A black coral, Bathypathes thermophila Chimienti, sp. nov. is described from the Saudi Arabian coasts of the Gulf of Aqaba and north Red Sea (Neom area) using an integrated taxonomic approach. The morphological distinctiveness of the new species is confirmed by molecular analyses. The species thrives in warm and high salinity waters typical of the Red Sea at bathyal depths. It can form colony aggregations on muddy bottoms with scattered, small hard substrates. Colonies are monopodial, feather-like, and attached to a hard substrate through a thorny basal plate. Pinnules are simple, arranged biserially and alternately, and all the same length (up to approximately 20 cm) except for few, proximal ones. Spines are triangular, laterally compressed, subequal, smooth, and simple or rarely bifurcated. Polyps are elongated transversely, 1.5–2.0 mm in transverse diameter. Large colonies can have one or few branches, whose origin is discussed. The phylogenetic position of B. thermophila sp. nov. within the order Antipatharia, recovered using three mitochondrial markers, shows that it is nested within the family Schizopathidae. It is close to species in the genera Parantipathes, Lillipathes, Alternatipathes, and Umbellapathes rather than to the other available representatives of the genus Bathypathes, as currently defined based on morphology. In agreement with previous findings, our results question the evolutionary significance of morphological characters traditionally used to discriminate Antipatharia at higher taxonomic level.

Black corals, cox1-cox3, deep sea, igrN, igrW, Neom, Saudi Arabia

Black corals (Cnidaria, Anthozoa, Antipatharia) are ubiquitous to the world’s ocean, spanning cold deep to shallow tropical reefs. Traditionally, their description and classification rely on morphological traits, such as the corallum growth form, polyps shape and distribution, number of mesenteries, and size, shape and ornamentation of the skeletal spines (e.g., Opresko 2002; Brugler et al. 2013; Molodtsova and Opresko 2017; Opresko and Molodtsova 2021). With the advent of molecular analyses aiming at the study of phylogenetic relationships and taxa boundaries, several inconsistencies between the phylogenies and the current taxonomy of black corals were revealed. This has led to several Antipatharia families and genera currently recognised as polyphyletic (Brugler et al. 2013; Bo et al. 2018; Barret et al. 2020; Lü et al. 2021). For example, the intergenic spacer between nad5-IGR-nad1 (igrN), which is the most variable region of the mitochondrial genome of black corals, in combination with trnW-IGR-nad2 (igrW), and the spacer between cox3 and cox1 (cox3-cox1), have been used to clarify the phylogenetic position and describe new genera and species within the order Antipatharia (Thoma et al. 2009; Brugler et al. 2013; MacIsaac et al. 2013; Horowitz et al. 2020; Opresko and Molodtsova 2021). Moreover, the rRNA internal transcribed spacer region (comprising the 18S, ITS1, ITS2, and 5.8S) has been used in a growing number of publications to elucidate phylogenetic relationships within the families Antipathidae Ehrenberg, 1834, Aphanipathidae Opresko, 2004, and Schizopathidae Brook, 1889 (Lapian et al. 2007; Bo et al. 2018; Barret et al. 2020), as well as in population connectivity studies (Terrana et al. 2021). Finally, the use of next generation sequencing techniques, such as ultra-conserved elements, has recently proven useful in inferring relationships at species level in black corals (Horowitz et al. 2020).

Within the family Schizopathidae, the genus Bathypathes Brook, 1889 includes monopodial black corals and currently accounts for 14 valid species (Molodtsova and Opresko 2021; Molodtsova et al. 2022). It occurs in the Pacific, Indian, Atlantic, and Southern oceans, and has been recorded at depths ranging from 102 to 5393 m (Brook 1889; Opresko 2002; Opresko and Molodtsova, 2021; Molodtsova et al. 2022), although its shallowest record (Thomson 1905) is currently considered doubtful. In fact, those of the genus Bathypathes are mostly deep-sea species, with few representatives in the mesophotic zone. With deep-sea technologies allowing the exploration of these unseen depths, new Bathypathes species have been recently described and, similarly to all the deep-sea antipatharians known thus far, they live in cold waters.

The Red Sea rift is a young ocean basin (Purkis et al. 2012; Augustin et al. 2021) characterised by environmental conditions elsewhere considered extreme for most of the marine fauna. With sea surface temperatures exceeding 32 °C in the summer and deeper water temperatures always higher than 21 °C (Manasrah et al. 2019), the Red Sea arguably provides some of the warmest natural conditions for marine fauna. The basin represents a distinct biogeographic province located at the periphery of the larger Indo-Pacific region, and it is characterised by strong environmental gradients and high endemism of marine organisms (Di Battista et al. 2016; Berumen et al. 2019). Among Red Sea anthozoans, black corals are poorly known except for few museum records (e.g., Brook 1889; Wagner et al. 2012) and spot information about their reproduction and associated fauna (Richmond and Hunter 1990; Herler 2007). The black coral fauna of the Saudi Arabia Red Sea is virtually unstudied from an integrated systematics point of view. This is particularly true in the scantly explored and rapidly developing Neom area, which includes the northern Red Sea Saudi Arabian coast and islands north of Duba, delimited by a narrow coastal strip rapidly descending down to more than 2000 m depth, and the Saudi coast of the Gulf of Aqaba, a 180 km long and 25 km wide semi-enclosed gulf with a NNE-SSW orientation, an average depth of 800 m and a maximum depth of 1852 m. The 2020 OceanX-Neom Red Sea Expedition allowed to explore and assess the marine resources in Neom territory with the ultimate goal to inform Saudi Arabia national conservation strategies. In this context, and with the overall objective to characterise for the first time the Red Sea black coral diversity, a reference collection of Antipatharia including all observed in situ macro-morphologies was obtained. During the benthic surveys, several colonies of monopodial, feather-like black corals were observed from 195 to 688 m depth. Later, morphological study of the sampled material led to their assignation to the genus Bathypathes Brook, 1889 (e.g., Brook 1889; Totton 1923; Opresko 2002; Opresko and Molodtsova (2021), thus representing the first record of this genus in the Red Sea.

This study reports the description of a new species of Bathypathes found at bathyal depths in the highly saline and warm waters of the Red Sea, representing the first record for the family Schizopathidae in the basin. In particular, B. thermophila sp. nov. from the Neom area is described based on traditional morphological characters, and its phylogenetic position within the order Antipatharia is inferred genetically using three mitochondrial loci and including available representatives of all the seven Antipatharia families. This study demonstrates that (a) B. thermophila sp. nov. is a new species of Schizopathidae commonly present in the bathyal zone of the Red Sea; (b) black coral diversity in the basin is still poorly known and species new to taxonomy are likely to occur; and (c) traditional morphological characters used to describe genera and species in the order might be subject to convergent evolution and the taxonomy of the order is in need of revision.

Within the Family Schizopathidae, species with a monopodial, unbranched corallum are ascribed to the genera Bathypathes, Schizopathes, Abyssopathes Opresko, 2002, Saropathes, Alternatipathes, and Parantipathes. Our specimens lack the triangular-shaped pinnulated section typical of Alternatipathes and Schizopathes, the latter also characterised by unattached colonies with a hook-like holdfast for support (Opresko 2002; Molodtsova and Opresko 2017). Moreover, our specimens have only two rows of primary pinnules, simple and lateral, unlike the genera Abyssopathes (three rows of pinnules: two lateral and one or more anterior), Saropathes (primary pinnules in four rows, with subpinnules) and Parantipathes (six or more rows of pinnules) (Opresko 2002).

Based on morphological characters considered diagnostic in black coral taxonomy, we assigned the examined material to the genus Bathypathes and described it as a new species. From a molecular point of view, data from three loci, consistently and concordantly placed B. thermophila sp. nov. in a clade closely related to the genus Parantipathes rather than with the other available sequences of Bathypathes. This is relatively unsurprising as previous works already highlighted that the genus Bathypathes, as currently defined based on morphological characters, is polyphyletic. For example, rDNA phylogenetic reconstructions showed that Bathypathes, comprising representatives of the type species, B. patula, clusters with Stauropathes (Bo et al. 2018; Lü et al. 2021), and one nuclear sequence of Bathypathes sp. (MG023167-YPM IZ 028566) is close to the genus Telopathes (Bo et al. 2018; Lü et al. 2021). Given that Bathypathes, Stauropathes and Telopathes also share some morphological similarities, the morphological characters used to distinguish Bathypathes from other genera seem to lack evolutionary meaning (Barret et al. 2020) and further analyses are likely to reveal that B. thermophila sp. nov. falls within a different genus. Previous phylogenetic reconstructions based on the same mitochondrial regions have included representatives of B. patula (e.g., Brugler et al. 2013; Bilewitch and Tracey 2020). However, some of these samples were recently used by Opresko and Molodtsova (2021) to describe a new species within the genus, B. alaskensis, while the sequences from others have never been made available online for comparison. While acknowledging the disagreement between morphological and genetic assignation of the newly described species, in absence of available sequences of the genus Bathypathes type species, we decided to adopt a conservative approach and describe B. thermophila as a new species within the genus based on traditional morphological characters, still widely used in Antipatharia descriptions.

The overall ML analyses based on the three loci were mostly concordant and recovered a consistent reconstruction of the phylogenetic relationships within the order Antipatharia, in agreement with previously published molecular findings. The three mitochondrial phylogenetic reconstructions obtained consistently placed B. thermophila sp. nov. within a distinct molecular lineage including the sequences of all available representatives of the family Schizopathidae and one representative of the family Cladopathidae Kinoshita, 1910 (Sibopathes macrospina Opresko, 1993), with the exception of cox3-cox1 reconstruction, where no sequences of Sibopathes were available (Fig. 7a, b, Suppl. material 3). The inclusion of S. macrospina within this molecular lineage is consistent with previous results, since the family Schizopathidae is currently considered polyphyletic only due to the position of S. macrospina with the genus Parantipathes (Brugler et al. 2013). Other representative genera of the family Cladopathidae (Trissopathes Opresko, 2003, Chrysopathes Opresko, 2003, Cladopathes Brook, 1889, Heteropathes Opresko, 2011) are nested in a separate clade. Opresko (1993) already discussed the similarity of skeletal characters between the genera Parantipathes and Sibopathes, and Brugler et al. (2013) suggested that the morphological characters used to discriminate the latter could be derived. Barret et al. (2020) reconstructed the phylogenetic relationships of black corals on the base of complete mitochondrial genomes, and recovered a concordant topology, with the placement of S. macrospina within the Schizopathidae.

Antipatharians are currently largely understudied in the Red Sea, particularly in the mesophotic and aphotic zones. Due to the unique environmental features of this body of water, and its geographic position at the periphery of the greater Indo-Pacific region, a detailed study of Red Sea black corals can greatly contribute to our understanding of the evolution, phylogenetic relationships and biogeography of the whole group, ultimately pushing towards its pending taxonomic revision. Moreover, a reassessment of the morphological characters so far considered informative and diagnostic for black corals taxonomy is needed. In this respect, our molecular reconstructions and their comparison with the observed morphological features represent a first step in this direction and provide a baseline for future works. Future studies of Red Sea black corals will ultimately need to integrate nuclear and Next Generation Sequencing data. Indeed, molecular taxonomy is highlighting similar patterns at different taxonomic levels within the entire order Antipatharia and suggests that a molecular revolution similar to the one which has taken place in the last 20 years for other metazoans in general, and cnidarians in particular, is timely.

Bathypathes thermophila sp. nov. is described for the Neom region in the north Saudi Arabian Red Sea and represents the first black coral species described from the basin, the first record for the family Schizopathidae, as well as the only member of this family known thus far to live in relatively warm waters at certain depths. Considering the unique ecological and geological features of the Red Sea rift and the peculiar coral fauna that has adapted to live there, it is hardly surprising that the first systematic sampling effort to target black corals diversity and distribution led to the discovery of a new species. Indeed, as the study of the Neom reference collection proceeds, more taxa new to science are likely to be discovered. The study of their phylogenetic relationships and distribution, like in the case of Bathypathes thermophila sp. nov., will contribute to our knowledge of black corals and, ultimately, to a revision of their current taxonomic framework, increasingly exposed by molecular investigations to be plagued by polyphyly.

We warmly thank Neom, and in particular Thamer Habis, Razan Khamis, Peter Mackelworth, Paul Marshall, Justin Mynar, and Giacomo Palavacini for organising, coordinating, and facilitating the Red Sea Expedition in 2020. We would like to thank OceanX and the crew of OceanXplorer for their operational and logistical support for the duration of this expedition. In particular, we would like to acknowledge the ROV and Sub teams for data acquisition, sample collection and support of scientific operations on board OceanXplorer. We would also like to thank OceanX Media, for documenting and communicating this work with the public. We are grateful to Ivan Agerton, on behalf of OceanX Media, for photographs in Fig. 6c and d, Christina Alcon for the support in the DNA extraction and amplification, and Alessandro Genovese for facilitating the use of the SEM at KAUST Imaging Core Lab.