Phylogenetic relationships of Mediterranean black corals (Cnidaria : Anthozoa : Hexacorallia) and implications for classification within the order Antipatharia
M. Bo A G , M. Barucca B , M. A. Biscotti B , M. R. Brugler C D , A. Canapa B , S. Canese E , C. Lo Iacono F and G. Bavestrello A
+ Author Affiliations
- Author Affiliations
A Università degli Studi di Genova, Corso Europa, 16132, Genova, Italy.
B Università Politecnica delle Marche, Via Brecce Bianche, 60131, Ancona, Italy.
C Division of Invertebrate Zoology, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024, USA.
D Biological Sciences Department, NYC College of Technology (CUNY), 300 Jay Street, Brooklyn, NY 11201, USA.
E ISPRA, Via Vitaliano Brancati, 00144 Roma, Italy.
F National Oceanography Centre, University of Southampton Waterfront Campus, European Way, Southampton SO14 3ZH, UK.
G Corresponding author. Email: marzia.bo@unige.it
Invertebrate Systematics 32(5) 1102-1110 https://doi.org/10.1071/IS17043
Submitted: 20 April 2017 Accepted: 14 March 2018 Published: 9 October 2018
Abstract
The Mediterranean black coral fauna includes type species of four antipatharian genera belonging to four different families, therefore phylogenetic studies hold great potential for enhancing systematics within the order. The analysis of six Mediterranean antipatharian species by means of nuclear sequence data of internal transcribed spacer (ITS1 and ITS2) rDNA confirms the separation into different families, as was previously noted on a morphological basis, with a clear distinction of the family Leiopathidae, whose position is supported by a unique number of mesenteries and lack of spines on thicker ramifications. The position of a newly recorded black coral species for the Mediterranean basin belonging to the genus Phanopathes is discussed. Antipathes dichotoma, the type species of the genus Antipathes, on which the order Antipatharia was based, does not group with other members of the family Antipathidae. Supporting a recent finding based on mitochondrial markers, this suggests a critical need for revision of the families that will be impacted by reassignment of this nomenclaturally important taxon.
Additional keywords: biodiversity, nuclear DNA, systematics.
References
Bavestrello, G., Cattaneo-Vietti, R., Di Camillo, C. G., and Bo, M. (2012). Helicospiral growth in the whip black coral Cirrhipathes sp. (Antipatharia, Antipathidae). The Biological Bulletin 222, 17–25.| Helicospiral growth in the whip black coral Cirrhipathes sp. (Antipatharia, Antipathidae).Crossref | GoogleScholarGoogle Scholar |
Bo, M., Tazioli, S., Spanò, N., and Bavestrello, G. (2008). Antipathella subpinnata (Antipatharia, Myriopathidae) in Italian seas. Italian Journal of Zoology 75, 185–195.
| Antipathella subpinnata (Antipatharia, Myriopathidae) in Italian seas.Crossref | GoogleScholarGoogle Scholar |
Bo, M., Bavestrello, G., Canese, S., Giusti, M., Salvati, E., Angiolillo, M., and Greco, S. (2009a). Characteristics of a black coral meadow in the twilight zone of the central Mediterranean Sea. Marine Ecology Progress Series 397, 53–61.
| Characteristics of a black coral meadow in the twilight zone of the central Mediterranean Sea.Crossref | GoogleScholarGoogle Scholar |
Bo, M., Barucca, M., Biscotti, M. A., Canapa, A., Lapian, H. F. N., Olmo, E., and Bavestrello, G. (2009b). Description of Pseudocirrhipathes (Cnidaria: Anthozoa: Hexacorallia: Antipathidae) a new genus of whip black corals from the Indo-Pacific. Italian Journal of Zoology 76, 392–402.
| Description of Pseudocirrhipathes (Cnidaria: Anthozoa: Hexacorallia: Antipathidae) a new genus of whip black corals from the Indo-Pacific.Crossref | GoogleScholarGoogle Scholar |
Bo, M., Bavestrello, G., Canese, S., Giusti, M., Angiolillo, M., Cerrano, C., Salvati, E., and Greco, S. (2011). Coral assemblages off the Calabrian Coast (South Italy) with new observations on living colonies of Antipathes dichotoma. Italian Journal of Zoology 78, 231–242.
| Coral assemblages off the Calabrian Coast (South Italy) with new observations on living colonies of Antipathes dichotoma.Crossref | GoogleScholarGoogle Scholar |
Bo, M., Canese, S., Spaggiari, C., Pusceddu, A., Bertolino, M., Angiolillo, M., Giusti, M., Loreto, M. F., Salvati, E., Greco, S., and Bavestrello, G. (2012a). Deep coral oases in the South Tyrrhenian Sea. PLoS One 7, e49870.
| Deep coral oases in the South Tyrrhenian Sea.Crossref | GoogleScholarGoogle Scholar |
Bo, M., Bavestrello, G., Barucca, M., Makapedua, D. M., Poliseno, A., Canapa, A., and Olmo, E. (2012b). Morphological and molecular characterization of the problematic whip black coral genus Stichopathes (Hexacorallia: Antipatharia) from Indonesia (North Sulawesi, Celebes Sea). Zoological Journal of the Linnean Society 166, 1–13.
Bo, M., Canese, S., and Bavestrello, G. (2014). Discovering Mediterranean black coral forests: Parantipathes larix (Anthozoa: Hexacorallia) in the Tuscan Archipelago, Italy. Italian Journal of Zoology 81, 112–125.
| Discovering Mediterranean black coral forests: Parantipathes larix (Anthozoa: Hexacorallia) in the Tuscan Archipelago, Italy.Crossref | GoogleScholarGoogle Scholar |
Bo, M., Bavestrello, G., Angiolillo, A., Calcagnile, L., Canese, S., Cannas, R., Cau, Al., D’Elia, M., D’Oriano, F., Follesa, M. C., Quarta, G., and Cau, A. (2015). Persistence of pristine deep-sea coral gardens in the Mediterranean Sea (SW Sardinia). PLoS One 10, e0119393.
| Persistence of pristine deep-sea coral gardens in the Mediterranean Sea (SW Sardinia).Crossref | GoogleScholarGoogle Scholar |
Brook, G. (1889). Report on the Antipatharia. Reports of the Scientific Results of the Voyage of the Challenger, Zoology 32, 5–222.
Brugler, M. R., and France, S. C. (2007). The complete mitochondrial genome of the black coral Chrysopathes formosa (Cnidaria: Anthozoa: Antipatharia) supports classification of antipatharians within the subclass Hexacorallia. Molecular Phylogenetics and Evolution 42, 776–788.
| The complete mitochondrial genome of the black coral Chrysopathes formosa (Cnidaria: Anthozoa: Antipatharia) supports classification of antipatharians within the subclass Hexacorallia.Crossref | GoogleScholarGoogle Scholar |
Brugler, M. R., Opresko, D. M., and France, S. C. (2013). The evolutionary history of the order Antipatharia (Cnidaria: Anthozoa: Hexacorallia) as inferred from mitochondrial and nuclear DNA: implications for black coral taxonomy and systematics. Zoological Journal of the Linnean Society 169, 312–361.
| The evolutionary history of the order Antipatharia (Cnidaria: Anthozoa: Hexacorallia) as inferred from mitochondrial and nuclear DNA: implications for black coral taxonomy and systematics.Crossref | GoogleScholarGoogle Scholar |
Chen, C.A., Chang, C.C., Wei, N.V., Chen, C.H., Lein, Y.T., Lin, H.E., Dai, C.F., and Wallace, C.C. (2004). Secondary structure and phylogenetic utility of the ribosomal internal transcribed spacer 2 in the scleractinian corals. Zoological Studies 43, 759–771.
de Matos, V., Gomes-Pereira, J. N., Tempera, F., Ribeiro, P. A., Braga-Henriques, A., and Porteiro, F. (2014). First record of Antipathella subpinnata (Anthozoa, Antipatharia) in the Azores (NE Atlantic), with description of the first monotypic garden for this species. Deep-sea Research. Part II, Topical Studies in Oceanography 99, 113–121.
| First record of Antipathella subpinnata (Anthozoa, Antipatharia) in the Azores (NE Atlantic), with description of the first monotypic garden for this species.Crossref | GoogleScholarGoogle Scholar |
Ellis, J., and Solander, D. (1786). ‘The Natural History of Many Curious and Uncommon Zoophytes Collected by the Late John Ellis, Systematically Arranged and Described by the Late Daniel Solander.’ (White and Son: London, UK.)
Emig, C., and Geistdoerfer, P. (2005). The Mediterranean deep-sea fauna: historical evolution, bathymetric variations and geographical changes. Carnets Geol/Notebooks Geology, Art 2004/01 (CG2004_A01_CCE-PG), pp. 1–10.
Esper, E. J. C. (1794). Fortsetzungen der Pflanzenthiere. In ‘Die Planzentiere in Abbildungen Nach der Natur mit Farben Erleuchtet Nebst Beschreibungen. Vol. 2’. pp. 303. (Kaspeschen: Nürberg, Germany.)
Gaino, E., Bavestrello, G., Boyer, M., Scoccia, F., and Bo, M. (2013). Biological and ecological relevance of black corals (Antipatharia) in the benthic environment. In ‘Corals: Classification, Habitat and Ecological Significance’. (Ed. M. A. Liñán-Cabello.) pp. 37–74. (NOVA Science Publishers, Inc.: New York, NY.)
Grange, K. R. (1985). Distribution, standing crop, population structure, and growth rates of black coral in the southern fiords of New Zealand. New Zealand Journal of Marine and Freshwater Research 19, 467–475.
| Distribution, standing crop, population structure, and growth rates of black coral in the southern fiords of New Zealand.Crossref | GoogleScholarGoogle Scholar |
Gravier, C. J. (1918). Note sur les Antipathaires du Golfe de Naples. Pubblicazioni della Stazione Zoologica di Napoli 2, 223–240.
Grigg, R. W. (1965). Ecological studies of black coral in Hawaii. Pacific Science 19, 244–260.
Huelsenbeck, J. P., and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17, 754–755.
| MRBAYES: Bayesian inference of phylogeny.Crossref | GoogleScholarGoogle Scholar |
Katoh, K., and Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.
| MAFFT multiple sequence alignment software version 7: improvements in performance and usability.Crossref | GoogleScholarGoogle Scholar |
Lapian, H. F. N., Barucca, M., Bavestrello, G., Biscotti, M. A., Bo, M., Canapa, A., Tazioli, S., and Olmo, E. (2007). A systematic study of some black corals species (Antipatharia, Hexacorallia) based on rDNA internal transcribed spacers sequences. Marine Biology 151, 785–792.
| A systematic study of some black corals species (Antipatharia, Hexacorallia) based on rDNA internal transcribed spacers sequences.Crossref | GoogleScholarGoogle Scholar |
MacIsaac, K. G., Best, M., Brugler, M. R., Kenchington, E. L. R., Anstey, L. J., and Jordan, T. (2013). Telopathes magna gen. nov., spec. nov. (Cnidaria: Anthozoa: Antipatharia: Schizopathidae) from deep waters off Atlantic Canada and the first molecular phylogeny of the deep-sea family Schizopathidae. Zootaxa 3700, 237–258.
| Telopathes magna gen. nov., spec. nov. (Cnidaria: Anthozoa: Antipatharia: Schizopathidae) from deep waters off Atlantic Canada and the first molecular phylogeny of the deep-sea family Schizopathidae.Crossref | GoogleScholarGoogle Scholar |
Mastrototaro, F., d’Onghia, G., Corriero, G., Matarrese, A., Maiorano, P., Panetta, P., Gherardi, M., Longo, C., Rosso, A., Sciuto, F., Sanfilippo, R., Gravili, C., Boero, F., Taviani, M., and Tursi, A. (2010). Biodiversity of the white coral bank off Cape Santa Maria di Leuca (Mediterranean Sea): an update. Deep-sea Research. Part II, Topical Studies in Oceanography 57, 412–430.
| Biodiversity of the white coral bank off Cape Santa Maria di Leuca (Mediterranean Sea): an update.Crossref | GoogleScholarGoogle Scholar |
Milne-Edwards, H., and Haime, J. (1857). ‘Histoire Naturelle des Coralliaires ou Polypes Proprement Dits.’ (Librairie Encyclopédique de Roret: Paris, France.)
Molodtsova, T. N. (2006). Black corals (Antipatharia: Anthozoa: Cnidaria) of the north-eastern Atlantic. In ‘Biogeography of the Atlantic Seamounts’. (Eds A. N. Mironov, A. V. Gebruk, and A. J. Southward.) pp. 141–151. (KMK Scientific Press: Moscow.)
Molodtsova, T. N. (2011). A new species of Leiopathes (Anthozoa: Antipatharia) from the Great Meteor seamount (North Atlantic). Zootaxa 3138, 51–64.
Molodtsova, T. N., and Opresko, D. M. (2017). Black corals (Anthozoa: Antipatharia) of the Clarion-Clipperton Fracture Zone. Marine Biodiversity 47, 349–365.
| Black corals (Anthozoa: Antipatharia) of the Clarion-Clipperton Fracture Zone.Crossref | GoogleScholarGoogle Scholar |
Ocaña, O., Opresko, D. M., and Brito, A. (2007). First record of the black coral Antipathella wollastoni (Anthozoa: Antipatharia) outside of Macaronesian waters. Revista de la Academia Canaria de Ciencias 18, 125–138.
Opresko, D. M. (1998). Three new species of Leiopathes (Cnidaria: Anthozoa: Antipatharia) from southern Australia. Records of the South Australian Museum 31, 99–111.
Opresko, D. M. (2001). Revision of the Antipatharia (Cnidaria: Anthozoa). Part I. Establishment of a new family, Myriopathidae. Zoologische Mededelingen, Leiden 75, 343–370.
Opresko, D. M. (2002). Revision of the Antipatharia (Cnidaria: Anthozoa). Part II. Schizopathidae. Zoologische Mededelingen Leiden 76, 411–442.
Opresko, D. M. (2003). Revision of the Antipatharia (Cnidaria: Anthozoa). Part III. Cladopathidae. Zoologische Mededelingen Leiden 77, 495–536.
Opresko, D. M. (2004). Revision of the Antipatharia (Cnidaria: Anthozoa). Part IV. Establishment of a new family, Aphanipathidae. Zoologische Mededelingen Leiden 78, 209–240.
Opresko, D. M., and Försterra, G. (2004). Orden Antipatharia (corales negros o espinosos). In ‘El Mar Mediterraneo: Fauna, Flora, Ecologia’. (Ed. R. Hofrichter.) pp. 506–509. (Omega: Barcelona, Spain.)
Pallas, P. S. (1766). ‘Elenchus Zoophytorum Sistens Generum Adumbrationes Generaliores et Specierum Cognitarum Succinctas Descriptiones cum Selectis Auctorum Synonymis.’ (Apud Petrum van Cleef: Hagæ-Comitum, the Netherlands.)
Pax, F. (1940). Anthozoa. In ‘Klassen und Ordnungen des Tierreich Vol. 2’. (Ed. H. G. Bronn.) pp. 267–280. (Winter CF Publisher: Leipzig, Germany.)
Posada, D., and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.
| Modeltest: testing the model of DNA substitution.Crossref | GoogleScholarGoogle Scholar |
Reyss, D. (1973). Les canyons sous-marins de lamer Catalane. IV. Etude synécologique des peuplements de macrofaune benthique. Vie et Milieu 23, 101–142.
Roule, L. (1905). Description des Antipathaires et Cérianthaires recueillis par S.A.S. le Prince de Monaco dans l’Atlantique Nord. Résultats des Campagnes Scientifiques du Prince de Monaco 30, 1–99.
Schultze, L. S. (1896). Beitrag zur Systematik der Antipatharien. Abhandlungen der Senckenbergische naturforschende Gesellschaft 23, 1–40.
Spalding, M. D., Fox, H. E., Allen, G. R., Davidson, N., Ferdaña, Z. A., Finlayson, M., Halpern, B. S., Jorge, M. A., Lombana, A., Sara, A. L., Martin, K. D., McManus, E., Molnar, J., Recchia, C. A., and Robertson, J. (2007). Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. Bioscience 57, 573–583.
| Marine ecoregions of the world: a bioregionalization of coastal and shelf areas.Crossref | GoogleScholarGoogle Scholar |
Tazioli S. Bo M. Boyer M. Rotinsulu H. Bavestrello G. 2007
Tescione, G. (1973). ‘The Italians and Their Coral Fishing.’ (Fausto Fiorentino: Napoli, Italy.)
von Koch, G. (1889). Die Antipathiden des Golfes von Neapel. Mitteilungen aus der Zoologischen Station zu Neapel Zugleich ein Repertorium für Mittelmeerkunde 9, 187–204.
Wagner, D., and Opresko, D. M. (2015). Description of a new species of Leiopathes (Antipatharia: Leiopathidae) from the Hawaiian Islands. Zootaxa 3974, 277–289.
| Description of a new species of Leiopathes (Antipatharia: Leiopathidae) from the Hawaiian Islands.Crossref | GoogleScholarGoogle Scholar |
Wagner, D., Brugler, M. R., Opresko, D. M., France, S. C., Montgomery, A. D., and Toonen, R. J. (2010). Using morphometrics, in situ observations and genetic characters to distinguish among commercially valuable Hawaiian black coral species; a redescription of Antipathes grandis Verrill, 1928 (Antipatharia: Antipathidae). Invertebrate Systematics 24, 271–290.
| Using morphometrics, in situ observations and genetic characters to distinguish among commercially valuable Hawaiian black coral species; a redescription of Antipathes grandis Verrill, 1928 (Antipatharia: Antipathidae).Crossref | GoogleScholarGoogle Scholar |
Wagner, D., Luck, D. G., and Toonen, R. J. (2012). The biology and ecology of black corals (Cnidaria: Anthozoa: Hexacorallia: Antipatharia). Advances in Marine Biology 63, 67–132.
| The biology and ecology of black corals (Cnidaria: Anthozoa: Hexacorallia: Antipatharia).Crossref | GoogleScholarGoogle Scholar |
Warner, G. F. (1981). Species descriptions and ecological observations of black corals (Antipatharia) from Trinidad. Bulletin of Marine Science 31, 147–163.
