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Systematics of the coral genus Craterastrea (Cnidaria,Anthozoa, Scleractinia) and description of a newfamily through combined morphological and molecularanalysesFrancesca Benzoni a b , Roberto Arrigoni a , Fabrizio Stefani c & Jarosław Stolarski d

a Department of Biotechnology and Biosciences, University of Milano-Bicocca, Piazza dellaScienza 2, 20126, Milan, Italyb Institut de Recherche pour le Développement, UMR227 CoReUs2, 101 Promenade RogerLaroque, BP A5, 98848 Nouméa Cedex, New Caledoniac Water Research Institute-National Research Council (IRSA-CNR), Via del Mulino 19, 20861,Brugherio (MB), Italyd Institute of Paleobiology, Polish Academy of Sciences, Twarda 51/55, PL-00–818,Warszawa, PolandPublished online: 19 Dec 2012.

To cite this article: Francesca Benzoni , Roberto Arrigoni , Fabrizio Stefani & Jarosław Stolarski (2012): Systematics of thecoral genus Craterastrea (Cnidaria, Anthozoa, Scleractinia) and description of a new family through combined morphologicaland molecular analyses, Systematics and Biodiversity, 10:4, 417-433

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Systematics and Biodiversity (2012), 10(4): 417–433

Research Article

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

FRANCESCA BENZONI1,2, ROBERTO ARRIGONI1, FABRIZIO STEFANI3 & JAROSŁAW STOLARSKI4

1Department of Biotechnology and Biosciences, University of Milano-Bicocca, Piazza della Scienza 2, 20126 Milan, Italy2Institut de Recherche pour le Developpement, UMR227 CoReUs2, 101 Promenade Roger Laroque, BP A5, 98848 Noumea Cedex,New Caledonia3Water Research Institute-National Research Council (IRSA-CNR), Via del Mulino 19, 20861 Brugherio (MB), Italy4Institute of Paleobiology, Polish Academy of Sciences, Twarda 51/55, PL-00–818, Warszawa, Poland

(Received 14 August 2012; revised 17 October 2012; accepted 24 October 2012)

The monotypic genus Craterastrea was assigned to the family Siderastreidae owing to the similarity of its septalmicromorphology to that of Coscinaraea. Subsequently, it was synonymized with Leptoseris, family Agariciidae, based oncorallum macromorphology. Since then, it has remained poorly studied and has been known only from a small number ofspecimens from relatively deep reef environments in the Red Sea and the Chagos archipelago, northern Indian Ocean.Access to museum collections enabled examination of type material and the recovery of coral skeletons from theSeychelles, Madagascar, and Mayotte, southern Indian Ocean. A recent survey in Mayotte allowed the in situ imaging ofCraterastrea in shallow and turbid reef environments and sampling for molecular analyses. The molecular analyses were inagreement with the examination of micromorphology and microstructure of skeletons by revealing that Craterastrea levis,the only species in the genus, differs much from Leptoseris foliosa, with which it was synonymized. Moreover, Craterastreais closely related to Coscinaraea, Horastrea and Anomastraea. However, these genera, currently ascribed to theSiderastreidae, are genetically distant to Siderastrea, the family’s type genus, and Pseudosiderastrea. Hence, we restore thegenus Craterastrea, describe the new family Coscinaraeidae due to its deep evolutionary divergence from theSiderastreidae, and provide revised diagnoses of the four genera in the family. The description of the new familyCoscinaraeidae is a further step in the challenging but ongoing process of revision of the taxonomy of scleractinian coralsas a result of the molecular systematics revolution.

Key words: Anomastraea irregularis, COI, Coscinaraea monile, Coscinaraeidae, Craterastrea levis, Horastrea indica,Leptoseris foliosa, microstructure, new family, rDNA, Siderastreidae

IntroductionScleractinian coral systematics is undergoing a consider-able revolution due to current progress in molecular phy-logenetics. Molecular analyses have indicated that the or-der Scleractinia is divided into three major clades i.e. theRobust, Complex and Basal clades (Romano & Palumbi,1996; Romano & Cairns, 2000; Chen et al., 2002; Fukamiet al., 2004, 2008; Le Goff-Vitry et al., 2004; Kerr, 2005;Nunes et al., 2008; Kitahara et al., 2010; Huang et al.,2011; Stolarski et al., 2011). Phylogenetic analyses haveshown that many traditional families and genera are para- or

Correspondence to: Francesca Benzoni. E-mail: [email protected]

polyphyletic. For example, based on concordant resultsfrom different nuclear and mitochondrial markers, the fam-ily Siderastreidae is deeply polyphyletic (Fukami et al.,2008; Huang, 2012), with Siderastrea Blainville, 1830(the family’s type genus) and Pseudosiderastrea Yabe &Sugiyama, 1935 being closely related (Pichon et al., 2012).These genera belong to the Complex clade (Romano &Cairns, 2000; Chen et al., 2004; Benzoni et al., 2007),whereas the other genera still recognized in the family(Horastrea Pichon, 1971, Anomastraea Marenzeller, 1901,Coscinaraea Milne Edwards & Haime, 1848) belong to theRobust clade and are closely related to the Fungiidae Dana,1846 (Benzoni et al., 2007, 2012; Kitahara et al., 2010;Huang, 2012) (see Discussion and Fig. 47). Conversely,although monophyly of the family Agariciidae is being

ISSN 1477-2000 print / 1478-0933 onlineC© 2012 The Natural History Museum

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418 F. Benzoni et al.

questioned with respect to the placement of PachyserisMilne Edwards & Haime, 1849 (Fukami et al., 2008) andCoeloseris Vaughan, 1918 (Kitahara et al., in press), it hasrecently gained the deep-water coral genus DactylotrochusWells, 1954 (Kitahara et al., in press), with all taxa ascribedto it belonging to the Complex Clade (Huang, 2012).

Huang (2012) included Craterestrea ( = Craterastrea)levis in a cladogram of scleractinian corals in the Robustclade of the tree of life of the order Scleractinia. However,no molecular data were available for this taxon and the au-thor included it in the super tree based on morphologicaldata. In this tree the genus appears most closely related toCoscinaraea and Psammocora, and then to Horastrea,Anomastraea and Pseudosiderastrea, while Siderastrea isplaced in the Complex clade (Huang, 2012). However, for-mal taxonomic actions were not undertaken as in manycases where molecular analyses have proven the inadequacyof the traditional taxonomy, with some notable recent excep-tions (e.g. Gittenberger et al., 2011; Benzoni et al., 2012;Budd et al., in press; Kitahara et al., in press).

The monotypic genus Craterastrea was described byHead (1983) in the family Siderastreidae Vaughan & Wells,1943 due to the similarity of its septal micromorphologyto that of Coscinaraea. Head (1983) based his descriptionon material from Egypt previously identified as Leptoserishawaiiensis Vaughan, 1907 (Agariciidae Gray, 1847) byMatthai (1948) and Ma (1959) and on specimens he col-lected in Sudan (Head, 1983). He provided detailed illus-trations of the new taxon’s typical macro and micromor-phology. The species was later reported again from theRed Sea and from the Chagos archipelago in the IndianOcean (Fig. 1) (Sheppard, 1980, 1981, 1987, 1998b; Shep-pard & Sheppard, 1991). The majority of known recordsof C. levis are from deep reef environments (below 35 m)(Head, 1983; Sheppard & Sheppard, 1991) with the ex-ception of one specimen from 5 m from ‘dimly lit turbidwaters’ in the harbour of Port Sudan (Head, 1983). Despiteillustrations of the skeleton in the original description of thetaxon (Head, 1983) including SEM images to show the dif-ferences between Craterastrea levis and Leptoseris glabraDinesen, 1980, Veron (1993) decided that C. levis is a ju-nior synonym of Leptoseris foliosa Dinesen, 1980. This de-cision led de facto to the synonymy of the monotypic genusCraterastrea with the agariciid Leptoseris Milne Edwards& Haime, 1849. These synonymies have not been contra-dicted (Veron, 1995, 2000; UNEP-WCMC, 2005) and havenever been reassessed. Today, in the era of online taxonomicdatabases, Craterastrea is recognized as a valid taxon by theWorld Register of Marine Species (WoRMS, 2012) follow-ing Sheppard (1998b). However, in the CITES list of coralspecies (CITES, 2011), which is used for the regulationof international commercial trade of endangered species,Craterastrea is considered a synonym of Leptoseris(UNEP-WCMC, 2012), thus accepting Veron’s (1993,2000) decision. Along the same lines, there is simply ‘no

Figs 1–2. Geographic distribution of Craterastrea levis: 1, speciesrecords in the Indian Ocean; 2, sampling localities of C. levis atMayotte Island. Star indicates the position of the type locality,circles of the sampling locality of museum specimens, squares ofspecimens collected in Mayotte during the Tara Oceans expedi-tion.

entries found’ when searching Craterastrea in the IUCNRed List of threatened species (IUCN, 2012).

In the present study, we examined the status of thegenus Craterastrea and its significance for formalizing sec-tions of the molecular family tree of Scleractinia. After re-examination of the Craterastrea levis type material, a surveywas conducted in the Scleractinia collections of some nat-ural history museums with major coral collections search-ing for specimens identified as Leptoseris but showingCraterastrea morphology. Subsequently, C. levis was sam-pled for genetic and morphologic analyses during the TaraOceans scientific expedition to Mayotte (Fig. 2). Hence, weaddressed for this first time the phylogenetic relationshipsbetween Craterastrea levis and Leptoseris foliosa and withthe other genera in the Siderastreidae by using a mitochon-drial (COI) and a nuclear (rDNA) marker, and macromor-phological, micromorphological, and microstructural data.A new family was established to accommodate the generapreviously ascribed to the Siderastreidae that belong to theRobust clade.

Materials and methodsMuseum collections and other examinedspecimensType material and other specimens (including thin sections)examined are deposited in the institutes listed hereafter.

Abbreviations:BMNH The Natural History Museum (formerly

British Museum of Natural History), London, UKIRD Institut de Recherche pour le Developpement,

Noumea, New CaledoniaMNHN Museum National d’Histoire Naturelle, Paris,

France

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Systematics of Craterastrea and description of the Coscinaraeidae Fam. nov. 419

MTQ Museum of Tropical Queensland, Townsville,Australia

RMNH Naturalis Biodiversity Center (formerly Ri-jksmuseum van Natuurlijke Historie, Leiden), Leiden, theNetherlands

TWCMS Tyne and Wear Museums (Natural Sciences)Chagos (Indian Ocean) Coral Collection, Newcastle uponTyne, UK

UNIMIB Universita di Milano-Bicocca, Milan, ItalyUSNM United States National Museum of Natural

History, Washington, DC, USAZMUC Zoological Museum, University of Copen-

hagen, Copenhagen, DenmarkZPAL Institute of Paleobiology, Polish Academy of

Sciences, Poland

Type specimens of Craterastrea levis, Leptoseris foliosa,Coscinaraea monile and Horastrea indica were examined.The holotype of Anomastraea irregularis could not be lo-cated, but other specimens from South Africa and Yemenwere studied instead. Furthermore, original descriptionsand illustrations of these taxa were used.

SamplingCraterastrea levis was sampled in Mayotte in May 2010during the third leg of the Reef Biodiversity project of theTara Oceans scientific expedition (Karsenti et al., 2011)(Fig. 2). Leptoseris foliosa was collected in New Caledoniaduring the first author’s stay at the Institut de Recherche andDeveloppement in Noumea (IRD) in 2011. Digital imagesof living corals in the field were taken with a Canon G9 inan Ikelite underwater housing system.

Coral specimens were collected, tagged and from eachselected specimen a fragment of c. 1 cm2 was broken offand preserved in absolute ethanol for molecular analysis.The remaining corallum was placed for 48 hours in sodiumhypochlorite to remove all soft parts, rinsed in fresh wa-ter and dried for microscopic observation. Images of thecleaned skeletons were taken with a Canon G9 digitalcamera.

Molecular analysesExtraction of coral DNA was performed using a QiagenDNeasy R© Blood & Tissue kit (Qiagen Inc., Valencia, CA,USA). DNA concentration of extracts was quantified usinga Nanodrop 1000 spectrophotometer (Thermo Scientific,Wilmington, DE, USA).

The cytochrome c oxidase subunit I gene (COI) and aportion of rDNA (a fraction of ITS2 and 5.8S) were am-plified and sequenced to infer phylogenetic relationships ofthe genus Craterastrea at family and species level, respec-tively. A COI fragment of about 650 bp was amplified us-ing coral-specific COI primers MCOIF and the protocol by

Fukami et al. (2004). Amplification of an rDNA portion ofabout 700 bp was performed using the coral specific primerA18S (Takabayashi et al., 1998) and the universal primerITS4 (White et al., 1990) following the protocol by Benzoniet al. (2011). PCR products were purified and sequencedby Macrogen Inc. (Seoul, South Korea), using the sameprimers that had been used for the PCR reaction. The newlyobtained mitochondrial and nuclear sequences of Crateras-trea levis and Leptoseris foliosa were aligned with ho-mologous sequences of the family Siderastreidae obtainedfrom previous works (Benzoni et al., 2007, 2010; Stefaniet al., 2007) and with sequences of the families Agarici-idae and Fungiidae published by Fukami et al. (2008) andGittenberger et al. (2011). Tubastraea aurea (Complexclade) was selected as a suitable outgroup given its higherdivergence from the examined taxa (Fukami et al., 2008).

Chromatograms were viewed, edited and assembled us-ing CodonCode Aligner 3.7.0 (CodonCode Corporation,Dedham, MA, USA). Sequences were aligned with the de-fault parameters of BioEdit Sequence Alignment Editor7.0.9.1 (Hall, 1999). Indels, invariable and parsimony in-formative sites were detected with DnaSP 5.10.01 (Librado& Rozas, 2009). Indels were treated as a fifth character inphylogenetic analyses.

Analyses for phylogenetic inference were conducted us-ing three methods: maximum parsimony (MP), Bayesianinference (BI) and maximum likelihood (ML). To examinewhether the sequences from the two loci should be com-bined in a single analysis, a partition-homogeneity test wasrun in PAUP∗ 4.0b10 (Swofford, 2003), and significancewas estimated by 1000 repartitions. This test, describedas the incongruence-length divergence test by Farris et al.(1995), indicated no conflicting phylogenetic signals be-tween the datasets (P = 0.95). Therefore, COI and rDNAwere linked and datasets from both molecular markers wereconcatenated into a single data matrix.

Maximum parsimony analysis was performed withPAUP∗ 4.0b10, with heuristic searches using stepwise ad-dition and performing tree-bisection-reconnection (TBR)branch swapping. Consistence in the nodes was assessed by500 bootstrap replicates with random addition of taxa. Thesoftware MrModeltest2.3 (Nylander, 2004) in conjunctionwith PAUP∗ 4.0b10 were used to select nucleotide substi-tution models. The best model estimated by the AkaikeInformation Criterion (AIC) was General Time Reversiblerate matrix with a proportion of sites being invariant and theremainder following a gamma distribution (the GTR+I+�

model). Bayesian inference analyses were conducted us-ing MrBayes 3.1.2 (Huelsenbeck & Ronquist, 2001;Ronquist & Huelsenbeck, 2003). Two independent runsfor four Markov chains were conducted for 2.7 milliongenerations, and the tree was sampled every 10 gener-ations. Based on checking the parameter estimates andconvergence using Tracer 1.5 (Drummond & Rambaut,2007), the first 67 501 trees were discarded as burn-in. A

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Fig. 3. Bayesian tree of the combined rDNA and COI datasets. Posterior Bayesian probabilities (> 70%), MP and ML bootstrap values(> 50%) are shown at nodes. Dashes (-) indicate nodes that are statistically unsupported.

maximum likelihood (ML) tree was calculated with PhyML3.0 (Guindon & Gascuel, 2003) using the default parame-ters and the robustness of the phylogeny were tested by 500bootstrap replications.

Morphological analysesBoth macro and micromorphological characters (sensuBudd & Stolarski, 2009) of Craterastrea levis and Lep-toseris foliosa were examined using light microscopy (ZeissStemi DV4 stereo-microscope) and SEM, respectively. ForSEM, specimens were mounted using silver glue, sputter-coated with conductive gold film and examined using aVega Tescan Scanning Electron Microscopy at the SEMLaboratory, University of Milano-Bicocca, and a FEI XL20Scanning Electron Microscopy at the Institute of Paleobi-ology, Polish Academy of Sciences. For microstructuralobservations the skeletal material was fixed with aralditeand polished with aluminium oxide (Buehler TOPOL 3 fi-nal polishing suspension with particle size 0.25 μm). For

terminology of skeletal macro-structures in Leptoseris wereferred to Dinesen (1980).

ResultsPhylogenetic analysesCOI and rDNA sequences were obtained for a total of foursamples, two of Craterastrea levis (MY095 and MY305)and two of Leptoseris foliosa (HS2854 and HS2873). Thefinal concatenated alignment consisted of 50 sequences(Table 1) and 783 pb, of which 455 bp for COI, 220 bpfor ITS2 and 108 bp for 5.8S region. 211 nucleotide siteswere variable and 177 parsimony informative, with a to-tal of 304 mutations. BI, MP and ML methods producedsimilar topologies, with no contrasting signals. Bayesiantopology with branch support indicated by Bayesian pos-terior probability scores (PPBI), MP bootstrapping support(BTMP) and ML bootstrapping support (BTML) is reportedin Fig. 3.

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Table 1. Specimens included in the molecular analyses (Fig. 40). For each specimen the collection code (if available), the identificationand the COI and rDNA EMBL sequence codes are given.

CODE Species COI rDNA

HS2854 Leptoseris foliosa HE978506 HE978501HS2873 Leptoseris foliosa HE978507 HE978502UNIMIB-TO MY095 Craterastrea levis HE978510 HE978505UNIMIB-TO MY305 Craterastrea levis HE978509 HE978504- Tubastraea aurea AB441235 AY722796- Siderastrea radians AB441212 AY322604- Siderastrea siderea AB441211 AY322603- Siderastrea stellata AB441213 AB441407- Gardineroseris planulata AB441218 AB441409- Pavona cactus AB441216 AB441408- Oulastrea crispata AB441197 AY722781K124 Anomastraea irregularis AM494869 AM230624K131 Anomastraea irregularis AM494870 AM231716K122 Coscinaraea monile AM494859 AM230599K117 Coscinaraea monile AM494858 AM230598RE516 Horastrea indica AM494864 AM230605RE518 Horastrea indica AM494865 AM230605W600 Coscinaraea columna HE978508 HE978503Y219 Psammocora albopicta FM865871 FM986360I110 Psammocora contigua AM494849 AM230604M48 Psammocora contigua AM494847 AM230602I97 Psammocora haimiana AM494856 FM986368M26 Psammocora haimiana AM494855 AM749206W613 Psammocora digitata FM865876 FM986371HS1376 Psammocora digitata FM865873 FM986361M43 Psammocora nierstraszi FM865878 AM230606M7 Psammocora profundacella AM494853 AM230617M18 Psammocora profundacella FM865879 AM230619MA254 Psammocora nierstraszi AM494850 AM230601- Cycloseris costulata EU149890 EU149820- Cycloseris cyclolites EU202719 EU149821- Ctenactis albitentaculata EU149869 EU149813- Ctenactis echinata EU149899 EU149817- Danafungia scruposa EU149872 EU149827- Fungia fungites EU149892 EU149829- Halomitra pileus EU149875 EU149838- Heliofungia actiniformis EU149885 EU149839- Heliofungia fralinae EU149901 EU149825- Herpolitha limax EU149886 EU149841- Lithophyllon concinna EU149893 EU149832- Lithophyllon undulatum EU149887 EU149844- Lobactis scutaria EU149862 EU149830- Pleuractis granulosa EU149884 EU149835- Pleuractis paumotensis EU149911 EU149850- Podabacia crustacea EU149907 EU149845- Podabacia motuporensis EU149898 EU149846- Polyphyllia talpina EU149915 EU149853- Sandalolitha dentata EU149918 EU149856- Sandalolitha robusta EU149917 EU149857- Zoopilus echinatus EU149916 EU149858

Siderastrea, the type genus of the family Siderastreidae,is highly divergent from the other Siderastreidae (sensuVeron, 2000). All the species of Siderastrea included inthis phylogenetic tree, namely S. radians (Pallas, 1766),S. siderea (Ellis & Solander, 1786), and S. stellata Ver-rill, 1868, form a very well-supported group (PPBI, BTMP,

BTML = 100, Fig. 3), previously indicated as clade IX byFukami et al. (2008). Leptoseris foliosa clusters togetherwith the genera Pavona Lamarck, 1801 and GardineroserisScheer & Pillai, 1974 in the Agariciidae clade.

Within the Robust, clade XI of Fukami et al. (2008)contains a large number of species split into three major

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Figs 4–11. In situ images of Leptoseris foliosa (4, 6, 8, 10) andCraterastrea levis (5, 7, 9, 11) showing growth forms and coloura-tion at different stages of colony development and overall simi-larity between the two taxa: 4, encrusting corallum of specimenIRD HS 2861; 5, one calice corallum of C. levis showing thetypical shape resembling the anthocaulus stage in the Fungiidae(UNIMIB TO–MY098; same specimen shown in Figs 12, 23);6, encrusting corallum of L. foliosa with foliose edges (NewCaledonia, Prony Bay, 20 m); 7, cyathiform colony of C. levis(UNIMIB TO–MY148; same specimen shown in Fig. 13) circularinset shows a corallite; 8, fan-shaped colony of L. foliosa (NewCaledonia, Prony Bay, 15 m) circular inset shows a corallite; 9,fan-shaped colony of C. levis (UNIMIB TO–MY095; same speci-men shown in Figs 14–15); 10, foliose colony of L. foliosa formingtiers of whorls (New Caledonia, Prony Bay, 10 m); 11, large colonyof C. levis showing a corrugated surface due to the presence ofirregular rounded protuberances (Boueni Bay, Mayotte Island).Scale bars represent 1 cm.

family-level lineages, the Siderastreidae (pars), thePsammocoridae Chevalier & Beauvais, 1987, and theFungiidae. Oulastrea crispata (Lamarck, 1816) is a highlydistinctive outgroup for these three groups and shows un-resolved evolutionary relationships. Craterastrea levis isin one of the lineages, and closely related to Coscinaraeamonile (Forskal, 1775), Horastrea indica Pichon, 1971, andAnomastraea irregularis Marenzeller, 1901. The average

Figs 12–15. Different corallum morphology of Craterastrea levisspecimens sampled for this study: 12, UNIMIB TO–MY098 (samespecimen shown in Figs 5, 23); 13, UNIMIB TO–MY148 (samespecimen shown in Fig. 7); 14, top view of specimen UNIMIBTO–MY095 (same specimen shown in Fig. 9); 15, side view ofthe same specimen as 14. Scale bars represent 1 cm.

distance of Craterastrea levis from Leptoseris foliosa is17.8 ± 1.4%, and from the Agariciidae clade is 18.2 ±1.4%. These values are higher than the genetic distance be-tween Craterastrea levis and other taxa in the same clade,i.e. 2.3 ± 0.4%. The sister group of this clade includingall the Siderastreidae except Siderastrea is the Psammo-coridae clade, comprising all the species of Psammocoraincluded in this study and Coscinaraea columna (Dana,1846), as already shown by Benzoni et al. (2010). The thirdmajor group, the Fungiidae clade, includes all genera ofFungiidae in agreement with Gittenberger et al. (2011) andBenzoni et al. (2012). As mentioned in the introduction,the remaining genus in the Siderastreidae, Siderastrea, is inthe Complex clade.

Morphological analysesA detailed description of morphological characters betweenLeptoseris foliosa and Craterastrea levis and their compar-ison is presented hereafter.

Leptoseris foliosa Dinesen, 1980(Figs 4, 6, 8, 10, 16, 18, 20, 22, 24, 25, 28–32)

Leptoseris foliosa Dinesen, 1980: Plate 14 Figs 1–3; Veron,2000.Leptoseris tenuis Yabe & Sugiyama, 1941: Pl. 62,Figs 4–4c, 5–5a, Pl. 64, Fig. 1; Veron & Pichon, 1980:Figs 115–20, 742.TYPE MATERIAL: The holotype (BM 1979.4.6.1) and twoparatypes are deposited at the BMNH, 6 paratypes at theQueensland Museum, 1 at the USNM.TYPE LOCALITY: Lizard Island, Australia.

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Figs 16–23. Comparison of skeleton morphology of Leptoserisfoliosa (16, 18, 20, 22) and Craterastrea levis (17, 19, 21, 23):16, corallite arrangement in L. foliosa IRD HS 2903; 17, corallitearrangement in C. levis USNM 82530; 18, protocorallite (largerin the centre) and other corallites in L. foliosa IRD HS 2855; 19,protocorallite (larger in the centre) and other corallites in C. levisRMNH 19147; 20, corallites of L. foliosa IRD HS 346; 21, coral-lites of C. levis UNIMIB TO–MY096; 22, detail of protocorallitein L. foliosa (same specimen as Fig. 18); 23, detail of protocoral-lite in C. levis UNIMIB TO–MY098 (same specimen as Figs 5,12). Dashed circles in 18 and 20 indicate the corallite outline.Scale bars represent 5 mm.

OTHER EXAMINED MATERIAL: MTQ G 43565 Aus-tralia; IRD HS 283 Prony Bay, Anse Sebert, 20 m(28/8/1986) coll. P. Laboute; IRD HS 346 Prony Bay,Grande Rade Est, 10 m (10/2/1987) coll. G. Bargibant;IRD HS 351 Prony Bay, Ilot Casy, 15 m (9/2/1987) coll.J.L. Menou; IRD HS 352 Prony Bay, Ilot Casy, 12 m(9/2/1987) coll. J.L. Menou; IRD HS 872 Prony Bay,Ilot Casy (9/2/1987); IRD HS 2682 IRD ST0033, 16 m(9/6/2009) coll. G. Lasne; IRD HS 2680 IRD ST0033, 16 m(9/6/2009) coll. G. Lasne; IRD HS 2854 Prony Bay, IRDST 117, 20 m (23/2/2011) coll. F. Benzoni, E. Folcher &A. Renaud; IRD HS 2855 Prony Bay, IRD ST 117, 15 m(23/2/2011) coll. F. Benzoni, E. Folcher & A. Renaud; IRD

Figs 24–27. Comparison of patterns of septal structures in Lep-toseris foliosa (24, 25) and Craterastrea levis (26, 27): 24, Xshaped crossing of septocostae in L. foliosa (IRD HS 346); 25,detail of 24 showing rounded septa granulations in L. foliosa; 26,X shaped crossing of interstomatous septa in C. levis (UNIMIBTO–MY095); 27, detail of 26 showing septal paddles perpendic-ular to the septum direction with granules finely ornamented bymultiple spikes. Scale bars represent: Figs 24, 26, 5 mm; Figs 25,27, 200 μm.

Figs 28–32. Micromorphology and microstructure of Leptoserisfoliosa: 28, top view of part of a corallite and septocostae (rectan-gle indicates the part shown in 29); 29, detail of 28 showing clus-ters of Centres of Rapid Accretion aligned on lateral septal facesto form more or less continuous lists (menianae) (arrows) parallelto the septum direction (dashed line); 30, longitudinal view ofsepta, arrows indicate menianae running along septal side (circleindicates the part shown in 31); 31, enlargement of 30 showingclose up of menianae; 32, longitudinal etched section of septumshowing the central zone of Rapid Accretion Deposits form reg-ular branches (dashed lines) towards the menianae. Occurrenceof menianae/aligned granulations parallel to the septum is typi-cal of agariciids which form well-defined clade within complexcorals. All SEM images: 32, broken and etched section (ZPALR–SCL–709) of IRD HS 2854. Scale bars represent: Fig. 28,500 μm; Fig. 29, 200 μm; Fig. 30, 500 μm; Fig. 31, 100 μm;Fig. 32, 50 μm.

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Figs 33–40. Micromorphology and microstructure of Crateras-trea levis: 33, longitudinal section of a corallum showing highlyperforated structure; 34, top view of the colony surface showingtwo calices; 35, paddle-like structures (arrows) perpendicular toseptum direction (dashed line); 36, detail of a paddle-shaped struc-tures formed by Clusters of Centres of Rapid Accretion (arrows),this feature is typical of many representatives of robust coral clade;37, transverse thin section showing septal paddles (arrows); 38,transverse, etched sections of septa showing Rapid Accretion De-posits forming small depressions (dots); 39, longitudinal thin sec-tion; 40, detail of 39 showing how septal paddle-shaped structuresare not continuous along the septum but are formed in regularmanner: in longitudinal broken (33) and thin (39, 40) sectionsthey form small platforms (arrows). SEM (33–36, 38) and opticalmicroscope (37, 39–40) images; oblique (33), distal/transverse(34–38) and longitudinal (39, 40) views. SPECIMENS: 33, 37,39, 40: R-SCL081; 34–36, 38: R–SCL–711. Scale bars represent:Fig. 33, 1 mm; Fig. 34, 2 mm; Fig. 35, 200 μm; Fig. 36, 100 μm;Fig. 37, 500 μm; Fig. 38, 100 μm; Fig. 39, 500 μm; Fig. 40,100 μm.

HS 2861 Prony Bay, IRD ST 117, 15 m (23/2/2011) coll.F. Benzoni, E. Folcher & A. Renaud; IRD HS 2873 PronyBay, IRD ST 394, Prony Bay, Carenage, 5–15 m (23/2/2011)coll. F. Benzoni, E. Folcher & A. Renaud; IRD HS 2877Prony Bay, ST 394, Carenage, 5–15 m (23/2/2011) coll.F. Benzoni, E. Folcher & A. Renaud; IRD HS 2973 PronyBay, ST 117, 32 m (22/3/2011) coll. F. Benzoni, E. Folcher& A. Renaud.

DescriptionCorallum encrusting (Fig. 4) or with free margins formingfoliose (Fig. 6) or fan-shaped (Fig. 8) colonies, sometimes

forming whorls (Fig. 10). Larger colonies can be attachedat the centre or at one side of the corallum. Colony surfacesmooth (Figs 4, 6, 16) or ridged (Figs 8, 10), with corallitesfound at the bottom of the valleys separating the ridges. Noproximal cushions are formed although nodules unrelatedto the calices can form. Corallites are arranged in concentricseries around the protocorallite which is larger in diame-ter (Figs 18, 22). Calice outline circular in the inner partof the corallum (Fig. 18, dashed circle) and progressivelymore oval towards the corallum margin, with longer diam-eter perpendicular to the corallum radius (Fig. 20, dashedcircle). The fossa is round or elliptical (Fig. 20, 22). Col-umella present formed by one solid boss in all the corallites(Fig. 20) except the protocorallite which can have 1–4 pro-cesses (Fig. 22). Septa unequal (Fig. 20). Septocostae equal,compact and straight (Fig. 22), sometimes fusing or divid-ing and forming X-shaped crossings (Fig. 24), imperforate(Fig. 30), margin ornamented with granulations (Fig. 25,28, 29). Granulations on septal sides form elongated ag-gregations or merge into menianae parallel to the growingseptal margin (Figs 29, 30, 31). Granulations (menianae)are produced by regular divergence of the mid-septal RapidAccretion Deposits zone (Fig. 32).

In vivo colour ranges from greenish beige to light brownwith paler colony margins (Figs 4, 6, 8, 10).

Craterastrea levis Head, 1983(Figs 5, 7, 9, 11, 12–15, 17, 19, 21, 23, 26, 27, 33–40)

Craterastrea levis Head, 1983: Figs 6–9, 11–14.Craterestrea levis Huang, 2012.Leptoseris hawaiiensis Matthai, 1948, Pl. 4, Figs 9, 10; Ma,1959, Plates 26, 27.Leptoseris foliosa Veron, 1993; Veron, 2000.Coscinaraeid new gen, new sp. Sheppard, 1980.TYPE MATERIAL: The holotype (BM 1981.4.1.4) and twoparatypes (BM 1981.4.1.5; BM 1981.4.1.6) are depositedat the BMNH and were examined.TYPE LOCALITY: Towartit, Port Sudan, Sudan.EXAMINED MATERIAL: BMNH 1981.4.1.4. Holotype,Towartit, Port Sudan, Sudan, 40 m (1973) coll. S.Head; BMNH 1981.4.1.5 Paratype West Harvey reef,Towartit, Port Sudan, Sudan, 37 m (1973) coll. S. Head;BMNH 1981.4.1.6 Paratype West Harvey reef, Towartit,Port Sudan, Sudan, 37 m (1973) coll. S. Head; BMNH1950.1.11.330 Ghardaqa, Egypt, 46 m (30/7/1933) coll. C.Crossland; unregistered (collection code: TWCMS J1834)(1975) Chagos, exp. JS01 (identified as Coscinaraea);USNM 82529 Chagos Archipelago, more than 50 m(28/11/1979) coll. C. Sheppard.NEW RECORDS: USNM 82530 Eilat, Israel, 65–70 m(1972) coll. J. Lang; RMNH 19147 Seychelles, 45–55 m,dredged (identified as Leptoseris hawaiiensis); RMNH34540 (partim) Madagascar (identified as Leptoseris fo-liosa); MTQ G 61808 Nosy Be, Madagascar (January2002) coll. JEN Veron (identified as Leptoseris foliosa);

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MTQ G 61807 Nosy Be, Madagascar (January 2002)coll. JEN Veron (identified as Leptoseris foliosa); MNHN20398 Tulear, Madagascar, 30 m (14/9/1963) coll. M.Pichon (identified as Leptoseris cf incrustans); MNHN20399 Tulear, Madagascar, 26 m (8/9/1965) coll. M. Pi-chon, (identified as Leptoseris cf incrustans); MNHN20400 Tulear, Madagascar, 28 m (21/9/1965) coll. M.Pichon (identified as Leptoseris cf incrustans); MNHN20401 North Grande Circle, Tulear, Madagascar, 25–35 m(8/10/1965) coll. M. Pichon (identified as Leptoseris cfincrustans); MNHN 20402 Tulear, Madagascar, coll. M.Pichon (identified as Leptoseris cf incrustans); MNHN20403 Tulear, Madagascar, coll. M. Pichon (identified asLeptoseris cf incrustans); MNHN unregistered (collectioncode MAY 12–122), Double barriere face N’gouja, May-otte Island, Mission BARMAY (24/4/2005) coll. G. Faure(identified as Leptoseris cf incrustans); MNHN unregis-tered Banc du Boa (collection code MAY 12–122), May-otte Island Mission BARMAY (18/4/2005) coll. G. Faure(identified as Leptoseris cf incrustans); MNHN unregis-tered (collection code MAY 12–122) Bai Soud, Mamoudzu,Mayotte Island (31/5/1983) coll. G. Faure (identified as Lep-toseris cf incrustans); UNIMIB TO–MY013 Mayotte Is-land, Site TO–MY 1 I. Blanche (12◦S 42,981; 45◦E 10,455)20 m (30/5/2010) coll. F. Benzoni; UNIMIB TO–MY014Mayotte Island, Site TO–MY 1 I. Blanche (12◦S 42,981;45◦E 10,455) 15 m (30/5/2010) coll. F. Benzoni; UNIMIBTO–MY025 Mayotte Island, Site TO–MY 2 I. Verte (12◦S43,416; 45◦E 8,856) 25 m (30/5/2010) coll. F. Benzoni;UNIMIB TO–MY094 Mayotte Island, Site TO–MY 11Boueni Bay (12◦S 54,698; 45◦E 7,871) 15 m (4/6/2010)coll. F. Benzoni; UNIMIB TO–MY095 Mayotte Island,Site TO–MY 11 Boueni Bay (12◦S 54,698; 45◦E 7,871)15 m (4/6/2010) coll. F. Benzoni; UNIMIB TO–MY096Mayotte Island, Site TO–MY 11 Boueni Bay (12◦S 54,698;45◦E 7,871) 15 m (4/6/2010) coll. F. Benzoni; UNIMIBTO–MY097 Mayotte Island, Site TO–MY 11 Boueni Bay(12◦S 54,698; 45◦E 7,871) 15 m (04/06/2010) coll. F. Ben-zoni; UNIMIB TO–MY098 Mayotte Island, Site TO–MY11 Boueni Bay (12◦S 54,698; 45◦E 7,871) 20 m (4/6/2010)coll. F. Benzoni; UNIMIB TO–MY108 Mayotte Island, SiteTO–MY 13 Boueni outer barrier (12◦S 56,376; 45◦E 3,256)(05/06/2010) coll. F. Benzoni; UNIMIB TO–MY120 May-otte Island, Site TO–MY 14 (12◦S 52,534; 45◦E 16,834)(06/06/2010) coll. F. Benzoni; UNIMIB TO–MY148 May-otte Island, Site TO–MY 17 Bouzi (12◦S 48,749; 45◦E14,486) (7/6/2010) coll. F. Benzoni; UNIMIB TO–MY149Mayotte Island, Site TO–MY 17 Bouzi (12◦S 48,749; 45◦E14,486) (7/6/2010) coll. F. Benzoni; UNIMIB TO–MY150Mayotte Island, Site TO–MY 17 Bouzi (12◦S 48,749; 45◦E14,486) (7/6/2010) coll. F. Benzoni; UNIMIB TO–MY151Mayotte Island, Site TO–MY 17 Bouzi (12◦S 48,749; 45◦E14,486) (7/6/2010) coll. F. Benzoni; UNIMIB TO–MY305Mayotte Island, Site TO–MY 31 Boueni Bay 2 (12◦S54,698; 45◦E 7,871) (16/6/2010) coll. F. Benzoni.

REMARKS: The genus is monotypic.

DescriptionThe corallum is thin, unifacial, crateriform (Figs 5, 7, 9, 11)and attached to the substrate by a peduncle generally foundat the centre of the undersurface (Fig. 15). In small colonieswith one calice the corallum (Figs 5, 12) resembles the an-thocaulus stage in free-living Fungiidae (Hoeksema, 1989:Fig. 43) but in the latter the umbrella is concave and notconvex. In some colonies only part of the lamina growsand the corallum appears secondarily foliose, attached pe-ripherally (Figs 9, 14). Colony surface is generally even(Figs 5, 9, 12, 14, 17). In some colonies irregular roundedprotuberances analogous to proximal cushions in the genusLeptoseris can occur (Figs 7, 11, 13). These can eitherdevelop in correspondence with calices or far from them.The first calice is generally larger than the others, whichare approximately 4 mm in diameter (Figs 19, 23). Thecolonial stage is reached through intratentacular budding,initially circumoral and followed by irregular marginal di-vision (Figs 14, 19). Calices are spaced far apart over thecolony surface (Fig. 13) and tend to be even sparser to-wards the margin of the corallum (Figs 14, 17). Althoughin some specimens a tendency to form concentric rows ofcorallites can be observed (Fig. 14), in general this is sel-dom observed. The calice margin is hardly detectable dueto the continuity between septa between calices and theireven thickness (Figs 19, 21, 23, 29).

The columella is formed by multiple processes in allthe corallites (Figs 21, 23) although they are more nu-merous, though not larger, in the protocorallite (Fig. 23).Septa and septocostae equal (Figs 21–23), perforated andstraight, sometimes fusing or dividing and forming X-shaped crossings (Fig. 26). These septocostae are highlyperforated (Figs 33, 37, 39, 40) and ornamented with typ-ical septal paddles perpendicular to the septum direction(Figs 26, 27, 33, 35, 36). Each paddle consists of numerouscentres of Rapid Accretion which radiate in all directions(blue arrows in Fig. 36), therefore in etched sections RapidAccretion Deposits occur in many places (Fig. 38). Thegranules of the paddles are finely ornamented by multiplespikes. Septal paddles are not continuous along the sep-tum but appear in regular manner forming small platforms(Figs 26, 37, 38). Although the platforms resemble shortmenianae or pennular structures of some Mesozoic corals(Morycowa & Roniewicz, 1995) they are formed in addi-tion to predominant paddles which are perpendicular to theseptal plane. Septa and septocostae are regularly connectedlaterally by synapticulae which form a fine and regularthree-dimensional mesh with the trabeculae forming theseptocostae (Fig. 33).

In vivo colour ranges from greenish beige to light brownwith paler colony margins (Figs 5, 7, 9, 11).

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Although the growth forms of C. levis and L. foliosaare to a large extent overlapping, some differences weredetected. Both species are colonial forming encrusting tofoliose coralla. However, in L. foliosa the corallum is gener-ally encrusting at the base and foliose in the peripheral partwhile in C. levis it forms crater-like colonies (Figs 12–15)(Head, 1983) starting almost as a fungiid anthocaulus stage(Hoeksema, 1989: Fig. 43). This was observed for the firsttime in Mayotte where a complete series of specimens wascollected including single-polyp coralla (Figs 5, 12). Nosuch one corallite stage was observed in L. foliosa, althoughall the presumably young colonies (few calices and ratherregular in outline) we observed were encrusting. Both C.levis and L. foliosa are characterized by small calices, ex-cept the generally central protocorallite, which is larger(Figs 18, 19, 22, 23), poorly defined theca, and a thamnas-terioid arrangement of the septa which can be very long(up to 10 times the calice diameter or more, especially inCraterastrea). Although calices are on average of slightlydifferent size in the two species, larger in C. levis than inL. foliosa, their diameter ranges overlap. In L. foliosa theytend to be more evenly sized throughout the colony, whilein C. levis their size can be more variable (Fig. 13). Thesedifferences are, however, difficult to detect to the nakedeye because of the overall small dimensions of the calicalstructures and the poorly visible calice wall. In both speciescalices can be very far apart although in C. levis this ismore often observed and their distances can be remark-ably longer. Furthermore, while in L. foliosa they tend tobe arranged in concentric rows and to attain a more ovaloutline further from the colony centre (Figs 18, 20), thisis seldom observed in C. levis coralla where the generalcalice arrangement pattern is much less regular from thecentre of the colony towards its periphery and calices aremore evenly circular in outline. Nevertheless, the arrange-ment of the long septa is strikingly similar in both species(Figs 24, 26) and contributes to the similarity of the overallmacromorphology between the two species. It is proposedthat while for L. foliosa the term septocostae as definedby Dinesen (1980) is conserved, the term interstomatoussepta is preferred for C. levis following the definition, andontological explanation, given by Hoeksema (1989).

TaxonomyOrder Scleractinia Bourne, 1900

Family Coscinaraeidae Fam. nov.

TYPE GENUS: Coscinaraea Milne Edwards and Haime,1848.ETYMOLOGY: Named after the designated type genusCoscinaraea.DIAGNOSIS: Corallum colonial, attached. Corallites ceri-oid or plocoid, forming monocentric to polycentric series,wall synapticulothecal or septothecal. Septa completely or

partially perforated, joined by one or more rows of synap-ticulae, fusing towards the fossa. Septal margin ornamen-tation composed of paddle-shaped spiked ridges orientedtransversally to the septal plane. Septa sides granular. Col-umella present, papillary, formed by multiple processes (ex-tremities of trabeculae) developing from the inner marginof the septa towards the fossa.

DescriptionThe family is comprised of colonial taxa characterizedby different macro-morphology, including encrusting, mas-sive, cup-shaped or submassive colonies. The shape, sizeand arrangement of the corallites are very different betweengenera (Benzoni et al., 2007). Corallite arrangement can beplocoid or cerioid. Corallite outline is polygonal, irregularor circular, and monocentric to polycentric. Corallite wallis synapticulathecal in all genera except Horastrea whichhas a septothecal wall (Benzoni et al., 2007). Althoughpetaloid septa (sensu Benzoni et al., 2010) can occasion-ally form at the merger of three or more calices in Cosci-naraea, and can sometimes be observed also in specimensof Horastrea, they do not form in Anomastraea or Crat-erastrea. Rows of enclosed petaloid septa, typically foundin the Psammocoridae (Benzoni et al., 2007, 2010) neverform in the Coscinaraeidae. In all taxa septa are perforated,characterized by granular ornamentation on the lateralsides, and ornamented by paddle-shaped spiked ridges ori-ented transversally to the septal plane on the upper margin(Benzoni et al., 2007). Septa are typically joined by synap-ticulae and fuse within the calice towards the fossa. In allthe coscinaraeids a papillary columella is formed by the tra-becular processes extending from the inner margin of thesepta and fusing with similar processes from other septa toform a perforated central structure.

Genus Coscinaraea Milne Edwards & Haime, 1848(Figs 41–42)

TYPE SPECIES: Madrepora monile Forskal, 1775: 133,Holotype examined (Fig. 41).REVISED DIAGNOSIS: Corallum colonial, attached, en-crusting, massive or submassive. Corallites cerioid, formingmonocentric to polycentric series (Fig. 42), wall synapticu-lothecal, perforate (Benzoni et al., 2007). Septa perforate,joined by synapticulae, fusing towards the fossa (insets inFigs 41–42). Septal margin ornamentation composed ofpaddle-shaped granules perpendicular to the septal plane(Benzoni et al., 2007). Septa sides granular. Columelladeveloped, formed by multiple processes. Costae on thecolony wall unequal to sub-equal.DISTRIBUTION: Red Sea, Indian Ocean and western Pa-cific Ocean.REMARKS: Despite the recent taxonomic revision of C.wellsi, now belonging to the fungiid genus Cycloseris

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Figs 41–46. Macromorphological features of the genera ascribedto the Coscinaraeidae fam. nov. other than Craterastrea: 41, Holo-type of Coscinaraea monile (a sub-fossil hence the darker colour),inset shows detail of a corallite; 42, specimen UNIMIB K122 (Fig.3; Table 1) from Kuwait, inset shows detail of a corallite; 43, Ho-rastrea indica, side view of specimen UNIMIB–TO MY228 fromMayotte; 44, top view of specimen UNIMIB–TO MY229 fromMayotte, inset shows detail of a corallite; 45, Anomastraea irreg-ularis specimen BMNH 1961.7.17.69 from South Africa; 46, oneof the specimens included in the molecular analyses in this studyUNIMIB K131 (Fig. 3; Table 1) from Kuwait, inset shows detailof a corallite. Scale bars represent 1 cm.

(Benzoni et al., 2007, 2012), the genus is most likely stillpolyphyletic (see Fig. 40 and the Discussion).

Genus Horastrea Pichon, 1971(Figs 43–44)

TYPE SPECIES: Horastrea indica Pichon, 1971: 165–171,Figs 1–6, Holotype examined.REVISED DIAGNOSIS: Corallum colonial, attached, mas-sive (Fig. 43). Corallites plocoid, circular or irregular inoutline (Fig. 43), forming monocentric to polycentric se-ries (Pichon, 1971), wall septothecal (Benzoni et al., 2007).Septa perforated along the inner margin, otherwise mostlycompact, joined by 2–3 rows of synapticulae, fusing to-wards the fossa (inset in Fig. 44). Septa ornamentation com-posed of paddle-shaped granules (Benzoni et al., 2007).Columella developed, formed by multiple processes per-pendicular to the septal plane. Costae continuous betweenadjacent calices, unequal to sub-equal.

DISTRIBUTION: Western and southern Indian Ocean(Madagascar; Mayotte) (Obura, 2012a).REMARKS: The genus is monotypic.

Genus Anomastraea von Marenzeller, 1901(Figs 45–46)

TYPE SPECIES: Anomastraea irregularis Marenzeller,1901: 124–125, Figs 3, 3a.REVISED DIAGNOSIS: Corallum colonial, attached, en-crusting to massive (Fig. 45). Corallites cerioid, polygonalin outline (Fig. 46), predominantly monocentric, seldombi- or tricentric, wall synapticulothecal, perforate (Benzoniet al., 2007). Septa partly perforate, joined by one row ofsynapticulae, fusing towards the fossa (inset in Fig. 46).Septa ornamentation composed of paddle-shaped granulesperpendicular to the septal plane (Benzoni et al., 2007).Septa sides granular. Columella developed, formed by mul-tiple processes.DISTRIBUTION: Red Sea and Indian Ocean.REMARKS: The genus is monotypic.

Genus Craterastrea Head, 1983

TYPE SPECIES. Craterastrea levis Head, 1983: 428–432,Figs 8–14, Holotype examined.REVISED DIAGNOSIS: Corallum colonial, attached,forming cup shaped colonies. Corallites plocoid, few innumber and distant, wall synapticulothecal, perforate. Septaperforate, joined by synapticulae, fusing towards the fossa.Septa ornamentation composed of paddle-shaped granules.Columella developed, formed by multiple processes. Costaeon the colony wall unequal to sub-equal.DISTRIBUTION: Red Sea and Indian Ocean (seeabove).REMARKS: The genus is monotypic.

DiscussionSince the beginning of the so-called molecular revolutionin scleractinian coral taxonomy and systematics (Stolarski& Roniewicz, 2001) the inconsistency of orders, the poly-phyly of families and genera, the existence of cryptic taxa,of hybridization and of new species have been highlighted(Romano & Palumbi, 1996; Fukami et al., 2004, 2008;Combosch et al., 2008; Pinzon & LaJeunesse, 2010; Souter,2010; Kitahara et al., 2010; Benzoni et al., 2011; Huanget al., 2011; Stefani et al., 2011; Lin et al., 2012; Pichonet al., 2012). New micromorphological and microstruc-tural characters proved to be more phylogenetically infor-mative than those traditionally used in hard coral taxon-omy (Benzoni et al., 2007; Budd & Stolarski, 2009, 2011;Janiszewska et al., 2011; Stolarski et al., 2011). In this pa-per, the combined molecular and morphological approachwas used for the first time to re-discover and resurrect a

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Fig. 47. Schematic timeline of the classification of the genera in the Coscinaraeidae Fam. nov., since the description of the familySiderastreidae by Vaughan & Wells (1943) and in the principal studies including them in molecular analyses until the present study. Thegenera related to the Coscinaraeidae and their changes in classification or in the same molecularly defined clade have been included. Thegenera included in the Coscinaraeidae in the present study are in bold. For each study we indicated on which kind of data the classificationwas done (macromorphological, micromorphological and microstructural, molecular). Synonymies and placements at subgenus level areindicated.

genus erroneously synonymized with one distantly relatedto it.

The first step allowing the re-examination of Crateras-trea and its resurrection as well as the description of thefamily Coscinaraeidae was the study of collections in nat-ural history museums.

Recovery of a long-forgotten taxon inhistorical collectionsDue to its distribution in the deeper parts of the reefsor in turbid waters, and likely because of the synonymywith the strikingly similar Leptoseris foliosa (Veron, 1993),Craterastrea levis has remained largely unstudied and un-searched for. However, as shown in this study, the specieswas occasionally collected in different parts of the In-dian Ocean and deposited in various museums beforeits formal description (Head, 1983) and after its syn-onymization. Specimens from the Seychelles, Mayotte Is-land and Madagascar were invariably identified as oneor another species of Leptoseris (L. foliosa, L. hawaiien-sis, L. cf incrustans) with the notable exception of onespecimen from Chagos identified as Coscinaraea sp. andone from Israel actually identified as C. levis by J.W.Wells (http://collections.nmnh.si.edu/search/iz/). Interest-ingly, this specimen was collected in 1972, 15 years be-

fore Edwards & Head (1987) reported that Craterastreadoes ‘not penetrate into the Gulf of Aqaba’. Although C.levis has never been recorded in the Maldives, the latestchecklists (Pichon & Benzoni, 2007; Bigot & Amir, 2012)only included dives to a maximum depth of 30 m and thetaxon might have been overlooked, hence its presence inthe archipelago at greater depths cannot be excluded. There-discovery and study of museum specimens not only al-lowed extending the known geographic distribution of C.levis but also directed us, through the notes of their collec-tors, towards more targeted sampling in Mayotte (Fig. 2).Recently, Hoeksema et al. (2011) have highlighted howhistorical collections can have unforeseen importance asbaselines to determine biotic change of coral reefs. How-ever, it should also be remembered that collections still havemuch information to provide also as repositories of knownand unknown biological diversity (see also Benzoni et al.,2010).

The in situ, skeleton and molecular results obtained inthis study allowed a thorough comparison of C. levis andL. foliosa and led to the formal resurrection of the genusCraterastrea and to the description of a new family to ac-commodate this genus and its close allies among the Robustcorals rather than in the Siderastreidae among the Complexones. The different aspects of these findings and taxonomicdecisions are discussed hereafter.

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http://collections.nmnh.si.edu/search/iz/


Craterastrea levis and Leptoseris foliosa:morphological convergence of twodistantly related taxaThe phylogenetic reconstruction of the relationship betweenthe two taxa based on two different markers (rDNA andCOI) revealed once and for all that C. levis and L. foliosa aretwo valid evolutionary and taxonomic entities. Leptoserisfoliosa is monophyletic with the agariciid taxa examined inthis study in the Complex clade. Craterastrea is closely re-lated to Coscinaraea, Horastrea and Anomastraea, and allthese taxa are related to the Psammocoridae and the Fungi-idae in the Robust clade. This being said, the morphologi-cal similarity between these taxa at first glance is strikingand it has certainly played a major role in the taxonomicconfusion between the two. However, a closer inspectionof a representative number of specimens in this study hasalso revealed consistent differences, which tend to becomemore obvious going from the observation of the macro-and micromorphology to the microstructure. In fact, thetwo species are markedly different in microscopic skeletalfeatures: the structure of the columella (made of one processin L. foliosa and multiple papillary processes in C. levis),the thickness of septa, the granulation of the paddles whichare observed on the septal margin, the arrangement of theseptal side granulation, and the septa and septocostae perfo-ration. It is at the micromorphological and microstructurallevel that the two species are most differentiated. The moststriking microstructural difference between these speciesis a pattern of distribution of centres of rapid accretion onseptal faces. In Leptoseris foliosa clusters of these centresform elongated aggregations which produce more or lesscontinuous lists (menianae) parallel to the septum. This fea-ture is typical of all agariciids which form a well-definedclade within the Complex clade corals (see also Kitaharaet al., 2010, in press). Conversely, in Craterastrea levis cen-tres of rapid accretion form aggregations perpendicular tothe septum, their further growth resulting in the formationof paddle-like structures. This feature is common amongrepresentatives of the Robust clade (Cuif et al., 2003; Budd& Stolarski, 2011).

Ecology of Craterastrea levisDespite the evolutionary divergence of Craterastrea fromLeptoseris, the two genera tend to inhabit similar poorly litenvironments (deep or turbid). Both species can be typi-cally found in relatively shallow waters in protected lagoonembayments characterized by a high sedimentation of ter-rigenous input (for Leptoseris foliosa see Dinesen, 1980).Craterastrea levis is also found in clear waters but it occursmuch deeper, such as in the Chagos archipelago where itcan be abundant below 70 m (Sheppard & Sheppard, 1991).No data are available on the distribution of L. foliosa in theouter barrier, however, Dinesen (1980) reports a specimen

collected in more exposed conditions from a cave at 20 m.Besides the agariciid fashion of the corallum growth form,in vivo observations of C. levis in this study confirmed whatwas already observed by Sheppard & Sheppard (1991) onthis species’ extreme reduction of the proportion of colonysurface ‘occupied by the plankton trapping polyps and amaximization of the proportion given the photosyntheticcoenosarc’. Indeed, it could be that the peculiar morphologyof the polyps and their adaptations to nutrition needs in deepwaters in some Leptoseris species (Fricke & Schuhmacher,1983; Fricke et al., 1987; Schlichter, 1991; Schlichter &Fricke, 1991) is similar in Craterastrea.

Solving an old riddle and setting thetaxonomic record straightFigure 47 summarizes the taxonomic riddle representedby the Siderastreidae from the formal family descriptionby Vaughan & Wells (1943) until this study. The authorsbased their taxonomic decisions on skeleton morphology,included the following genera in the Siderastreidae: Cosci-naraea, Anomastraea (with subgenus Pseudosiderastrea),Maeandroseris ( = Psammocora see Benzoni et al., 2010),and the type genus Siderastrea. Although Wells (1956)overall largely agreed with such classification, he moved thegenus Oulastrea from the Agariciidae to the Faviidae. Moreimportant taxonomic changes were operated by Chevalier& Beauvais (1987) who considered Pseudosiderastrea ajunior synonym of Siderastrea and accepted the inclu-sion of Horastrea described in the meanwhile by Pichon(1971). They moved Oulastrea into the Siderastreidae, anddescribed the family Psammocoridae including the genusPsammocora and other related genera later synonymizedwith it (Benzoni et al., 2007, 2010). Chevalier & Beauvais(1987) did not include Craterastrea in their treatment. LaterVeron (2000) restored Pseudosiderastrea as a valid genusin the Siderastreidae, moved Psammocora to the Sideras-treidae, Oulastrea back into the Faviidae, and kept Crat-erastrea as a junior synonym of Leptoseris following hisformer decision (Veron, 1993).

In 1996, Romano & Palumbi published a molecular phy-logenetic analysis of 16S rDNA, including Psammocoraand Coscinaraea, and reported for the first time the twomajor clades of the Scleractinia, the Complex and the Ro-bust. Fukami et al. (2008) used mitochondrial trees (COIand CytB) to show that the family Siderastreidae is split be-tween the Complex (Siderastrea in clade IX) and the Robustclade (Psammocora, Coscinaraea in clade XI which alsoincluded Oulastrea). Benzoni et al. (2007) included for thefirst time micromorphological, microstructure and molec-ular data from all taxa included in the Siderastreidae sensuVeron (2000), except Craterastrea. They showed that whileSiderastrea and Pseudosiderastrea are Complex clade taxa,Coscinaraea, Horastrea, Anomastraea and Psammocora

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are all Robust clade taxa. The latter genus has peculiarcharacters which justified its inclusion in the resurrectedfamily Psammocoridae (Benzoni et al., 2007).

In the present study macro- and micromorphology, mi-crostructure and molecular data demonstrated that Crat-erastrea is closely related to Coscinaraea and its alliescurrently ascribed to the Siderastreidae and belonging tothe Robust clade. Moreover, the genus is distantly relatedto Leptoseris and the Agariciidae in the Complex clade.Since the type genus of the family and the type species ofthis genus are found in the Complex clade, while the gen-era Coscinaraea, Horastrea, Anomastraea and Craterastreabelong to the Robust corals, a new family is described toseparate them. Although we did not include Pseudosideras-trea in our analyses, the recent work by Pichon et al. (2012)shows the close relationship of this taxon with Sideras-trea based on the partial mitochondrial cytochrome (Cyt) bgene and confirms its placement by Benzoni et al. (2007) inthe Siderastreidae in the Complex clade. Although Oulas-trea belongs to the Robust corals, it is only distantly re-lated to the Coscinaraeidae (Fukami et al., 2008) and wasnot included in the new family. Regardless of the afore-mentioned and described variability in colony and coralliteshape and size, the family Coscinaraeidae is characterizedby diagnostic characters concerning septa (i.e. pattern offusion, paddle-shaped ornamentation and microstructures),which are consistent throughout the genera and speciesascribed to the family. The Coscinaraeidae are evolution-arily closely related to the Psammocoridae. Despite similarstructure of the corallite wall and septa ornamentation, thetwo are considered distinct on the basis of the presenceof series of enclosed petaloid septa (EPS) correspondingto extrapolypal tentacles in vivo in the Psammocoridae, aunique feature among scleractinian corals (Benzoni et al.,2007, 2010). The inclusion of the one sequence of Cosci-naraea columna examined by Benzoni et al. (2010) in thePsammocoridae clade suggests that the genus is still poly-phyletic even after the re-assignment of Coscinaraea wellsiVeron & Pichon (1980) to the genus Cycloseris (Benzoniet al., 2012). Interestingly, three of the four genera includedin the Coscinaraeidae, namely Craterastrea, Horastrea andAnomastraea, are monotypic and are found exclusively inthe Indian Ocean, while Coscinaraea extends its distribu-tion into the Pacific (Sheppard et al., 1992; Veron, 2000).This distinctive distribution seems to support the ongo-ing discussion on the evolutionary distinctiveness of IndianOcean coral taxa (Stefani et al., 2011; Arrigoni et al., 2012)and of the existence of an Indian Ocean centre of diversity(Obura, 2012b).

In this study we resurrected the genus Craterastrea andpresented new information on C. levis geographic distri-bution and the species ecology. The species’ cryptic habitand its preference for shallow lagoon habitats or for themesophotic zone imply challenges for its conservation. Thisinformation should be included in the major online biodi-

versity databases as well as formally considered by the in-ternational regulations on the trade of endangered species.For example, in the list of CITES corals occurring in Aus-tralian waters (ABRS, 2011) C. levis is listed under ‘Othernames – Do not use’ for Leptoseris foliosa. This being said,the actual presence of C. levis outside the Indian Ocean stillhas to be investigated. Also, its inclusion in the IUCN RedList of Threatened species list is necessary.

For the first time, the morpho-molecular approach to thestudy of scleractinian coral integrated systematics has ledto the resurrection of a valid genus and species erroneouslysynonymized with a distantly related genus. The descrip-tion of the new family Coscinaraeidae is a further step inthe challenging but ongoing process of the revision of thetaxonomy of scleractinian corals based on the molecularsystematics revolution.

AcknowledgementsThe authors are grateful to B.W. Hoeksema (Naturalis),C.R.C. Sheppard (University of Warwick), and an anony-mous reviewer for useful suggestions, which helped im-prove the manuscript. We are indebted to D. Obura(CORDIO) for his help in English editing. Sampling inMayotte was possible thanks to the Tara Oceans scientificexpedition and the OCEANS Consortium. We are gratefulin particular to E. Karsenti (EMBL) and E. Bougois (TaraExpeditions) for allowing reef research during the expe-dition, to S. Kandels-Lewis (EMBL), R. Trouble (FondsTara), R. Friederich (World Courier) and to Captain H.Bourmaud and the Tara crew in general and to M. Oriotand J.J. Kerdraon in particular. We are especially indebtedto L. Bigot (ECOMAR) for his assistance and support forfieldwork in Mayotte. Sampling in New Caledonia was pos-sible thanks to the support of the Institut de Recherche pourle Developpement and to C. Payri, J. Butscher, A. Arnaudand E. Folcher. We are grateful to the Province Sud of NewCaledonia for sampling permits in the Prony Bay, and tothe Direction de l’Agriculture et de la Foret (DAF) and toA. Gigou and D. Laybourne for assistance with collectionand CITES permits in Mayotte. We thank A. Andouche(MNHN), A. Cabrinovic (BMNH), S. Cairns (USNM),B. Done (MTQ), B.W. Hoeksema (RMNH), K. Johnson(BMNH), M. Lowe (BMNH) and C. Wallace (MTQ) foraccess to museum collections, and O.S. Tendal (ZMUC) forthe loan of type material by Forskal. The first author wishesto thank C. Sheppard for his comments and for validatingthe identification of the collected specimens. M. Pichon,B. Thomassin and G. Faure are acknowledged for usefulcomments in the first phase of the morphological analysesand for indications on sampling localities in Mayotte. Weare grateful to UNIMIB Lab 2014 and to Diego, Danielaand Andrea in particular for allowing use of the Nanodrop1000 spectrophotometer, and to E. Reynaud (Adequation &

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Developpement) for kindly donating part of the UNIMIBlaboratory instruments for this study.

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