Skip to main content

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

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Acosta A (2001) Asexual reproduction in a zoanthid by fragmentation: the role of exogenous factors. Bull Mar Sci 68:363–381

    Google 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 36:151–166

    Google Scholar 

  3. Acosta A, Sammarco PW, Duarte LF (2005) New fission processes in the zoanthid Palythoa caribaeorum: description and quantitative aspects. Bull Mar Sci 76:1–26

    Google 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 40:195–204

    Article  Google 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, Paris

  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 59:543–555

    Google Scholar 

  7. Briggs JC (2003) Marine centres of origin as evolutionary engines. J Biogeogr 30:1–18

    Article  Google Scholar 

  8. Briggs JC, Bowen BW (2012) A realignment of marine biogeographic provinces with particular reference to fish distributions. J Biogeogr 39:12–30

    Article  Google Scholar 

  9. Briggs JC, Bowen BW (2013) Marine shelf habitat: biogeography and evolution. J Biogeogr 40:1023–1035

    Article  Google Scholar 

  10. Burnett WJ (2002) Longitudinal variation in algal symbionts (zooxanthellae) from the Indian Ocean zoanthid Palythoa caesia. Mar Ecol Prog Ser 234:105–109

    Article  Google 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 138–139

    Google 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 121:153–160

    Article  Google 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 122:665–673

    Article  Google 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 16:55–68

    Article  Google 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. 1–7

    Google Scholar 

  16. Carlgren O (1939) South African Actiniaria and Zoantharia. Kungliga Svenska Vetenskapsakademiens Handlingar, ser. 3, 17(3):1–148, pls. 1–3

  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 106:1818–1826

    CAS  Article  PubMed  Google 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 25:257–270

    Article  Google 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:e0116944

    Article  PubMed  PubMed Central  Google 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 115:28–35

    CAS  Article  PubMed  Google 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 43:423–439

    Article  Google Scholar 

  22. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32:1792–1797

    CAS  Article  PubMed  PubMed Central  Google 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 table

    Google Scholar 

  24. Ekman S (1953) Zoogeography of the sea. Sigwick and Jackson, London

    Google Scholar 

  25. Esper EJC (1805) Die Pflanzenthiere in Abbildungen nach der Natur mit Farben erleuchtet nebst Beschreibungen. Raspe, Nürnberg. Theilen 1–3, Lieferungen 13

  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 3:294–299

    CAS  PubMed  Google Scholar 

  28. Fujii T, Reimer JD (2013) A new family of diminutive zooxanthellate zoanthids (Hexacorallia: Zoantharia). Zool J Linnean Soc 169:509–522

    Article  Google Scholar 

  29. Goreau T (1959) The ecology of Jamaican coral reefs I. Species composition and zonation. Ecology 40:67–90

    Article  Google 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. 6

  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 94–106

    Google 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

    CAS  Article  PubMed  Google 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. 58–60

  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 4:673–701

    Google 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 22:160–174

    CAS  Article  PubMed  Google Scholar 

  36. Herberts C (1972) Etude systématique de quelques zoanthaires tempérés et tropicaux. Tethys Supplement 3:69–156

    Google 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. 1–14

  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 733:31–43

    Article  Google 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 66:167–174

  40. Irei Y, Nozawa Y, Reimer JD (2011) Distribution patterns of five zoanthid species in Okinawa Island, Japan. Zool Stud 50:426–433

  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 1736:1–7

    Google 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 43:61–70

    Article  Google Scholar 

  43. Karlson RH (1983) Disturbance and monopolization of a spatial resource by Zoanthus sociatus (Coelenterata, Anthozoa). Bull Mar Sci 13:118–131

    Google 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 28:1647–1649

    Article  PubMed  PubMed Central  Google Scholar 

  45. Kelecom A, Solé-Cava AM (1982) Comparative study of zoanthid sterols the genus Palythoa (Hexacorallia, Zoanthidea). Comp Biochem Physiol 72B:677–682

    CAS  Google Scholar 

  46. Khushali PM, Pradeep MC (2013) Brachycnemic zooxanthellate zoanthids (Cnidaria: Zoantharia) of Saurashtra coast: a preliminary survey. Res J Mar Sci 1:10–13

    Google 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]

  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 6:1–10

    Article  Google 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. 363

  51. Lamouroux JVF (1816) Histoire des polypiers coralligènes flexibles, vulgairement nommés zoophytes. F. Poisson, Caen, lxxxiv + [1] + 559 + [1] pp., pls. 1–19

  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 5:1–3

    Article  Google 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)]

  54. Miyashita M, Sasaki M, Hattori I, Sakai M, Tanino K (2004) Total synthesis of norzoanthamine. Science 305:495–499

    CAS  Article  PubMed  Google 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 25:173–190

    Article  Google Scholar 

  56. Ong CW, Reimer JD, Todd PA (2013) Morphologically plastic responses to shading in the zoanthids Zoanthus sansibaricus and Palythoa tuberculosa. Mar Biol 160:1053–1064

    Article  Google 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 pls

  58. Pax F, Muller I (1956) Zoanthaires de la Mer Rouge. Annales de l’Institut Océanographique 32:1–77

    Google Scholar 

  59. Polak O, Loya Y, Brickner I (2011) The widely-distributed Indo-Pacific zoanthid Palythoa tuberculosa: a sexually conservative strategist. Bull Mar Sci 87:605–621

    Article  Google Scholar 

  60. Rafinesque CS (1815) Analyse de la nature ou tableau de l’univers et des corps organisés. [The Author], Palerme [= Palermo]

  61. Reimer AA (1971) Feeding behavior in the Hawaiian zoanthids Palythoa and Zoanthus. Pac Sci 25:512–520

    Google 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 22:103–120

    Google 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 21:517–525

    CAS  Article  PubMed  Google 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 23:87–94

    CAS  Article  PubMed  Google 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):255–262

    CAS  Article  Google 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 399–410

  67. Reimer JD, Takishita K, Ono S, Tsukahara J, Maruyama T (2007c) Molecular evidence suggesting intraspecific hybridization in Zoanthus (Anthozoa: Hexacorallia). Zool Sci 24:346–359

    CAS  Article  PubMed  Google Scholar 

  68. Reimer JD, Sinniger F, Hickman CP (2008) Zoanthid diversity (Anthozoa: Hexacorallia) in the Galapagos Islands: a molecular examination. Coral Reefs 27:641–654

    Article  Google 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 50:363–371

    Google Scholar 

  70. Reimer JD, Poliseno A, Hoeksema BW (2014) Shallow-water zoantharians (Cnidaria, Hexacorallia) from the Central Indo-Pacific. ZooKeys 57:1–57

    Article  Google 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 63:334–356

    Google 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 13:93–103

    Article  Google 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 46:113–127

    Article  Google 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 8:157

    Article  PubMed  PubMed Central  Google Scholar 

  77. Ryland JS (2015) Size-defined morphotypes in Zoanthus (Hexacorallia: Zoantharia) populations on shores in KwaZulu-Natal, South Africa. Zootaxa 3986:332–356

    Article  PubMed  Google Scholar 

  78. Ryland JS, Lancaster JE (2003) Revision of methods for separating species of Protopalythoa (Hexacorallia: Zoanthidea) in the tropical West Pacific. Invert Syst 17:407–428

    Article  Google 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 95:301–309

    Article  Google Scholar 

  80. Santos MEA, Kitahara MV, Lindner A, Reimer JD (2016) Overview of the order Zoantharia (Cnidaria: Anthozoa) in Brazil. Mar Biodivers 46:547–559

    Article  Google 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 1–14

  82. Sebens K (1977) Autotrophic and heterotrophic nutrition of coral reef zoanthids. Proc 3rd Int Coral Reef Symp 1:397–404

  83. Shearer TL, Van Oppen MJ, Romano SL, Wörheide G (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Mol Ecol 11:2475–2487

  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 147:1121–1128

    CAS  Article  Google Scholar 

  85. Sinniger F, Reimer JD, Pawlowski J (2008) Potential of DNA sequences to identify zoanthids (Cnidaria: Zoantharia). Zool Sci 25:1253–1260

    CAS  Article  PubMed  Google 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 16:463–468

    Article  Google 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 117:3–5

    Google 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 3796:81–107

    Article  Google 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 15:123

    Article  PubMed  PubMed Central  Google 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, MA

    Google Scholar 

  92. Verrill AE (1928) Hawaiian shallow water Anthozoa. Bull Bernice P Bishop Museum 49:1–30

    Google Scholar 

  93. Villaça R, Pitombo FB (1997) Benthic communities of shallow-water reefs of Abrolhos, Brazil. Rev Bras Oceanogr 45:35–43

    Article  Google Scholar 

  94. Walsh GE, Bowers RL (1971) A review of the Hawaiian zoanthids with descriptions of three new species. Zool J Linnean Soc 50:161–180

    Article  Google 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

Download references

Acknowledgements

This research was supported by award No. 1389-CRG1 and baseline funding from the King Abdullah University of Science and Technology (KAUST) to M.L.B. The following people from KAUST are thanked for logistical support: A. magnum Kattan, J. Bouwmeester, L. Chen, J. DiBattista, A. Gusti, A. Macauley, C. Nelson, M. Priest, and T. Sinclair-Taylor of KAUST, and the crew of the MY ‘Dream Master’. J.P. Hobbs, F. Benzoni, D. Uyeno, A.M. Kattan, and V. Chaldez are thanked for sampling help. J.D.R. was additionally supported in part by a Japan Society for the Promotion of Science “Kiban B” grant entitled “Global evolution of Brachycnemina and their Symbiodinium”. Two anonymous reviewers greatly improved an earlier version of this manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to James Davis Reimer.

Additional information

Communicated by M. M. El-Sherbiny

Electronic supplementary material

Supplementary Figure S1

Maximum 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)

Supplementary Figure S2

Maximum 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)

Supplementary Table S1

Some taxonomic historical notes of Brachycnemina species-group names in the Red Sea. (XLSX 17 kb)

Supplementary Table S2

Brachycnemina specimens from the northern Red Sea collected in this study, their collection information, GenBank Accession Numbers, and identification. (XLSX 19.7 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Reimer, J.D., Montenegro, J., Santos, M.E.A. et al. Zooxanthellate zoantharians (Anthozoa: Hexacorallia: Zoantharia: Brachycnemina) in the northern Red Sea. Mar Biodiv 47, 1079–1091 (2017). https://doi.org/10.1007/s12526-017-0706-3

Download citation

Keywords

  • Saudi Arabia
  • Taxonomy
  • Zoogeography
  • Cnidaria
  • Species diversity