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Contributions to Zoology, 81 (3) – 2012

Phylogenetic position and taxonomy of Cycloseris explanulata and C. wellsi (Scleractinia: Fungiidae): lost mushroom corals find their way home

Francesca Benzoni1,2,4, Roberto Arrigoni1, Fabrizio Stefani1, Bastian T. Reijnen3, Simone Montano1, Bert W. Hoeksema3

1.  Department of Biotechnology and Biosciences, University of Milano-Bicocca, Piazza della Scienza 2, 20126 Milan, Italy

2.  Institut de Recherche pour le Développement, UMR227 Coreus2, 101 Promenade Roger Laroque, BP A5, 98848 Noumea Cedex, New Caledonia

3.  Department of Marine Zoology, Netherlands Centre for Biodiversity Naturalis, PO Box 9517, 2300 RA Leiden, The Netherlands


Keywords: COI,Coscinaraea wellsi,Psammocora explanulata,rDNA.


The scleractinian species Psammocora explanulata and Coscinaraea wellsi were originally classified in the family Siderastreidae, but in a recent morpho-molecular study it appeared that they are more closely related to each other and to the Fungiidae than to any siderastreid taxon. A subsequent morpho-molecular study of the Fungiidae provided new insights regarding the phylogenetic relationships within that family. In the present study existing molecular data sets of both families were analyzed jointly with those of new specimens and sequences of P. expla­nulata and C. wellsi. The results indicate that both species actually belong to the Cycloseris clade within the family Fungiidae. A reappraisal of their morphologic characters based on museum specimens and recently collected material substantiate the molecular results. Consequently, they are renamed Cycloseris ex­planulata and C. wellsi. They are polystomatous and encrusting like C. mokai, another species recently added to the genus, whereas all Cycloseris species were initially thought to be monostomatous and free-living. In the light of the new findings, the taxonomy and distribution data of C. explanulata and C. wellsi have been updated and revised. Finally, the ecological implications of the evolutionary history of the three encrusting polystomatous Cycloseris species and their free-living monostomatous congeners are discussed.


The taxonomy of scleractinian corals is undergoing a revolution. Molecular analyses have indicated that this anthozoan order is divided over two major clades (Robust and Complex) and a basal clade consisting of various para- and polyphyletic genera and families (Romano and Palumbi, 1996; Romano and 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). Molecular data have corrected or supported old taxonomic views based on morphological characters and have lead to new insights, some of which are supported by re-examined morphological characters regarding skeletal microstructures (Fukami et al., 2000; Stolarski and Roniewicz, 2001; Benzoni et al., 2007, 2010, 2011; Stefani et al., 2007, 2008, 2011; Wallace et al., 2007; Huang et al., 2009; Budd et al., 2010).

In the monophyletic Indo-Pacific coral family Fungiidae Dana, 1846, 40 out of 50 species are free-living and 10 are attached (Hoeksema, 1989, 2009, 2012b; Gittenberger et al., 2011). Many species have large coralla that occur abundantly in mixed assemblages on shallow reefs (Claereboudt, 1988; Hoeksema and Moka, 1989; Hoeksema, 1991a, 2012a; Goffredo and Chadwick-Furman, 2000; Elahi, 2008; Hoeksema and Koh, 2009; Hoeksema and Matthews, 2011). Some species may form monospecific aggregations as a result of asexual reproduction by budding or fragmentation (Nishihira and Poung-In, 1989; Yamashiro and Nishihira, 1998; Hoeksema, 2004; Hoeksema and Gittenberger, 2010; Hoeksema and Waheed, 2011; Hoeksema and Yeemin, 2011). Owing to their remarkable life histories, ecology, and striking appearances, the Fungiidae have received much attention with regard to their evolutionary history, which resulted in phylogeny reconstructions based on morphological characters and life history traits (Wells, 1966; Cairns, 1984; Hoeksema 1989, 1991b, 1993; Hoeksema et al., 2012).

Recent molecular studies gave new insights with regard to the phylogeny of the Fungiidae. The encrusting polystomatous species Lithophyllon mokai Hoeksema, 1989 appears to be most closely related to Cycloseris, a genus otherwise consisting of free-living monostomatous species (Gittenberger et al., 2011), whereas based on morphology it was considered a sister taxon of the attached foliaceaous species L. undulatum Rehberg, 1892 (Hoeksema, 1989, 1991b, 2009). Furthermore, two encrusting polystomatous species classified with the Siderastreidae Vaughan and Wells, 1943, Psammocora explanulata Van der Horst, 1922 (Fig. 1A-D), and Coscinaraea wellsi Veron and Pichon, 1980 (Fig. 1E-H), appear to be more closely related to one another and to some Fungiidae than to the original congeners. These hypotheses are supported by morphological investigations, which reveal that these two species display typical fungiid skeletal structures which had not been previously noted in these taxa (Benzoni et al., 2007). However, so far these species have not yet been formally revised and their closest relatives among the Fungiidae have remained unknown.


Fig. 1. Psammocora explanulata (A-D) and Coscinaraea wellsi (E-H) in situ. A) HS 1769, Cap Bourail, New Caledonia; B) HS 1397, Côte Oubliée, New Caledonia; C) Al Mukallah, Yemen; D) Mayotte Island; E) Coscinaraea monile (left) and C. wellsi (right), Burum, Yemen; F) UNIMIB S061 Ras Nosrani, South Sinai, Egypt; G) UNIMIB I 080 Mapia House Reef, Manado, Sulawesi, Indonesia; H) UNIMIB I 108 Negheri, Manado, Sulawesi, Indonesia.

Molecular and morphological hypotheses are often in conflict suggesting that the taxonomic positions of the taxa need to be revised. However, the taxonomic consequences of the genetic results are often not formalized from a taxonomic point of view. The molecular phylogeny of Psammocora explanulata and Coscinaraea wellsi has revealed a taxonomic misplacement, which constitutes a historical constraint as long as they remain in the genus or family to which they were originally assigned based on a misinterpreted morphology. Hence, in lack of a proper study of their type specimens and other collected material, and of supporting field observations, their taxonomic revision stagnates. Therefore, in the present study, the phylogenetic positions of these two species within the Fungiidae are re-examined based on newly obtained mitochondrial COI and nuclear rDNA sequences from material collected throughout the Indo-Pacific and the joint datasets from Benzoni et al. (2007) and Gittenberger et al. (2011). Furthermore, the molecular hypothesis was tested by re-examining the morphological characters of the species in question. Hence, on the basis of the genetic results and of morphological studies, their taxonomic positions are revised. Finally, the study of historical museum material and illustrated specimens allows a reappraisal of their morphologic variability and geographic distribution, which has become increasingly relevant since coral species may have disappeared from areas where they previously occurred (Hoeksema and Koh, 2009; van der Meij et al., 2010; Hoeksema et al., 2011; van der Meij and Visser, 2011).

Material and methods


Sampling took place at various localities in the Indo-Pacific (Fig. 2). Specimens were collected for molecular analyses in Egypt (Gulf of Aqaba, Red Sea), Yemen (Gulf of Aden), Socotra Island, Kenya, Mayotte Island, La Réunion, Chagos (Indian Ocean), Indonesia, and New Caledonia (Pacific Ocean). Digital images of living corals in the field were taken with a Canon G9 in an Ikelite underwater housing. Coral specimens were collected, labelled, and fragments of ca 1 cm2 were subsampled and preserved in absolute ethanol for molecular analysis. The remaining corallum was placed in sodium hypochlorite for 48 hours to remove all soft tissue, rinsed in freshwater and dried for microscopic examination. Images of cleaned skeletons were taken with a Canon G9 digital camera.


Fig. 2. Map of the sampling localities (black dots) and for examined museum specimens (white dots). Numbers within each circle correspond to the following localities: 1 = Gulf of Aqaba; 2 = Saudi Arabia, Red Sea; 3 = Djibouti; 4 = Yemen (Gulf of Aden); 5 = Socotra Island; 6 = Kenya; 7 = Seychelles; 8 = Mayotte Island; 9 = Madagascar; 10 = La Réunion; 11 = Maldives; 12 = Chagos, BIOT; 13 = Thailand (Andaman Sea); 14 = Sumatra, Indonesia; 15 = Vietnam; 16 = Sabah, Malaysia; 17 = Manado, Indonesia; 18 = Ambon, Indonesia; 19 = Ternate, Indonesia; 20 = Shikoku, Japan; 21 = Murray Islands, Australia; 22 = from Palm Island to Lizard Island, Australia; 23 = Lord Howe Island, Australia; 24 = Middleton Reef, Australia; 25 = Chesterfield Islands, New Caledonia; 26 = Marshall Islands; 27 = Line Islands, Kiribas; 28 = Society Islands, French Polynesia; 29 = Austral Islands, French Polynesia.

Museum collections and other examined specimens

Type material and specimens examined for this study are deposited in the following institutes.




Australian Institute of Marine Science, Townsville, Australia


The Natural History Museum (formerly British Museum of Natural History), London, UK


Environment Protection Authority, Sana’a and Socotra, Yemen


Institut de Recherche pour le Développement, Nouméa, New Caledonia


Museum National d’Histoire Naturelle, Paris, France


Museum of Tropical Queensland, Townsville, Australia


Netherlands Centre for Biodiversity Naturalis (former Rijksmuseum van Natuurlijke Historie collection), Leiden, the Netherlands


Università degli Studi di Milano-Bicocca, Milan, Italy


United States National Museum of Natural History, Washington, USA


Netherlands Centre for Biodiversity Naturalis (former Zoölogisch Museum Amsterdam collection), Leiden, the Netherlands

Type specimens of Psammocora explanulata were examined in the BMNH and ZMA collections. Three of them (BMNH 1937.11.17.116, ZMA Coel. 1072, and ZMA Coel. 1071) are indicated as ‘Syntype’ on their label, while for specimen BMNH 1937.11.17.69 the indication ‘Type’ is given. The holotype of Coscinaraea wellsi USNM 44818 was examined, as well as the specimens of C. wellsi at MTQ that are depicted with the original species description (Veron and Pichon, 1980).

Specimen identification

The specimens were identified by use of the original descriptions and illustrations of Psammocora explanu­lata and Coscinaraea wellsi by Van der Horst (1922) and Veron and Pichon (1980), respectively. Species descriptions and illustrations in other widely used references were also examined (Wells, 1954; Veron and Pi­chon, 1976; Scheer and Pillai, 1983; Veron, 1986, 2000; Sheppard and Sheppard, 1991; Hoeksema and van Of­wegen, 2004; Fenner, 2005; Dai and Horng, 2009; Pichon et al., 2010). The morphological terms used follow the terminology explained and illustrated by Hoeksema (1989).

DNA extraction, COI and rDNA amplification and sequencing

Analyses of sequences from the mitochondrial cytochrome c oxidase subunit I gene (COI, partially) and a selection of nuclear rDNA (the entire ITS1, 5.8S, ITS2 and a fragment of 18S and 28S) were used to infer phylogenetic relationships between the examined taxa. COI and rDNA were both amplified from most, but not for all, specimens of Psammocora explanulata and Coscinaraea wellsi analyzed in this study. The list of examined samples and successful amplifications is reported in Table 1. Both markers have been previously used to assess evolutionary relationships among the Anthozoa (Benzoni et al., 2007, 2010; Stefani et al., 2008; Forsman et al., 2009; Gittenberger et al., 2011). The DNA was extracted from ethanol-preserved tissues using a DNeasy® Tissue Kit (QIAGEN, Qiagen Inc., Valencia, CA, USA). Each extract was quantified using a Nanodrop 1000 spectrophotometer (Thermo Scientific).


Table 1. List of specimens from which sequences and morphological data were obtained. For each specimen the code, identification, sampling locality, and Genbank accession code for sequences generated in this study are provided. * For sampling details, see lists of examined material.

A COI fragment of ca. 500 bp was amplified using fungiid-specific COI primers fungCOIfor1 (5’- CTG CTC TTA GTA TGC TTG TA -3’) and fungCOIrev2 (5’- TTG CAC CCG CTA ATA CAG -3’) by Gittenberger et al. (2011). A PCR mix (50 µl) consisted of 1X Buffer, 2 mM MgCl2 , 0.2 µM of forward and reverse primer, 0.1 mM dNTPs, 2 units of Taq DNA polymerase and ~30 ng DNA. The protocol was 94°C (4 min), followed by 30 cycles of 94°C (1 min), 53°C (30 sec) and 72°C (1 min), followed by 72°C (5 min). An approximately 800 bp long region of rDNA was amplified and sequenced with the universal primer ITS4 (5’- TCC TCC GCT TAT TGA TAT GC -3’) (White et al., 1990) and coral-specific primer A18S (5’- GAT CGA ACG GTT TAG TGA GG -3’) (Takabayashi et al., 1998). Amplifications were performed in a 50 µl volume, using 1X Buffer, 2 mM MgCl2 , 0.4 µM of forward and reverse primer, 0.1 mM dNTPs, 2 units of Taq DNA polymerase and ~30 ng DNA. PCR cycling was as follows: 96°C (2 min), followed by 30 cycles of 96°C (10 sec), 50°C (30 sec) and 72°C (4 min), followed by 72°C (5 min). PCR products were purified and directly sequenced using an automated 3730xl DNA Analyzer (Applied Biosystem, Foster City, CA, USA). Sequences obtained in this study have been deposited in GenBank, and accession numbers are listed in Table 1.

Phylogenetic analyses

The obtained COI and rDNA sequences were aligned with other available homologues from the families Siderastreidae and Fungiidae (Benzoni et al., 2007; Gittenberger et al., 2011). In particular all the genera of the former family, and 14 out of 15 of the latter were included in the analyses, thus excluding only the genus Cantharellus Hoeksema and Best, 1984. Among the 11 species currently recognized in the genus Cyclo­seris, only the six analyzed by Gittenberger et al. (2011) were included in the present analyses. Sequences were viewed, edited and assembled using CodonCode Aligner 2.0.6 (CodonCode Corporation, Dedham, MA, USA). Multiple alignments were finally adjusted using BioEdit (Hall, 1999). Identification of invariable, polymorphic and parsimony informative sites was conducted with DnaSP 5.10.01 (Librado and Rozas, 2009). Intra and interspecific pairwise distances (uncorrected p-distances) were calculated in MEGA 4.0.2 (Tamura et al., 2007).

Phylogenetic relationships were reconstructed using Maximum Parsimony (MP), Maximum Likelihood (ML) and Bayesian Inference (BI). For both markers MP analyses were performed with PAUP* 4.0b10 (Swofford, 2003) using a heuristic search with starting trees obtained by random stepwise addition, with 10 replicates, and the tree bisection-reconnection (TBR) branch swapping algorithm. Bootstrap replicates (n=500) were used to assess the robustness of the internal nodes of the trees. For the ML and BI analyses, nucleotide substitution model parameters were determined by using MrModeltest2.3 (Nylander, 2004). Based on arguments presented by Posada and Buckley (2004), we used the Akaike Information Criterion (AIC) to select best-fit models. The model GTR+I+G (gamma=0.4791 and p-invar=0.4595) was suggested as best fit for COI, and for the rDNA, the model SYM+I+G (gamma=0.6387 and p-invar=0.5340) was selected instead. ML reconstructions were performed with PhyML 3.0 (Guindon and Gascuel, 2003) using the default parameters. The reliability of the ML tree was assessed by bootstrap analyses, with 500 replications. BI analyses were conducted with MrBayes 3.1.2 (Huelsenbeck and Ronquist, 2001; Ronquist and Huelsenbeck, 2003), using the previously determined models of nucleotide evolution. In the case of COI, a Markov Chain Monte Carlo analysis was applied with four chains running for 1,500,000 generations, saving the current tree every 10 generations. Subsequently, a consensus tree was produced (with a burnin of 37500 trees) indicating the Bayesian posterior probabilities of each node. The rDNA phylogeny was obtained on the basis of 6,000,000 generations, sampling trees every 100 generations. The first 30,000 trees were discarded as burnin. Convergence of parameters estimates were monitored using Tracer 1.5 (Drummond and Rambaut, 2007) and by using the statistics provided by MrBayes.


COI phylogeny

Seven COI sequences for Coscinaraea wellsi and five for Psammocora explanulata were obtained. All sequences for Coscinaraea wellsi except the one from Ternate, Indonesia, shared the same haplotype. After alignment, 455 base pairs were obtained for the COI fragment, containing 329 invariable, 17 uninformative, and 109 parsimony informative base pairs with a total of 170 mutations. No indels were detected. Galaxea fascicularis (clade V and Complex group) was selected as outgroup due to its divergence from Siderastrea (clade IX and Complex group) and clade XI (Robust group) based on the mitochondrial tree proposed by Fukami et al. (2008).

All phylogenetic methods (BI, MP, ML) provided trees with the same overall topology, i.e. all specimens were assigned to the same clades, and the relationships among these clades were stable (Fig. 3). Siderastrea de Blainville, 1830, the type genus of the family Siderastreidae, is highly divergent from the other Siderastreidae (sensu Veron, 2000) as already shown in previous molecular studies (Benzoni et al., 2007; Fukami et al., 2008; Kitahara et al., 2010). The genera Coscinaraea Milne Edwards and Haime, 1848, Psammocora Dana, 1846, Horastrea Pichon 1971, and Anomastraea Marenzeller, 1901, form a strongly supported group including the Siderastreidae and Psammocoridae clades in Fig. 3. This, together with the Fungiidae and the genera Oulastrea Milne Edwards and Haime, 1848, and Leptastrea Milne Edwards and Haime, 1848 (both traditionally ascribed to the Faviidae) form a larger and well supported clade (Fig. 3). All the taxa in this larger clade were assigned to clade XI by Fukami et al. (2008). However, in our analysis Oulastrea crispata (Lamarck, 1816) appears to be highly distinctive and basal to the remainder of this clade (Fukami et al., 2008). Two main subclades are evidenced in clade XI. One subclade comprises the remaining siderastreids, with the exception of C. wellsi and P. explanulata. The other subclade includes all fungiids, all specimens of C. wellsi and P. explanulata, and Leptastrea. Moreover, C. wellsi and P. explanulata are closely related to each other together with the genera Cycloseris Milne Edwards and Haime, 1849 and Pleuractis Verrill, 1864. This group is also well supported by different phylogenetic analyses (posterior probability=99, MP bootstrap=88, ML bootstrap=83). The close relationships between C. wellsi and P. explanulata among the Cycloseris species are also supported by pairwise distances. The genetic distance of C. wellsi and P. explanulata compared to the Cycloseris species is very low (0.1 ± 0.04% in both cases). Conversely, significantly higher values are evidenced between C. wellsi and its congeners Coscinaraea monile (Forskål, 1775) (3.1 ± 0.8%) and C. columna (Dana, 1846) (3.0 ± 0.8%), and between P. explanulata and the other Psammocora species (3.9 ± 0.8%).


Fig. 3. Phylogenetic tree based on the mitochondrial gene COI inferred by Bayesian inference. The clade support values are a posteriori probabilities transformed to a percentage (BI), bootstrap values from maximum parsimony (MP) and bootstrap values from maximum likelihood (ML), in this order. Sequences generated in this study are in bold.

rDNA phylogeny

A total of eight sequences of C. wellsi and six of P. explanulata were obtained for the rDNA locus. Direct sequencing produced reliable electropherograms and no ambiguous nucleotide peaks. The aligned matrix was 678 base pairs long, 419 positions were constant, 128 positions were polymorphic, and 64 base pairs potentially parsimony-informative. Finally, 127 indel sites were found, and they were treated as a fifth character in phylogenetic analyses. Oulastrea crispata was selected as outgroup owing to its high divergence within clade XI sensu Fukami et al. (2008) based on mitochondrial phylogeny (Fig. 3), and because sequences from other outgroups were not available for this marker.

The general topology of the phylogeny reconstructions obtained with MP, ML and Bayesian procedures was congruent (Fig. 4), with minor differences in the relationships among sequences in the terminal clades and reflecting the same topology as observed in COI phylogeny.


Fig. 4. Phylogenetic tree based on rDNA (spanning the entire ITS1, 5.8S, ITS2 and a portion of 28S and 18S) inferred by Bayesian inference. The clade support values are a posteriori probabilities transformed to a percentage (BI), bootstrap values from maximum parsimony (MP) and bootstrap values from maximum likelihood (ML), in this order. Sequences generated in this study are in bold.

Two main subclades within clade XI sensu Fukami (2008) are partially recognizable. Coscinaraea columna (Dana, 1846) and Psammocora contigua (Esper, 1794) form a well-supported group, separated from C. wellsi and P. explanulata. The average distance of C. wellsi from C. columna is 5.5 ± 0.9%, while genetic divergence between P. explanulata and P. contigua is 5.0 ± 0.8%. Thus, even in this case, the two species are distantly related to their supposed congeners. The Fungiidae and C. wellsi and P. explanulata form an unresolved clade due to a large basal polytomy. Nevertheless, all monophyletic groups represented by more than one species are the same as those recovered in the nuclear phylogeny of Fungiidae by Gittenberger et al. (2011) and therefore not discussed again. All the examined specimens of C. wellsi and P. explanulata are in a well-supported group including Pleuractis gravis (Nemenzo, 1955), P. spec. 1 and all Cycloseris species. These two species show a close phylogenetic relationship to Cycloseris, as corroborated by average distances between C. wellsi and Cycloseris (1.4 ± 0.4%) and between P. explanulata and Cycloseris (1.7 ± 0.4%). C. wellsi and P. explanulata form two resolved but not monophyletic lineages due to the presence of Cycloseris sinensis Milne Edwards and Haime, 1851 in the C. wellsi clade, and of Cycloseris costulata (Ortmann, 1889) in the P. explanulata clade.

A reappraisal of the morphology and distribution of Cycloseris explanulata and of C. wellsi is given in the Appendix. Based on the aforementioned molecular evidence and morphologic observations discussed hereafter, the taxonomic position of the two species is revised and both are formally assigned to the genus Cycloseris within the family Fungiidae.


Phylogeny, taxonomy, and distribution of Cycloseris explanulata and Cycloseris wellsi

The joint analyses of the databases of Benzoni et al. (2007) and Gittenberger et al. (2011), and the study of a large collection of specimens of Cycloseris wellsi and C. explanulata (Appendix) confirmed that both species are genetically and structurally more related to each other and to the Fungiidae than to Coscinaraea or Psammocora, the genera to which they originally belonged, respectively (Benzoni et al., 2007). Both species share typical structural characters typical for the Fungiidae (i.e. interstomatous septa, tentacular lobes, fulturae) and which are not found in any other of the taxa ascribed to the Siderastreidae. Conversely, they lack typical structures found in the genera to which they were originally assigned. For example, in both Cycloseris wellsi and C. explanulata the structure of the colony wall is septothecal, the septa are joined by fulturae, and the costae developed, whereas in Psammocora and Coscinaraea the corallum wall is synapticulothecal, the septa are joined by synapticulae and costae are not developed (Benzoni et al., 2007). Furthermore, both these attached and polystomatous taxa share a combination of morphologic characters that are typical of Cycloseris, i.e. a solid corallum wall, the presence of fine and sharp septal margin and lateral septa ornamentation, and of costae covered by fine protuberances (Hoeksema, 1989). Moreover, both the mitochondrial (Fig. 3) and the nuclear marker (Fig. 4) indicate that among the fungiids C. wellsi and C. explanulata are most closely related to species in the monophyletic genus Cycloseris. In particular, all examined specimens of C. wellsi were recovered in the same clade as Cycloseris cyclolites (Lamarck, 1816), the type species of the genus. The phylogenetic trees in Figs. 3 and 4 show complementary information with no conflicting signals. Indeed no species or species groups are found in different or contrasting clades. The only differences concern the resolution of some species groups detected in COI rather than in rDNA trees. In general, the COI phylogenies resolve evolutionary relationships at a more basal taxonomic level detecting four well-supported clades in these corals, namely the Siderastreidae (Complex clade), Sidera­streidae (Robust clade), Psammocoridae, and Fungiidae clades. This is in agreement with the well known slow substitution rate of COI in corals (Hellberg, 2006; Huang et al., 2008). On the contrary, rDNA phylogeny does not recover the monophyly of Fungiidae clade but it is useful to investigate phylogenetic relationships at genus and species level within this clade. While in the mitochondrial cladogram Psammocora explanulata and Coscinaraea wellsi are grouped together with no genetic differentiation in the mitochondrial tree (Fig. 3), in the rDNA cladogram the position of these two species is well-resolved (Fig. 4) due to the higher resolution of ITS1 and ITS2 regions (Chen et al., 2004; Wei et al., 2006).

Despite having been traditionally assigned to two different genera, C. wellsi and C. explanulata are morphologically very similar (Veron and Pichon, 1980; Veron, 2000) (Figs. 1, 6, 8). In the taxonomic literature the former species has been confused with the latter (see the synonymies above) and one of the ‘syntypes’ of C. explanulata (ZMA Coel. 1071, Fig. 8F) is actually a specimen of C. wellsi (cf. UNIMIB KE 404, Fig. 8E). This is not surprising considering the morphological similarity and the co-occurrence of both species in similar environments (also shared with C. mokai) and their overlapping wide Indo-Pacific distribution ranges (Figs. 7 and 9). This being said, C. wellsi has larger calices, more septa reaching the fossa, longer and more winding interstomatous septa, and longer enclosed petaloid septa. Finally, in daytime C. explanulata tentacles are mostly extended (Fig. 1A-D) whilst C. wellsi polyps are mostly retracted (Fig. 1E-H).

On the basis of the examined material, the known geographic distribution ranges of C. explanulata and C. wellsi are updated and extended when compared to those presented by Veron (2000). The distribution ranges of both species show much overlap, extending from eastern Africa and the Red Sea to Hawaii and French Polynesia (Figs. 7, 9). New records for C. wellsi are from the Gulf of Aden (Djibouti and Socotra Island) Kenya and French Polynesia and for C. explanulata from Vietnam, the Line Islands, and New Caledonia (Appendix).

Attached and polystomatous Cycloseris species

Attached species among the Fungiidae appear to be more common than previously assumed (Hoeksema, 1989, 2009). They belong to the genera Cantharellus, Lithophyllon, Podabacia, and Cycloseris (Gittenberger et al., 2011). The phylogenetic and taxonomic position of Cantharellus with three small monostomatous species is uncertain but it is probably closely related to Cycloseris (Hoeksema, 1989; Gittenberger et al., 2011). The genera Lithophyllon and Podabacia consist of polystomatous species, which are foliaceaous and may attain large sizes (Hoeksema, 1989, 1991b, 2009). With the present inclusion of C. explanulata and C. wellsi in the Fungiidae, the number of ten attached species among 50 mushroom coral species (Gittenberger et al., 2011) has increased to 12 among 52.

The earlier inclusion of the encrusting polystomatous species C. mokai in Cycloseris by Gittenberger et al. (2011) was unexpected because Cycloseris originally used to consist of free-living monostomatous species. Specimens of C. mokai are usually found in lower reef slope habitats, mostly above sandy bottoms, where they live attached to the vertical sides of rocks, which may help to prevent burial (Hoeksema, 2012a). The possession of multiple mouths may spread the risk of mouth clogging and feeding obstruction in conditions of heavy sedimentation (Hoeksema, 1991b). From a phylo-ecological perspective, C mokai may be derived from an ancestor that lived on sediment but because it lost the capacity to detach itself (a morphological or life history character state reversal), its vertical distribution range became shallower (an ecological character state reversal) (Hoeksema, in prep.).

Cycloseris explanulata and C. wellsi belong to separate lineages within Cycloseris (Figs. 4 and 5) and their ancestors may have undergone a similar fate as those of C. mokai. According to the present phylogeny reconstruction it appears that all three species had free-living ancestors that lived on sandy substrates in the proximity of lower reef slopes, where they may have settled as planula larvae (see e.g. Hoeksema, 2012a). Moreover, the three species belong to three separate lineages within the genus Cycloseris, each comprising both attached and polystomatous species in addition to free-living and monostomatous corals (Fig. 5). The three attached Cycloseris species are usually small and have many mouths in close proximity to each other, which may be an advantage in conditions of limited substratum surface (Hoeksema, 1991b). The present scenario confirms that homoplasy (convergence), including character reversals from both morphological and ecological perspective, is a common phenomenon among mushroom corals (Hoeksema, 1991b; Gittenberger et al., 2011).


Fig. 5. Detail of the rDNA phylogeny showing the Cycloseris clade (highlighted in grey in Fig. 3) modified to indicate the presence of attached and polystomatous species and free-living and monostomatous species in each of its main lineages (I – III). A) Cycloseris mokai, Prony Bay, New Caledonia, new geographic record (image from the IRD Nouméa Lagplon archive); B) C. tenuis, Sulawesi, Indonesia (photo BWH); C) C. explanulata, Mayotte Island; D) C. costulata, Bali, Indonesia (photo BWH); E) C. wellsi, Bali, Indonesia (photo BWH); F) C. sinensis, Banc Gail, New Caledonia (image from the IRD Nouméa Lagplon archive). Black squares indicate attached and polystomatous taxa, white squares free-living and monostomatous ones. Please note that letters placed after the squares in the tree on the left hand side of the figure correspond to the photo labels on the right hand side.

The present study confirms the utility of re-examining morphological characters in the light of new molecular data as already demonstrated by previous studies (e.g. Budd and Stolarski 2009, 2011; Benzoni et al., 2011). This allowed the re-assignment of two misclassified mushroom corals to the family Fungiidae, based on the re-examination of historical museum material and analyses of new specimens with DNA samples recently collected by the authors (e.g. Djibouti, Kenya, the Line Islands, New Caledonia, Sabah, Yemen). This confirms that historical and new collections of skeletons and DNA are of paramount importance for the development of our knowledge of the diversity, phylogeny, and biogeography of hard corals and other marine organisms (Hoeksema et al., 2011; Karsenti et al., 2011).


The authors are grateful to three anonymous reviewers for constructive critics on the manuscript. We wish to thank D. Obura (CORDIO) for sampling in Kenya and in Chagos. Specimens in New Caledonia were collected for this study thanks to the help of C. Payri (IRD Noumea), G. Lasne, J.L. Menou, J. Butscher, E. Folcher and the RV Alis captain and crew. We thank Michel Pichon (MTQ) and Yannick Geynet (IREMIA) and the Corail Plongée staff for assistance with sampling in La Réunion; E. Dutrieux (CREOCEAN), C.H. Chaineau (Total SA), R. Hirst and M. AbdulAziz (YLNG), M.A. Ahmad and F.N. Saeed (EPA Socotra), C. Riva, A. Caragnano (UNIMIB), and S. Basheen (Professional Divers Yemen) in Yemen; M. Fouda and K.A. Harhash (EEAA), all the Ras Mohammed National Park staff, Y. Khalifa and the Albatros Top Diving staff in Egypt. Sampling in Djibouti was possible thanks to the Tara Oceans scientific expedition and the OCEANS Consortium and to the collaboration of A.O. Dini (l’Aménagement du Territoire et de l’Environnement de Djibouti), M. Jalludin and M. Nabil (CERD) and J-F. Breton (IFAR Djibouti). We are grateful in particular to E. Karsenti (EMBL) for allowing reef research during the expedition, O. Quesnel, S. Kandels-Lewis (EMBL), and Captain O. Marien and the Tara crew in general, and to M. Oriot and S. Audrain in particular. We are also indebted to R. Friederich (World Courier) and R. Troublé (Fonds Tara). The O6 team support is greatly acknowledged. 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 & Développement) for kindly donating part of the UNIMIB laboratory instruments for this study.

Received: 6 October 2011

Revised and accepted: 4 April 2012

Published online: 4 July 2012

Editor: R.W.M. van Soest


Benzoni F. 2007. Le problème des frontières entre espèces chez les coraux scléractiniaires: Le cas du genre Psammocora. Perpignan (France): D. Phil. Thesis, Ecole Pratique des Hautes Etudes.

Benzoni F, Stefani F, Stolarski J, Pichon M, Mitta G, Galli P. 2007. Debating phylogenetic relationships of the scleractinian Psammocora: molecular and morphological evidences. Contributions to Zoology 76: 35-54.

Benzoni F, Stefani F, Pichon M, Galli P. 2010. The name game: morpho-molecular species boundaries in the genus Psammocora (Cnidaria, Scleractinia). Zoological Journal of the Linnean Society 160: 421-456.

Benzoni F, Arrigoni R, Stefani F, Pichon M. 2011. Phylogeny of the coral genus Plesiastrea (Cnidaria, Scleractinia). Contributions to Zoology 80: 231-249.

Budd AF, Stolarski J. 2009. Searching for new morphological characters in the systematics of scleractinian reef corals: comparison of septal teeth and granules between Atlantic and Pacific Mussidae. Acta Zoologica 90: 142-165.

Budd AF, Stolarski J. 2011. Corallite wall and septal microstructure in scleractinian reef corals: comparison of molecular clades within the family Faviidae. Journal of Morphology 272: 66-88.

Budd AF, Romano SL, Smith ND, Barbeitos MS. 2010. Rethinking the phylogeny of scleractinian corals: a review of morphological and molecular data. Integrative and Comparative Biology 50: 411-427.

Cairns SD. 1984. An application of phylogenetic analysis to the Scleractinia: Family Fungiidae. Paleontographica Americana 54: 49-57.

Chen CA, Wallace CC, Wolstenholme J. 2002. Analysis of the mitochondrial 12S rRNA gene supports a two-clade hypothesis of the evolutionary history of scleractinian corals. Molecular Phylogenetics and Evolution 23: 137-149.

Chen CA, Chang CC, Wei NV, Chen CH, Lein YT, Lin HE, Dai CF, Wallace CC. 2004. Secondary structure and phylogenetic utility of the ribosomal internal transcribed spacer 2 (ITS2) in scleractinian corals. Zoological Studies 43: 759-771.

Claereboudt M. 1988. Spatial distribution of fungiid coral population on exposed and sheltered reef slopes in Papua New Guinea. Proceedings of the 6th International Coral Reef Symposium, Townsville, Australia 2: 715-720.

Dai CF, Horng S. 2009. Scleractinia Fauna of Taiwan II. The Robust Group. Taipei: National Taiwan University.

Dana JD. 1846. Zoophytes. U.S. Exploratory Expeditions 1836-1842. 7: 1-740.

De Blainville HMD. 1830. Zoophytes. In: Levrault FG (ed.) Dictionnaire des sciences naturelles, dans lequel on traitre méthodiquement des differéns êtres de la nature, considérés soit en eux-mêmes, d’après l’état actuel de nos connoissances, soit relativement a l’utlité qu’en peuvent retirer la edicine, l’agriculture, le commerce et les arts. Tome 60. Paris: Le Normat.

Drummond AJ, Rambaut A. 2007. "BEAST: Bayesian evolutionary analysis by sampling trees." BMC Evolutionary Biology 7: 214.

Elahi R. 2008. Effects of aggregation and species identity on the growth and behavior of mushroom corals. Coral Reefs 27: 881-885.

Eschscholtz JF. 1824. Bericht über die zoologische Ausbeute während der Reise von Kronstadt bis St. Peter- und Paul. Isis 6: 734-738, pl. 5.

Esper EJC. 1794-98. Die Pflanzenthiere in Ubbildungen nach der Natur. Germany: Kaspeschen, Nürnberg: Raspischen Buchhandlung.

Fenner D. 2005. Corals of Hawaii. Honolulu: Mutual Publishing.

Forskål P. 1775. Descriptiones animalium avium, amphibiorum, piscium, insectorum, vermium; quæ in itinere orientali observavit Petrus Forskål. Hauniae: Heineck et Faber.

Forsman ZH, Barshis DJ, Hunter CL, Toonen RJ. 2009. Shape-shifting corals: molecular markers show morphology is evolutionarily plastic in Porites. BMC Evolutionary Biology 9: 45.

Fukami H, Omori M, Hatta M. 2000. Phylogenetic relationships in the coral family Acroporidae, reassessed by inference from mitochondrial genes. Zoological Science 17: 689-696.

Fukami H, Budd AF, Paulay G, Sole-Cava A, Chen CA, Iwao K, Knowlton N. 2004. Conventional taxonomy obscures deep divergence between Pacific and Atlantic corals. Nature 427: 832-835.

Fukami H, Chen CA, Budd AF, Collins A, Wallace C, Chuang YY, Chen C, Dai CF, Iwao K, Sheppard C, Knowlton N. 2008. Mitochondrial and nuclear genes suggest that stony corals are monophyletic but most families of stony corals are not (order Scleractinia, class Anthozoa, phylum Cnidaria). PLoS ONE 3: e3222.

Gill GA. 1980. The fulturae (“compound synapticulae”), their structure and reconsideration of their systematic value. Acta Palaeontologica Polonica 25: 301-310.

Gittenberger A, Reijnen BT, Hoeksema BW. 2011. A molecularly based phylogeny reconstruction of mushroom corals (Scleractinia: Fungiidae) with taxonomic consequences and evolutionary implications for life history traits. Contributions to Zoology 80: 107-132.

Goffredo S, Chadwick-Furman NE. 2000. Abundance and distribution of mushroom corals (Scleractinia: Fungiidae) on a coral reef at Eilat, northern Red Sea. Bulletin of Marine Science 66: 241-245.

Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by Maximum Likelihood. Systematic Biology 52: 696-704.

Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95-98.

Hellberg ME. 2006. No variation and low synonymous substitution rates in coral mtDNA despite high nuclear variation. BMC Evolutionary Biology 6: 24.

Hoeksema BW. 1989. Taxonomy, phylogeny and biogeography of mushroom corals (Scleractinia: Fungiidae). Zoologische Verhandelingen, Leiden 254: 1-295.

Hoeksema BW. 1991a. Control of bleaching in mushroom coral populations (Scleractinia: Fungiidae) in the Java Sea: stress tolerance and interference by life history strategy. Marine Ecology Progress Series 74: 225-237.

Hoeksema BW. 1991b. Evolution of body size in mushroom corals (Scleractinia: Fungiidae) and its ecomorphological consequences. Netherlands Journal of Zoology 41: 122-139.

Hoeksema BW. 1993. Historical biogeography of Fungia (Pleuractis) spp. (Scleractinia: Fungiidae), including a new species from the Seychelles. Zoologische Mededelingen 67: 639-654.

Hoeksema BW. 2004. Impact of budding on free-living corals at East Kalimantan, Indonesia. Coral Reefs 23: 492.

Hoeksema BW. 2009. Attached mushroom corals (Scleractinia: Fungiidae) in sediment-stressed reef conditions at Singapore, including a new species and a new record. Raffles Bulletin of Zoology Supplement 22: 81-90.

Hoeksema BW. 2012a. Distribution patterns of mushroom corals (Scleractinia: Fungiidae) across the Spermonde Shelf, South Sulawesi. Raffles Bulletin of Zoology 60: 183-212.

Hoeksema BW. 2012b. Mushroom corals (Scleractinia, Fungiidae) of Espiritu Santo (Vanuatu, West Pacific), with the description of a new species. Zoosystema 34: 429-443.

Hoeksema BW, Best MB. 1984. Cantharellus noumeae (gen. nov., spec. nov.), a new scleractinian coral (Fungiidae) from New Caledonia. Zoologische Mededelingen, Leiden 58: 323-328.

Hoeksema BW, Gittenberger A. 2010. High densities of mushroom coral fragments at West Halmahera, Indonesia. Coral Reefs 29: 691.

Hoeksema BW, Koh EGL. 2009. Depauperation of the mushroom coral fauna (Fungiidae) of Singapore (1860s-2006) in changing reef conditions. Raffles Bulletin of Zoology Supplement 22: 91-101.

Hoeksema BW, Matthews JL. 2011. Contrasting bleaching patterns in mushroom coral assemblages at Koh Tao, Gulf of Thailand. Coral Reefs 30: 95.

Hoeksema BW, Moka W. 1989. Species assemblages and phenotypes of mushroom corals (Fungiidae) related to coral reef habitats in the Flores Sea. Netherlands Journal of Sea Research 23: 149-160.

Hoeksema BW, van Ofwegen LP. 2004. Fauna Malesiana (CD ROM), Indo-Malayan Reef Corals: A Generic Overview.

Hoeksema BW, Waheed Z. 2011. Initial phase of autotomy in fragmenting Cycloseris corals at Semporna (eastern Sabah, Malaysia). Coral Reefs 30: 1087.

Hoeksema BW, Yeemin T. 2011. Late detachment conceals serial budding by the free-living coral Fungia fungites in the Inner Gulf of Thailand. Coral Reefs 30: 975.

Hoeksema BW, van der Land J, van der Meij SET, van Ofwegen LP, Reijnen BT, van Soest RWM, de Voogd NJ. 2011. Unforeseen importance of historical collections as baselines to determine biotic change of coral reefs: the Saba Bank case. Marine Ecology 32: 135-141.

Hoeksema BW, van der Meij SET, Fransen CHJM. 2012. The mushroom coral as a habitat. Journal of the Marine Biological Association of the United Kingdom 92: 647-663.

Horst CJ van der. 1921. The Madreporaria of the Siboga Expedition. Part II. Madreporaria Fungiida. Monographe 16b: 1-46, pls. 1-6. Leiden: Brill.

Horst CJ van der. 1922. The Percy Sladen Trust Expedition to the Indian Ocean in 1905, under the leadership of Mr J Stanley Gardiner, M.A. No. IX. Madreporaria: Agariciidae. Transactions of the Linnean Society (2nd Series Zoology) 18: 417-429, pls. 31-32.

Huang D, Meier M, Todd PA, Chou ML. 2008. Slow mitochondrial COI sequence evolution at the base of the Metazoan tree and its implications for DNA barcoding. Journal of Molecular Evolution 66: 167-174.

Huang D, Meier R, Todd PA, Chou LM. 2009. More evidence for pervasive paraphyly in scleractinian corals: systematic study of Southeast Asian Faviidae (Cnidaria; Scleractinia) based on molecular and morphological data. Molecular Phylogenetics and Evolution 50: 102-116.

Huang D, Licuanan WY, Baird AH, Fukami H. 2011. Cleaning up the ‘Bigmessidae’: Molecular phylogeny of scleractinian corals from Faviidae, Merulinidae, Pectiniidae and Trachyphylliidae. BMC Evolutionary Biology 11: 37.

Huelsenbeck JP, Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755.

Karsenti E, Acinas SG, Bork P, Bowler C, De Vargas C, Raes J, Sullivan M, Arendt D, Benzoni F, Follows M, Jaillon O, Gorsky G, Hingamp P, Iudicone D, Kandels-Lewis S, Krzic U, Not F, Ogata H, Pesant S, Reynaud E, Sardet C, Sieracki M, Speich S, Velayoudon D, Weissenbach J, Wincker P, and the Tara Oceans Consortium. 2011. A holistic approach to marine eco-systems biology. PLoS Biology 9: e1001177.

Kerr AM. 2005. Molecular and morphological supertree of stony corals (Anthozoa: Scleractinia) using matrix representation parsimony. Biological Reviews 80: 543-558.

Kitahara MV, Cairns SD, Stolarski J, Blair D, Miller DJ. 2010. A comprehensive phylogenetic analysis of the Scleractinia (Cnidaria, Anthozoa) based on mitochondrial CO1 sequence data. PLoS One 5(7): e11490.

Lamarck JBP. 1801. Système des Animaux sans vertèbres, ou Tableau général des classes, des ordres et des genres de ces animaux; présentant leurs caractères essentiels et leur distribution d’après les considérations de leurs rapports naturels et de leur organisation, et suivant l’arrangement établi dans les galeries du Muséum d’Histoire naturelle, parmi leurs dépouilles conservées ; précédé du Discours d’ouverture de l’an VIII de la République. Paris: Déterville.

Lamarck JBP. 1816. Histoire naturelle des animaux sans vertèbres. Vol. 2, Verdier, Paris.

Le Goff-Vitry MC, Rogers AD, Baglow D. 2004. A deep-sea slant on the molecular phylogeny of the Scleractinia. Molecular Phylogenetics and Evolution 30: 167-177.

Librado P, Rozas J. 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.

Marenzeller E. 1901. Ostafrikanische Steinkorallen. Mitteilungen Aus Dem Naturhistorischen Museum in Hamburg 18: 117-134.

Meij SET van der, Visser RR. 2011. The Acropora humilis group (Scleractinia) of the Snellius expedition (1929-30). Raffles Bulletin of Zoology 59: 9-17.

Meij SET van der, Suharsono, Hoeksema BW. 2010. Long-term changes in coral assemblages under natural and anthropogenic stress in Jakarta Bay (1920-2005). Marine Pollution Bulletin 60: 1442-1454.

Milne Edwards M, Haime J. 1848. Recherches sur les polypiers. Mém. 1. Observations sur la structure et le dévelopment des polypiers en général. Annales Des Sciences Naturelles 9: 37-89.

Milne Edwards M, Haime J. 1849. Memoire sur las polypiers appartenant a la famille des oculinides, au groupe intermediaire des pseuastreides et a la famille des fongides. Comptes rendus de l’Académie des Sciences 29: 67-73.

Milne Edwards M, Haime J. 1851. Recherches sur les polypiers; 6me mémoire. Monographie des fongides. Annales Des Sciences Naturelles 15: 73-144.

Nemenzo F. 1955. Systematic studies on Philippine shallow water scleractinians: I. Suborder Fungiida. Natural and Applied Science Bulletin 15: 3-84.

Nishihira M, Poung-In S. 1989. Distribution and population structure of a free‑living coral, Diaseris fragilis, at Khang Khao Island in the Gulf of Thailand. Galaxea 8: 271-282.

Nishihira M, Veron JEN. 1995. Corals of Japan. Kaiyusha Publishers Co. Ltd, Tokyo (in Japanese).

Nunes F, Fukami H, Vollmer SV, Norris RD, Knowlton N. 2008. Re-evaluation of the systematics of the endemic corals of Brazil by molecular data. Coral Reefs 27: 423-432.

Nylander JAA. 2004. MrModeltest v2. Evolutionary Biology Centre, Uppsala University.

Ortmann A. 1889. Beobachtungen an Steinkorallen von der Südküste Ceylons. Zoologischen Jahrbüchern. Abtheilungfür Systematik, Geographic und Biologie der Thiere 4: 493-590.

Pichon M. 1971. Comparative study of the main features of some coral reefs of Madagascar, Reunion and Mauritius. Symposia of the Zoological Society of London 28: 185-216.

Pichon M, Benzoni F, Chaineau CH, Dutrieux E. 2010. Field guide of the hard corals of the southern coast of Yemen. Paris: Biotope.

Posada D, Buckley TR. 2004. Model selection and model averaging in phylogenetics: advantages of the AIC and Bayesian approaches over likelihood ratio tests. Systematic Biology 53: 793-808.

Quelch JJ. 1884. Preliminary notice of new genera and species of Challenger reef-corals. Annals and Magazine of Natural History 13: 292-297.

Rehberg H. 1892. Neue and wenig bekannte Korallen. Abhandlungen aus dem Gebiete der Naturwissenschaften Hamburg 12: 1-50.

Romano SL, Cairns SD. 2000. Molecular phylogenetic hypotheses for the evolution of scleractinian corals. Bulletin of Marine Science 67: 1043-1068.

Romano SL, Palumbi RS. 1996. Evolution of scleractinian corals inferred from molecular systematics. Science 271: 640-642.

Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.

Scheer G, Pillai CSG. 1983. Report on the stony corals from the Red Sea. Zoologica, (Stuttgart) 133: 1-198.

Sheppard CRC, Sheppard ALS. 1991. Corals and coral communities of Saudi Arabia. Fauna of Arabia 12: 1-170.

Stefani F, Benzoni F, Pichon M, Cancelliere C, Galli P. 2007. A multidisciplinary approach to the definition of species boundaries in branching species of the coral genus Psammocora (Cnidaria, Scleractinia). Zoologica Scripta 37: 71-91.

Stefani F, Benzoni F, Pichon M, Mitta G, Galli P. 2008. Genetic and morphometric evidence for unresolved species boundaries in the coral genus Psammocora (Cnidaria; Scleractinia). Hydrobiologia 596: 153-172.

Stefani F, Benzoni F, Sung Yin Y, Pichon M, Galli P, Chen CA. 2011. Comparison of morphological and genetic analyses reveal cryptic divergence and morphological plasticity in Stylophora (Cnidaria, Scleractinia). Coral Reefs 30: 1033-1049.

Stolarski J, Roniewicz E. 2001. Towards a new synthesis of evolutionary relationships and classification of Scleractinia. Journal of Paleontology 75: 1090-1108.

Stolarski J, Kitahara MV, Miller DJ, Cairns SD, Mazur M, Meibom A. 2011. The ancient evolutionary origins of Scleractinia revealed by azooxanthellate corals. BMC Evolutionary Biology 11: 316.

Swofford DL. 2003. PAUP* Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4.b.10. Sunderland, Massachusetts, Sinauer Associates.

Takabayashi M, Carter DA, Loh WKT, Hoegh-Guldberg O. 1998. A coral-specific primer for PCR amplification of the internal transcribed spacer region in ribosomal DNA. Molecular Ecology 7: 925-931.

Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596-1599.

Turak E, DeVantier L. 2011. Field guide to reef-building corals of Brunei Darussalam. Brunei Darussalam, Ministry of Industry and Primary Resources.

Vaughan TW, Wells JW. 1943. Revision of the suborders, families, and genera of the Scleractinia. Geological Society of America, Special Paper 44: 1-363.

Veron JEN. 1986. Corals of Australia and the Indo-Pacific. Angus and Robertson, North Ryde, Australia.

Veron JEN. 2000. Corals of the world. Townsville: Australian Institute of Marine Science.

Veron JEN, Pichon M. 1976. Scleractinia of Eastern Australia Families Thamnasteriidae, Astrocoeniidae, Pocilloporidae. Australian Institute of Marine Sciences Monograph Series 1: 1-86.

Veron JEN, Pichon M. 1980. Scleractinia of Eastern Australia Families Agaraciidae, Siderastreidae, Fungiidae, Oculinidae, Merulinidae, Mussidae, Pectiniidae, Caryophylliidae, Dendrophylliidae. Australian Institute of Marine Sciences Monograph Series 4: 1-471.

Verrill AE. 1864. List of polyps and corals sent by the Museum of. Comparative Zoology to other Institutions in exchange, with annotations. Bulletin of the Museum of Comparative Zoology 1: 29-60.

Wallace CC, Chen CA, Fukami H, Muir PR. 2007. Recognition of separate genera within Acropora based on new morphological, reproductive and genetic evidence from Acropora togianensis, and elevation of the subgenus Isopora Studer, 1878 to genus (Scleractinia: Astrocoeniidae; Acroporidae). Coral Reefs 26: 231-239.

Wei NV, Wallace CC, Dai CF, Moothien Pillay KR, Chen CA. 2006. Analyses of the ribosomal internal transcribed spacers (ITS) and the 5.8S gene indicate that extremely high rDNA heterogeneity is a unique feature in the scleractinian coral genus Acropora (Scleractinia; Acroporidae). Zoological Studies 45: 404-418.

Wells JW. 1954. Recent corals of the Marshall Islands. United States Geological Survey professional paper 260-1: 385-486.

Wells JW. 1966. Evolutionary development in the scleractinian family Fungiidae. Symposium of the Zoological Society of London 16: 223-246.

White TJ, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols. A Guide to Methods and Application. San Diego, California, USA: Academic Press Inc.

Yamashiro H, Nishihira M. 1998. Experimental study of growth and asexual reproduction in Diaseris distorta (Michelin, 1843) a free-living fungiid coral. Journal of Experimental Marine Biology and Ecology 225: 253-267.


A reappraisal of the morphology and distribution of Cycloseris explanulata and Cycloseris wellsi

Family Fungiidae Dana, 1846

Genus Cycloseris Milne Edwards and Haime, 1849

For a complete diagnosis of this genus refer to Hoeksema (1989).

Cycloseris explanulata (van der Horst, 1922)

Psammocora explanulata van der Horst (1922: partim pl. 32, figs. 7-8); Wells (1954: pl. 157, figs. 9-10); Veron and Pichon (1976: 28-30, figs. 27-32); Scheer and Pillai (1983: 20, pl. 1, fig. 9); Sheppard and Sheppard (1991: 81, fig. 69, pl. 48); Veron (1986: 277); Veron (2000); Fenner (2005: 72); Pichon et al. (2010: 212-213, figs. 1-4); Turak and DeVantier (2011: p. 105).

Lithophyllon mokai - sensu Hoeksema and van Of­wegen (2004) partim; Veron (2000: 306).

Psammocora sp. Hoeksema and van Ofwegen (2004) partim

Examined material

Type material: BMNH 1937.11.17.69 (Lectotype, present designation) Providence, Seychelles (coll. J.S. Gardiner) 91.5-142 m; BMNH 1937.11.17.116 (Paralectotype) Providence, Seychelles (coll. J.S. Gardiner) 53 m; ZMA Coel.1072 (Paralectotype) Providence, Seychelles, 106-142.6 m.

Other material: Egypt, AIMS unregistered (coll. J.E.N. Veron). Saudi Arabia, NHM 1991.6.4.67 Yambu (coll. C.R.C. Sheppard) 15 m; MTQ G 57709 Sharm Jozai, Duba (26°57.6’ N 35°58.0’ E) 07.vii.1998 (coll. E. Turak, L. Devantier). Yemen, UNIMIB BU018 Burum (14°19.710’ N 48°59.903’ E) 22.iii.2008 (coll. F. Benzoni, M. Pichon); UNIMIB BU067 Burum (14°18.421’ N 48°58.068’ E) 19.iii.2009 (coll. F. Benzoni, M. Pichon); UNIMIB BA116 Sikha Island, Bir Ali (13°55.648’ N 48°23.234’ E) 22.xi.2008 (coll. F. Benzoni, S. Montano) 20 m. Socotra, EPA/Senckenberg C138S Kal Farun (12°26.4’ N 52°08.9’ E) 11.iv.1999; MTQ G 57712 Kal Farun (12°26.4’ N 52°08.9’ E) 11.iv.1999 (coll. L. Devantier); UNIMIB SO079 Hawlaf (12°40.808’ N 54°04.504’ E) 14.iii.2010 (coll. F. Benzoni, A. Caragnano); UNIMIB SO138 Qeso shore (12°40.212’ N 53°26.893’ E) 18.iii.2010 (coll. F. Benzoni, A. Caragnano) 7 m. Seychelles, RMNH Coel.19095 Bird Island (03°42’ S 55°12’ E) 21.xii.1992 (coll. B.W. Hoeksema) 8-21 m; RMNH Coel.19096 Alphonse Atoll (07°00’ S 52°43’ E) 03.i.1993 (coll. B.W. Hoeksema); RMNH Coel.19094 Aride Island (04°13’ S 55°40’ E 18/19.xii.1992) (coll. B.W. Hoeksema); RMNH Coel.19097 Alphonse Atoll (07°02’ S 52°44’ E) (coll. B.W. Hoeksema) 8 m. Mayotte, MNHN 20360 Banc de la Zélée, (12°25.6’ S 46°16.2’ E) 09.iv.1973 (coll. G. Faure) 32-52 m; UNIMIB MA 243, 2004 (coll. F. Seguin); UNIMIB MA 447 (12°47.602’ S 44°58.860’ E) 16.iv.2005 (coll. F. Benzoni); UNI­MIB MA 449 Banc de Boa (12°41.178’ S 45°02.296’ E) 18.iv.2005 (coll. F. Benzoni) 16 m; UNIMIB MA 451B (12°50.183’ S 44°56.488’ E) 19.iv.2005 (coll. F. Benzoni) 17 m; UNIMIB MA 453 Moutsoumbatsou (12°50.183’ S 44°56.488’ E) 19.iv.2005 BA (coll. D. Obura) 22 m; UNIMIB MA 454 Moutsoumbatsou (12°50.183’ S 44°56.488’ E) 19.iv.2005 (coll. F. Benzoni) 19 m; UNIMIB MA 461 Faro Boueni (12°54.684’ S 44°58.089’ E) 22.iv.2005 (coll. F. Seguin); UNI­MIB MA463 Faro Boueni (12°54.684’ S 44°58.089’ E) 22.iv.2005 (coll. F. Benzoni) 12 m; UNIMIB TO MY124 (12°52.534’ N 45°16.834’ E) (coll. F. Benzoni); UNIMIB TO MY138 (12°53.980’ N 45°15.416’ E) (coll. F. Benzoni); UNIMIB TO MY142 (12°53.980’ N 45°15.416’ E) (coll. F. Benzoni). La Réunion, MNHN 20357 St. Gilles, 14.ix.1973 (coll. G. Faure); MNHN 20358 St. Gilles, 26.viii.1976 (coll. G. Faure); UNIMIB REU513 Petit Moteur, St. Gilles, 01.xi.2005 (coll. F. Benzoni, M. Pichon); MNHN 20359 (coll. G. Faure). Madagascar, MNHN 20389, Tuléar (coll. M. Pichon). Maldives, UNIMIB M014 Bulhalafushi 27.iv.2004 (coll. F. Benzoni) 15 m. Chagos, NHM TWCMS H11910 Ile de Coin, Peros Banhos, 1978, 22 m; NHM TWCMS H11916 Ile de Coin, Peros Banhos, 1978; NHM TWCMS H11925 Ile de Coin, Peros Banhos, 1978; NHM TWCMS C14748, 1975, 38 m; UNIMIB CHA521 I. Diamant, Peros Banhos, 11.iii.2006 (coll. D. Obura) 20 m; UNIMIB CHA522 I. Diamant, Peros Banhos, 11.iii.2006 (coll. D. Obura) 20 m; UNIMIB CHA524 I. Puole, Peros Banhos, 12.iii.2006 (coll. D. Obura) 20 m; UNIMIB CHA525 Eagle Islands 13.iii.2006 (coll. D. Obura) 21 m; UNIMIB CHA540 I. Passe, Peros Banhos 10.iii.2006 (coll. D. Obura) 19 m. Thailand, NHM 1977.2.25.17, Pangah Bay, 19.ix.1975 (coll. H. Ditlev) 10 m. Indonesia, RMNH Coel.33609 S coast of Erie, Ambon (03°45’ S 128°08’ E) 12.xi.1996 (coll. B.W. Hoeksema); RMNH Coel.33643 Ambon (03°43’ S 128°16’ E), (coll. B.W. Hoeksema) 15-20 m; MTQ G 57718 Bunaken Island, Sulawesi (01°38’ N 124°45’ E) 22.vii.2002 (coll. E. Turak); MTQ G 57719 Manado Tua, Sulawesi (01°38’ N 124°43’ E) 21.vii.2003 (coll. E. Turak); RMNH Coel.23308 Padang, Sumatra, 27.iv.1995 (coll. B.W. Hoeksema). Australia, AIMS 1813 Orpheus, Palm Island (coll. J.E.N. Veron); AIMS 1804 Orpheus, Palm Island (coll. J.E.N. Veron); JCU 3243 Lizard Island (coll. M. Pichon). New Caledonia, IRD HS 1397 N’Goë, Toupeti, Côte Oubliée (21°37.4117’ S 166°26.7299’ E) 17.iii.07 (coll. F. Benzoni, G. Lasne) 10-15 m; IRD HS 1769 Cap Goulevin (21°32.294’ S 165°14°286’ E) 01.xi.2007 (coll. F. Benzoni, G. Lasne) 33 m. Marshall Islands, USNM 44820 Bikini, 1954 (coll. J. Wells); MTQ G 57309 Dog tooth point, Rongelap (11°46.7’ N 166°86.6’ E) 13.vii.2003 (coll. Z. Richards); MTQ G 56300 Rongelap (11°31. 2’ N 166°50.5’ E) 02.viii.2002 (coll. Z. Richards); RMNH Coel.14545 Enewetak Atoll, xii.1976. Line Islands, UNIMIB LI490 Kiritimati Kir-09, 08.viii.2005 (coll. D. Obura) 10-17 m; UNIMIB LI493 Kiritimati Kir-11, 09.viii.2005 (coll. D. Obura) 10-17 m. French Polynesia, MNHN 20326 Baie d’Opunohu, Moorea, Society Islands (coll. J.P. Chevalier).

Morphology. Animals polystomatous. Corallum attached, generally thinly encrusting and following the underlying substrate (Fig. 1A-D). Colonies irregular in outline although smaller colonies can be circular (Fig. 1A). Calices scattered over the corallum surface without any particular arrangement (Fig. 6), they can be more closely packed (Fig. 6D) or more distant (Fig. 6B). Calice diameter between 2.6 and 3.1 mm. Thicker and more exsert septa (five to seven) alternate with thinner septa flush with the corallum surface. The former are mostly petaloid in shape (Fig. 6). Continuous septa going from one fossa to the other between adjacent calices, previously referred to as septocostae (Van der Horst, 1921, 1922; Veron and Pichon, 1976), can be observed in some specimens (Fig. 6A-D; Veron and Pichon, 1976, Figs 28, 31-32). These are actually interstomatous septa (Benzoni, 2007) homologous to those found in the Fungiidae (sensu Hoeksema, 1989). Enclosed petaloid septa derived from the alternate fusion of lower and higher order septa are found between calices like in the genus Psammocora Dana, 1846 (Benzoni et al., 2007, 2010). They range from 1.4 to 1.7 mm in length (Benzoni, 2007). Morphologic affinities between the pattern of septa fusion in C. explanulata and in the fungiid genus Polyphyllia Blainville, 1830 have been remarked by Van der Horst (1922) in the original species description. While enclosed septa with a petaloid outline are always observed in C. explanulata, interstomatous septa are developed in some specimens (Fig. 6E-H), and are mostly found between closely neighboring corallites (Veron and Pichon, 1976, Figs 31-32), i.e. less than one calice away from each other. Exsert tentacular lobes are typically found on top of thicker septa and enclosed petaloid septa in this species (Fig. 6). Septal margins are ornamented by ridges composed of short series of minute granules oriented transversally to the septal plane forming distinct septal paddles (Benzoni et al. 2007, Fig. 3G). Septal sides are ornamented by minute granules. Septa in C. explanulata are connected by buttress-like structures developing below the septal edge and joining the septa sides (Benzoni et al. 2007, Fig. 5B). These structures defined as fulturae are typical for the Fungiidae (see Gill, 1980, pl.1:1 for Fungia Lamarck, 1801; Hoeksema, 1989, Fig. 652 for Herpolitha Eschscholtz, 1824; Fig. 656 for Sandalolitha Quelch, 1884; Fig. 664 for Lithophyllon Rehberg, 1892). Fulturae differ from the synapticulae found, inter alia, in the Siderastreidae which are typically isolated from each other and are often developed near the septal edge (Gill, 1980). Columella always present, papillary, and formed by six to 15 tightly packed vertical processes all of the same size (Fig. 6H). Colony wall septothecal and compact. Costae are found on the lower side of the corallum, they are small and ornamented by minute rounded granulations. Unfortunately, they are often obscured due to the attached growth mode, and by the incrustations of crustose coralline algae and invertebrates. These are small and ornamented by minute rounded granulations.


Fig. 6. Morphology and variability of skeletal structures in Cycloseris explanulata A) Lectotype (NHM 1937.11.17.69) Providence, Seychelles (91.5-142 m); B) Paralectotype (ZMA Coel. 1072) Providence, Seychelles (106-142.6 m); C) specimen IRD HS 1769 from Cap Goulevin, New caledonia (33 m) (same specimen as in Fig. 4B); D) specimen UNIMIB LI490 Kiritimati, Line Islands; E) specimen MNHN 20358 St. Gilles, La Réunion; F) specimen NHM TWCMS H11910 from Ile de Coin, Peros Banhos, Chagos (22 m); G) specimen UNIMIB MA 451B from Mayotte; H) specimen UNIMIB MA 461 from Faro Boueni, Mayotte.

Geographical distribution. Cycloseris explanulata occurs throughout the Indo-Pacific. Based on the present material and published illustrations it is recorded from Egypt, Saudi Arabia, Yemen, Socotra Island, Maldives, Chagos, Seychelles, Mayotte, Madagascar, La Réunion, Thailand, Indonesia, Vietnam, Papua New Guinea, Australia, New Caledonia, the Marshall Islands, Hawaii, the Line Islands, and French Polynesia (Fig. 7).


Fig. 7. Records of Cycloseris explanulata. The star indicates type locality, grey circles indicate records from specimens examined in this study, and empty circles figures from published illustrations.

Cycloseris wellsi (Veron and Pichon, 1980)

Psammocora explanulata Van der Horst, 1922 partim; Veron (2000: p. 156, Figs. 1-2)

Coscinaraea ostraeformis - sensu Wells (1954: pl. 155, Figs 5-6), not van der Horst (1922)

Coscinaraea wellsi Veron and Pichon (1980); Nishihira and Veron (1995); Veron (1986: p. 284); Veron (2000: p. 167); Hoeksema and van Ofwegen (2004); Fenner (2005: 71); Turak and DeVantier (2011: p. 110)

Lithophyllon mokai - sensu Hoeksema and van Ofwegen (2004) partim

Examined material

Type material: USNM 44818 (Holotype) Bikini Atoll, Ralik Chain, Marshall Islands, 14.viii.1947 (coll. J.W. Wells) 53.38-76.25 m.

Other material: Egypt, UNIMIB S 060 Ras Nosrani, South Sinai (27°57.989’ N 34°25.190’ E) 16.v.2004 (coll. F. Benzoni) 20 m; UNIMIB S 061 Ras Nosrani, South Sinai (27°57.989’ N 34°25.190’ E) 16.v.2004 (coll. F. Benzoni) 24 m; UNIMIB S 062 Ras Nosrani, South Sinai (27°57.989’ N 34°25.190’E) 16.v.2004 (coll. F. Benzoni) 23.5 m. Israel, RMNH Coel.24180 Eilat, Gulf of Aqaba 20.iv.1996 (coll. S. Goffredo) 45 m. Djibouti, UNIMIB TO DJ043 Oblal (11°51.680’ N 43°06.480’ E) 28.i.2010 (coll. F. Benzoni) 10 m; UNI­MIB TO DJ099 Kalaf, Ablali (11°43.787’ N 42°46.417’ E) 29.i.2010 (coll. F. Benzoni) 15 m; UNIMIB TO DJ176 Maskali (11°43.064’ N 43°09.359’ E) 01.ii.2010 (coll. F. Benzoni) 18 m. Yemen, UNIMIB MU095 Al Mukallah (14°31.067’ N 49°10.335’ E) 18.iii.2007 (coll. F. Benzoni, M. Pichon); UNIMIB MU102 Al Mukallah (14°31.067’ N 49°10.335’ E) 18.iii.2007 (coll. F. Benzoni, M. Pichon); UNIMIB MU164 Al Mukallah (14°30.793’ N 49°10.339’ E) 20.iii.2007 (coll. F. Benzoni, M. Pichon) 18 m; UNIMIB BU017 Burum (14°19.710’ N 48°59.903’ E) 22.iii.2008 (coll. F. Benzoni, M. Pichon). Socotra, UNIMIB SO051 Ras Adho (12°38.672’ N 54°16.043’ E) 13.iii.2010 (coll. F. Benzoni, M. Pichon). Kenya, UNIMIB KE403 Kiunga, 14.iii.2005 (coll. D. Obura); UNIMIB KE404 Cha Chano, 12.iii.2005 (coll. D. Obura); UNIMIB KE405 Kiunga, 12.iii.2005 (coll. D. Obura). Seychelles, ZMA Coel.1071 (Syntype of Psammocora explanulata) Amirante, Seychelles, 11.x.1905, >36.5 m. Mayotte, UNIMIB MA 452B (12°50.183’ S 44°56.488’ E) 19.iv.2005 (coll. F. Benzoni, M. Pichon); UNIMIB MA 465 Passe Bateaux (12°59.530’ S 44°59.136’ E) 23.iv.2005 (coll. F. Benzoni, D. Obura); UNIMIB MA 478 pointe Paskélé (13°00.350’ S 45°07.208’ E) 26.iv.2005 (coll. D. Obura); UNIMIB TO MY123 (12°52.534’ N 45°16.834’ E) (coll. F. Benzoni) 22 m. La Réunion, MNHN 470 (partim, only larger specimen), 1841 (coll. L. Rousseau). Thailand, UNIMIB LP 191 Laem Pakarang, Khao Lak (08°43.612’ N 98°13.121 E) 12.xii.2006 (coll. F. Benzoni, D. Basso) 16 m. Vietnam, AIMS unregistered 27 (coll. J.E.N. Veron). Malaysia, RMNH Coel.39965 Singamata Pancang, Semporna region, eastern Sabah (04°31.350’N 118°37.001’ E) 12.xii.2010 (coll. B.W. Hoeksema) 20 m. Indonesia, UNIMIB I 080 Mapia House Reef, Manado, Sulawesi (01°27.527’ N 124°46.007’ E) (coll. F. Benzoni) 23 m; UNIMIB I 108 Negheri, Manado Tua, Sulawesi (01°36.902’ N 124°42.020’ E) (coll. F. Benzoni) 38 m; UNIMIB I 114 Molas Ship Wreck, Molas, Sulawesi (01°31.906’ N 124°49.518’ E) (coll. F. Benzoni). Japan, AIMS 12017 Tosa­shimizu, Shikoku (coll. J.E.N. Veron). Australia, MTQ G 59726 Lord Howe Island (31°28’ S 159°09’ E); MTQ G 45740 Murray Islands, Queensland (09°55’ S 144°05’ E) 10-25 m; MTQ G 45737 Maer Island, Murray Islands, Queensland (09°55’ S 144°05’ E) 0-15 m; AIMS (BOX45) unregistered, Elizabeth Middleton Reef loc. 474. New Caledonia, IRD HS 2081 Ile Longue ST1159, Chesterfield Islands (19°52.710’ S 158°18.720’ E) 11.vii.2008 (coll. G. Lasne) 65 m. French Polynesia, MNHN unregistered, Tubua’i, Austral Islands, v.1979 (coll. J.P. Chevalier) 100 m («Marara» dredging).

Morphology. Animals polystomatous. Corallum attached (Fig. 1E-H). Colonies are encrusting and with a circular or oval outline (Fig. 1E-F), their margins sometimes detached from the substratum (Fig. 1E, G). Calices scattered over the corallum surface or in a serial arrangement especially towards the margins (Fig. 1F, G; Fig. 8). Calice diameter between 3.5 and 5.1 mm. Septa unequal and alternating, thicker septa may be more exsert than thinner ones (Fig. 8C). Six to 10 thicker septa may reach the fossa (Fig. 8). Interstomatous septa between calices up to 1.3 calices away from each other. In some corallites all septa reaching the fossa can be interstomatous (Fig. 8G). Elongated enclosed petaloid septa running parallel to interstomatous septa over the corallum surface are also commonly observed. These can be short and straight (Fig. 8C-E) or long and attain irregular shapes (Fig. 8H). Exsert tentacular lobes are typically observed on top of thicker septa and of enclosed petaloid septa, and at both ends of interstomatous septa in the holotype and in many specimens (Fig. 8B-C). However, they can be reduced and barely visible in other specimens (Fig. 8D-F). Septal margins are ornamented by septal paddles (Benzoni et al., 2007, Fig. 4B). Septal sides are ornamented by minute granules. Septa in C. wellsi are connected by fulturae (Benzoni et al., 2007, Fig. 5C). Columella always present, papillary, and formed by nine to 21 tightly packed vertical processes of equal size (Fig. 8H). Colony wall septothecal and compact, ornamented by fine costae (Veron and Pichon, 1980). Costae in C. wellsi and their ornamentation are very similar to those of Lithophyllon mokai (Hoeksema, 1989: Fig. 594).

Distribution. Cycloseris wellsi occurs throughout the Indo-Pacific. Based on the present material and published illustrations C. wellsi has been recorded from Egypt, Djibouti, Yemen, Socotra Island, Kenya, Seychelles, Mayotte, La Réunion, Thailand, Indonesia, Vietnam, Malaysia, Philippines, Taiwan, Japan, Papua New Guinea, Australia, New Caledonia, Hawaii, and French Polynesia (Fig. 9).


Fig. 8. Morphology and variability of skeletal structures in Cycloseris wellsi A-B) Holotype (USNM 44818) Bikini Atoll, Marshall Islands (53.38-76.25 m); C) specimen IRD HS 2081 Chesterfield Islands, New Caledonia; D) specimen UNIMIB MU102 Al Mukallah, Yemen; E) specimen UNIMIB KE 404 Kiunga, Kenya; F) ZMA Coel. 1071 (‘Syntype’ of Psammocora explanulata) Amirante, Seychelles (> 36.5 m); G) specimen UNIMIB S 061 Ras Nosrani, South Sinai, Egypt (24 m); specimen UNIMIB I 080 Mapia House Reef, Manado, Sulawesi (23 m).


Fig. 9. Records of Cycloseris wellsi. The star indicates type locality, grey circles indicate records from specimens examined in this study, and empty circles figures from published illustrations.