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Article
Published: 2018-09-06

Morphological and genetic divergence between Mediterranean and Caribbean populations of Madracis pharensis (Heller 1868) (Scleractinia, Pocilloporidae): too much for one species?

Department of Biotechnology and Biosciences, University of Milano-Bicocca, Piazza della Scienza, 2, 20126 Milan, Italy Institut de Recherche pour le Développement, UMR9220 ENTROPIE, 101 Promenade Roger Laroque, BP A5, 98848 Nouméa Cedex, New Caledonia
Department of Biotechnology and Biosciences, University of Milano-Bicocca, Piazza della Scienza, 2, 20126 Milan, Italy Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Saudi Arabia
Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Saudi Arabia
Institute of Marine Sciences—National Research Council, (ISMAR-CNR), Via Gobetti 101, 40129 Bologna, Italy Biology Department, Woods Hole Oceanographic Institution, 266 Woods Hole Road, Woods Hole, MA 02543, USA Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Naples, Italy
Global Change Institute, The University of Queensland, Brisbane QLD 4072, Australia CARMABI, Piscaderabaai z/n, PO Box 2090, Willemstad, Curaçao
CARMABI, Piscaderabaai z/n, PO Box 2090, Willemstad, Curaçao CCMAR—Centre of Marine Sciences, University of Algarve, 8005-139 Faro, Portugal
Coleoptera Madracis senaria Madracis kirbyi rDNA ATP8 corallite diameter

Abstract

The colonial stony coral genus Madracis is cosmopolitan, lives in shallow and deep water habitats, and includes zooxanthellate, azooxanthellate and facultative symbiotic species. One of its species, Madracis pharensis, has been recorded from the Mediterranean and East Atlantic, where it forms small knobby and facultative zooxanthellate colonies (also named M. pharensis f. pharensis), and from the tropical Caribbean, where it also occurs in a massive and zooxanthellate form (named M. pharensis f. luciphila by some). These two forms have been previously found to host different Symbiodinium species. In this study, species boundaries and phylogenetic relationships between these two Madracis pharensis forms (from the Mediterranean Sea and the Caribbean), M. senaria, and the Indo-west Pacific M. kirbyi were analyzed through an integrated systematics approach, including corallite dimensions, micromorphology and two molecular markers (ITS and ATP8). Significant genetic and morphological differences were found between all the examined Madracis species, and between M. pharensis from the Mediterranean Sea and M. pharensis f. luciphila from the Caribbean in particular. Based on these results, the latter does not represent a zooxanthellate ecomorph of the former but a different species. Its identity remains to be ascertained and its relationship with the Caribbean M. decactis, with which it bears morphologic resemblance, must be investigated in further studies. Overall, the presence of cryptic Madracis species in the Easter and Central Atlantic Ocean remains to be evaluated.

 

References

  1. Arrigoni, R., Vacherie, B., Benzoni, F., Stefani, F., Karsenti, E., Jaillon, O., Not, F., Nunes, F., Payri, C., Wincker, P. & Barbe V. (2017) A new sequence dataset of SSU rRNA gene for Scleractinia and its phylogenetic and ecological applications. Molecular Ecology Resources, 17, 1054–1071.
    https://doi.org/10.1111/1755-0998.12640

    Bandelt, H.J., Forster, P. & Röhl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37–48.
    https://doi.org/10.1093/oxfordjournals.molbev.a026036

    Benzoni, F., Arrigoni, R., Stefani, F. & Pichon, M. (2011) Phylogeny of the coral genus Plesiastrea (Cnidaria, Scleractinia). Contributions to Zoology, 80, 231–248.

    Bongaerts, P., Frade, P.R., Ogier, J.J., Hay, K.B., van Bleijswijk, J., Englebert, N., Vermeij, M.J.A., Bak, R.P.M., Visser, P.M. & Hoegh-Guldberg, O. (2013) Sharing the slope: depth partitioning of agariciid corals and associated Symbiodinium across shallow and mesophotic habitats (2-60 m) on a Caribbean reef. BMC Evolutionary Biology, 13, 205.
    https://doi.org/10.1186/1471-2148-13-205

    Bongaerts, P., Frade, P.R., Hay, K.B., Englebert, N., Latijnhouwers, K., Bak, R.P.M., Vermeij, M.J.H. & Hoegh-Guldberg, O. (2014) The lower mesophotic zone of a Southern Caribbean reef: limited by temperature rather than light? Scientific Reports, 5, 7652.
    https://doi.org/10.5479/si.00810282.504

    Cairns, S.D. (1991) A revision of the ahermatypic Scleractinia of the Galápagos and Cocos Islands. Smithsonian Contributions to Zoology, 504, 1–32.
    https://doi.org/10.5479/si.00810282.557.i

    Cairns, S.D. (1994) Scleractinia of the Temperate North Pacific. Smithsonian Contributions to Zoology 557, 1–150.

    Cairns, S.D. (1999) Cnidaria Anthozoa: Deep-Water azooxanthellate Scleractinia from Vanuatu and Wallis and Futuna Islands. Annales du Muséum national d'histoire naturelle, 180, 31–167.

    Cairns, S.D. (2000) A revision of the shallow-water azooxanthellate Scleractinia of the western Atlantic. Studies on the Natural History of the Caribbean Region, 75, 1–231.

    Cairns, S.D., Jaap, W.C. & Lang, J.C. (2009) Scleractinia (Cnidaria) of the Gulf of Mexico. In: Felder, D.L. & Camp, D.K. (Eds.), Gulf of Mexico Origins, Waters, and Biota. Biodiversity. Texas A and M Press, College Station Texas, pp. 333–347.

    Cairns, S.D., Hoeksema, B.W. &Van Der Land, J. (1999) Appendix: List of extant stony corals. Atoll Research Bulletin, 459, 13–46.

    Cairns, S.D. & Kitahara, M. (2012) An illustrated key to the genera and subgenera of the recent azooxanthellate Scleractinia (Cnidaria, Anthozoa), with an attached glossary. ZooKeys, 227, 1–47.
    https://doi.org/10.3897/zookeys.227.3612

    Cairns, S.D. & Zibrowius, H. (1997) Cnidaria, Anthozoa: azooxanthellate Scleractinia from the Philippine and Indonesian regions. Mémoires du Muséum d'histoire naturelle, 172, 27–243.

    Capel, K.C.C., Segal, B., Lindner, A. & Bertuol, P. (2012) Corallith beds at the edge of the tropical South Atlantic. Coral Reefs, 31, 75.
    https://doi.org/10.1007/s00338-011-0818-3

    Chen, C., Chiou, C.Y., Dai, C.F. & Chen, C.A. (2008) Unique mitogenomic features in the scleractinian family Pocilloporidae (Scleractinia: Astrocoeniina). Marine Biotechnology, 10, 538–553.
    https://doi.org/10.1007/s10126-008-9093-x

    Fenner, D. (1993) Species distinctions among several Caribbean stony corals. Bulletin of Marine Science, 53, 1099–1116

    Filatov, M.V., Frade, P.R., Bak, R.P.M., Vermeij, M.J.A. & Kaandorp, J.A. (2013) Comparison between colony morphology and molecular phylogeny in the Caribbean scleractinian coral genus Madracis. PLoS ONE, 8, e71287.
    https://doi.org/10.1371/journal.pone.0071287

    Flot, J.F., Magalon, H., Cruaud, C., Couloux, A., Tillier, S. (2008a) Patterns of genetic structure among Hawaiian corals of the genus Pocillopora yield clusters of individuals that are compatible with morphology. Comptes Rendus Biologies, 331, 239–247.

    Flot, J.F., Licuanan, W.Y., Nakano, Y., Payri, C., Cruaud, C. & Tillier, S. (2008b) Mitochondrial sequences of Seriatopora corals show little agreement with morphology and reveal the duplication of a tRNA gene near the control region. Coral Reefs, 27, 789–794.

    Flot, J.F., Blanchot, J., Charpy, L., Cruaud, C., Licuanan, W.Y., Nakano, Y., Payri, C. & Tillier, S. (2011) Incongruence between morphotypes and genetically delimited species in the coral genus Stylophora: phenotypic plasticity, morphological convergence, morphological stasis or interspecific hybridization? BMC Ecology, 4, 11–22.

    Frade, P.R., De Jongh, F., Vermeulen, F., Van Bleijswijk, J. & Bak, R.P.M. (2008a) Variation in symbiont distribution between closely related coral species over large depth ranges. Molecular Ecology, 17, 691–703.

    Frade, P.R., Englebert, N., Faria, J., Visser, P.M. & Bak, R.P.M. (2008b) Distribution and photobiology of Symbiodinium types in different light environments for three colour morphs of the coral Madracis pharensis: is there more to it than total irradiance? Coral Reefs, 27, 913–925.

    Frade, P.R., Bongaerts, P., Winkelhagen, A.J.S., Tonk, L. & Bak, R.P.M. (2008c) In situ photobiology of corals over large depth ranges: a multivariate analysis on the roles of environment, host, and algal symbiont. Limnology and Oceanography, 53, 2711–2723.

    Frade, P.R., Reyes-Nivia, M.C., Faria, J., Kaandorp, J.A., Luttikhuizen, P.C. & Bak, R.P.M. (2010) Semi-permeable species boundaries in the coral genus Madracis: introgression in a brooding coral system. Molecular Phylogenetics and Evolution, 57, 1072–1090.
    https://doi.org/10.1016/j.ympev.2010.09.010

    Fricke, H.W. & Hottinger, L. (1983) Coral bioherms below the euphotic zone in the Red Sea. Marine Ecology Progress Series, 11, 113–117.
    https://doi.org/10.3354/meps011113

    Fukami, H., Chen, C.A., Budd, A.F., Collins, A.G., Wallace, C.C., Chuang, Y.Y., Dai, C.F., Iwao, K., Sheppard, C.R.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.
    https://doi.org/10.1371/journal.pone.0003222

    Gerovasileiou, V., Chintiroglou, C.C., Vafidis, D., Koutsoubas, D., Sini, M., Dailianis, T., Issaris, Y., Akritopoulou, E., Dimarchopoulou, D. & Voultsiadou, E. (2015) Census of biodiversity in marine caves of the eastern Mediterranean Sea. Mediterrean Marine Science, 16, 245–265.
    https://doi.org/10.12681/mms.1069

    Goreau, T.F. & Wells, J.W. (1967) The shallow-water Scleractinia of Jamaica: revised list of speciesand their vertical distribution range. Bulletin of Marine Science, 17, 442–453.

    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.

    Heller, C. (1968) Die Zoophyten und Echinodermen des Adriatischen Meeres. Kaiserliche Koniglichen Zoologisch Botanisch Gesellschaft, Wien, 88 pp.

    Huang, D. (2012) Threatened reef corals of the world. PLoS ONE, 7, e34459.
    https://doi.org/10.1371/journal.pone.0034459

    Hickman CP (2008) Corals and other radiates of Galapagos. Sugar Spring Press, Lexington, Virginia, USA

    Kaandorp, J.A., Koopman, E.A., Sloot, P.M.A., Bak, R.P.M., Vermeij, M.J.A. & Lampmann, L.E.H. (2003) Simulation and analysis of flow patterns around the scleractinian coral Madracis mirabilis (Duchassaing and Michelotti). Philosophical Transactions of the Royal Society B: Biological Sciences, 358, 1551–1557.
    https://doi.org/10.1098/rstb.2003.1339

    Kaandorp, J.A., Sloot, P.M.A., Merks, R.M.H., Bak, R.P.M. & Vermeij, M.J.A. (2005) Morphogenesis of the branching coral Madracis mirabilis. Proceedings of the Royal Society of London B: Biological Sciences, 272,127–133.
    https://doi.org/10.1098/rspb.2004.2934

    Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780.
    https://doi.org/10.1093/molbev/mst010

    Katoh, K., Misawa, K., Kuma, K. & Miyata, T. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30, 3059–3066.
    https://doi.org/10.1093/nar/gkf436

    Keshavmurthy, S., Yang, S., Alamaru, A., Chuang, Y., Pichon, M., Obura, D., Fontana, S., De Palmas, S., Stefani, F., Benzoni, F., MacDonald, A., Noreen, A.M.E., Chen, C., Wallace, C.C., Moothien Pillay, R., Denis, V., Amri, A.Y., Reimer, J.D., Mezaki, T., Sheppard, C., Loya, Y., Abelson, A., Mohammed, M.S., Baker, A.C., Mostafavi, P.G., Suharsono, B.A. & Chen, C.A. (2013) DNA barcoding reveals the coral “laboratory-rat”, Stylophora pistillata encompasses multiple identities. Scientific Reports, 3, 1520.
    https://doi.org/10.1038/srep01520

    Kitahara, M.V., Cairns, S.D., Stolarski, J., Blair, D. & Miller, D.J. (2010) A comprehensive phylogenetic analysis of the Scleractinia (Cnidaria, Anthozoa) based on mitochondrial CO1 sequence data. PLoS ONE, 5, e11490.
    https://doi.org/10.1371/journal.pone.0011490

    Klueter, A. & Andreakis, N. (2013) Assessing genetic diversity in the scleractinian coral Stylophora pistillata (Esper 1797) from the Central Great Barrier Reef and the Coral Sea. Systematics and Biodiversity, 11, 67–76.
    https://doi.org/10.1080/14772000.2013.770419

    Laborel, J. & Vacelet, J. (1958) Étude des peuplements d’une grotte sous-marine du golfe de Marseille. Bulletin de l'Institut océanographique de Monaco, 1120, 1–20.

    Laborel, J. (1967) A revised list of Brazilian scleractinian corals and description of a new species. Postilla Yale Peabody Museum, 107, 1–14.

    LaJeunesse, T.C., Parkinson, J.E. & Reimer, J. (2012) A genetics-based description of Symbiodinium minutum sp. nov. and S. Psygmophilum sp. nov. (Dinophyceae), two dinoflagellates symbiotic with cnidaria. Journal of Phycology, 48, 1380–1391.
    https://doi.org/10.1111/j.1529-8817.2012.01217.x

    Librado, P. & Rozas, J. (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452.
    https://doi.org/10.1093/bioinformatics/btp187

    Lyman, T. (1859) On a new species of coral (Astraea decactis). Proceedings of the Boston Society of Natural History, 6, 260–263.

    Locke, J.M., Weil, E. & Coates, K.A. (2007) A newly documented species of Madracis (Scleractinia: Pocilloporidae) from the Caribbean. Proceedings of the Biological Society of Washington, 120, 214–226.
    https://doi.org/10.2988/0006-324X(2007)120[214:ANDSOM]2.0.CO;2

    Milne Edwards, H. & Haime, J. (1849) Mémoire sur les polypiers appartenant a la famille des Oculinides, au groupe intermediate des Pseudoastréides et à la famille des Fongides. Comptes rendus hebdomadaires des seances de l'Academie des sciences. Serie D: Sciences Naturelles, 29, 67–73.

    Morri, C., Vafidis, D., Peirano, A., Chintiroglou, C.C. & Bianchi, C.N. (2000) Anthozoa from a subtidal hydrothermal area of Milos Island (Aegean Sea), with notes on the construction potential of the scleractinian coral Madracis pharensis. Italian Journal of Zoology, 67, 319–325.
    https://doi.org/10.1080/11250000009356331

    Muramatsu, D. & Lang da Silveira, F. (2008) Gametogenesis in Madracis decactis Lyman, 1859 (Cnidaria, Scleractinia) from Ilha Grande Bay (Rio de Janeiro), southeastern Brazil. Brazilian Journal of Oceanography, 56, 297–305.
    https://doi.org/10.1590/S1679-87592008000400005

    Neves, E. & Johnsson, R. (2009) Taxonomic revision of the southwestern Atlantic Madracis and the description of Madracis fragilis n. sp. (Scleractinia: Pocilloporidae), a new coral species from Brazil. Scientia Marina, 73, 739–746.
    https://doi.org/10.3989/scimar.2009.73n4735

    Özalp, H.B., Alparslan, M. (2015) Distribution and morphology of the colonial scleractinian Madracis pharensis (Cnidaria, Anthozoa) in the Dardanelles (Marmara Sea, Turkey). Acta Zoologica Bulgarica, 67, 429–434.

    Pinzon, J.H., Sampayo, E., Cox, E., Chauka, L.J., Chen, C.A., Voolstra, C.R. & LaJeunesse, T.C. (2013) Blind to morphology: genetic identifies several widespread ecologically common species and few endemics among Indo-Pacific cauliflower corals (Pocillopora, Scleractinia). Journal of Biogeography, 40, 1595–1608.
    https://doi.org/10.1111/jbi.12110

    Reyes Bonilla, H., Martinez Olguin, E. & Reyna, G.A. (1995) First Record of Madracis sp. cf. M. pharensis (Heller, 1868) on Continental Eastern Pacific Shores. Bulletin of the Southern California Academy of Sciences, 94, 172–175.

    Romano, S.L. & Cairns, S.D. (2000) Molecular phylogenetic hypothesis for the evolution of scleractinian corals. Bulletin of Marine Science, 67, 1043–1068.

    Santodomingo, N., Reyes, J., Gracia, A., Martínez, A., Ojeda, G. & García, C. (2007) Azooxanthellate Madracis coral communities off San Bernardo Islands (Colombian Caribbean). Bulletin of Marine Science, 81 (Supplement 1), 273–287.

    Scheer, G. & Pillai, C.S.G. (1983) Report on the stony corals from the Red Sea. Zoologica, 131, 1–198.

    Schmidt-Roach, S., Lundgren, P., Miller, K.J., Gerlach, G., Noreen, A.M.E. & Andreakis, N. (2012) Assessing hidden species diversity in the coral Pocillopora damicornis from Eastern Australia. Coral Reefs, 32, 161–172.
    https://doi.org/10.1007/s00338-012-0959-z

    Schmidt-Roach, S., Miller, K.J., Lundgren, P. & Andreakis, N. (2014) With eyes wide open: a revision of species within and closely related to the Pocillopora damicornis species complex (Scleractinia; Pocilloporidae) using morphology and genetics. Zoological Journal of the Linnean Society, 170, 1–33.
    https://doi.org/10.1111/zoj.12092

    Sheppard, C.R.C. & Sheppard, A.L.S. (1991) Corals and coral communities of Arabia. Fauna of Arabia, 12, 3–170.

    Simes, R.J. (1986) An improved Bonferroni procedure for multiple tests of significance. Biometrika, 73, 751–754.
    https://doi.org/10.1093/biomet/73.3.751

    Spjotvoll, E. & Stoline, M.R. (1973) An extension of the method of multiple comparisons to include the cases with unequal sample sizes. Journal of the American Statistical Association, 68, 975–978.

    Stefani, F., Benzoni, F., Sung Yin, Y., Pichon, M., Galli, P. & Chen, C.A. (2011) Comparison of morphological and genetic analyses reveal cryptic divergence and morphological plasticity in Stylophora (Cnidaria, Scleractinia). Coral Reefs, 30, 1033–1049.
    https://doi.org/10.1007/s00338-011-0797-4

    Stolarski, J., Kitahara, M.V., Miller, D.J., Cairns, S.D., Mazur, M. & Meibom, A. (2011) The ancient evolutionary origins of Scleractinia revealed by azooxanthellate corals. BMC Evolutionary Biology, 11, 316.
    https://doi.org/10.1186/1471-2148-11-316

    Takabayashi,u8 M., Carter, D., Loh, W. & Hoegh-Guldberg, O. (1998) A coral specific primer for PCR amplification of the internal transcribed spacer region in ribosomal DNA. Molecular Ecology, 7, 928–930.

    Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution, 30, 2725–2729.
    https://doi.org/10.1093/molbev/mst197

    Vermeij, M.J.A., Kaandorp, J.A., Bak, R.P.M. & Lampmann, L.E.H. (2001) Three-dimensional morphological analysis of growth forms of Madracis mirabilis. In: Kaandorp, J.A. & Kuebler, J. (Eds.), The Algorithmic Beauty of Seaweeds, Sponges and Corals. Springer Verlag, New York, pp. 1–158.

    Vermeij, M.J.A., Delvoye, L. & Bak, R.P.M. (2002) Fluorescence in the Caribbean coral genus Madracis. Photosynthetica, 40, 423–429.
    https://doi.org/10.1023/A:1022635327172

    Vermeij, M.J.A. & Bak, R.P.M. (2002a) How are coral populations structured by light? Marine light regimes and the distribution of Madracis. Marine Ecology Progress Series, 233, 105–116.

    Vermeij, M.J.A. & Bak, R.P.M. (2002b) Corals on the move: rambling of Madracis pharensis polyps early after settlement. Coral Reefs, 21, 262–263.

    Vermeij, M.J.A., Diekmann, O.E. & Bak, R.P.M. (2003a) A new species of Scleractinian coral (Cnidaria, Anthozoa), Madracis carmabi n. sp. from the Southern Caribbean. Bulletin of Marine Science, 73, 679–684.

    Vermeij, M.J.A., Broker, K., Sampayo, E. & Bak, R.P.M. (2003b) Planulae release in the Caribbean genus Madracis. Marine Ecology Progress Series, 247, 75–84.

    Vermeij, M.J.A. & Bak, R.P.M. (2003c) Species specific population structures of five closely related Madracis morphospecies along a depth gradient (5-60m) at a Caribbean coral reef. Bulletin of Marine Science, 73, 725–744.

    Vermeij, M.J.A., Broker, K., Sampayo, E. & Bak, R.P.M. (2004) Gametogenesis in the Caribbean genus Madracis. Coral Reefs, 23, 206–214.

    Vermeij, M.J.A. & Sandin, S.A. (2006) Coral species complexes through space and time: an illustration of their dynamics using Madracis in the Caribbean. Proceedings of the 10th International Coral Reef Symposium, Okinawa, Japan, 116–121.

    Veron, J.E.N. & Pichon, M. (1976) Scleractinia of Eastern Australia. Monograph Series of the Australian Institute for Marine Science I. Australian Govt. Pub. Service, Canberra, 86 pp.
    https://doi.org/10.5962/bhl.title.60617

    Veron, J.E.N. (1986) Corals of Australia and the Indo-Pacific. Angus & Robertson, Sydney, 644 pp.

    Veron, J.E.N. (2000) Corals of the World. Australian Institute of Marine Science and CRR Queensland Townsville, 1382 pp.

    Wells, J.W. (1956) Scleractinia. In: Moore, R.C. (Ed.), Treatise on invertebrate paleontology. Part F: Coelenterata. Geological Society of America and University of Kansas Press, Lawrence, Kansas: 328–444. [F328–F444]

    Wells, J.W. (1973a) New and old scleractinian corals from Jamaica. Bulletin of Marine Science, 23, 16–58.

    Wells, J.W. (1973b) Two new hermatypic scleractinian corals from the West Indies. Bulletin of Marine Science, 23, 925–932.

    Wells, J.W. (1983) Annotated list of the scleractinian corals of the Galapagos. In: Glynn, P.W. & Wellington, G.M. (Eds.), Corals and coral reefs of the Galapagos Islands. University of California Press Berkley and Los Angeles, pp. 211–291.

    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 Inc. San Diego, pp. 315–322.
    https://doi.org/10.1016/B978-0-12-372180-8.50042-1

    Zibrowius, H. (1980) Les scléractiniaires de la Méditerranée et de l'Atlantique nord-oriental. Mémoires de l'Institut Océanographique, Monaco, 11, 1–55.

    Zibrowius, H., Wirtz, P., Nunes, F.L.D., Hoeksema, B.W. & Benzoni, F. (2017) Shallow-water scleractinian corals of Ascension Island, Central South Atlantic. Journal of the Marine Biological Association of the United Kingdom, 97, 713–725.
    https://doi.org/10.1017/S0025315414001465

    Zlatarski, V.N. & Martinez Estalella, N. (1982) Les Scléractiniaires de Cuba avec des données sur les organisms associés. Editions l’Académie Bulgare des Sciences, Sofia, 471 pp.

How to Cite

BENZONI, F., ARRIGONI, R., BERUMEN, M. L. ., TAVIANI, M., BONGAERTS, P., & FRADE, P. R. (2018). Morphological and genetic divergence between Mediterranean and Caribbean populations of <em>Madracis pharensis</em> (Heller 1868) (Scleractinia, Pocilloporidae): too much for one species?. Zootaxa, 4471(3), 473–492. https://doi.org/10.11646/zootaxa.4471.3.3