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Systematics of the coral genus Craterastrea (Cnidaria,
Anthozoa, Scleractinia) and description of a new
family through combined morphological and molecular
analyses
Francesca Benzoni
a b
a
c
, Roberto Arrigoni , Fabrizio Stefani & Jarosław Stolarski
d
a
Department of Biotechnology and Biosciences, University of Milano-Bicocca, Piazza della
Scienza 2, 20126, Milan, Italy
b
Institut de Recherche pour le Développement, UMR227 CoReUs2, 101 Promenade Roger
Laroque, BP A5, 98848 Nouméa Cedex, New Caledonia
c
Water Research Institute-National Research Council (IRSA-CNR), Via del Mulino 19, 20861,
Brugherio (MB), Italy
d
Institute of Paleobiology, Polish Academy of Sciences, Twarda 51/55, PL-00–818,
Warszawa, Poland
Published online: 19 Dec 2012.
To cite this article: Francesca Benzoni , Roberto Arrigoni , Fabrizio Stefani & Jarosław Stolarski (2012): Systematics of the
coral genus Craterastrea (Cnidaria, Anthozoa, Scleractinia) and description of a new family through combined morphological
and molecular analyses, Systematics and Biodiversity, 10:4, 417-433
To link to this article: http://dx.doi.org/10.1080/14772000.2012.744369
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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 combined
morphological and molecular analyses
FRANCESCA BENZONI1,2, ROBERTO ARRIGONI1, FABRIZIO STEFANI3 & JAROSŁAW STOLARSKI4
Downloaded by [Universita' Milano Bicocca] at 23:45 22 May 2013
1
Department of Biotechnology and Biosciences, University of Milano-Bicocca, Piazza della Scienza 2, 20126 Milan, Italy
Institut de Recherche pour le Développement, UMR227 CoReUs2, 101 Promenade Roger Laroque, BP A5, 98848 Nouméa Cedex,
New Caledonia
3
Water Research Institute-National Research Council (IRSA-CNR), Via del Mulino 19, 20861 Brugherio (MB), Italy
4
Institute of Paleobiology, Polish Academy of Sciences, Twarda 51/55, PL-00–818, Warszawa, Poland
2
(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 septal
micromorphology to that of Coscinaraea. Subsequently, it was synonymized with Leptoseris, family Agariciidae, based on
corallum macromorphology. Since then, it has remained poorly studied and has been known only from a small number of
specimens 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 the
Seychelles, Madagascar, and Mayotte, southern Indian Ocean. A recent survey in Mayotte allowed the in situ imaging of
Craterastrea in shallow and turbid reef environments and sampling for molecular analyses. The molecular analyses were in
agreement 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, Craterastrea
is closely related to Coscinaraea, Horastrea and Anomastraea. However, these genera, currently ascribed to the
Siderastreidae, are genetically distant to Siderastrea, the family’s type genus, and Pseudosiderastrea. Hence, we restore the
genus Craterastrea, describe the new family Coscinaraeidae due to its deep evolutionary divergence from the
Siderastreidae, and provide revised diagnoses of the four genera in the family. The description of the new family
Coscinaraeidae is a further step in the challenging but ongoing process of revision of the taxonomy of scleractinian corals
as 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
Introduction
Scleractinian coral systematics is undergoing a considerable revolution due to current progress in molecular phylogenetics. Molecular analyses have indicated that the order Scleractinia is divided into three major clades i.e. the
Robust, Complex and Basal clades (Romano & Palumbi,
1996; Romano & Cairns, 2000; Chen et al., 2002; Fukami
et 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 have
shown that many traditional families and genera are para- or
Correspondence to: Francesca Benzoni. E-mail: francesca.
[email protected]
ISSN 1477-2000 print / 1478-0933 online
C 2012 The Natural History Museum
http://dx.doi.org/10.1080/14772000.2012.744369
polyphyletic. For example, based on concordant results
from different nuclear and mitochondrial markers, the family 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 the
Robust 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
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418
F. Benzoni et al.
questioned with respect to the placement of Pachyseris
Milne Edwards & Haime, 1849 (Fukami et al., 2008) and
Coeloseris Vaughan, 1918 (Kitahara et al., in press), it has
recently gained the deep-water coral genus Dactylotrochus
Wells, 1954 (Kitahara et al., in press), with all taxa ascribed
to it belonging to the Complex Clade (Huang, 2012).
Huang (2012) included Craterestrea ( = Craterastrea)
levis in a cladogram of scleractinian corals in the Robust
clade of the tree of life of the order Scleractinia. However,
no molecular data were available for this taxon and the author included it in the super tree based on morphological
data. In this tree the genus appears most closely related to
Coscinaraea and Psammocora, and then to Horastrea,
Anomastraea and Pseudosiderastrea, while Siderastrea is
placed in the Complex clade (Huang, 2012). However, formal taxonomic actions were not undertaken as in many
cases where molecular analyses have proven the inadequacy
of the traditional taxonomy, with some notable recent exceptions (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 by
Head (1983) in the family Siderastreidae Vaughan & Wells,
1943 due to the similarity of its septal micromorphology
to that of Coscinaraea. Head (1983) based his description
on material from Egypt previously identified as Leptoseris
hawaiiensis Vaughan, 1907 (Agariciidae Gray, 1847) by
Matthai (1948) and Ma (1959) and on specimens he collected in Sudan (Head, 1983). He provided detailed illustrations of the new taxon’s typical macro and micromorphology. The species was later reported again from the
Red Sea and from the Chagos archipelago in the Indian
Ocean (Fig. 1) (Sheppard, 1980, 1981, 1987, 1998b; Sheppard & Sheppard, 1991). The majority of known records
of C. levis are from deep reef environments (below 35 m)
(Head, 1983; Sheppard & Sheppard, 1991) with the exception of one specimen from 5 m from ‘dimly lit turbid
waters’ in the harbour of Port Sudan (Head, 1983). Despite
illustrations of the skeleton in the original description of the
taxon (Head, 1983) including SEM images to show the differences between Craterastrea levis and Leptoseris glabra
Dinesen, 1980, Veron (1993) decided that C. levis is a junior synonym of Leptoseris foliosa Dinesen, 1980. This decision led de facto to the synonymy of the monotypic genus
Craterastrea with the agariciid Leptoseris Milne Edwards
& Haime, 1849. These synonymies have not been contradicted (Veron, 1995, 2000; UNEP-WCMC, 2005) and have
never been reassessed. Today, in the era of online taxonomic
databases, Craterastrea is recognized as a valid taxon by the
World Register of Marine Species (WoRMS, 2012) following Sheppard (1998b). However, in the CITES list of coral
species (CITES, 2011), which is used for the regulation
of 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, species
records in the Indian Ocean; 2, sampling localities of C. levis at
Mayotte Island. Star indicates the position of the type locality,
circles of the sampling locality of museum specimens, squares of
specimens collected in Mayotte during the Tara Oceans expedition.
entries found’ when searching Craterastrea in the IUCN
Red List of threatened species (IUCN, 2012).
In the present study, we examined the status of the
genus Craterastrea and its significance for formalizing sections of the molecular family tree of Scleractinia. After reexamination of the Craterastrea levis type material, a survey
was conducted in the Scleractinia collections of some natural history museums with major coral collections searching for specimens identified as Leptoseris but showing
Craterastrea morphology. Subsequently, C. levis was sampled for genetic and morphologic analyses during the Tara
Oceans scientific expedition to Mayotte (Fig. 2). Hence, we
addressed for this first time the phylogenetic relationships
between Craterastrea levis and Leptoseris foliosa and with
the other genera in the Siderastreidae by using a mitochondrial (COI) and a nuclear (rDNA) marker, and macromorphological, micromorphological, and microstructural data.
A new family was established to accommodate the genera
previously ascribed to the Siderastreidae that belong to the
Robust clade.
Materials and methods
Museum collections and other examined
specimens
Type 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, UK
IRD Institut de Recherche pour le Développement,
Nouméa, New Caledonia
MNHN Muséum National d’Histoire Naturelle, Paris,
France
Systematics of Craterastrea and description of the Coscinaraeidae Fam. nov.
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MTQ Museum of Tropical Queensland, Townsville,
Australia
RMNH Naturalis Biodiversity Center (formerly Rijksmuseum van Natuurlijke Historie, Leiden), Leiden, the
Netherlands
TWCMS Tyne and Wear Museums (Natural Sciences)
Chagos (Indian Ocean) Coral Collection, Newcastle upon
Tyne, UK
UNIMIB Università di Milano-Bicocca, Milan, Italy
USNM United States National Museum of Natural
History, Washington, DC, USA
ZMUC Zoological Museum, University of Copenhagen, Copenhagen, Denmark
ZPAL 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 located, but other specimens from South Africa and Yemen
were studied instead. Furthermore, original descriptions
and illustrations of these taxa were used.
Sampling
Craterastrea levis was sampled in Mayotte in May 2010
during the third leg of the Reef Biodiversity project of the
Tara Oceans scientific expedition (Karsenti et al., 2011)
(Fig. 2). Leptoseris foliosa was collected in New Caledonia
during the first author’s stay at the Institut de Recherche and
Développement in Nouméa (IRD) in 2011. Digital images
of living corals in the field were taken with a Canon G9 in
an Ikelite underwater housing system.
Coral specimens were collected, tagged and from each
selected specimen a fragment of c. 1 cm2 was broken off
and preserved in absolute ethanol for molecular analysis.
The remaining corallum was placed for 48 hours in sodium
hypochlorite to remove all soft parts, rinsed in fresh water and dried for microscopic observation. Images of the
cleaned skeletons were taken with a Canon G9 digital
camera.
Molecular analyses
Extraction of coral DNA was performed using a Qiagen
R
Blood & Tissue kit (Qiagen Inc., Valencia, CA,
DNeasy
USA). DNA concentration of extracts was quantified using
a Nanodrop 1000 spectrophotometer (Thermo Scientific,
Wilmington, DE, USA).
The cytochrome c oxidase subunit I gene (COI) and a
portion of rDNA (a fraction of ITS2 and 5.8S) were amplified and sequenced to infer phylogenetic relationships of
the genus Craterastrea at family and species level, respectively. A COI fragment of about 650 bp was amplified using coral-specific COI primers MCOIF and the protocol by
419
Fukami et al. (2004). Amplification of an rDNA portion of
about 700 bp was performed using the coral specific primer
A18S (Takabayashi et al., 1998) and the universal primer
ITS4 (White et al., 1990) following the protocol by Benzoni
et al. (2011). PCR products were purified and sequenced
by Macrogen Inc. (Seoul, South Korea), using the same
primers that had been used for the PCR reaction. The newly
obtained mitochondrial and nuclear sequences of Craterastrea levis and Leptoseris foliosa were aligned with homologous sequences of the family Siderastreidae obtained
from previous works (Benzoni et al., 2007, 2010; Stefani
et al., 2007) and with sequences of the families Agariciidae and Fungiidae published by Fukami et al. (2008) and
Gittenberger et al. (2011). Tubastraea aurea (Complex
clade) was selected as a suitable outgroup given its higher
divergence from the examined taxa (Fukami et al., 2008).
Chromatograms were viewed, edited and assembled using CodonCode Aligner 3.7.0 (CodonCode Corporation,
Dedham, MA, USA). Sequences were aligned with the default parameters of BioEdit Sequence Alignment Editor
7.0.9.1 (Hall, 1999). Indels, invariable and parsimony informative sites were detected with DnaSP 5.10.01 (Librado
& Rozas, 2009). Indels were treated as a fifth character in
phylogenetic analyses.
Analyses for phylogenetic inference were conducted using three methods: maximum parsimony (MP), Bayesian
inference (BI) and maximum likelihood (ML). To examine
whether the sequences from the two loci should be combined in a single analysis, a partition-homogeneity test was
run in PAUP∗ 4.0b10 (Swofford, 2003), and significance
was estimated by 1000 repartitions. This test, described
as the incongruence-length divergence test by Farris et al.
(1995), indicated no conflicting phylogenetic signals between the datasets (P = 0.95). Therefore, COI and rDNA
were linked and datasets from both molecular markers were
concatenated into a single data matrix.
Maximum parsimony analysis was performed with
PAUP∗ 4.0b10, with heuristic searches using stepwise addition and performing tree-bisection-reconnection (TBR)
branch swapping. Consistence in the nodes was assessed by
500 bootstrap replicates with random addition of taxa. The
software MrModeltest2.3 (Nylander, 2004) in conjunction
with PAUP∗ 4.0b10 were used to select nucleotide substitution models. The best model estimated by the Akaike
Information Criterion (AIC) was General Time Reversible
rate matrix with a proportion of sites being invariant and the
remainder following a gamma distribution (the GTR+I+
model). Bayesian inference analyses were conducted using MrBayes 3.1.2 (Huelsenbeck & Ronquist, 2001;
Ronquist & Huelsenbeck, 2003). Two independent runs
for four Markov chains were conducted for 2.7 million
generations, and the tree was sampled every 10 generations. Based on checking the parameter estimates and
convergence using Tracer 1.5 (Drummond & Rambaut,
2007), the first 67 501 trees were discarded as burn-in. A
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420
F. Benzoni et al.
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 PhyML
3.0 (Guindon & Gascuel, 2003) using the default parameters and the robustness of the phylogeny were tested by 500
bootstrap replications.
terminology of skeletal macro-structures in Leptoseris we
referred to Dinesen (1980).
Results
Morphological analyses
Phylogenetic analyses
Both macro and micromorphological characters (sensu
Budd & Stolarski, 2009) of Craterastrea levis and Leptoseris foliosa were examined using light microscopy (Zeiss
Stemi DV4 stereo-microscope) and SEM, respectively. For
SEM, specimens were mounted using silver glue, sputtercoated with conductive gold film and examined using a
Vega Tescan Scanning Electron Microscopy at the SEM
Laboratory, University of Milano-Bicocca, and a FEI XL20
Scanning Electron Microscopy at the Institute of Paleobiology, Polish Academy of Sciences. For microstructural
observations the skeletal material was fixed with araldite
and polished with aluminium oxide (Buehler TOPOL 3 final polishing suspension with particle size 0.25 μm). For
COI and rDNA sequences were obtained for a total of four
samples, two of Craterastrea levis (MY095 and MY305)
and two of Leptoseris foliosa (HS2854 and HS2873). The
final concatenated alignment consisted of 50 sequences
(Table 1) and 783 pb, of which 455 bp for COI, 220 bp
for ITS2 and 108 bp for 5.8S region. 211 nucleotide sites
were variable and 177 parsimony informative, with a total of 304 mutations. BI, MP and ML methods produced
similar topologies, with no contrasting signals. Bayesian
topology with branch support indicated by Bayesian posterior probability scores (PPBI ), MP bootstrapping support
(BTMP ) and ML bootstrapping support (BTML ) is reported
in Fig. 3.
Systematics of Craterastrea and description of the Coscinaraeidae Fam. nov.
421
Table 1. Specimens included in the molecular analyses (Fig. 40). For each specimen the collection code (if available), the identification
and the COI and rDNA EMBL sequence codes are given.
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CODE
HS2854
HS2873
UNIMIB-TO MY095
UNIMIB-TO MY305
K124
K131
K122
K117
RE516
RE518
W600
Y219
I110
M48
I97
M26
W613
HS1376
M43
M7
M18
MA254
-
Species
COI
rDNA
Leptoseris foliosa
Leptoseris foliosa
Craterastrea levis
Craterastrea levis
Tubastraea aurea
Siderastrea radians
Siderastrea siderea
Siderastrea stellata
Gardineroseris planulata
Pavona cactus
Oulastrea crispata
Anomastraea irregularis
Anomastraea irregularis
Coscinaraea monile
Coscinaraea monile
Horastrea indica
Horastrea indica
Coscinaraea columna
Psammocora albopicta
Psammocora contigua
Psammocora contigua
Psammocora haimiana
Psammocora haimiana
Psammocora digitata
Psammocora digitata
Psammocora nierstraszi
Psammocora profundacella
Psammocora profundacella
Psammocora nierstraszi
Cycloseris costulata
Cycloseris cyclolites
Ctenactis albitentaculata
Ctenactis echinata
Danafungia scruposa
Fungia fungites
Halomitra pileus
Heliofungia actiniformis
Heliofungia fralinae
Herpolitha limax
Lithophyllon concinna
Lithophyllon undulatum
Lobactis scutaria
Pleuractis granulosa
Pleuractis paumotensis
Podabacia crustacea
Podabacia motuporensis
Polyphyllia talpina
Sandalolitha dentata
Sandalolitha robusta
Zoopilus echinatus
HE978506
HE978507
HE978510
HE978509
AB441235
AB441212
AB441211
AB441213
AB441218
AB441216
AB441197
AM494869
AM494870
AM494859
AM494858
AM494864
AM494865
HE978508
FM865871
AM494849
AM494847
AM494856
AM494855
FM865876
FM865873
FM865878
AM494853
FM865879
AM494850
EU149890
EU202719
EU149869
EU149899
EU149872
EU149892
EU149875
EU149885
EU149901
EU149886
EU149893
EU149887
EU149862
EU149884
EU149911
EU149907
EU149898
EU149915
EU149918
EU149917
EU149916
HE978501
HE978502
HE978505
HE978504
AY722796
AY322604
AY322603
AB441407
AB441409
AB441408
AY722781
AM230624
AM231716
AM230599
AM230598
AM230605
AM230605
HE978503
FM986360
AM230604
AM230602
FM986368
AM749206
FM986371
FM986361
AM230606
AM230617
AM230619
AM230601
EU149820
EU149821
EU149813
EU149817
EU149827
EU149829
EU149838
EU149839
EU149825
EU149841
EU149832
EU149844
EU149830
EU149835
EU149850
EU149845
EU149846
EU149853
EU149856
EU149857
EU149858
Siderastrea, the type genus of the family Siderastreidae,
is highly divergent from the other Siderastreidae (sensu
Veron, 2000). All the species of Siderastrea included in
this phylogenetic tree, namely S. radians (Pallas, 1766),
S. siderea (Ellis & Solander, 1786), and S. stellata Verrill, 1868, form a very well-supported group (PPBI , BTMP ,
BTML = 100, Fig. 3), previously indicated as clade IX by
Fukami et al. (2008). Leptoseris foliosa clusters together
with the genera Pavona Lamarck, 1801 and Gardineroseris
Scheer & 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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422
F. Benzoni et al.
Figs 12–15. Different corallum morphology of Craterastrea levis
specimens sampled for this study: 12, UNIMIB TO–MY098 (same
specimen shown in Figs 5, 23); 13, UNIMIB TO–MY148 (same
specimen shown in Fig. 7); 14, top view of specimen UNIMIB
TO–MY095 (same specimen shown in Fig. 9); 15, side view of
the same specimen as 14. Scale bars represent 1 cm.
Figs 4–11. In situ images of Leptoseris foliosa (4, 6, 8, 10) and
Craterastrea levis (5, 7, 9, 11) showing growth forms and colouration at different stages of colony development and overall similarity between the two taxa: 4, encrusting corallum of specimen
IRD HS 2861; 5, one calice corallum of C. levis showing the
typical 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 (New
Caledonia, Prony Bay, 20 m); 7, cyathiform colony of C. levis
(UNIMIB TO–MY148; same specimen shown in Fig. 13) circular
inset shows a corallite; 8, fan-shaped colony of L. foliosa (New
Caledonia, Prony Bay, 15 m) circular inset shows a corallite; 9,
fan-shaped colony of C. levis (UNIMIB TO–MY095; same specimen shown in Figs 14–15); 10, foliose colony of L. foliosa forming
tiers of whorls (New Caledonia, Prony Bay, 10 m); 11, large colony
of C. levis showing a corrugated surface due to the presence of
irregular rounded protuberances (Bouéni Bay, Mayotte Island).
Scale bars represent 1 cm.
family-level lineages, the Siderastreidae (pars), the
Psammocoridae Chevalier & Beauvais, 1987, and the
Fungiidae. Oulastrea crispata (Lamarck, 1816) is a highly
distinctive outgroup for these three groups and shows unresolved evolutionary relationships. Craterastrea levis is
in one of the lineages, and closely related to Coscinaraea
monile (Forskål, 1775), Horastrea indica Pichon, 1971, and
Anomastraea irregularis Marenzeller, 1901. The average
distance of Craterastrea levis from Leptoseris foliosa is
17.8 ± 1.4%, and from the Agariciidae clade is 18.2 ±
1.4%. These values are higher than the genetic distance between Craterastrea levis and other taxa in the same clade,
i.e. 2.3 ± 0.4%. The sister group of this clade including
all the Siderastreidae except Siderastrea is the Psammocoridae clade, comprising all the species of Psammocora
included in this study and Coscinaraea columna (Dana,
1846), as already shown by Benzoni et al. (2010). The third
major group, the Fungiidae clade, includes all genera of
Fungiidae in agreement with Gittenberger et al. (2011) and
Benzoni et al. (2012). As mentioned in the introduction,
the remaining genus in the Siderastreidae, Siderastrea, is in
the Complex clade.
Morphological analyses
A detailed description of morphological characters between
Leptoseris foliosa and Craterastrea levis and their comparison 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 two
paratypes are deposited at the BMNH, 6 paratypes at the
Queensland Museum, 1 at the USNM.
TYPE LOCALITY: Lizard Island, Australia.
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Systematics of Craterastrea and description of the Coscinaraeidae Fam. nov.
423
Figs 24–27. Comparison of patterns of septal structures in Leptoseris foliosa (24, 25) and Craterastrea levis (26, 27): 24, X
shaped 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 (UNIMIB
TO–MY095); 27, detail of 26 showing septal paddles perpendicular to the septum direction with granules finely ornamented by
multiple spikes. Scale bars represent: Figs 24, 26, 5 mm; Figs 25,
27, 200 μm.
Figs 16–23. Comparison of skeleton morphology of Leptoseris
foliosa (16, 18, 20, 22) and Craterastrea levis (17, 19, 21, 23):
16, corallite arrangement in L. foliosa IRD HS 2903; 17, corallite
arrangement in C. levis USNM 82530; 18, protocorallite (larger
in the centre) and other corallites in L. foliosa IRD HS 2855; 19,
protocorallite (larger in the centre) and other corallites in C. levis
RMNH 19147; 20, corallites of L. foliosa IRD HS 346; 21, corallites of C. levis UNIMIB TO–MY096; 22, detail of protocorallite
in L. foliosa (same specimen as Fig. 18); 23, detail of protocorallite 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 Australia; 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, Ilôt Casy, 15 m (9/2/1987) coll.
J.L. Menou; IRD HS 352 Prony Bay, Ilôt 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, IRD
ST 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 28–32. Micromorphology and microstructure of Leptoseris
foliosa: 28, top view of part of a corallite and septocostae (rectangle indicates the part shown in 29); 29, detail of 28 showing clusters of Centres of Rapid Accretion aligned on lateral septal faces
to form more or less continuous lists (menianae) (arrows) parallel
to the septum direction (dashed line); 30, longitudinal view of
septa, arrows indicate menianae running along septal side (circle
indicates the part shown in 31); 31, enlargement of 30 showing
close up of menianae; 32, longitudinal etched section of septum
showing the central zone of Rapid Accretion Deposits form regular branches (dashed lines) towards the menianae. Occurrence
of menianae/aligned granulations parallel to the septum is typical of agariciids which form well-defined clade within complex
corals. All SEM images: 32, broken and etched section (ZPAL
R–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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424
F. Benzoni et al.
Figs 33–40. Micromorphology and microstructure of Craterastrea levis: 33, longitudinal section of a corallum showing highly
perforated structure; 34, top view of the colony surface showing
two calices; 35, paddle-like structures (arrows) perpendicular to
septum direction (dashed line); 36, detail of a paddle-shaped structures 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 Deposits forming small depressions (dots); 39, longitudinal thin section; 40, detail of 39 showing how septal paddle-shaped structures
are not continuous along the septum but are formed in regular
manner: in longitudinal broken (33) and thin (39, 40) sections
they form small platforms (arrows). SEM (33–36, 38) and optical
microscope (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 Prony
Bay, IRD ST 394, Prony Bay, Carenage, 5–15 m (23/2/2011)
coll. F. Benzoni, E. Folcher & A. Renaud; IRD HS 2877
Prony Bay, ST 394, Carenage, 5–15 m (23/2/2011) coll.
F. Benzoni, E. Folcher & A. Renaud; IRD HS 2973 Prony
Bay, ST 117, 32 m (22/3/2011) coll. F. Benzoni, E. Folcher
& A. Renaud.
Description
Corallum encrusting (Fig. 4) or with free margins forming
foliose (Fig. 6) or fan-shaped (Fig. 8) colonies, sometimes
forming whorls (Fig. 10). Larger colonies can be attached
at the centre or at one side of the corallum. Colony surface
smooth (Figs 4, 6, 16) or ridged (Figs 8, 10), with corallites
found at the bottom of the valleys separating the ridges. No
proximal cushions are formed although nodules unrelated
to the calices can form. Corallites are arranged in concentric
series around the protocorallite which is larger in diameter (Figs 18, 22). Calice outline circular in the inner part
of the corallum (Fig. 18, dashed circle) and progressively
more oval towards the corallum margin, with longer diameter perpendicular to the corallum radius (Fig. 20, dashed
circle). The fossa is round or elliptical (Fig. 20, 22). Columella present formed by one solid boss in all the corallites
(Fig. 20) except the protocorallite which can have 1–4 processes (Fig. 22). Septa unequal (Fig. 20). Septocostae equal,
compact and straight (Fig. 22), sometimes fusing or dividing and forming X-shaped crossings (Fig. 24), imperforate
(Fig. 30), margin ornamented with granulations (Fig. 25,
28, 29). Granulations on septal sides form elongated aggregations or merge into menianae parallel to the growing
septal margin (Figs 29, 30, 31). Granulations (menianae)
are produced by regular divergence of the mid-septal Rapid
Accretion Deposits zone (Fig. 32).
In vivo colour ranges from greenish beige to light brown
with 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 two
paratypes (BM 1981.4.1.5; BM 1981.4.1.6) are deposited
at 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; BMNH
1950.1.11.330 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); RMNH
34540 (partim) Madagascar (identified as Leptoseris foliosa); MTQ G 61808 Nosy Bé, Madagascar (January
2002) coll. JEN Veron (identified as Leptoseris foliosa);
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Systematics of Craterastrea and description of the Coscinaraeidae Fam. nov.
MTQ G 61807 Nosy Bé, Madagascar (January 2002)
coll. JEN Veron (identified as Leptoseris foliosa); MNHN
20398 Tuléar, Madagascar, 30 m (14/9/1963) coll. M.
Pichon (identified as Leptoseris cf incrustans); MNHN
20399 Tuléar, Madagascar, 26 m (8/9/1965) coll. M. Pichon, (identified as Leptoseris cf incrustans); MNHN
20400 Tuléar, Madagascar, 28 m (21/9/1965) coll. M.
Pichon (identified as Leptoseris cf incrustans); MNHN
20401 North Grande Circle, Tuléar, Madagascar, 25–35 m
(8/10/1965) coll. M. Pichon (identified as Leptoseris cf
incrustans); MNHN 20402 Tuléar, Madagascar, coll. M.
Pichon (identified as Leptoseris cf incrustans); MNHN
20403 Tuléar, Madagascar, coll. M. Pichon (identified as
Leptoseris cf incrustans); MNHN unregistered (collection
code MAY 12–122), Double barrière face N’gouja, Mayotte Island, Mission BARMAY (24/4/2005) coll. G. Faure
(identified as Leptoseris cf incrustans); MNHN unregistered Banc du Boa (collection code MAY 12–122), Mayotte Island Mission BARMAY (18/4/2005) coll. G. Faure
(identified as Leptoseris cf incrustans); MNHN unregistered (collection code MAY 12–122) Bai Soud, Mamoudzu,
Mayotte Island (31/5/1983) coll. G. Faure (identified as Leptoseris cf incrustans); UNIMIB TO–MY013 Mayotte Island, Site TO–MY 1 I. Blanche (12◦ S 42,981; 45◦ E 10,455)
20 m (30/5/2010) coll. F. Benzoni; UNIMIB TO–MY014
Mayotte Island, Site TO–MY 1 I. Blanche (12◦ S 42,981;
45◦ E 10,455) 15 m (30/5/2010) coll. F. Benzoni; UNIMIB
TO–MY025 Mayotte Island, Site TO–MY 2 I. Verte (12◦ S
43,416; 45◦ E 8,856) 25 m (30/5/2010) coll. F. Benzoni;
UNIMIB TO–MY094 Mayotte Island, Site TO–MY 11
Bouéni 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 Bouéni Bay (12◦ S 54,698; 45◦ E 7,871)
15 m (4/6/2010) coll. F. Benzoni; UNIMIB TO–MY096
Mayotte Island, Site TO–MY 11 Bouéni Bay (12◦ S 54,698;
45◦ E 7,871) 15 m (4/6/2010) coll. F. Benzoni; UNIMIB
TO–MY097 Mayotte Island, Site TO–MY 11 Bouéni Bay
(12◦ S 54,698; 45◦ E 7,871) 15 m (04/06/2010) coll. F. Benzoni; UNIMIB TO–MY098 Mayotte Island, Site TO–MY
11 Bouéni Bay (12◦ S 54,698; 45◦ E 7,871) 20 m (4/6/2010)
coll. F. Benzoni; UNIMIB TO–MY108 Mayotte Island, Site
TO–MY 13 Bouéni outer barrier (12◦ S 56,376; 45◦ E 3,256)
(05/06/2010) coll. F. Benzoni; UNIMIB TO–MY120 Mayotte Island, Site TO–MY 14 (12◦ S 52,534; 45◦ E 16,834)
(06/06/2010) coll. F. Benzoni; UNIMIB TO–MY148 Mayotte Island, Site TO–MY 17 Bouzi (12◦ S 48,749; 45◦ E
14,486) (7/6/2010) coll. F. Benzoni; UNIMIB TO–MY149
Mayotte Island, Site TO–MY 17 Bouzi (12◦ S 48,749; 45◦ E
14,486) (7/6/2010) coll. F. Benzoni; UNIMIB TO–MY150
Mayotte Island, Site TO–MY 17 Bouzi (12◦ S 48,749; 45◦ E
14,486) (7/6/2010) coll. F. Benzoni; UNIMIB TO–MY151
Mayotte Island, Site TO–MY 17 Bouzi (12◦ S 48,749; 45◦ E
14,486) (7/6/2010) coll. F. Benzoni; UNIMIB TO–MY305
Mayotte Island, Site TO–MY 31 Bouéni Bay 2 (12◦ S
54,698; 45◦ E 7,871) (16/6/2010) coll. F. Benzoni.
425
REMARKS: The genus is monotypic.
Description
The corallum is thin, unifacial, crateriform (Figs 5, 7, 9, 11)
and attached to the substrate by a peduncle generally found
at the centre of the undersurface (Fig. 15). In small colonies
with one calice the corallum (Figs 5, 12) resembles the anthocaulus stage in free-living Fungiidae (Hoeksema, 1989:
Fig. 43) but in the latter the umbrella is concave and not
convex. In some colonies only part of the lamina grows
and the corallum appears secondarily foliose, attached peripherally (Figs 9, 14). Colony surface is generally even
(Figs 5, 9, 12, 14, 17). In some colonies irregular rounded
protuberances analogous to proximal cushions in the genus
Leptoseris can occur (Figs 7, 11, 13). These can either
develop in correspondence with calices or far from them.
The first calice is generally larger than the others, which
are approximately 4 mm in diameter (Figs 19, 23). The
colonial stage is reached through intratentacular budding,
initially circumoral and followed by irregular marginal division (Figs 14, 19). Calices are spaced far apart over the
colony surface (Fig. 13) and tend to be even sparser towards the margin of the corallum (Figs 14, 17). Although
in some specimens a tendency to form concentric rows of
corallites can be observed (Fig. 14), in general this is seldom observed. The calice margin is hardly detectable due
to the continuity between septa between calices and their
even thickness (Figs 19, 21, 23, 29).
The columella is formed by multiple processes in all
the corallites (Figs 21, 23) although they are more numerous, though not larger, in the protocorallite (Fig. 23).
Septa and septocostae equal (Figs 21–23), perforated and
straight, sometimes fusing or dividing and forming Xshaped crossings (Fig. 26). These septocostae are highly
perforated (Figs 33, 37, 39, 40) and ornamented with typical septal paddles perpendicular to the septum direction
(Figs 26, 27, 33, 35, 36). Each paddle consists of numerous
centres of Rapid Accretion which radiate in all directions
(blue arrows in Fig. 36), therefore in etched sections Rapid
Accretion Deposits occur in many places (Fig. 38). The
granules of the paddles are finely ornamented by multiple
spikes. Septal paddles are not continuous along the septum but appear in regular manner forming small platforms
(Figs 26, 37, 38). Although the platforms resemble short
menianae or pennular structures of some Mesozoic corals
(Morycowa & Roniewicz, 1995) they are formed in addition to predominant paddles which are perpendicular to the
septal plane. Septa and septocostae are regularly connected
laterally by synapticulae which form a fine and regular
three-dimensional mesh with the trabeculae forming the
septocostae (Fig. 33).
In vivo colour ranges from greenish beige to light brown
with paler colony margins (Figs 5, 7, 9, 11).
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F. Benzoni et al.
Although the growth forms of C. levis and L. foliosa
are to a large extent overlapping, some differences were
detected. Both species are colonial forming encrusting to
foliose coralla. However, in L. foliosa the corallum is generally encrusting at the base and foliose in the peripheral part
while 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 first
time in Mayotte where a complete series of specimens was
collected including single-polyp coralla (Figs 5, 12). No
such one corallite stage was observed in L. foliosa, although
all the presumably young colonies (few calices and rather
regular in outline) we observed were encrusting. Both C.
levis and L. foliosa are characterized by small calices, except the generally central protocorallite, which is larger
(Figs 18, 19, 22, 23), poorly defined theca, and a thamnasterioid arrangement of the septa which can be very long
(up to 10 times the calice diameter or more, especially in
Craterastrea). Although calices are on average of slightly
different size in the two species, larger in C. levis than in
L. foliosa, their diameter ranges overlap. In L. foliosa they
tend to be more evenly sized throughout the colony, while
in C. levis their size can be more variable (Fig. 13). These
differences are, however, difficult to detect to the naked
eye because of the overall small dimensions of the calical
structures and the poorly visible calice wall. In both species
calices can be very far apart although in C. levis this is
more often observed and their distances can be remarkably longer. Furthermore, while in L. foliosa they tend to
be arranged in concentric rows and to attain a more oval
outline further from the colony centre (Figs 18, 20), this
is seldom observed in C. levis coralla where the general
calice arrangement pattern is much less regular from the
centre of the colony towards its periphery and calices are
more evenly circular in outline. Nevertheless, the arrangement of the long septa is strikingly similar in both species
(Figs 24, 26) and contributes to the similarity of the overall
macromorphology between the two species. It is proposed
that while for L. foliosa the term septocostae as defined
by Dinesen (1980) is conserved, the term interstomatous
septa is preferred for C. levis following the definition, and
ontological explanation, given by Hoeksema (1989).
Taxonomy
Order Scleractinia Bourne, 1900
Family Coscinaraeidae Fam. nov.
TYPE GENUS: Coscinaraea Milne Edwards and Haime,
1848.
ETYMOLOGY: Named after the designated type genus
Coscinaraea.
DIAGNOSIS: Corallum colonial, attached. Corallites cerioid or plocoid, forming monocentric to polycentric series,
wall synapticulothecal or septothecal. Septa completely or
partially perforated, joined by one or more rows of synapticulae, fusing towards the fossa. Septal margin ornamentation composed of paddle-shaped spiked ridges oriented
transversally to the septal plane. Septa sides granular. Columella present, papillary, formed by multiple processes (extremities of trabeculae) developing from the inner margin
of the septa towards the fossa.
Description
The family is comprised of colonial taxa characterized
by different macro-morphology, including encrusting, massive, cup-shaped or submassive colonies. The shape, size
and arrangement of the corallites are very different between
genera (Benzoni et al., 2007). Corallite arrangement can be
plocoid or cerioid. Corallite outline is polygonal, irregular
or circular, and monocentric to polycentric. Corallite wall
is synapticulathecal in all genera except Horastrea which
has a septothecal wall (Benzoni et al., 2007). Although
petaloid septa (sensu Benzoni et al., 2010) can occasionally form at the merger of three or more calices in Coscinaraea, and can sometimes be observed also in specimens
of Horastrea, they do not form in Anomastraea or Craterastrea. Rows of enclosed petaloid septa, typically found
in the Psammocoridae (Benzoni et al., 2007, 2010) never
form in the Coscinaraeidae. In all taxa septa are perforated,
characterized by granular ornamentation on the lateral
sides, and ornamented by paddle-shaped spiked ridges oriented transversally to the septal plane on the upper margin
(Benzoni et al., 2007). Septa are typically joined by synapticulae and fuse within the calice towards the fossa. In all
the coscinaraeids a papillary columella is formed by the trabecular processes extending from the inner margin of the
septa and fusing with similar processes from other septa to
form a perforated central structure.
Genus Coscinaraea Milne Edwards & Haime, 1848
(Figs 41–42)
TYPE SPECIES: Madrepora monile Forskål, 1775: 133,
Holotype examined (Fig. 41).
REVISED DIAGNOSIS: Corallum colonial, attached, encrusting, massive or submassive. Corallites cerioid, forming
monocentric to polycentric series (Fig. 42), wall synapticulothecal, perforate (Benzoni et al., 2007). Septa perforate,
joined by synapticulae, fusing towards the fossa (insets in
Figs 41–42). Septal margin ornamentation composed of
paddle-shaped granules perpendicular to the septal plane
(Benzoni et al., 2007). Septa sides granular. Columella
developed, formed by multiple processes. Costae on the
colony wall unequal to sub-equal.
DISTRIBUTION: Red Sea, Indian Ocean and western Pacific Ocean.
REMARKS: Despite the recent taxonomic revision of C.
wellsi, now belonging to the fungiid genus Cycloseris
Systematics of Craterastrea and description of the Coscinaraeidae Fam. nov.
427
DISTRIBUTION: Western and southern Indian Ocean
(Madagascar; Mayotte) (Obura, 2012a).
REMARKS: The genus is monotypic.
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Genus Anomastraea von Marenzeller, 1901
(Figs 45–46)
TYPE SPECIES: Anomastraea irregularis Marenzeller,
1901: 124–125, Figs 3, 3a.
REVISED DIAGNOSIS: Corallum colonial, attached, encrusting to massive (Fig. 45). Corallites cerioid, polygonal
in outline (Fig. 46), predominantly monocentric, seldom
bi- or tricentric, wall synapticulothecal, perforate (Benzoni
et al., 2007). Septa partly perforate, joined by one row of
synapticulae, fusing towards the fossa (inset in Fig. 46).
Septa ornamentation composed of paddle-shaped granules
perpendicular to the septal plane (Benzoni et al., 2007).
Septa sides granular. Columella developed, formed by multiple processes.
DISTRIBUTION: Red Sea and Indian Ocean.
REMARKS: The genus is monotypic.
Genus Craterastrea Head, 1983
Figs 41–46. Macromorphological features of the genera ascribed
to the Coscinaraeidae fam. nov. other than Craterastrea: 41, Holotype 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, Horastrea indica, side view of specimen UNIMIB–TO MY228 from
Mayotte; 44, top view of specimen UNIMIB–TO MY229 from
Mayotte, inset shows detail of a corallite; 45, Anomastraea irregularis specimen BMNH 1961.7.17.69 from South Africa; 46, one
of the specimens included in the molecular analyses in this study
UNIMIB K131 (Fig. 3; Table 1) from Kuwait, inset shows detail
of a corallite. Scale bars represent 1 cm.
(Benzoni et al., 2007, 2012), the genus is most likely still
polyphyletic (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, massive (Fig. 43). Corallites plocoid, circular or irregular in
outline (Fig. 43), forming monocentric to polycentric series (Pichon, 1971), wall septothecal (Benzoni et al., 2007).
Septa perforated along the inner margin, otherwise mostly
compact, joined by 2–3 rows of synapticulae, fusing towards the fossa (inset in Fig. 44). Septa ornamentation composed of paddle-shaped granules (Benzoni et al., 2007).
Columella developed, formed by multiple processes perpendicular to the septal plane. Costae continuous between
adjacent calices, unequal to sub-equal.
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 in
number and distant, wall synapticulothecal, perforate. Septa
perforate, joined by synapticulae, fusing towards the fossa.
Septa ornamentation composed of paddle-shaped granules.
Columella developed, formed by multiple processes. Costae
on the colony wall unequal to sub-equal.
DISTRIBUTION: Red Sea and Indian Ocean (see
above).
REMARKS: The genus is monotypic.
Discussion
Since the beginning of the so-called molecular revolution
in scleractinian coral taxonomy and systematics (Stolarski
& Roniewicz, 2001) the inconsistency of orders, the polyphyly 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; Huang
et al., 2011; Stefani et al., 2011; Lin et al., 2012; Pichon
et al., 2012). New micromorphological and microstructural characters proved to be more phylogenetically informative than those traditionally used in hard coral taxonomy (Benzoni et al., 2007; Budd & Stolarski, 2009, 2011;
Janiszewska et al., 2011; Stolarski et al., 2011). In this paper, the combined molecular and morphological approach
was used for the first time to re-discover and resurrect a
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428
F. Benzoni et al.
Fig. 47. Schematic timeline of the classification of the genera in the Coscinaraeidae Fam. nov., since the description of the family
Siderastreidae by Vaughan & Wells (1943) and in the principal studies including them in molecular analyses until the present study. The
genera related to the Coscinaraeidae and their changes in classification or in the same molecularly defined clade have been included. The
genera included in the Coscinaraeidae in the present study are in bold. For each study we indicated on which kind of data the classification
was done (macromorphological, micromorphological and microstructural, molecular). Synonymies and placements at subgenus level are
indicated.
genus erroneously synonymized with one distantly related
to it.
The first step allowing the re-examination of Craterastrea and its resurrection as well as the description of the
family Coscinaraeidae was the study of collections in natural history museums.
Recovery of a long-forgotten taxon in
historical collections
Due to its distribution in the deeper parts of the reefs
or in turbid waters, and likely because of the synonymy
with the strikingly similar Leptoseris foliosa (Veron, 1993),
Craterastrea levis has remained largely unstudied and unsearched for. However, as shown in this study, the species
was occasionally collected in different parts of the Indian Ocean and deposited in various museums before
its formal description (Head, 1983) and after its synonymization. Specimens from the Seychelles, Mayotte Island and Madagascar were invariably identified as one
or another species of Leptoseris (L. foliosa, L. hawaiiensis, L. cf incrustans) with the notable exception of one
specimen from Chagos identified as Coscinaraea sp. and
one from Israel actually identified as C. levis by J.W.
Wells (http://collections.nmnh.si.edu/search/iz/). Interestingly, this specimen was collected in 1972, 15 years be-
fore Edwards & Head (1987) reported that Craterastrea
does ‘not penetrate into the Gulf of Aqaba’. Although C.
levis has never been recorded in the Maldives, the latest
checklists (Pichon & Benzoni, 2007; Bigot & Amir, 2012)
only included dives to a maximum depth of 30 m and the
taxon might have been overlooked, hence its presence in
the archipelago at greater depths cannot be excluded. The
re-discovery and study of museum specimens not only allowed extending the known geographic distribution of C.
levis but also directed us, through the notes of their collectors, towards more targeted sampling in Mayotte (Fig. 2).
Recently, Hoeksema et al. (2011) have highlighted how
historical collections can have unforeseen importance as
baselines to determine biotic change of coral reefs. However, it should also be remembered that collections still have
much information to provide also as repositories of known
and unknown biological diversity (see also Benzoni et al.,
2010).
The in situ, skeleton and molecular results obtained in
this study allowed a thorough comparison of C. levis and
L. foliosa and led to the formal resurrection of the genus
Craterastrea and to the description of a new family to accommodate this genus and its close allies among the Robust
corals rather than in the Siderastreidae among the Complex
ones. The different aspects of these findings and taxonomic
decisions are discussed hereafter.
Systematics of Craterastrea and description of the Coscinaraeidae Fam. nov.
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Craterastrea levis and Leptoseris foliosa:
morphological convergence of two
distantly related taxa
The phylogenetic reconstruction of the relationship between
the two taxa based on two different markers (rDNA and
COI) revealed once and for all that C. levis and L. foliosa are
two valid evolutionary and taxonomic entities. Leptoseris
foliosa is monophyletic with the agariciid taxa examined in
this study in the Complex clade. Craterastrea is closely related to Coscinaraea, Horastrea and Anomastraea, and all
these taxa are related to the Psammocoridae and the Fungiidae in the Robust clade. This being said, the morphological similarity between these taxa at first glance is striking
and it has certainly played a major role in the taxonomic
confusion between the two. However, a closer inspection
of a representative number of specimens in this study has
also revealed consistent differences, which tend to become
more obvious going from the observation of the macroand micromorphology to the microstructure. In fact, the
two species are markedly different in microscopic skeletal
features: the structure of the columella (made of one process
in L. foliosa and multiple papillary processes in C. levis),
the thickness of septa, the granulation of the paddles which
are observed on the septal margin, the arrangement of the
septal side granulation, and the septa and septocostae perforation. It is at the micromorphological and microstructural
level that the two species are most differentiated. The most
striking microstructural difference between these species
is a pattern of distribution of centres of rapid accretion on
septal faces. In Leptoseris foliosa clusters of these centres
form elongated aggregations which produce more or less
continuous lists (menianae) parallel to the septum. This feature is typical of all agariciids which form a well-defined
clade within the Complex clade corals (see also Kitahara
et al., 2010, in press). Conversely, in Craterastrea levis centres of rapid accretion form aggregations perpendicular to
the septum, their further growth resulting in the formation
of paddle-like structures. This feature is common among
representatives of the Robust clade (Cuif et al., 2003; Budd
& Stolarski, 2011).
Ecology of Craterastrea levis
Despite the evolutionary divergence of Craterastrea from
Leptoseris, the two genera tend to inhabit similar poorly lit
environments (deep or turbid). Both species can be typically found in relatively shallow waters in protected lagoon
embayments characterized by a high sedimentation of terrigenous input (for Leptoseris foliosa see Dinesen, 1980).
Craterastrea levis is also found in clear waters but it occurs
much deeper, such as in the Chagos archipelago where it
can be abundant below 70 m (Sheppard & Sheppard, 1991).
No data are available on the distribution of L. foliosa in the
outer barrier, however, Dinesen (1980) reports a specimen
429
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 what
was already observed by Sheppard & Sheppard (1991) on
this species’ extreme reduction of the proportion of colony
surface ‘occupied by the plankton trapping polyps and a
maximization of the proportion given the photosynthetic
coenosarc’. Indeed, it could be that the peculiar morphology
of the polyps and their adaptations to nutrition needs in deep
waters 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 the
taxonomic record straight
Figure 47 summarizes the taxonomic riddle represented
by the Siderastreidae from the formal family description
by Vaughan & Wells (1943) until this study. The authors
based their taxonomic decisions on skeleton morphology,
included the following genera in the Siderastreidae: Coscinaraea, 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 the
genus Oulastrea from the Agariciidae to the Faviidae. More
important taxonomic changes were operated by Chevalier
& Beauvais (1987) who considered Pseudosiderastrea a
junior synonym of Siderastrea and accepted the inclusion of Horastrea described in the meanwhile by Pichon
(1971). They moved Oulastrea into the Siderastreidae, and
described the family Psammocoridae including the genus
Psammocora and other related genera later synonymized
with it (Benzoni et al., 2007, 2010). Chevalier & Beauvais
(1987) did not include Craterastrea in their treatment. Later
Veron (2000) restored Pseudosiderastrea as a valid genus
in the Siderastreidae, moved Psammocora to the Siderastreidae, Oulastrea back into the Faviidae, and kept Craterastrea as a junior synonym of Leptoseris following his
former decision (Veron, 1993).
In 1996, Romano & Palumbi published a molecular phylogenetic analysis of 16S rDNA, including Psammocora
and Coscinaraea, and reported for the first time the two
major clades of the Scleractinia, the Complex and the Robust. Fukami et al. (2008) used mitochondrial trees (COI
and CytB) to show that the family Siderastreidae is split between the Complex (Siderastrea in clade IX) and the Robust
clade (Psammocora, Coscinaraea in clade XI which also
included Oulastrea). Benzoni et al. (2007) included for the
first time micromorphological, microstructure and molecular data from all taxa included in the Siderastreidae sensu
Veron (2000), except Craterastrea. They showed that while
Siderastrea and Pseudosiderastrea are Complex clade taxa,
Coscinaraea, Horastrea, Anomastraea and Psammocora
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430
F. Benzoni et al.
are all Robust clade taxa. The latter genus has peculiar
characters which justified its inclusion in the resurrected
family Psammocoridae (Benzoni et al., 2007).
In the present study macro- and micromorphology, microstructure and molecular data demonstrated that Craterastrea is closely related to Coscinaraea and its allies
currently ascribed to the Siderastreidae and belonging to
the Robust clade. Moreover, the genus is distantly related
to Leptoseris and the Agariciidae in the Complex clade.
Since the type genus of the family and the type species of
this genus are found in the Complex clade, while the genera Coscinaraea, Horastrea, Anomastraea and Craterastrea
belong to the Robust corals, a new family is described to
separate them. Although we did not include Pseudosiderastrea in our analyses, the recent work by Pichon et al. (2012)
shows the close relationship of this taxon with Siderastrea based on the partial mitochondrial cytochrome (Cyt) b
gene and confirms its placement by Benzoni et al. (2007) in
the Siderastreidae in the Complex clade. Although Oulastrea belongs to the Robust corals, it is only distantly related to the Coscinaraeidae (Fukami et al., 2008) and was
not included in the new family. Regardless of the aforementioned and described variability in colony and corallite
shape and size, the family Coscinaraeidae is characterized
by diagnostic characters concerning septa (i.e. pattern of
fusion, paddle-shaped ornamentation and microstructures),
which are consistent throughout the genera and species
ascribed to the family. The Coscinaraeidae are evolutionarily closely related to the Psammocoridae. Despite similar
structure of the corallite wall and septa ornamentation, the
two are considered distinct on the basis of the presence
of series of enclosed petaloid septa (EPS) corresponding
to extrapolypal tentacles in vivo in the Psammocoridae, a
unique feature among scleractinian corals (Benzoni et al.,
2007, 2010). The inclusion of the one sequence of Coscinaraea columna examined by Benzoni et al. (2010) in the
Psammocoridae clade suggests that the genus is still polyphyletic even after the re-assignment of Coscinaraea wellsi
Veron & Pichon (1980) to the genus Cycloseris (Benzoni
et al., 2012). Interestingly, three of the four genera included
in the Coscinaraeidae, namely Craterastrea, Horastrea and
Anomastraea, are monotypic and are found exclusively in
the Indian Ocean, while Coscinaraea extends its distribution into the Pacific (Sheppard et al., 1992; Veron, 2000).
This distinctive distribution seems to support the ongoing discussion on the evolutionary distinctiveness of Indian
Ocean 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 and
presented new information on C. levis geographic distribution and the species ecology. The species’ cryptic habit
and its preference for shallow lagoon habitats or for the
mesophotic zone imply challenges for its conservation. This
information should be included in the major online biodi-
versity databases as well as formally considered by the international regulations on the trade of endangered species.
For example, in the list of CITES corals occurring in Australian waters (ABRS, 2011) C. levis is listed under ‘Other
names – Do not use’ for Leptoseris foliosa. This being said,
the actual presence of C. levis outside the Indian Ocean still
has to be investigated. Also, its inclusion in the IUCN Red
List of Threatened species list is necessary.
For the first time, the morpho-molecular approach to the
study of scleractinian coral integrated systematics has led
to the resurrection of a valid genus and species erroneously
synonymized with a distantly related genus. The description of the new family Coscinaraeidae is a further step in
the challenging but ongoing process of the revision of the
taxonomy of scleractinian corals based on the molecular
systematics revolution.
Acknowledgements
The authors are grateful to B.W. Hoeksema (Naturalis),
C.R.C. Sheppard (University of Warwick), and an anonymous reviewer for useful suggestions, which helped improve the manuscript. We are indebted to D. Obura
(CORDIO) for his help in English editing. Sampling in
Mayotte was possible thanks to the Tara Oceans scientific
expedition and the OCEANS Consortium. We are grateful
in particular to E. Karsenti (EMBL) and E. Bougois (Tara
Expeditions) for allowing reef research during the expedition, to S. Kandels-Lewis (EMBL), R. Troublé (Fonds
Tara), R. Friederich (World Courier) and to Captain H.
Bourmaud and the Tara crew in general and to M. Oriot
and J.J. Kerdraon in particular. We are especially indebted
to L. Bigot (ECOMAR) for his assistance and support for
fieldwork in Mayotte. Sampling in New Caledonia was possible thanks to the support of the Institut de Recherche pour
le Développement and to C. Payri, J. Butscher, A. Arnaud
and E. Folcher. We are grateful to the Province Sud of New
Caledonia for sampling permits in the Prony Bay, and to
the Direction de l’Agriculture et de la Forêt (DAF) and to
A. Gigou and D. Laybourne for assistance with collection
and 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) for
access to museum collections, and O.S. Tendal (ZMUC) for
the loan of type material by Forskål. The first author wishes
to thank C. Sheppard for his comments and for validating
the identification of the collected specimens. M. Pichon,
B. Thomassin and G. Faure are acknowledged for useful
comments in the first phase of the morphological analyses
and for indications on sampling localities in Mayotte. We
are grateful to UNIMIB Lab 2014 and to Diego, Daniela
and Andrea in particular for allowing use of the Nanodrop
1000 spectrophotometer, and to E. Reynaud (Adéquation &
Systematics of Craterastrea and description of the Coscinaraeidae Fam. nov.
Développement) for kindly donating part of the UNIMIB
laboratory instruments for this study.
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