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Research Article
A new genus of soft coral (Octocorallia, Malacalcyonacea, Cladiellidae) and three new species from Indo-Pacific coral reefs
expand article infoCatherine S. McFadden‡, Yehuda Benayahu§, Kaveh Samimi-Namin|#
‡ Harvey Mudd College, Claremont, United States of America
§ Tel Aviv University, Tel Aviv, Israel
| Natural History Museum, London, United Kingdom
¶ Marine Evolution and Ecology Group, Naturalis Biodiversity Center, Leiden, Netherlands
# University of Oxford, Oxford, United Kingdom

Corresponding author: Catherine S. McFadden ( mcfadden@hmc.edu )

Academic editor: James Reimer
© 2024 Catherine S. McFadden, Yehuda Benayahu, Kaveh Samimi-Namin.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: McFadden CS, Benayahu Y, Samimi-Namin K (2024) A new genus of soft coral (Octocorallia, Malacalcyonacea, Cladiellidae) and three new species from Indo-Pacific coral reefs. ZooKeys 1188: 275-304. https://doi.org/10.3897/zookeys.1188.110617
ZooBank: urn:lsid:zoobank.org:pub:528120A6-2EC0-4796-B37B-5E51FD1FE7AA
Open Access

Abstract

Molecular systematic studies of the anthozoan class Octocorallia have revealed widespread incongruence between phylogenetic relationships and taxonomic classification at all levels of the Linnean hierarchy. Among the soft coral taxa in order Malacalcyonacea, the family Alcyoniidae and its type genus Alcyonium have both been recognised to be highly polyphyletic. A recent family-level revision of Octocorallia established a number of new families for genera formerly considered to belong to Alcyoniidae, but revision of Alcyonium is not yet complete. Previous molecular studies have supported the placement of Alcyonium verseveldti (Benayahu, 1982) in family Cladiellidae rather than Alcyoniidae, phylogenetically distinct from the other three genera in that family. Here we describe a new genus, Ofwegenum gen. nov. to accommodate O. verseveldti comb. nov. and three new species of that genus, O. coronalucis sp. nov., O. kloogi sp. nov., and O. colli sp. nov., bringing the total number of species in this genus to four. Ofwegenum gen. nov. is a rarely encountered genus so far known from only a few locations spanning the Indian and western Pacific Oceans. We present the morphological characters of each species and use molecular data from both DNA barcoding and target-enrichment of conserved elements to explore species boundaries and phylogenetic relationships within the genus.

Key words

DNA barcoding, molecular phylogeny, new combination, northern Red Sea, Ofwegenum gen. nov., Oman, Réunion, sclerites, target-enrichment, taxonomy, ultraconserved elements

Introduction

Zooxanthellate soft corals belonging to the octocorallian order Malacalcyonacea are among the most common, conspicuous, and ecologically important sessile organisms on shallow-water coral reefs throughout the Indo-Pacific; on some reefs, total percent cover of soft corals may exceed that of the reef-building scleractinian corals (Tursch and Tursch 1982; Dinesen 1983; Dai 1991; Fabricius 1997; Fabricius and Dommisse 2000). Despite their ubiquity, the taxonomy of even the most common genera of soft corals is poorly understood, and until recently a majority of the large, fleshy, zooxanthellate genera that dominate space on shallow reefs were classified in family Alcyoniidae Lamouroux, 1812 (Fabricius and Alderslade 2001). This family, along with its type genus Alcyonium Linnaeus, 1758, has long been a repository for genera and species whose morphological characters do not cleanly fit the diagnoses of other families (Alderslade 2000; Williams 2000; McFadden and van Ofwegen 2013). A recent revision of class Octocorallia based on novel phylogenomic evidence has now re-circumscribed Alcyoniidae to include only azooxanthellate and mostly cold-water taxa (McFadden et al. 2022). New families have been established and previously suppressed families reinstated to accommodate the tropical genera formerly considered to be alcyoniids (McFadden et al. 2022), and some species of Alcyonium have been transferred to new genera and families (Alderslade 2000; Williams 2000; McFadden and Hochberg 2003; McFadden and van Ofwegen 2013, 2017). Revision of Alcyonium is, however, far from complete, and among the species still classified in that genus is A. verseveldti (Benayahu, 1982), originally described as Metalcyonium verseveldti, a rare species known only from a few collections in the Red Sea. Molecular phylogenetic studies suggest that this species belongs to family Cladiellidae McFadden, van Ofwegen & Quattrini, 2022, but not to any of the established genera within that family (i.e., Cladiella Gray, 1869, Klyxum Alderslade, 2000, and Aldersladum Benayahu & McFadden, 2011; see Benayahu et al. 2012; McFadden et al. 2022).

Pfeffer (1889) established the genus Metalcyonium (Octocorallia, Alcyoniidae) for two species of soft corals from South Georgia, M. clavatum Pfeffer, 1888 and M. capitatum Pfeffer, 1888, without designating a type species. His description of this genus lacked much detail, merely noting that the colonies were unbranched and club-shaped (i.e., clavate) with a distinct polyp-bearing region (polyparium) and a narrower, sterile stalk. He also observed that the polyps retracted into calyces that were distributed over the surface of the polyparium (Pfeffer 1889). He described the sclerites as warty “Doppelspindeln” (a term often used for a spindle with a median waist; Bayer et al. 1983), denser in the calyces than in the stalk, and absent from the neck of the polyp. Kükenthal (1906) concluded that in all aspects of its morphology other than the unbranched colony growth form Metalcyonium resembled Alcyonium. He relegated Metalcyonium to the status of a subgenus, diagnosing it succinctly as “Alcyonien von unverzweigter, walzenförmiger oder konischer Körperform” (Kükenthal 1906: 43, i.e., alcyonians with unbranched, cylindrical, or conical colony form). Subsequent authors (e.g., Thomson 1910, 1921) did not accept Kükenthal’s revision and assigned additional species of soft corals with unbranched, clavate or capitate colony forms to Metalcyonium throughout the early 20th century.

Utinomi (1958) further validated the genus, stating “it is undoubted that Metalcyonium is a unique group embracing the species which are clavate, capitate or mushroom-shaped and ordinarily unbranched in form” (1958: 110). He suggested, however, that M. clavatum, which he erroneously stated to be the type species of Metalcyonium, might belong instead to the genus Bellonella Gray, 1862 because its colony shape is relatively digitiform rather than capitate. In a subsequent publication, Utinomi (1964) designated M. capitatum as the type species of Metalcyonium. Williams (1986) argued that the capitate colony growth form alone did not justify the separation of the genus Metalcyonium from Alcyonium because species such as M. patagonicum May, 1899 and M. variabile J. S. Thomson, 1921 can exhibit a range of forms intermediate between digitiform and capitate. He transferred all capitate species of Metalcyonium, including the type species M. capitatum, to Alcyonium, thereby invalidating the genus. Verseveldt and Bayer (1988) then redescribed Pfeffer’s original type material and moved both M. clavatum and M. capitatum to Bellonella, synonymising Metalcyonium with that genus.

Among the species of Metalcyonium transferred by Williams (1986) to Alcyonium was M. verseveldti Benayahu, 1982, found in the warm tropical waters of the northern Red Sea. Molecular phylogenetic analyses that have included this species place it in a clade with the tropical Indo-Pacific genera Cladiella Gray, 1869 and Klyxum Alderslade, 2000 (Benayahu et al. 2012), phylogenetically distant from Alcyonium (see McFadden et al. 2022).

Here, we re-examine the type material and establish a new genus for M. verseveldti. In addition, we describe three new species of the genus from the Indian and western Pacific Oceans (Fig. 1). We present features of the sclerites of each species and examine the genetic distinctions among species using single-locus DNA barcodes and multi-locus sequence data from target-enrichment of conserved elements (UCEs and exons).

Figure 1. 

Distribution of the Ofwegenum gen. nov. species in the Indo-Pacific region. The colour shades represent the different marine realms. Yellow = West Indo-Pacific, blue = Central Indo-Pacific, red = East Africa, green = temperate Australasia; PG = Persian Gulf, AS = Arabian Sea, RS = Red Sea, GO = Gulf of Oman, OM = Oman.

Materials and methods

Morphological studies

The study examined the holotype and paratypes of Metalcyonium verseveldti Benayahu, 1982 and other relevant material deposited at the museums listed below. Morphological features, including shape and dimensions of the preserved colonies, were recorded; terminology follows McFadden et al. (2022) and Bayer et al. (1983). To examine the sclerites, tissue samples were treated with 10% sodium hypochlorite followed by repeated rinses in distilled water. Wet preparations of the clean sclerites were examined under a Nikon Eclipse 80i light microscope at ×100–200 magnification. Scanning Electron Microscope (SEM) mounts were prepared from the sclerites. The mounts were coated with Pd/Au or Cr and viewed under a Quanta 200 FEG (Field Emission Gun) ESEM operated at 5–20 kV or Au coated and viewed under a Hitachi TM-1000 ESEM at Tel Aviv University and Jeol 6480LV SEM operated at 10 kV, with Pt coating at Naturalis Biodiversity Center, Leiden.

Abbreviations

NBC Naturalis Biodiversity Center (formerly Rijksmuseum van Natuurlijke Historie, RMNH) Leiden, The Netherlands;

NTM Museum and Art Gallery of the Northern Territory, Darwin, Australia;

QM Queensland Museum, Brisbane, Australia;

SMNHTAU Steinhardt Museum of Natural History at Tel Aviv University, Tel Aviv, Israel;

UF Florida Natural History Museum, Florida, United States.

Molecular phylogenetic analyses

DNA was extracted from EtOH-preserved tissue samples using a DNeasy Blood & Tissue Kit (Qiagen, Inc.). Fragments of the mitochondrial mtMutS and COI (+igr1) genes and nuclear 28S rDNA were amplified by polymerase chain reaction (PCR) and sequenced using published primers and protocols (McFadden et al. 2014). New sequences were added to an alignment of family Cladiellidae analysed previously by Benayahu et al. (2012) (Table 1) that included one of the specimens described here and realigned using the L-INS-i method in MAFFT (Katoh et al. 2005). Pairwise genetic distances (uncorrected p) among taxa for each gene region were determined using MEGA v.5 (Tamura et al. 2011).

Table 1.
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GenBank accession numbers for specimens of Ofwegenum gen. nov. and other genera of Cladiellidae included in molecular analyses (Fig. 16). Raw UCE sequence reads are deposited under project number PRJNA1035147.

Species Museum Locality mtMutS 28S COI UCEs
Ofwegenum coronalucis UF 15819 Oman NA OR483157 OR487130 NA
SMNHTAU_Co_39048 Oman OR487121 OR483155 OR487131 SAMN 38083212
UF 17263 Oman OR487122 OR483156 OR487134 SAMN 38083211
UF 15877 Oman OR487123 OR483158 OR487132 NA
BOMAN-09174 Oman OR487124 OR483159 NA NA
UF 15882 Oman OR487125 OR483160 OR487133 NA
Ofwegenum aff. coronalucis SMNHTAU_ Co_38223 Aquarium trade, USA OR487121 OR483157 OR487130 SAMN 38083213
Ofwegenum verseveldti SMNHTAU_ Co_33097 Israel GU356012 JX991219 GU355978 SAMN 38083214
Ofwegenum kloogi SMNHTAU_ Co_34426 Reunion OR487117 OR483152 OR487128 SAMN 38083210
SMNHTAU_ Co_38229 Reunion OR487118 OR483153 NA NA
Ofwegenum colli NTM C13089 Australia OR487120 NA NA NA
Aldersladum jengi SMNHTAU_ Co_33607 Taiwan JX991144 JX991201 JX991220 NA
Aldersladum sodwanum SMNHTAU_ Co_31520 Kenya JX991193 JX991213 JX991236 NA
Cladiella australis SMNHTAU_ Co_36313 Taiwan MH516863 MH516878 MH516513 SAMN 38083203
SMNHTAU_ CO_36912 Taiwan MH516570 MH516881 MH516515 SAMN 38083204
SMNHTAU_ Co_36987 Taiwan MH516571 MH516882 MH516516 SAMN 38083205
SMNHTAU_ Co_36042 Madagascar OR487126 OR483164 OR487135 SAMN 38083206
Cladiella bottae SMNHTAU_ Co_34648 Taiwan JX991145 JX991204 JX991223 NA
Cladiella kashmani SMNHTAU_ Co_32334 Kenya JX991195 JX991215 JX991238 NA
SMNHTAU_ Co_32246 Kenya JX991194 JX991214 JX991237 NA
Cladiella pachyclados SMNHTAU_ Co_33604 Taiwan JX991146 JX991206 JX991225 NA
SMNHTAU_ Co_35507 Palau JX991197 JX991216 JX991240 NA
Cladiella sphaerophora SMNHTAU_ Co_34132 Israel GQ342471 JX203653 GQ342386 NA
Cladiella tuberculoides SMNHTAU_ Co_34686 Taiwan JX991227 JX991148 JX991208 NA
SMNHTAU_ Co_34642 Taiwan JX991226 JX991147 JX991207 NA
Cladiella tuberosa SMNHTAU_ Co_34669 Taiwan JX991149 JX991209 JX991228 NA
Klyxum sp. UF 2684 N. Marianas OR487127 OR483162 NA SAMN 38083207
QM G330915 Australia NA OR483163 NA SAMN 38083208
CKT396 Taiwan NA OR483161 NA SAMN 38083209
Klyxum adii SMNHTAU_ Co_32636 Kenya JX991199 JX991217 JX991242 NA
Klyxum flaccidum SMNHTAU_ Co_32221 Kenya JX991200 JX991218 JX991243 NA
Klyxum utinomii SMNHTAU_ Co_34639 Taiwan JX991151 JX991212 JX991232 NA
SMNHTAU_ Co_34127 Israel GQ342476 JX203654 GQ342392 NA

Preliminary phylogenetic analyses of each gene region using PhyML (Guindon and Gascuel 2003) revealed congruence of gene trees, therefore genes were concatenated for further analyses. To minimise the effects of missing data on the analyses, a 471 bp fragment of the mtMutS gene was concatenated with 28S rDNA; COI was not included in the concatenated alignment. Optimal models of evolution for each gene (mtMutS: HKY+F; 28S: TN+F+I) were found using ModelFinder (Kalyaanamoorthy et al. 2017) and a maximum likelihood tree was constructed using IQTree v. 2.1.2 (Minh et al. 2020) with an edge-linked partition model (Chernomor et al. 2016) and 10,000 ultrafast bootstraps (Hoang et al. 2018). A partitioned analysis was run using MrBayes v. 3.2.1 (Ronquist et al. 2012), applying a HKY model to mtMutS and a GTR+ G model to 28S rDNA. MrBayes was run for 3,000,000 generations (until standard deviation of split partitions < 0.01) with a burn-in of 25% and default Metropolis coupling parameters.

Target-enrichment sequencing of conserved elements

For one or a few representatives of each species and several outgroup taxa (Cladiella, Klyxum), DNA was quantified using a Qubit 2.0 fluorometer and quality-checked (for 260:230 and 260:280 ratios) using a NanoDrop spectrophotometer. DNA samples (300–1000 ng) were sent to Arbor Biosystems (Ann Arbor, MI) for library preparation, target enrichment and sequencing. Libraries were prepared using a Kapa Hyper Prep Kit (Kapa Biosystems) with dual-indexed iTru adaptors. myBaits protocol v. 4 (Arbor Biosystems) was used to target and enrich pools of 8 libraries using the octocoral-v. 2 bait set of Erickson et al. (2020). Enriched libraries were sequenced on one lane of Illumina HiSeq 2500 (150 bp PE reads).

Sequences were processed using the phyluce pipeline (Faircloth 2016) as outlined in Erickson et al. (2020). Briefly, reads were cleaned using illumiprocessor (Faircloth 2013) and Trimmomatic v. 0.35 (Bolger et al. 2014), then assembled into contigs using Spades v. 3.1 (Bankevich et al. 2012) with –careful and –cov-cutoff 2 parameters. phyluce_assembly_match_contigs_to_probes was used to identify loci by matching probes to contigs with a minimum coverage of 70% and minimum identity of 70%. phyluce_assembly_get_fastas_from_match_counts was used to extract loci which were then aligned using MAFFT v. 7.130b (Katoh and Standley 2013). Sequences for seven outgroup taxa belonging to the genera Cladiella and Klyxum were included in the alignment. Aligned loci were edge-trimmed using phyluce_align_seqcap_align, and phyluce_align_get_only_loci_with_min_taxa was used to concatenate loci into a data matrix with 75% of taxa present for each locus. A maximum likelihood tree was constructed using IQTree v. 2.1.2 (Minh et al. 2020). ModelFinder (Kalyaanamoorthy et al. 2017) was used to select the best model of evolution (-m MFP), and an analysis was run with 1000 ultrafast bootstraps (Hoang et al. 2018) and 1000 replicates of an SH-like approximate likelihood ratio test (SH-aLRT) (Guindon et al. 2010).

Results

Systematics

Subphylum Anthozoa Ehrenberg, 1831

Class Octocorallia Haeckel, 1866

Order Malacalcyonacea McFadden, van Ofwegen & Quattrini, 2022

Family Cladiellidae McFadden, van Ofwegen & Quattrini, 2022

Ofwegenum gen. nov.

https://zoobank.org/10C92BD3-D724-42A5-A050-09F112AA33B7

Diagnosis

Soft corals with encrusting or capitate growth forms; small (1–2 cm diameter), stalked capitula may be joined basally to form a low mat. Polyps monomorphic, non-retractile but contractile; pinnules with or without terminal branches. Coenenchymal sclerites are spindles and rods, smooth but with low, simple tubercles and areas of thickening forming concentric, raised rings. Polyp sclerites similar, usually arranged ‘en chevron’ in the polyp body, lacking a distinct collaret-and-points arrangement. Tentacles and pinnules contain numerous platelets and flattened rods (i.e., finger- biscuits, see Bayer et al. 1983) with varying features such as lateral median constrictions, side notches, or depressions at one or both ends resembling a figure-eight, arranged mostly on the aboral side of the tentacles. Some species also have tiny sclerites around the mouth. Live colonies with blue, green, or brown colouration in the coenenchyme; pinnules brown. Sclerites colourless. Zooxanthellate.

Type species

Metalcyonium verseveldti Benayahu, 1982: 197–201.

Etymology

The generic name Ofwegenum (gender: neuter) honours the late Dr. Leendert P. van Ofwegen (1953–2021), a close friend and an eminent octocoral taxonomist (Hoeksema 2021), in memory of his prolific contribution to the knowledge of this group.

Key to the species of Ofwegenum gen. nov

1 Colonies encrusting, not capitate and without stalk O. kloogi
– Colonies capitate, with stalk 2
2 Crosses and irregular sclerites up to 0.05 mm, around the polyp mouth O. coronalucis
– No sclerites around the polyp mouth 3
3 Coenenchymal sclerites up to 0.70 mm long, tentacle sclerites mostly figure-eight platelets O. verseveldti
– Coenenchymal sclerites up to 0.40 mm long, tentacle sclerites mostly flattened rods or bone-shaped platelets up to 0.15 mm long O. colli

Ofwegenum colli sp. nov.

https://zoobank.org/E72328A2-B94F-4574-BBD2-BE72255AF6F6
Figs 1, 3A, B, 4, 5, 6

Material examined

Holotype. Australia • Queensland, N.E. Bay Great Palm Island; 18.7500°S, 146.6500°N; 6–7 m depth; 22 April 1981; coll. J. Coll; silty bottom, on a dead coral; NTM C13089.

Paratypes. Australia • 7 colonies, same data as holotype; NTM C015578 • 5 colonies, same data as holotype; NTM C3827 • 1 colony, same data as holotype; NTM C3828 • 3 colonies, same data as holotype; May 1982; NTM C3829.

Description

The holotype is a fragment of a colony measuring 14 by 13 mm (Fig. 3A). Its polypary expands over a 2 mm thick, spreading crust-like base. The surface of the polypary features some grooves, and the contracted polyps, up to 1 mm in diameter, are visible as low mounds (Fig. 3A). The coenenchyme has sclerites in the form of spindles (with tapered ends) and rods (with blunt ends) up to 0.50 mm long, with low, simple tubercles or areas of thickening forming concentric, raised rings (Fig. 4A). The polyp body contains similar but shorter rods that appear to be arranged ‘en chevron’ when the polyps are extended. The size of the sclerites decreases along the polyp body towards the base of the tentacles (Fig. 4A).

The tentacles and pinnules contain numerous platelets and flattened rods (i.e., finger-biscuits, see Bayer et al. 1983) up to 0.10 mm long (Fig. 4B) arranged on the aboral side of the tentacles. Some of these sclerites have lateral median constrictions, side notches, or depressions at one or both ends resembling a figure-eight shape, and some have bulbous ends resembling bones (Fig. 4B).

Colour

The ethanol-preserved colony is cream.

Morphological variations

The paratype colony NTM C3829 has smoother and shorter spindles and rods compared to the holotype (0.20 vs. 0.50 mm, respectively: Figs 4A, 6A). The tentacle sclerites are up to 0.15 mm long (Fig. 6B) compared to up to 0.10 mm in the holotype (Fig. 4B). The holotype NTM C13089 has some platelets with wider ends, resembling the shape of a bone (Fig. 4B), which are not present in the other type material of this species (Figs 5B, 6B).

Remarks

This species is capitate with smaller bud-like capitula occasionally emerging from the stalk. The sclerites of the paratypes correspond to those of the holotype but differ a bit in size. This species has the largest tentacle sclerites among the congeners, up to 0.15 mm long (Figs 4–6). No information is available on the living features of this species.

Distribution

Queensland, Australia.

Etymology

The species is named after the collector of the material, Prof. John Coll of James Cook University, North Queensland, a renowned chemical ecologist who has contributed prominently to the knowledge of soft corals.

Ofwegenum coronalucis sp. nov.

https://zoobank.org/1030A306-9E82-4E0E-8565-9D3D157A5406
Figs 1, 2A, B, 3H, I, 7, 8, 9, 10A–D, 11

Material examined

Holotype. Oman • Dhofar, Mirbat, Michel’s Reef; 16.9433°N, 54.7300°E; 25–30 m depth; 20 January 2022; coll. C.S. McFadden and K. Samimi-Namin; UF 17263 (BOMAN–08362).

Paratype. Oman • same data as holotype; SMNHTAU_Co_39048 (BOMAN–08351).

Other material

Oman • Dhofar, Mirbat, Frankincense; 16.9662°N, 54.6900°E; 24–30 m depth; 19 Jan 2022; coll. C.S. McFadden; UF 15819 (BOMAN–08345) • Dhofar, Mirbat, near Frankincense; 16.9688°N, 54.6877°E; 24–29 m depth; 21 Jan 2022; coll. C.S. McFadden and K. Samimi-Namin; UF15882 (BOMAN–09175) • same collection data as for preceding; UF 15877 (BOMAN–09166) • same collection data as for preceding; in situ photo, microscope slides and molecular data only; BOMAN–09174. Unknown • Aquarium trade, Chicago, IL, USA; July 2013; coll. A. Parrin; SMNHTAU_Co_38223.

Description

The holotype consists of several fragments of a colony; the largest is 10 mm in diameter (Fig. 3H). The colony consists of multiple capitate polyparia on sterile stalks; side branches connect adjacent stalks to one other at the base to form an encrusting mat. Most polyps are contracted, with polyps widely set on the polyparium (Figs 3H, 9A, B).

Figure 2. 

Morphological details of live Ofwegenum gen. nov. polyps A, B close up of Ofwegenum coronalucis sp. nov., holotype, UF 17263; arrows indicate the concentration of minute sclerites around the mouth opening and base of the tentacles C–F unknown species of Ofwegenum gen. nov. from the aquarium trade. Scale bars: approximately 5 mm (photographs A, B K. Samimi-Namin C–F Daniel Knop).

Figure 3. 

Preserved type colonies of Ofwegenum gen. nov. A O. colli sp. nov., holotype NTM C13089 B O. colli sp. nov. several paratype colonies NTM C015578 C O. aff. coronalucis, SMNHTAU_Co_38223 D O. kloogi sp. nov. holotype SMNHTAU_Co_34426, grooves on polypary are indicated by arrows, distal ends of tentacles protrude from polyp mounds E O. kloogi sp. nov., several paratype colonies SMNHTAU_Co_38299 F O. verseveldti comb. nov., holotype SMNHTAU_Co_25554 G O. verseveldti comb. nov., paratypes, SMNHTAU_Co_25544, grooves on polypary are indicated by arrow H O. coronalucis sp. nov., holotype, UF 17263 I O. coronalucis sp. nov., paratype SMNHTAU_Co_39048).

Figure 4. 

Ofwegenum colli sp. nov., holotype NTM C13089 A sclerites of the coenenchyme and polyp body B sclerites of the tentacles.

Figure 5. 

Ofwegenum colli sp. nov., paratype NTM C3827 A sclerites of the coenenchyme and polyp body B sclerites of the tentacles.

Figure 6. 

Ofwegenum colli sp. nov., paratype NTM C3829 A sclerites of the coenenchyme and polyp body B sclerites of the tentacles.

Sclerites of the coenenchyme are spindles and rods up to 0.40 mm long with low, simple tubercles or areas of thickening forming concentric, raised rings (Fig. 7A). The polyp body contains similar but shorter rods that appear to be arranged ‘en chevron’ when the polyp is extended (Fig. 2A). These sclerites are usually blunt and have a crystalline texture at both ends (Fig. 7A). The length of the sclerites decreases along the polyp body towards the base of the tentacles (Fig. 7A).

Figure 7. 

Ofwegenum coronalucis sp. nov., holotype UF 17263 A sclerites of the coenenchyme and polyp body B sclerites of the tentacles C sclerites around the polyp mouth opening. Scale at B also applies to C.

The tentacles and pinnules contain numerous platelets and flattened rods (i.e., finger-biscuits) up to 0.10 mm long (Fig. 7B), arranged on the aboral side of the tentacles (Fig. 2A, B). Some of these sclerites have median constrictions, side notches, or depressions at one or both ends resembling figure-eight shapes (Fig. 7B). There are also numerous irregularly shaped platelets with side notches or side branches, up to 0.05 mm in length (Fig. 7C), that are distributed around the mouth and base of the tentacles on the oral side. These sclerites are reflective in light (Fig. 2A, B).

Colour

In life, colonies appear brown with blue-green tentacles. After preservation in ethanol, they are creamy white. Sclerites colourless.

Morphological variations

UF 15882 and BOMAN–09174 have slightly thinner spindles and rods both in the coenenchyme and polyp body (Fig. 8A). In addition, the polyp sclerites have fewer side notches and depressions compared to the holotype (Fig. 8B). Photos of the live specimens suggest that some of the polyps do not have the reflective sclerites around the mouth (Figs 9E, F, 10C, D).

Figure 8. 

Ofwegenum coronalucis sp. nov., UF 15882 A sclerites of the coenenchyme and polyp body B sclerites of the tentacles C Sclerites around polyp mouth opening. Scale bars: 0.05 mm (B, C).

Figure 9. 

Ofwegenum coronalucis sp. nov. A, B colony and polyps of holotype, UF 17263 C, D colony and polyps of paratype, SMNHTAU_Co_39048 E, F colony and polyps of UF 15882. Scale bars: ~ 50 mm (A, E); ~ 5 mm (B–D, F) (photographs K. Samimi-Namin).

Figure 10. 

A, B Ofwegenum coronalucis sp. nov., UF 15877 C, D Ofwegenum coronalucis sp. nov., BOMAN–09174 E Ofwegenum kloogi sp. nov. holotype SMNHTAU_Co_34426. (Photos A–D C. S. McFadden E Y. Benayahu). Scale bars: ~ 5 mm (A–D); 5 cm (E).

Figure 11. 

Ofwegenum aff. coronalucis SMNHTAU_Co_38223 A sclerites of the coenenchyme and polyp body B sclerites of the tentacles.

SMNHTAU_Co_38223 comes from the aquarium trade in the U.S. Its commercial source is assumed to be Jakarta, Indonesia (A. Parrin, pers. comm. 12 Aug 2013), but the original collection locality remains unknown. This colony is tentatively assigned as O. aff. coronalucis based on its sclerite features and genetic similarity to this species (Fig. 16). However, it differs from the other material in having a blue colour in the coenenchyme and shorter tentacle sclerites up to 0.07 mm long. Such differences might be due to a prolonged exposure to the artificial aquarium environment.

Remarks

Ofwegenum coronalucis sp. nov. differs from its congeners in having irregularly shaped sclerites with side notches or side branches around the polyp mouth that reflect light (Figs 2A, B, 7C, 8C). Additionally, the tentacle platelets have narrow median constrictions compared to the other species (Figs 7B, 8B).

Distribution

Oman.

Etymology

The species name is from the Latin corona (crown) and lucis (of light), referring to the reflective ring of sclerites around the polyp mouth in the live specimens.

Ofwegenum kloogi sp. nov.

https://zoobank.org/F1E4D927-3C21-494B-9B53-B4EA88B49817
Figs 1, 3D, E, 10E, 12, 13

Material examined

Holotype. La Réunion • Saint-Paul, Cap la Houssaye; 21.0174°S, 55.2376°E; 17 m depth; 8 April 2008; SMNHTAU_Co_34426.

Paratype. La Réunion • 13 colonies/fragments; same data as holotype; SMNHTAU_Co_38229.

Description

The holotype is an encrusting colony, measuring 28 by 25 mm, attached to a calcareous fragment by a thin spreading base (<1 mm thick). The polypary features several narrow grooves (Fig. 3D). The polyps appear as low mounds. The distal tips of the tentacles occasionally protrude from the top of the polyp mounds.

The coenenchyme sclerites are spindles and rods up to 0.50 mm long, with low, simple tubercles or areas of thickening forming concentric, raised rings (Fig. 12A). The polyp body contains shorter spindles, up to 0.30 mm long (Fig. 12A), which appear to be arranged ‘en chevron’ when the polyp is extended. The length of the sclerites decreases along the polyp body towards the base of the tentacles (Fig. 12A).

Figure 12. 

Ofwegenum kloogi sp. nov. holotype SMNHTAU_Co_34426 A sclerites of the coenenchyme and polyp body B tentacle sclerites, with ellipsoidal platelets and flattened rods with lateral notches.

The tentacles and the pinnules contain numerous platelets and flattened rods (i.e., finger-biscuits) up to 0.07 mm long (Fig. 12B), arranged on the aboral side of the tentacles. Some of these sclerites have lateral median constrictions, side notches, or depressions at one or both ends (Fig. 12B).

Colour

In life the expanded tentacles are pale grey with an underlying bluish tint. The polyps have a blue mouth opening and blue line along the tentacles (Fig. 10E). The ethanol-preserved holotype is pale grey in colour.

Morphological variations

Paratype SMNHTAU_Co_38229 has slightly longer tentacle sclerites and shorter coenenchymal sclerites compared to the holotype (Fig. 13).

Remarks

This species features a distinct encrusting growth form and surface grooves on its polypary, most probably indicating a process of colony fission (Fig. 3D, E). Its tentacle sclerites are mainly ellipsoidal platelets and flattened rods with shallow to no median constrictions (Figs 12B, 13B). The colonies grow in dense patches on the reef (Fig. 10E).

Figure 13. 

Ofwegenum kloogi sp. nov., paratype, SMNHTAU_Co_38229 A sclerites of the coenenchyme and polyp body B tentacle sclerites, with ellipsoidal platelets and flattened rods with lateral notches.

Distribution

La Réunion.

Etymology

The species is named after the late Prof. Yoel Kloog, biochemist, former Dean of the Faculty of Life Sciences, Tel Aviv University, in honour of his friendship and lifetime contributions to science.

Ofwegenum verseveldti (Benayahu, 1982), comb. nov.

Figs 1, 3F, G, 14, 15

Material examined

Holotype. Egypt • Marsa Barieka, northern Red Sea, southern tip of Sinai Peninsula; 27.7500°N, 34.2333°E; 12 m depth; 3 July 1978; coll. Y. Benayahu; SMNHTAU_Co_25554 (previously NS16770).

Paratypes. Egypt • 33 colonies, same data as holotype; SMNHTAU_Co_25544 (previously NS16771) • same data as holotype; RMNH COEL. 13903.

Other material

Israel• Eilat, northern Gulf of Aqaba, mesophotic reef across from the Inter University Institute for Marine Sciences (IUI); 60 m depth; 20 September 2005; coll. S. Eibinder; SMNHTAU_Co_33097.

Re-description

(modified after Benayahu 1982). The holotype is a capitate colony, 11 mm in diameter with stalk approximately 14 mm high (Fig. 3F). The contracted polyps form conical or dome-shaped mounds, and the distal ends of some tentacles can be seen protruding from them. The coenenchyme sclerites are spindles and rods up to 0.80 mm long with low, simple tubercles or areas of thickening forming concentric, raised rings (Fig. 14A). The polyp body contains similar but shorter sclerites, up to 0.45 mm long (Fig. 14A), that appear to be arranged ‘en chevron’ when the polyp is extended. The size of the sclerites decreases along the polyp body towards the base of the tentacles.

Figure 14. 

Ofwegenum verseveldti comb. nov., holotype SMNHTAU_Co_25554 A sclerites of the coenenchyme and polyp body B sclerites of the tentacles.

The tentacles and pinnules include numerous crosses, flattened rods (i.e., finger-biscuits) and platelets up to 0.10 mm long (Fig. 14B), arranged on the aboral side of the tentacles. Some of these sclerites have median constrictions, side notches, or depressions at one or both ends that resemble a figure-eight shape (Fig. 14B). The platelets commonly have an asymmetrical outline and are wider at both ends (Fig. 14B).

Colour

In life the coenenchyme is uniquely dark blue. The expanded polyps are pale blue, with brown pinnules that reflect the presence of symbiotic algae. The ethanol-preserved colony is creamy yellow, and the tentacles are pale cream.

Morphological variations

The paratype colonies and the other material vary in size; some colonies feature two separate polyparies on a common stalk (Fig. 3G). RMNH COEL. 13903 has smoother spindles and rods in both the coenenchyme and polyp body (Fig. 15A) and has fewer figure-eight platelets (Fig. 15B) compared to the holotype.

Figure 15. 

Ofwegenum verseveldti comb. nov., paratype, RMNH COEL. 13903 A sclerites of the coenenchyme and polyp body B sclerites of the tentacles.

Remarks

Ofwegenum verseveldti comb. nov. is the only species with tentacle sclerites composed mainly of asymmetrical platelets resembling a figure-eight (Figs 14B, 15B). Additionally, it has the longest spindles and rods among the congeners (Figs 14A, 15A).

The current findings correspond to the original description of M. verseveldti (see Benayahu 1982). The new high-quality SEM images of the sclerites (Figs 14, 15) better present the species’ diagnostic morphological characters. The tentacle sclerites reported as ‘flattened rods with tiny pits’ in the original description are referred to here as figure-eight platelets. The maximum length of these sclerites was erroneously presented by Benayahu (1982: 198, up to 0.19 mm) and is now corrected to be up to 0.10 mm (Fig. 14B). In the original description the species was described as having polyp sclerites arranged as a collaret and points, however further examination of additional material shows that is not the case. When polyps are extended the spindles and rods appear to be arranged ‘en chevron’. Benayahu (1982) also did not mention anything about the presence or absence of zooxanthellae in specimens. Re-examination of the type material confirms that O. verseveldti is indeed zooxanthellate.

It should be noted that despite the extensive soft coral research conducted in the Gulf of Aqaba and and other parts of the Red Sea, since the collection of the type material of O. verseveldti comb. nov. it has been found only once at a mesophotic depth on the Eilat reef (see above: SMNHTAU_Co_33097) and is also only infrequently observed by some professional divers in that region. This species should thus be considered as a rare soft coral in the Red Sea.

Distribution

Northern Red Sea.

Molecular results

DNA barcoding

Sequences for mtMutS (735 bp), igr1 + COI (909 bp) and 28S rDNA (800 bp) were obtained for seven specimens representing three of the four species of Ofwegenum plus the species from the aquarium trade (SMNHTAU_Co_38223) (Table 1). We were unable to amplify COI for two specimens (SMNHTAU_Co_38229, BOMAN–09174) and mtMutS for another (UF 15819). Only a partial fragment of mtMutS (450 bp) was obtained for O. colli sp. nov. (NTM C13089).

All phylogenetic analyses separated Ofwegenum gen. nov. into a well-supported clade that was sister to Klyxum and differed from members of that genus by mean genetic distances (uncorrected p) ranging from 1.0% (± 0.06% SD) at COI to 4.4% (±1.7% SD) at 28S rDNA (Fig. 16A). Within the Ofwegenum clade, however, the relationships among species were poorly resolved. All Ofwegenum specimens had identical mtMutS and COI sequences with the exceptions of O. verseveldti comb. nov., which differed by a 1 bp substitution in mtMutS, and O. kloogi sp. nov. (SMNHTAU_Co_34226) which differed by a 1 bp substitution in COI. The partial mtMutS sequence for O. colli sp. nov. was identical to both O. kloogi sp. nov. and O. coronalucis sp. nov. At 28S rDNA, O. verseveldti, O. kloogi and O. coronalucis differed from one another by genetic distances (uncorrected p) of 0.5–0.8%. The aquarium trade specimen (SMNHTAU_Co_38223) was most similar to O. coronalucis, differing from the holotype UF 17263 by a 1 bp substitution. There was, however, variation among individuals of O. coronalucis, with two specimens from Oman (BOMAN–09174, UF 15882) differing from the others by ≤ 5 bp (uncorrected p = 0.6%). Both ML and Bayesian phylogenetic analysis of the concatenated alignment of mtMutS with 28S rDNA found moderate to strong support for a clade consisting of the two specimens of O. kloogi and a clade of the two specimens of O. coronalucis with divergent 28S sequences (BOMAN–09174, UF 15882) but did not resolve the relationships among the other taxa (Fig. 16A).

Figure 16. 

Phylogenetic relationships among species of Ofwegenum gen. nov. and other genera of the family Cladiellidae A maximum likelihood (ML) analysis of concatenated mtMutS and 28S rDNA barcoding loci. Numbers at nodes: ML bootstrap percentage (10,000 ultrafast bootstrap replicates)/Bayesian posterior probability. Asterisks indicate samples that are included in analysis of conserved elements B maximum likelihood analysis of 1,213 conserved element loci (75% occupancy matrix). All nodes have 100% bootstrap support and SH-aLRT = 100 unless indicated. All Co_ numbers are SMNHTAU.

Target-capture sequencing of conserved elements

A total of 2,509 loci (out of 3,023 targeted loci) was recovered from the assembled contigs, including the seven outgroup taxa (Table 1). The mean number of loci recovered per sample was 1,747 ± 205 SD (range: 1,297–1,977) with a mean length of 1,247 ± 92 bp SD (range: 1,121–1,395 bp). The 75% complete alignment matrix included 1,213 loci for a total length of 1,511,307 nucleotides.

The maximum likelihood analysis recovered an Ofwegenum clade that was strongly supported and genetically distinct from the outgroup taxa (Klyxum spp. and Cladiella australis) (Fig. 16B). Within Ofwegenum there was strong support for a clade of O. coronalucis (two specimens from Oman) plus the species from the aquarium trade (SMNHTAU_Co_38223). The phylogenetic relationships among O. verseveldti, O. kloogi and O. coronalucis, however, remained unresolved. The single specimens of O. verseveldti and O. kloogi that were included in the analysis were equally genetically distant from O. coronalucis, and there was only very weak support for O. kloogi belonging to a clade with O. coronalucis.

Discussion

The phylogenetic position of Ofwegenum gen. nov. as sister to the genus Klyxum in family Cladiellidae was well supported by both single-locus mitochondrial genes as well as the multi-locus nuclear gene analysis (Fig. 16). It shares with other members of this family polyp sclerites in the form of flattened rods and small plates with a median waist that often resemble a figure-eight. The current results demonstrate the taxonomic significance of these tentacular sclerites for species delimitation within Ofwegenum gen. nov. Like other Cladiellidae, only a single type of sclerite is found in the coenenchyme. The form of these sclerites—smooth spindles and rods with low protuberances that may form raised concentric rings—seems, however, to be unique within the family. Its growth form, which is encrusting or consists of small stalked polyparies in the range of a centimetre in diameter joined together in a mat, is also distinct from the predominantly lobate growth forms of other Cladiellidae. Finally, the bright blue alcohol-soluble pigments that give some Ofwegenum species their striking blue-green colour are unique among Cladiellidae, and rare among all octocorals. Whether or not this pigment is guaiazulene, a compound that has been found in the blue gorgonian Guaiagorgia and several other species (Grasshoff and Alderslade 1997) remains unknown.

Ofwegenum gen. nov. also shares with other genera of Cladiellidae a relatively invariant mitochondrial genome marked by little to no genetic differentiation among species at the loci commonly used for DNA barcoding (mtMutS, COI) (Benayahu et al. 2012). While 28S rDNA exhibits greater variation among species in this clade, higher levels of intraspecific variation in that gene can also confound assessment of species boundaries (McFadden et al. 2014) as observed in O. coronalucis (Fig. 16A). While multi-locus methods such as the target-enrichment approach employed here generally allow species to be delimited with greater confidence (Erickson et al. 2020), our analysis of Ofwegenum is hampered by low sample size. Only one specimen each of O. verseveldti and O. kloogi and no O. colli yielded DNA of sufficient quantity and quality for library preparation. The absence of the latter species from our phylogeny and our inability to assess intraspecific genetic variation in the other two greatly limit the inferences we can make about the phylogenetic relationships and degree of genetic differentiation among species of Ofwegenum. Although increased sample sizes will be necessary to better resolve the species’ relationships, the apparent rarity of this genus, with each species currently known from only 1–2 locations, may hinder future attempts to increase the phylogenetic sampling.

Although it is rarely encountered in nature, Ofwegenum is nonetheless present in the commercial aquarium trade. We examined and sequenced a specimen (SMNHTAU_Co_38223) obtained from a supplier in the U.S. that is genetically and morphologically most similar to O. coronalucis (Fig. 16). The original source location of this specimen remains unknown but was thought to be Indonesia (A. Parrin, pers. comm. 12 Aug 2013), where most of the material in the U.S. commercial trade originates (Wabnitz et al. 2003). Aquarist D. Knop shared with us photos of additional specimens sourced from Indonesia (Fig. 2C–F). Whether or not any of the species we have described (or perhaps an additional species) occurs naturally in Indonesia remains unknown. Rowlett (2020) reported that a species of Ofwegenum has been cultured in Queensland, Australia for exportation in the aquarium trade. Whether that species might be O. colli sp. nov., which occurs naturally in Queensland, or the O. aff. coronalucis that is found in the aquarium trade in the U.S. also remains unknown.

Conclusions

Here we established a new genus, Ofwegenum gen. nov., for Metalcyonium verseveldti Benayahu, 1982. We have redescribed the type of that species and establish it as a new combination, O. verseveldti. In addition, we have described three new species of Ofwegenum from shallow-water coral reefs in the Indo-Pacific region, bringing the total number of species in the genus to four. This genus appears to be rare on coral reefs, with each species known from only a few localities, some of which have been extensively explored. The four species have distinct, non-overlapping geographical distributions, and are currently known only from the northern Red Sea (O. verseveldti), Arabian Sea (O. coronalucis), central Indian Ocean (O. kloogi), and northeastern Australia (O. colli) (Fig. 1).

Acknowledgements

We thank Phil Alderslade, The Commonwealth Scientific and Industrial Research Organization (CSIRO), Hobart, Tasmania, Australia for providing material and S. Horner, Museum and Art Gallery of the Northern Territory, Darwin, Australia for curatorial information. We also thank the Interuniversity Institute for Marine Sciences, Eilat, Israel for use of their facilities, and S. Eibinder, Haifa University, Israel, for collecting the mesophotic samples. Collections in La Réunion were made possible due to a grant to Y. Benayahu from the “Conseil Régional de la Réunion” and “Association Parc Marin de la Réunion”. We thank E. Tessier, B. Cauvin, Y. Clain and the team of guards of the “Association Parc Marin de la Réunion” for help during the field work. We thank C. Bourmaud, J. P. Quod and M. Aknin and D. Huchon for help and advice during the La Réunion expedition. We thank Z. Kuplik for professional curatorial skills, K. Erickson for laboratory assistance, A. Quattrini for assistance with data analysis, V. Wexler for digital editing, and N. Paz for editorial assistance. Daniel Knop provided us with high resolution photos of his aquarium specimen. Environment Authority of Oman is appreciated for granting the collection permits, and we thank M.R. Claereboudt, S. Dobretsov (Sultan Qaboos University, Oman), G. Paulay (Florida Natural History Museum) and S. Wilson (Five Oceans Environmental Services LLC) for their support in Oman. J.H. Ausubel (Rockefeller University), and L. Brown (Lounsbery Foundation) are greatly appreciated for their support and encouragement to the last author. We would like to thank O. Breedy and J. Reimer for their constructive comments and suggestions, which helped improve the manuscript.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

This research received support from BSF–2019624 to Y. Benayahu and NSF DEB–1929319 and DEB–1856245 to C.S. McFadden. The research at NBC and partial fieldwork was supported by the Richard Lounsbery Foundation grant to K. Samimi-Namin.

Author contributions

Conceptualization: YB, CSM. Formal analysis: KSN, YB, CSM. Funding acquisition: YB, CSM. Project administration: CSM. Writing – original draft: CSM, YB, KSN. Writing – review and editing: CSM, YB, KSN.

Author ORCIDs

Catherine S. McFadden https://orcid.org/0000-0002-8519-9762

Yehuda Benayahu https://orcid.org/0000-0002-6999-0239

Kaveh Samimi-Namin https://orcid.org/0000-0002-7744-9944

Data availability

All of the data that support the findings of this study are available in the main text.

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