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Molecular examination of rocky shore brachycnemic zoantharians (Anthozoa: Hexacorallia) and their Symbiodinium symbionts (Dinophyceae) in the southwest Indian Ocean

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Abstract

The order Zoantharia is ubiquitous on the east coast of South Africa, but despite its widespread distribution its species are poorly represented in recent literature from the region. A previous study in this region has shown that Zoanthus natalensis Carlgren, 1938 and Z. durbanensis Carlgren, 1938 are most likely conspecific to the Pacific Z. kuroshio Reimer & Ono, 2006 and Z. vietnamensis Pax & Müller, 1957, respectively. The aims of the present study were to expand on the previous one by conducting a molecular examination of zoantharians found in the intertidal zone along the east coast of South Africa as well as to identify their Symbiodinium symbionts for comparison with conspecifics elsewhere. Symbiodinium identification can be a useful tool when dealing with species that are synonymous as they are likely to share Symbiodinium spp. from the same subclade. The molecular markers mitochondrial 16S ribosomal DNA (mt 16S rDNA), the nuclear internal transcribed spacer region of ribosomal DNA (ITS rDNA), and for the first time on South African zoantharians, the ITS rDNA region for Symbiodinium spp. were used. Seven species were identified. They were Isaurus tuberculatus, Palythoa nelliae, P. tuberculosa, Z. durbanensis, Z. gigantus, Z. natalensis, and Z. sansibaricus. A possible synonymy was found as Palythoa nelliae Pax, 1935 appears to match with the Pacific P. mutuki (Haddon & Shackleton, 1891). Symbiodinium subclade A1 was most often found with Z. natalensis and subclade C15/C91 was most frequently observed in Z. durbanensis. Subclade C1 was found with all Isaurus and Palythoa samples, and with most of Z. sansibaricus samples. Symbiodinium subclades in this study were generally the same as those reported from Indo-Pacific conspecifics.

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References

  • 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. doi:10.1007/s12526-010-0043-2

    Article  Google Scholar 

  • Baillie BK, Belda-Baillie CA, Maruyama T (2000) Conspecificity and Indo-Pacific distribution of Symbiodinium genotypes (Dinophyceae) from giant clams. J Phycol 36:1153–1161

    Article  CAS  Google Scholar 

  • Bazinet AL, Zwickl DJ, Cummings MP (2014) A gateway for phylogenetic analysis powered by grid computing featuring GARLI 2.0. Syst Biol 63:812–818. doi:10.1093/sysbio/syu031

    Article  PubMed  PubMed Central  Google Scholar 

  • Branch GM, Branch M, Bannister A (eds) (1981) The living shores of Southern Africa vol 1. C. Struik Cape Town

  • Branch GM, Griffiths CL, Branch L, Beckley LE (2008) Two Oceans: A Guide to the Marine Life of Southern Africa. Struik Cape Town

  • Bui T, Loh WKW, Carter DA (2003) Genetic diversity of symbiotic dinoflagellates from corals from one tree island, great barrier reef. GenBank, Australia

    Google Scholar 

  • 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 

  • 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. doi:10.1007/s003380050060

    Article  Google Scholar 

  • Carlgren O (1938) Kungliga Svenska vetenskapsakademiens handlingar [The royal Swedish academy of sciences documents] vol 17. South African Actinaria and Zoantharia, vol 3. Almqvist & Wiksells Boktryckeri-A-B, Stockholm

    Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deeds JR, Handy SM, White KD, Reimer JD (2011) Palytoxin found in Palythoa sp. zoanthids (Anthozoa, Hexacorallia) sold in the home aquarium trade. PLoS ONE 6(4):e18235. doi:10.1371/journal.pone.0018235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haddon AC, Shackleton AM (1891) Revision of the British Actiniae, Part 11. The Zoantheae. Sci Trans R Dublin Soc 4:609–672

    Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Herberts C (1972a) Contribution à l’étude écologique de quelques zoanthaires tempérés et tropicaux [Contribution to the ecological study of some temperate and tropical Zoantharia]. Mar Biol 13:127–136. doi:10.1007/BF00366563

    Article  Google Scholar 

  • Herberts C (1972b) Etude systématique de quelques zoanthaires tempérés et tropicaux [Systematic study of some temperate and tropical Zoantharia]. Téthys Suppl 3:69–156

    Google Scholar 

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

    Google Scholar 

  • 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 Biodiv 43:61–70. doi:10.1007/s12526-012-0119-2

    Article  Google Scholar 

  • Karlson RH (1983) Disturbance and monopolisation of a spatial resource by Zoanthus sociatus (Coelenterata: Anthozoa). Bull Mar Sci 33:118–131

    Google Scholar 

  • Kimura M (1981) Estimation of evolutionary distances between homologous nucleotide sequences. Proc Natl Acad Sci U S A 78:454–458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knowlton N (2000) Molecular genetic analyses of species boundaries in the sea. Hydrobiologia 420:73–90. doi:10.1023/A:1003933603879

    Article  CAS  Google Scholar 

  • LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400

    Article  Google Scholar 

  • Lasiak T, Dye A (1988) The ecology of the brown mussel Perna perna in Transkei, Southern Africa: implications for the management of a traditional food resource. Biol Conserv 47:245–257. doi:10.1016/0006-3207(89)90068-2

    Article  Google Scholar 

  • Le Goff-Vitry M, Rogers A, Baglow D (2004) A deep sea slant on the molecular phylogeny of the Scleractinia. Mol Phylogenet Evol 30:167–177

    Article  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DNAsp v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. doi:10.1093/bioinformatics/btp187

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.1007/s00227-012-2158-4

    Article  Google Scholar 

  • Pawlowski J, Holzmann M, Fahrni JF, Pochon XC, Lee JJ (2001) Molecular identification of algal endosymbionts in large miliolid Foraminifera: 2. Dinofiagellates. J Euk Microbiol 48:368–373

    Article  CAS  PubMed  Google Scholar 

  • Pax F (1910) Studien an westindischen Actinien [Studies on West Indian Actiniae]. Zool Jahrb 11:157–330

    Google Scholar 

  • Pochon XC, Pawlowski J, Zaninetti L, Rowan RG (2001) High genetic diversity and relative specificity among Symbiodinium-like endosymbiotic dinoflagellates in soritid foraminiferans. Mar Biol 139:1069–1078

    Article  Google Scholar 

  • Pochon XC, Putnam HM, Gates RD (2014) Multi-gene analysis of Symbiodinium dinoflagellates: a perspective on rarity, symbiosis, and evolution. Peer J 2:e394. doi:10.7717/peerj.394

    Article  PubMed  PubMed Central  Google Scholar 

  • Reimer JD (2010) Key to field identification of shallow water brachycnemic zoanthids (Order Zoantharia: Suborder Brachycnemina) present in Okinawa. Galaxea 12:23–29

    Article  Google Scholar 

  • Reimer J (2014). Brachycnemina. Accessed through: World Register of Marine Species at http://www.marinespecies.org/aphia.php?p=taxdetails&id=367224 on 2015-02-27

  • Reimer JD, Fujii T (2010) Four new species and one new genus of zoanthids (Cnidaria, Hexacorallia) from the Galápagos Islands. ZooKeys 42:1–36. doi:10.3897/zookeys.42.378

    Article  Google Scholar 

  • Reimer JD, Hickman CP (2009) Preliminary survey of zooxanthellate zoanthids (Cnidaria: Hexacorallia) of the Galápagos and associated symbiotic dinoflagellates (Symbiodinium spp.). Galápagos Res 66:14–19

    Google Scholar 

  • Reimer JD, Sinniger F (2010) Unexpected diversity in Canadian Pacific zoanthids (Cnidaria: Anthozoa: Hexacorallia): a molecular examination and description of a new species from the waters of British Columbia. Mar Biodivers 40:249–260. doi:10.1007/s12526-010-0045-0

    Article  Google Scholar 

  • 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 

  • 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. doi:10.2108/zsj.21.517

    Article  CAS  PubMed  Google Scholar 

  • Reimer JD, Ono S, Iwama A, Takishita K, Tsukahara J, Maruyama T (2006a) Morphological and molecular revision of Zoanthus (Anthozoa: Hexacorallia) from southwestern Japan, with descriptions of two new species. Zool Sci 23:261–275. doi:10.2108/zsj.23.261

    Article  PubMed  Google Scholar 

  • Reimer JD, Ono S, Iwama A, Tsukahara J, Maruyama T (2006b) High levels of morphological variation despite close genetic relatedness between Zoanthus aff. vietnamensis and Zoanthus kuroshio (Anthozoa: Hexacorallia). Zool Sci 23:755–761. doi:10.2108/zsj.23.755

    Article  CAS  PubMed  Google Scholar 

  • Reimer JD, Ono S, Takishita K, Tsukahara J, Maruyama T (2006c) Molecular evidence suggesting species in the zoanthid genera Palythoa and Protopalythoa (Anthozoa:Hexacorallia) are congeneric. Zool Sci 23:87–94. doi:10.2108/zsj.23.87

    Article  CAS  PubMed  Google Scholar 

  • Reimer JD, Takishita K, Maruyama T (2006d) Molecular identification of symbiotic dinoflagellates (Symbiodinium spp.) from Palythoa spp. (Anthozoa: Hexacorallia) in Japan. Coral Reefs 25:521–527

    Article  Google Scholar 

  • Reimer JD, Takishita K, Ono S, Maruyama T, Tsukahara J (2006e) Latitudinal and intracolony ITS-rDNA sequence variation in the symbiotic dinoflagellate genus Symbiodinium (Dinophyceae) in Zoanthus sansibaricus (Anthozoa: Hexacorallia). Phycol Res 54:122–132. doi:10.1111/j.1440-1835.2006.00419.x

    Article  CAS  Google Scholar 

  • 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. Invertebr Syst 21:255–262

    Article  CAS  Google Scholar 

  • Reimer JD, Ono S, Tsukahara J, Takishita K, Maruyama T (2007b) Non‐seasonal clade‐specificity and subclade microvariation in symbiotic dinoflagellates (Symbiodinium spp.) in Zoanthus sansibaricus (Anthozoa: Hexacorallia) at Kagoshima Bay, Japan. Phycol Res 55:58–65

    Article  CAS  Google Scholar 

  • Reimer JD, Takishita K, Ono S, Tsukahara J, Maruyama T (2007c) Molecular evidence suggesting interspecific hybridizationin Zoanthus spp. (Anthozoa: Hexacorallia). Zool Sci 24:346–359. doi:10.2108/zsj.24.346

    Article  CAS  PubMed  Google Scholar 

  • Reimer JD, Takishita K, Ono S, Maruyama T (2007d) Diversity and evolution in the zoanthid genus Palythoa (Cnidaria: Hexacorallia) utilizing nuclear ITS-rDNA. Coral Reefs 26:399–410

    Article  Google Scholar 

  • Reimer JD, Ono S, Tsukahara J, Iwase F (2008a) Molecular characterization of the zoanthid genus Isaurus (Anthozoa: Hexacorallia) and associated zooxanthellae (Symbiodinium spp.) from Japan. Mar Biol 153:351–363

    Article  CAS  Google Scholar 

  • Reimer JD, Sinniger F, Hickman CP (2008b) Zoanthid diversity (Anthozoa: Hexacorallia) in the Galápagos Islands: a molecular examination. Coral Reefs 27:641–654. doi:10.1007/s00338-008-0376-5

    Article  Google Scholar 

  • Reimer JD, Hirose M, Wirtz P (2010) Zoanthids of the Cape Verde Islands and their symbionts: previously unexamined diversity in the Northeastern Atlantic. Contrib Zool 79:147–163

    Google Scholar 

  • Reimer JD, Hirose M, Irei Y, Obuchi M, Sinniger F (2011a) The sands of time: rediscovery of the genus Neozoanthus (Cnidaria: Hexacorallia) and evolutionary aspects of sand incrustation in brachycnemic zoanthids. Mar Biol 158:983–993

    Article  Google Scholar 

  • Reimer JD, Hirose M, Yanagi K, Sinniger F (2011b) Marine invertebrate diversity in the oceanic Ogasawara Islands: a molecular examination of zoanthids (Anthozoa: Hexacorallia) and their Symbiodinium (Dinophyceae). Syst Biodivers 9:133–143. doi:10.1080/14772000.2011.569034

    Article  Google Scholar 

  • Reimer JD, Lin M, Fujii T, Lane DJW, Hoeksema BW (2012) The phylogenetic position of the solitary zoanthid genus Sphenopus (Cnidaria: Hexacorallia). Contrib Zool 81:43–54

    Google Scholar 

  • Reimer JD, Irei Y, Fujii T, Yang S (2013) Molecular analyses of shallow-water zooxanthellate zoanthids (Cnidaria: Hexacorallia) from Taiwan and their Symbiodinium spp. Zool Stud 52:38. doi:10.1186/1810-522X-52-38

    Article  Google Scholar 

  • Reimer JD, Poliseno A, Hoeksema BW (2014) Shallow-water zoantharians (Cnidaria, Hexacorallia) from the Central Indo-Pacific. ZooKeys 444:1–57. doi:10.3897/zookeys.444.7537

    Article  PubMed  Google Scholar 

  • 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. doi:10.1080/14772000.2014.968233

    Article  Google Scholar 

  • Rodriguez-Lanetty M, Hoegh-Guldberg O (2002) Genetic diversity of symbiotic dinoflagellates associated with the widespread coral Plesiastrea versipora in the north western Pacific Ocean. Unpublished

  • Rodriguez-Lanetty M, Loh W, Cater D, Hoegh-Guldberg O (2001) Latitudinal variability in symbiont specifcity within the widespread scleractinian coral Plesiastrea versipora. Mar Biol (Berl) 138:1175–1181

    Article  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. doi:10.1093/bioinformatics/btg180

    Article  CAS  PubMed  Google Scholar 

  • Ryland JS (1997) Reproduction in Zoanthidea (Anthozoa: Hexacorallia). Invert Reprod Dev 31:177–188

    Article  Google Scholar 

  • Ryland JS, Lancaster JE (2003) Revision of methods for separating species of Protopalythoa (Hexacorallia: Zoanthidea) in the tropical West Pacific. Invertebr Syst 17:407–428. doi:10.1071/IS02008

    Article  Google Scholar 

  • Ryland JS, Brasseur MM, Lancaster JE (2004) Use of cnidae in taxonomy: implications from a study of Acrozoanthus australiae (Hexacorallia, Zoanthidea). J Nat Hist 38:1193–1223

    Article  Google Scholar 

  • Sanchez A, Lasker H, Taylor D (2003) Phylogenetic analyses among octocorals (Cnidaria): mitochondrial and nuclear DNA sequences (lsu-rRNA, 16S and ssu-rRNA, 18S) support two convergent clades of branching gorgonians. Mol Phylogenet Evol 29:31–42

    Article  Google Scholar 

  • Santos SR, Taylor DJ, Kinzie RAI, Hidaka M, Sakai K, Coffroth MA (2002) Molecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S)-rDNA sequences. Mol Phylogenet Evol 23:97–111

    Article  CAS  PubMed  Google Scholar 

  • Silverstein RN, Correa MS, LaJeunesse TC, Baker AC (2011) Novel algal symbiont (Symbiodinium spp.) diversity in reef corals of Western Australia. Mar Ecol Prog Ser 422:63–75. doi:10.3354/meps08934

    Article  Google Scholar 

  • Sink KJ, Branch GM, Harris JM (2005) Biogeographic patterns in rocky intertidal communities in KwaZulu-Natal, South Africa. Afr J Mar Sci 27:37–41

    Article  Google Scholar 

  • Sinniger F, Haussermann V (2009) Zoanthids (Cnidaria: Hexacorallia: Zoantharia) from shallow waters of the southern Chilean fjord region, with descriptions of a new genus and two new species. Org Divers Evol 9:23–36. doi:10.1016/j.ode.2008.10.003

    Article  Google Scholar 

  • 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. doi:10.1007/s00227-005-0016-3

    Article  CAS  Google Scholar 

  • Sinniger F, Reimer JD, Pawlowski J (2008) Potential of DNA sequences to identify zoanthids (Cnidaria: Zoantharia). Zool Sci 25:1253–1260. doi:10.2108/zsj.25.1253

    Article  CAS  PubMed  Google Scholar 

  • Steyn E, Fielding P, Schleyer M (2008) The artisanal fishery for east coast rock lobsters Panulirus homarus along the wild coast, South Africa. Afr J Mar Sci 30:497–506

    Article  Google Scholar 

  • Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates Sunderland, Massachusetts

    Google Scholar 

  • Teske PR, von der Heyden S, McQuaid CD, Barker NP (2011) A review of marine phylogeography in southern Africa. S Afr J Sci 107(514):1–11. doi:10.4102/sajs.v107i5/6.514

    Google Scholar 

  • Xia X, Lemey P (2009) Assessing substitution saturation with DAMBE. The phylogenetic handbook: a practical approach to DNA and protein phylogeny, 2nd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Xia X, Xie Z, Salemi M, Chen L, Wang Y (2003) An index of substitution saturation and its application. Mol Phylogenet Evol 26:1–7

    Article  CAS  PubMed  Google Scholar 

  • Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD dissertation The University of Texas at Austin

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Acknowledgments

We would like to thank Prof. Mike Schleyer and the team at the Oceanographic Research Institute for collecting zoantharian specimens in Madagascar. We thank Justin Hart, Lindile Cele, Ryan Van Rooyen, and Christopher Jones for the time they put into sampling and analysing. We would like to thank Assoc. Prof. James Reimer for his readiness to give advice and assistance to the direction of this research. Thank you to the two anonymous reviewers and Dr. Bert W. Hoeksema who greatly improved this manuscript. Lastly, we would like to thank all members of the Marine Evolution Lab (MAREVOL) for the valuable contributions in the discussion of this project. This work was supported by the National Research Foundation under Grant 83704, and the Western Indian Ocean Marine Science Association under Grant MARG I Contract seven.

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  1. University of KwaZulu-Natal, School of Life Sciences, Marine Science, Durban, South Africa

    Michelle M. Risi & Angus H. H. Macdonald

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Correspondence to Michelle M. Risi.

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Communicated by B. W. Hoeksema

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Online Resource 1

Bayesian tree of the internal transcribed spacer of ribosomal DNA (ITS rDNA) sequences for Symbiodinium including sequences from this study for clade C. Values at branches represent Bayesian probabilities, MP, and ML bootstrap values. Sequences labelled without accession numbers were obtained in this study. For specimen information see Table 1. (GIF 148 kb)

High resolution image (TIFF 14634 kb)

Online Resource 2

Bayesian tree of the internal transcribed spacer of ribosomal DNA (ITS rDNA) sequences for Symbiodinium including sequences from this study for clade A. Values at branches represent Bayesian probabilities, MP, and ML bootstrap values. Sequences labelled without accession numbers were obtained in this study. For specimen information see Table 1. (GIF 74 kb)

High resolution image (TIFF 8126 kb)

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Risi, M.M., Macdonald, A.H.H. Molecular examination of rocky shore brachycnemic zoantharians (Anthozoa: Hexacorallia) and their Symbiodinium symbionts (Dinophyceae) in the southwest Indian Ocean. Mar Biodiv 46, 113–127 (2016). https://doi.org/10.1007/s12526-015-0331-y

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