Systematics of the coral genus Craterastrea (Cnidaria, Anthozoa, Scleractinia) and description of a new family through combined morphological and molecular analyses

Systematics and Biodiversity

Volumn 10, Issue 4, 2012, Pages 417-433

  Benzoni, Francesca ^a,b   Arrigoni, Roberto ^a   Stefani, Fabrizio ^c   Stolarski, Jarosław ^d  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

^b INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (New Caledonia)

^c Water Research Institute National Research Council IRSA CNR   (Italy)

^d INSTITUTE OF PALEOBIOLOGY   (Poland)

Author keywords

Anomastraea irregularis; COI; Coscinaraea monile; Coscinaraeidae; Craterastrea levis; Horastrea indica; Leptoseris foliosa; Microstructure; New family; RDNA; Siderastreidae

Indexed keywords

AGARICIIDAE; ANTHOZOA; CNIDARIA; COSCINARAEA; COSCINARAEA MONILE; HORASTREA; HORASTREA INDICA; LEPTOSERIS; LEPTOSERIS FOLIOSA; PSEUDOSIDERASTREA; SCLERACTINIA; SIDERASTREA; SIDERASTREIDAE;

EID: 84876452154     PISSN: 14772000     EISSN: 14780933     Source Type: Journal    
DOI: 10.1080/14772000.2012.744369     Document Type: Article

References (84)

1. ARRIGONI, R., STEFANI, F., PICHON, M., GALLI, P. & BENZONI, F. 2012. Molecular phylogeny of the Robust clade (Faviidae, Mussidae, Merulinidae and Pectiniidae): an Indian Ocean perspective. Molecular Phylogenetics and Evolution 65, 183-193.
2. AUSTRALIAN BIOLOGICAL RESOURCES STUDY (ABRS) 2011. List of CITES Corals Occurring in Australian Waters. NOTICE WTR2011/3 ANNEX A [updated at http://www.environment.gov.au/biodiversity/wildlife-trade/permits/pubs/ notice-cites-annex-a.pdf, accessed 10 August 2012].
3. BENZONI, F., STEFANI, F., STOLARSKI, J., PICHON, M., MITTA, G. & GALLI, P. 2007. Debating phylogenetic relationships of the scleractinian Psammocora: molecular and morphological evidences. Contributions to Zoology 76, 35-54.
4. BENZONI, F., STEFANI, F., PICHON, M. & GALLI, P. 2010. The name game: morpho-molecular species boundaries in the genus Psammocora (Cnidaria, Scleractinia). Zoological Journal of the Linnean Society 160, 421-456.
5. BENZONI, F., ARRIGONI, R., STEFANI, F. & PICHON, M. 2011. Phylogeny of the coral genus Plesiastrea (Cnidaria, Scleractinia). Contributions to Zoology 80, 231-249.
6. BENZONI, F., ARRIGONI, R., STEFANI, F., REIJNEN, B.T., MONTANO, S. & HOEKSEMA, B.W. 2012. Phylogenetic position and taxonomy of Cycloseris explanulata and C. wellsi (Scleractinia: Fungiidae): lost mushroom corals find their way home. Contributions to Zoology 81, 125-146.
7. BIGOT, L. & AMIR, H. 2012. Scleractinia corals of Baa Atoll (Maldives): first checklist and overview of stony corals community structure. Atoll Research Bulletin 590, 67-83.
8. BUDD, A.F. & STOLARSKI, J. 2009. Searching for new morphological characters in the systematics of scleractinian reef corals: comparison of septal teeth and granules between Atlantic and Pacific Mussidae. Acta Zoologica 90, 142-165.
9. BUDD, A.F. & STOLARSKI, J. 2011. Corallite wall and septal microstructure in scleractinian reef corals: comparison of molecular clades within the family Faviidae. Journal of Morphology 272, 66-88.
10. BUDD, A.F., FUKAMI, H., SMITH, N.D. & KNOWLTON, N. Taxonomic classification of the reef coral family Mussidae (Cnidaria: Anthozoa: Scleractinia). Zoological Journal of the Linnean Society (in press).
11. CHEN, C.A., WALLACE, C.C. & WOLSTENHOME, J. 2002. Analysis of the mitochondrial 12S rRNA gene supports a twoclade hypothesis of the evolutionary history of scleractinian corals. Molecular Phylogenetics and Evolution 23, 137-149.
12. CHEN, C.A., CHANG, C.C., WEI, N.V., CHEN, C.H., LEIN, Y.T., LIN, H.E., DAI, C.F. & WALLACE, C.C. 2004. Secondary structure and phylogenetic utility of the ribosomal Internal Transcribed Spacer 2 (ITS2) in scleractinian corals. Zoological Studies 43, 759-771.
13. CHEVALIER, J.P. & BEAUVAIS, L. 1987. Ordre des sclé ractiniaires: systématique. In: GRASSE, P.P., Ed., Traité de Zoologie. Anatomie, Systématique, Biologie. Masson, Paris, pp. 679-753.
14. CITES 2011. Coral Species, Synonyms, and Nomenclature References Currently Recognized in the UNEPWCMC database. AC26 Doc. 20 Annex 6 [updated at http://www.cites.org/common/com/AC/26/E26-20-A6.pdf, accessed 10 August 2012].
15. COMBOSCH, D., GUZMAN, H., SCHUHMACHER, H. & VOLLMER, S.V. 2008. Interspecific hybridization and restricted trans-Pacific gene flow in the Tropical Eastern Pacific Pocillopora. Molecular Ecology 17, 1304-1312.
16. CUIF, J.P., LECOINTRE, G., PERRIN, C., TILLER, A. & TILLIER, S. 2003. Patterns of septal biomineralization in Scleractinia compared with their 28S rRNA phylogeny. A dual approach for a newtaxonomic framework. Zoologica Scripta 32, 459-473.
17. DANA, J.D. 1846. Zoophythes. U.S. Exploratory Expeditions 1836-1842. 7, 1-740.
18. DINESEN, Z.D. 1980. A revision of the coral genus Leptoseris (Scleractinia: Fungiinae: Agariciidae). Memoirs of the Queensland Museum 20, 181-235.
19. DRUMMOND, A.J. & RAMBAUT, A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.
20. EDWARDS, A.J. & HEAD, S.M. 1987. Red Sea. Pergamon Press, Oxford.
21. FARRIS, J.S., KALLERSJO, M., KLUGE, A.G. & BULT, C. 1995. Constructing a significance test for incongruence. Systematic Biology 44, 570-572.
22. FRICKE, H.W. & SCHUHMACHER, H. 1983. The depth limits of the Red Sea stony corals: an ecophysiological problem (a deep diving survey by submersible). Marine Ecology Progress Series 4, 163-194.
23. FRICKE, H.W., VARESCHI, E. & SCHLICHTER, D. 1987. Photoecology of the coral Leptoseris fragilis in the Red Sea twilight zone (an experimental study by submersible). Oecologia 73, 371-381.
24. FUKAMI, H., BUDD, A.F., PAULAY, G., SOLE-CAVA, A., CHEN, C.A., IWAO, K. & KNOWLTON, N. 2004. Conventional taxonomy obscures deep divergence between Pacific and Atlantic corals. Nature 427, 832-835.
25. FUKAMI, H., CHEN, C.A., BUDD, A.F., COLLINS, A., WALLACE, C., CHUANG, Y.Y., CHEN, C., DAI, C.F., IWAO, K., SHEPPARD, C. & KNOWLTON, N. 2008. Mitochondrial and nuclear genes suggest that stony corals are monophyletic but most families of stony corals are not (order Scleractinia, class Anthozoa, phylum Cnidaria). PLoS One 3, e3222.
26. GITTENBERGER, A., REIJNEN, B.T. & HOEKSEMA, B.W. 2011. A molecularly based phylogeny reconstruction of mushroom corals (Scleractinia: Fungiidae) with taxonomic consequences and evolutionary implications for life history traits. Contributions to Zoology 80, 107-132.
27. GUINDON, S. & GASCUEL, O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696-704.
28. HALL, T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95-98.
29. HEAD, S.M. 1983. An undescribed species of Merulina and a new genus and species of siderastreid coral from the Red Sea. Journal of Natural History 17, 419-435.
30. HOEKSEMA, B.W. 1989. Taxonomy, phylogeny and biogeography of mushroom corals (Scleractinia: Fungiidae). Zoologische Verhandelingen 254, 1-295.
31. HOEKSEMA, B.W., VAN DER LAND, J., VAN DER MEIJ, S.E.T., VAN OFWEGEN, L.P., REIJNEN, B.T., VAN SOEST, R.W.M. & DE VOOGD, N.J. 2011. Unforeseen importance of historical collections as baselines to determine biotic change of coral reefs: the Saba Bank case. Marine Ecology 32, 135-141.
32. HUANG, D. 2012. Threatened reef corals of the world. PLoS One 7, e34459.
33. HUANG, D., LICUANAN, W.Y., BAIRD, A.H. & FUKAMI, H. 2011. Cleaning up the "Bigmessidae": molecular phylogeny of scleractinian corals from Faviidae, Merulinidae, Pectiniidae, and Trachyphylliidae. BMC Evolutionary Biology 11, 37.
34. HUELSENBECK, J. P. & RONQUIST, F. 2001. Mr Bayes: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754-755.
35. INSKIPP, T. & GILLETT, H.J. 2005. Checklist of CITES species and Annotated CITES Appendices and Reservations. Compiled by UNEPWCMC. CITES Secretariat, Geneva, Switzerland and UNEP-WCMC, Cambridge.
36. IUCN 2012. The IUCN Red List of Threatened Species. Version 2012.1 [updated at http://www.iucnredlist.org, accessed 19 June 2012].
37. JANISZEWSKA, K., STOLARSKI, J., BENZERARA, K., MEIBOM, A., MAZUR, M., KITAHARA, M. & CAIRNS, S.D. 2011. A unique skeletal microstructure of the deep-sea micrabaciid scleractinian corals. Journal of Morphology 272, 191-203.
38. KARSENTI, E., ACINAS, S.G., BORK, P., BOWLER, C., DEVARGAS, C., RAES, J., SULLIVAN, M., ARENDT, D., BENZONI, F., CLAVERIE, J.M., FOLLOWS, M., GORSKY, G., HINGAMP, P., IUDICONE, D., JAILLON, O., KANDELS-LEWIS, S., KRZIC, U., NOT, F., OGATA, H., PESANT, S., REYNAUD, E.G., SARDET, C., SIERACKI, M.E., SPEICH, S., VELAYOUDON, D., WEISSENBACH, J., WINCKER, P. & THE TARA OCEANS CONSORTIUM 2011. A holistic approach to marine eco-systems biology. PLoS Biology 9, e1001177.
39. KERR, A.M. 2005. Molecular and morphological supertree of stony corals (Anthozoa: Scleractinia) using matrix representation parsimony. Biology Review 80, 1-16.
40. KITAHARA, M.V., CAIRNS, S.D., STOLARSKI, J., BLAIR, D. & MILLER, D.J. 2010. Acomprehensive phylogenetic analysis of the Scleractinia (Cnidaria, Anthozoa) based on mitochondrial CO1 sequence data. PLoS One 5, e11490.
41. KITAHARA, M.V., STOLARSKI, J., CAIRNS, S., BENZONI, F., STAKE, J. & MILLER, D. The first modern solitary Agariciidae (Anthozoa, Scleractinia) revealed by molecular and microstructural analysis. Invertebrate Systematics, in press [updated at http://www.publish.csiro.au/view/journals/dsp-journals-pip- abstract-scholar1.cfm?nid=120&pip=IS11053, accessed 10 August 2012].
42. LE GOFF-VITRY, M.C., ROGERS, A.D. & BAGLOW, D. 2004. A deep-sea slant on the molecular phylogeny of the Scleractinia. Molecular Phylogenetics and Evolution 30, 167-177.
43. LIBRADO, P. & ROZAS, J. 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451-1452.
44. LIN, M.F., KITAHARA, M.V., TACHIKAWA, H., KESHAVMURTHY, S. & CHEN, C.A. 2012. A new shallow-water species, Polycyathus chaishanensis sp. nov. (Scleractinia: Caryophylliidae), from Chaishan, Kaohsiung, Taiwan. Zoological Studies 51, 213-221.
45. MA, T.Y.H. 1959. Effect of water temperature on growth rate of corals. Oceanographia Sinica Special Volume 1, 1-116.
46. MATTHAI, G. 1948. Colony formation in Fungiid corals Pavona, Echinophyllia, Leptoseris and Psammocora. Philosophical Transactions of the Royal Society of London Series B - Biological Sciences 223, 201-231.
47. MORYCOWA, E. & RONIEWICZ, E. 1995. Microstructural disparity between Recent fungiine and Mesozoic microsolenine scleractinians. Acta Palaeontologica Polonica 40, 361-385.
48. NUNES, F., FUKAMI, H., VOLLMER, S.V., NORRIS, R.D. & KNOWLTON, N. 2008. Re-evaluation of the systematics of the endemic corals of Brazil by molecular data. Coral Reefs 27, 423-432.
49. NYLANDER, J.A.A. 2004. MrModeltest v2. Evolutionary Biology Centre, Uppsala University.
50. OBURA, D.O. 2012a. The diversity and biogeography of Western Indian Ocean reef-building corals. PLoS ONE 7, e45013.
51. OBURA, D.O. 2012b. Evolutionary mechanisms and diversity in a western Indian Ocean center of diversity. Proceedings of the 12th International Coral Reef Symposium, Cairns, Australia 3-A2 [http://www.icrs2012.com/proceedings/ manuscripts/ICRS2012-3A-2.pdf, accessed 10 August 2012].
52. PICHON, M. 1971. Comparative study of the main features of some coral reefs of Madagascar, La Reunion and Mauritius. Symposium of the Zoological Society of London 28, 185-216.
53. PICHON, M. & BENZONI, F. 2007. Taxonomic re-appraisal of zooxanthellate Scleractinian Corals in the Maldive Archipelago. Zootaxa 1441, 21-33.
54. PICHON, M., CHUANG, Y.Y. & CHEN, C.A. 2012. Pseudosiderastrea formosa sp. nov. (Cnidaria: Anthozoa: Scleractinia) a new coral species endemic to Taiwan. Zoological Studies 51, 93-98.
55. PINZON, J.H. & LAJEUNESSE, T.C. 2010. Species delimitation of common reef corals in the genus Pocillopora using nucleotide sequence phylogenies, population genetics and symbiosis ecology. Molecular Ecology 20, 311-323.
56. ROMANO, S.L. & CAIRNS, S.D. 2000. Molecular phylogenetic hypotheses for the evolution of scleractinian corals. Bulletin of Marine Science 67, 1043-1068.
57. ROMANO, S.L. & PALUMBI, S.R. 1996. Evolution of scleractinian corals inferred from molecular systematics. Science 271, 640-642.
58. RONQUIST, F. & HUELSENBECK, J. P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574.
59. SCHLICHTER, D. 1991. A perforated gastrovascular cavity in Leptoseris fragilis, a new strategy to improve heterotrophic nutrition in corals. Naturwissenchaften 78, 467-469.
60. SCHLICHTER, D. & FRICKE, H.W. 1991. Mechanisms of amplification of photosynthetically active radiation in the symbiotic deep-water coral Leptoseris fragilis. Hydrobiologia 216/712, 493-983.
61. SHEPPARD, C.R.C. 1980. Cover, zonation and diversity on reef slopes of Chagos atolls, and population structures of the major species. Marine Ecology Progress Series 2, 193-205.
62. SHEPPARD, C.R.C. 1991. The reef and soft-substrate coral fauna of Chagos, Indian Ocean. Journal of Natural History 15, 607-621.
63. SHEPPARD, C.R.C. 1987. Coral species in the Indian Ocean and adjacent seas: a synonymized compilation and some regional distributional patterns. Atoll Research Bulletin 307, 1-32.
64. SHEPPARD, C.R.C. 1998a. Biodiversity patterns in Indian Ocean corals, and effects of taxonomic error in data. Biodiversity and Conservation 7, 847-868.
65. SHEPPARD, C.R.C. 1998b. Corals of the Indian Ocean. CD. SIDA Stockholm University, Stockholm.
66. SHEPPARD, C.R.C. & SHEPPARD, A.L.S. 1991. Corals and coral communities of Saudi Arabia. Fauna of Arabia 12, 1-170.
67. SHEPPARD, C., PRICE, A. & ROBERTS, C. 1992. Marine Ecology of the Arabian Region: Patterns and Processes in Extreme Tropical Environments. Academic Press, London.
68. SOUTER, P. 2010. Hidden genetic diversity in a key model species of coral. Marine Biology 157, 875-885.
69. STEFANI, F., BENZONI, F., PICHON, M., CANCELLIERE, C. & GALLI, P. 2007. A multidisciplinary approach to the definition of species boundaries in branching species of the coral genus Psammocora (Cnidaria, Scleractinia). Zoologica Scripta 37, 71-91.
70. STEFANI, F., BENZONI, F., YANG, S.Y., PICHON, M., GALLI, P. & CHEN, C.A. 2011. Comparison of morphological and genetic analyses reveals cryptic divergence and morphological plasticity in Stylophora (Cnidaria, Scleractinia). Coral Reefs 30, 1033-1049.
71. STOLARSKI, J. & RONIEWICZ, E. 2001. Towards a new synthesis of evolutionary relationships and classification of Scleractinia. Journal of Paleontology 75, 1090-1108.
72. STOLARSKI, J., KITAHARA, V.M., MILLER, D., CAIRNS, S.D., MAZUR, M. & MEIBOM, A. 2011. The ancient evolutionary origins of Scleractinia revealed by azooxanthellate corals. BMC Evolutionary Biology 11, 316.
73. SWOFFORD, D.L. 2003. PAUP* Phylogenetic Analysis using Parsimony (*and Other Methods). Version 4.b.10. Sunderland, MA, Sinauer Associates.
74. TAKABAYASHI, M., CARTER, D.A., LOH, W.K.T. & HOEGHGULDBERG, O. 1998. A coral-specific primer for PCR amplification of the internal transcribed spacer region in ribosomal DNA. Molecular Ecology 7, 925-931.
75. UNEP-WCMC 2005. Checklist of Fish and Invertebrates listed in the CITES Appendices and in EC Regulation 338/97. 7th Edition. JNCC Report, No. 379.
76. UNEP-WCMC 2012. UNEP-WCMC Species Database: CITES-Listed Species On the World Wide Web [updated at http://www.unep-wcmc-apps.org/isdb/CITES/Taxonomy/ taxgs-search2.cfm/isdb/CITES/Taxonomy/tax-gs-search2.cfm?displaylanguage= eng&GenName=craterastrea&SpcName, accessed 10 August 2012].
77. VAUGHAN, T.W. & WELLS, J.W. 1943. Revision of the Sub-orders, Families and Genera of the Scleractinia. Geological Society of America Special Paper 44, 1-363.
78. VERON, J.E.N. 1993. A biogeographic database of hermatypic coral species of the central Indo-Pacific, genera of the world. Australian Institute of Marine Science Monograph Series 10, 1-433.
79. VERON, J.E.N. 1995. Corals in Space and Time: the Biogeography and Evolution of the Scleractinia. University of New South Wales Press.
80. VERON, J.E.N. 2000. Corals of the World. Australian Institute of Marine Science, Townsville.
81. VERON, J.E.N. & PICHON, M. 1980. Scleractinia of Eastern Australia Families Agaraciidae, Siderastreidae, Fungiidae, Oculinidae, Merulinidae, Mussidae, Pectiniidae, Caryophylliidae, Dendrophylliidae. Australian Institute of Marine Science Monograph Series 4, 1-471.
82. WELLS, J.W. 1956. Scleractinia. In:MOORE, R.C., Ed., Treatise on Invertebrate Paleontology, Part F: Coelenterata. University of Kansas Press, Lawrence, pp. F328-F444.
83. WHITE, T.J., BRUNS, T., LEE, S. & TAYLOR, J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: INNIS, M.A., GELFAND, D.H., SNINSKY, J.J. & WHITE, T.J., Eds., PCR Protocols. A Guide to Methods and Application. Academic Press, San Diego.
84. WORMS, 2012. Craterastrea levis Head, 1983. Accessed through: World Register of Marine Species [updated at http://www.marinespecies.org/aphia.php?p= taxdetails&id=216131 on 2012-06-30, accessed 10 August 2012].