., F.R.S. and the Late Captain Frank Tourle Thomson, R.N. Prepared Under the Superintendence of the Late Sir C. Wyville Thomson, Knt., F.R.S., &C. regius Professor of Natural History in the University of Edinburgh Director of the Civilian Scientific Staff on Board and Now of John Murray, LL.D., Ph.D., &c. One of the Naturalists of the Expedition. Zoology—Vol. VI. Her Majesty’s Government, Edinburgh. pp. 1–136, pls. 1–14Google Scholar
  38. Hibino Y, Todd PA, Yang SY, Benayahu Y, Reimer JD (2013) Molecular and morphological evidence for conspecificity of two common Indo-Pacific species of Palythoa (Cnidaria: Anthozoa). Hydrobiologia 733:31–43CrossRefGoogle Scholar
  39. Huang D, Meier R, Todd PA, Chou LM (2008) Slow mitochondrial COI sequence evolution at the base of the metazoan tree and its implications for DNA barcoding. J Mol Evol 66:167–174Google Scholar
  40. Irei Y, Nozawa Y, Reimer JD (2011) Distribution patterns of five zoanthid species in Okinawa Island, Japan. Zool Stud 50:426–433Google Scholar
  41. Joseph S, Poriya P, Kundu R (2014) Probing the phylogenetic relationships of a few newly recorded intertidal zoanthids of Gujarat coast (India) with mt DNA COI sequences. Mitochondrial DNA 1736:1–7Google Scholar
  42. Kamezaki M, Higa M, Hirose M, Suda S, Reimer JD (2013) Different zooxanthellae types in populations of the zoanthid Zoanthus sansibaricus along depth gradients in Okinawa, Japan. Mar Biodivers 43:61–70CrossRefGoogle Scholar
  43. Karlson RH (1983) Disturbance and monopolization of a spatial resource by Zoanthus sociatus (Coelenterata, Anthozoa). Bull Mar Sci 13:118–131Google Scholar
  44. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649CrossRefPubMedPubMedCentralGoogle Scholar
  45. Kelecom A, Solé-Cava AM (1982) Comparative study of zoanthid sterols the genus Palythoa (Hexacorallia, Zoanthidea). Comp Biochem Physiol 72B:677–682Google Scholar
  46. Khushali PM, Pradeep MC (2013) Brachycnemic zooxanthellate zoanthids (Cnidaria: Zoantharia) of Saurashtra coast: a preliminary survey. Res J Mar Sci 1:10–13Google Scholar
  47. Klunzinger KB (1877) Die Korallthiere des Rothen Meeres. 1: Die Alcyonarien und Malacodermen. Verlag der Gutmann’schen Buchhandlung (Otto Enslin), Berlin [in German and Latin]Google Scholar
  48. Koupaei AN, Mostafavi PG, Mehrabadi JF, Fatemi SMR (2014) Molecular diversity of coral reef-associated zoanthids off Qeshm Island, northern Persian Gulf. Int Aquat Res 6:1–10CrossRefGoogle Scholar
  49. Koupaei AN, Mostavi PG, Mehrabadi JF, Fatemi SMR, Dehghani H (2015) Diversity of shallow water zoantharians in Hengam and Larak Islands, in the Persian Gulf. J Mar Biol Assoc UK:1–11. doi:10.1017/S002531541500079X
  50. Lamarck JBP (1801) Zoanthe. Zoantha. In: Systême des animaux vertèbres, ou Tableau général des classes, des ordres et des genres de ces animaux; Présentant leurs caractères essentiels et leur distribution, d’après la considération de leurs rapports naturels et leur organisation, et suivant l’arrangement établis dans les galeries du Muséum d’Histoire Naturelle, parmi leur dépouilles conservées; Précédé du discours d’ouverture du cours de zoologie, donné dans le Muséum National d’Histoire Naturelle l’an 8 de la République. L’Auteur et Déterville, Paris, p. 363Google Scholar
  51. Lamouroux JVF (1816) Histoire des polypiers coralligènes flexibles, vulgairement nommés zoophytes. F. Poisson, Caen, lxxxiv + [1] + 559 + [1] pp., pls. 1–19Google Scholar
  52. Longo GO, Krajewski JP, Segal B, Floeter SR (2012) First record of predation on reproductive Palythoa caribaeorum (Anthozoa: Sphenopidae): insights on the trade-off between chemical defences and nutritional value. Mar Biodivers Rec 5:1–3CrossRefGoogle Scholar
  53. Milne Edwards H (1857) Histoire naturelle des coralliaires ou polypes proprement dits. Tome premier. Roret, Paris, xxxiv + 326 pp. [5 Dec 1857 (Anonymous, 1857: 634)]Google Scholar
  54. Miyashita M, Sasaki M, Hattori I, Sakai M, Tanino K (2004) Total synthesis of norzoanthamine. Science 305:495–499CrossRefPubMedGoogle Scholar
  55. Oigman-Pszczol SS, Figueiredo MADO, Creed JC (2004) Distribution of benthic communities on the tropical rocky subtidal of Armação dos Búzios, southeastern Brazil. Mar Ecol 25:173–190CrossRefGoogle Scholar
  56. Ong CW, Reimer JD, Todd PA (2013) Morphologically plastic responses to shading in the zoanthids Zoanthus sansibaricus and Palythoa tuberculosa. Mar Biol 160:1053–1064CrossRefGoogle Scholar
  57. Pax F (1910) Studien an westindischen Actinien. Habilitationsschrift, welche nebst den beigefügten Thesen mit Genehmigung der hohen philosophischen Fakultät der Königlichen Universität Breslau zur Erlangung der Venia legendi. Montag, den 17. Oktober 1910, um 12 Uhr, im Musiksaale der Universität öffentlich verteidigen wird. Gustav Fischer, Jena, 166 + [2] pp., 10 plsGoogle Scholar
  58. Pax F, Muller I (1956) Zoanthaires de la Mer Rouge. Annales de l’Institut Océanographique 32:1–77Google Scholar
  59. Polak O, Loya Y, Brickner I (2011) The widely-distributed Indo-Pacific zoanthid Palythoa tuberculosa: a sexually conservative strategist. Bull Mar Sci 87:605–621CrossRefGoogle Scholar
  60. Rafinesque CS (1815) Analyse de la nature ou tableau de l’univers et des corps organisés. [The Author], Palerme [= Palermo]Google Scholar
  61. Reimer AA (1971) Feeding behavior in the Hawaiian zoanthids Palythoa and Zoanthus. Pac Sci 25:512–520Google Scholar
  62. Reimer JD, Todd PA (2009) Preliminary molecular examination of zooxanthellate zoanthids (Hexacorallia: Zoantharia) and associated zooxanthellae (Symbiodinium spp.) diversity in Singapore. Raffles Bull Zool 22:103–120Google Scholar
  63. Reimer JD, Ono S, Fujiwara Y, Takishita K, Tsukahara J (2004) Reconsidering Zoanthus spp. diversity: molecular evidence of conspecifity within four previously presumed species. Zool Sci 21:517–525CrossRefPubMedGoogle Scholar
  64. Reimer JD, Ono S, Takishita K, Tsukahara J, Maruyama T (2006) Molecular evidence suggesting species in the zoanthid genera Palythoa and Protopalythoa (Anthozoa: Hexacorallia) are congeneric. Zool Sci 23:87–94CrossRefPubMedGoogle Scholar
  65. Reimer JD, Hirano S, Fujiwara Y, Sinniger F, Maruyama T (2007a) Morphological and molecular characterization of Abyssoanthus nankaiensis, a new family, new genus and new species of deep-sea zoanthid (Anthozoa: Hexacorallia: Zoantharia) from a northwest Pacific methane cold seep. Invert Syst 21(3):255–262CrossRefGoogle Scholar
  66. Reimer JD, Takishita K, Ono S, Maruyama T (2007b) Diversity and evolution in the zoanthid genus Palythoa (Cnidaria: Hexacorallia) based on nuclear ITS-rDNA. Coral Reefs 399–410Google Scholar
  67. Reimer JD, Takishita K, Ono S, Tsukahara J, Maruyama T (2007c) Molecular evidence suggesting intraspecific hybridization in Zoanthus (Anthozoa: Hexacorallia). Zool Sci 24:346–359CrossRefPubMedGoogle Scholar
  68. Reimer JD, Sinniger F, Hickman CP (2008) Zoanthid diversity (Anthozoa: Hexacorallia) in the Galapagos Islands: a molecular examination. Coral Reefs 27:641–654CrossRefGoogle Scholar
  69. Reimer JD, Obuchi M, Irei Y, Fujii T, Nozawa Y (2011) Shallow-water brachycnemic zoanthids (Cnidaria : Hexacorallia) from Taiwan: a preliminary survey. Zool Stud 50:363–371Google Scholar
  70. Reimer JD, Poliseno A, Hoeksema BW (2014) Shallow-water zoantharians (Cnidaria, Hexacorallia) from the Central Indo-Pacific. ZooKeys 57:1–57CrossRefGoogle Scholar
  71. Reimer JD, Wee HB, Put A Jr, Hoeksema BW (2015) Zoantharia (Cnidaria: Anthozoa: Hexacorallia) of the South China Sea and Gulf of Thailand: species list based on past reports and new photographic records. Raffles Bull Zool 63:334–356Google Scholar
  72. Reimer JD, Kim S, Arai S, Keshavmurthy S, Choi K (2016a) First records of zooxanthellae Zoanthus (Anthozoa: Hexacorallia: Zoantharia) from Korea and Japan (East) Sea. Mar Biodivers. doi:10.1007/s12526-016-0567-1 Google Scholar
  73. Reimer JD, Herrera M, Gatins R, Roberts MB, Parkinson JE, Berumen ML (2016b) Latitudinal variation in the symbiotic dinoflagellate Symbiodinium of the common reef zoantharian Palythoa tuberculosa on the Saudi Arabian coast of the Red Sea. J Biogeogr. doi:10.1111/jbi.12795 Google Scholar
  74. Risi MM, Macdonald AHH (2015) Possible synonymies of Zoanthus (Anthozoa: Hexacorallia) species on the east coast of South Africa with Pacific congeners. Syst Biodivers 13:93–103CrossRefGoogle Scholar
  75. Risi MM, Macdonald AHH (2016) Molecular examination of rocky shore brachycnemic zoantharians (Anthozoa: Hexacorallia) and their Symbiodinium symbionts (Dinophyceae) in the southwest Indian Ocean. Mar Biodivers 46:113–127CrossRefGoogle Scholar
  76. Rocha LA, Rocha CR, Robertson DR, Bowen BW (2008) Comparative phylogeography of Atlantic reef fishes indicates both origin and accumulation of diversity in the Caribbean. BMC Evol Biol 8:157CrossRefPubMedPubMedCentralGoogle Scholar
  77. Ryland JS (2015) Size-defined morphotypes in Zoanthus (Hexacorallia: Zoantharia) populations on shores in KwaZulu-Natal, South Africa. Zootaxa 3986:332–356CrossRefPubMedGoogle Scholar
  78. Ryland JS, Lancaster JE (2003) Revision of methods for separating species of Protopalythoa (Hexacorallia: Zoanthidea) in the tropical West Pacific. Invert Syst 17:407–428CrossRefGoogle Scholar
  79. Santana EFC, Alves AL, Santos ADM, Cunha MGGS, Perez CD, Gomes PB (2015) Trophic ecology of the zoanthid Palythoa caribaeorum (Cnidaria: Anthozoa) on tropical reefs. J Mar Biol Assoc UK 95:301–309CrossRefGoogle Scholar
  80. Santos MEA, Kitahara MV, Lindner A, Reimer JD (2016) Overview of the order Zoantharia (Cnidaria: Anthozoa) in Brazil. Mar Biodivers 46:547–559CrossRefGoogle Scholar
  81. Savigny J-C (1811) Description de l’Égypte ou Recueil des observations et des recherches qui on été faites en Égypte pendant l’expédition de l’armee française, publié par les ordres de Sa Majesté l’empereur Napoléon le Grand. Histoire naturelle. Tome deuxième [Atlas]. Imprimerie Impériale, Paris, pls. Polypes 1–14Google Scholar
  82. Sebens K (1977) Autotrophic and heterotrophic nutrition of coral reef zoanthids. Proc 3rd Int Coral Reef Symp 1:397–404Google Scholar
  83. Shearer TL, Van Oppen MJ, Romano SL, Wörheide G (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Mol Ecol 11:2475–2487Google Scholar
  84. Sinniger F, Montoya-Burgos JI, Chevaldonné P, Pawlowski J (2005) Phylogeny of the order Zoantharia (Anthozoa, Hexacorallia) based on the mitochondrial ribosomal genes. Mar Biol 147:1121–1128CrossRefGoogle Scholar
  85. Sinniger F, Reimer JD, Pawlowski J (2008) Potential of DNA sequences to identify zoanthids (Cnidaria: Zoantharia). Zool Sci 25:1253–1260CrossRefPubMedGoogle Scholar
  86. Soares C, Pérez C, Maia MBS, Silva RS, Melo LFA (2006) Avaliação da atividade antiinflamatória e analgésica do extrato bruto hidroalcoólico do zoantídeo Palythoa caribaeorum (Duchassaing & Michelotti, 1860). Braz J Pharmacogn 16:463–468CrossRefGoogle Scholar
  87. Stampar SN, Francisco P, Luiz OJ Jr (2007) Predation on the zoanthid Palythoa caribaeorum (Anthozoa, Cnidaria) by a hawksbill turtle (Eretmochelys imbricata) (Reptilia, Vertebrata) in southeastern Brazil. Mar Turtle Newsletter 117:3–5Google Scholar
  88. Swain TD, Swain LM (2014) Molecular parataxonomy as taxon description: examples from recently named Zoanthidea (Cnidaria: Anthozoa) with revision based on serial histology of microanatomy. Zootaxa 3796:81–107CrossRefGoogle Scholar
  89. Swain TD, Schellinger JL, Strimaitis AM, Reuter KE (2015) Evolution of anthozoan polyp retraction mechanisms: convergent functional morphology and evolutionary allometry of the marginal musculature in order Zoanthidea (Cnidaria: Anthozoa: Hexacorallia). BMC Evol Biol 15:123CrossRefPubMedPubMedCentralGoogle Scholar
  90. Swain TD, Strimaitis AM, Reuter KE, Boudreau W (2016) Towards integrative systematics of Anthozoa (Cnidaria): evolution of form in the order Zoanthidea. Zool Scr:1–18. doi:10.1111/zsc.12195
  91. Vermeij GJ (1978) Biogeography and adaptation: patterns of marine life. Harvard University Press, Cambridge, MAGoogle Scholar
  92. Verrill AE (1928) Hawaiian shallow water Anthozoa. Bull Bernice P Bishop Museum 49:1–30Google Scholar
  93. Villaça R, Pitombo FB (1997) Benthic communities of shallow-water reefs of Abrolhos, Brazil. Rev Bras Oceanogr 45:35–43CrossRefGoogle Scholar
  94. Walsh GE, Bowers RL (1971) A review of the Hawaiian zoanthids with descriptions of three new species. Zool J Linnean Soc 50:161–180CrossRefGoogle Scholar
  95. WoRMS Editorial Board (2016). World Register of Marine Species. Available from http://www.marinespecies.org at VLIZ. Accessed 2016–11-26. doi:10.14284/170

Copyright information

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

Authors and Affiliations

  1. 1.Molecular Invertebrate and Systematics Ecology Laboratory, Graduate School of Engineering and ScienceUniversity of the RyukyusOkinawaJapan
  2. 2.Tropical Biosphere Research CenterUniversity of the RyukyusOkinawaJapan
  3. 3.Lee Kong Chian Museum of Natural HistoryNational University of SingaporeSingaporeRepublic of Singapore
  4. 4.Division of Biological and Environmental Sciences and Engineering, Red Sea Research CenterKing Abdullah University of Science and TechnologyThuwalSaudi Arabia

Personalised recommendations