Euryalida (Echinodermata, Ophiuroidea) from Northwest Africa

. From 2004 to 2012, ten multidisciplinary oceanographic surveys were conducted along the coast of Northwest Africa, between the Strait of Gibraltar and the northern border of Sierra Leone. A total of five species of Euryalida Lamarck, 1816 belonging to three families were captured at 29 of the 1298 stations sampled in the area. Among them, Astrodendrum juancarlosi sp. nov. is described and figured in this paper. Ophiocreas oedipus Lyman, 1879 is recorded for the first time on West African continental margin and Gorgonocephalus pustulatum (H.L. Clark, 1916), an Indo-Pacific species only known from South African coast in the Atlantic, is reported off Guinea-Bissau, greatly extending to the North its Atlantic distribution. In addition, Asteroschema inornatum Koehler, 1906, a northeast Atlantic species, is recorded for the first time in African waters, off Western Sahara, extending its range of distribution to the south. Our data also extend the bathymetric distribution of A. inornatum to shallower waters and of G. pustulatum to deeper waters. The association of some euryalids with certain species of pennatulaceans and gorgonians is also described.


Introduction
Brittle stars are a common and numerically important component of epibenthic assemblages in bathyal and abyssal bottoms, constituting a significant component of the deep-sea megafauna (Metaxas & Giffin 2004).Ophiuroid species are distributed in all oceans inhabiting all types of substrata and are present in most habitats, ranging from intertidal to hadal depths (Stöhr et al. 2012).Among the five classes of the phylum Echinodermata Klein, 1878, Ophiuroidea Gray, 1840 -which includes brittle stars, basket stars (euryalids with branching arms) and snake stars (euryalids with non-branching arms) -has the highest diversity, with more than 2200 described species (Stöhr et al. 2012(Stöhr et al. , 2021)).Despite the remarkable differences in their bathymetric range, shelf (0-200 m) and bathyal (200-3500 m) strata harbour approximately the same number of species, although there is a clear difference in species composition between both strata.In abyssal depths (3500-6500 m), however, species richness is considerably reduced (Stöhr et al. 2012(Stöhr et al. , 2021)).In several locations the bathymetric distribution pattern of ophiuroids seems influenced by food availability, concentration of dissolved oxygen and its relative trophic position (Haedrich et al. 1980;Summers & Nybakken 2000;García et al. 2002;Metaxas & Giffin 2004).In addition, some species have been recorded forming dense aggregations that can reach up to thousands of individuals per square meter -so-called 'ophiuroid seabeds' (Metaxas & Giffin 2004;Calero et al. 2018).Nevertheless, how much these patterns are biased by differences in spatial and bathymetric sampling efforts remains unresolved.
Species of Euryalida have simple or branched arms, which can coil on a vertical plane (Mortensen 1927;Hyman 1955;Baker 1980).This feature allows them to wind around corals, living epizoically on gorgonians or antiphatarians, but occasionally also on hard substrates (Baker 1980).
Euryalid species have a worldwide distribution and wide bathymetric ranges, and are found from depths of a few meters to over 4000 m (Baker 1980).This group is not well known, and available information is less advanced than for other ophiuroids.Currently, most of the studies on Euryalida has been carried out in the Indo-Pacific region (Okanishi et al. 2011(Okanishi et al. , 2018(Okanishi et al. , 2020;;Kim & Shin 2015;Baker et al. 2018;Okanishi & Fujita 2018).In the East Atlantic, they were mainly studied on the European coast and Boreal seas (Mortensen 1927;Madsen 1951;Gage et al. 1983;Paterson 1985) and there have been few reports of the group to date along the Northwest African coast (Calero 2017).
The present study represents a new contribution to the knowledge base of Euryalida (Echinodermata: Ophiuroidea) fauna off Northwest Africa.

Material and methods
The study area stretches for more than 5000 km along the Atlantic coast of Northwest Africa, from the Strait of Gibraltar (36º N) to the northern border of Sierra Leone (9º N).Species of Euryalida were collected at 29 of a total of 1298 stations sampled with commercial bottom trawl over soft bottoms, between 19 and 1888 m depth.The samples were collected during the ten multidisciplinary Spanish and Norwegian surveys conducted, in collaboration with marine research institutes from African countries, in the area between 2004 and 2012 (Fig. 1).
At each station, specimens were sorted on board to morpho-species level; then they were counted, wet weighed and preserved in 80% ethanol for further study in the laboratory.Specimens were identified in the Marine Zoology laboratory of the University of Vigo.The disc diameter (dd) was measured to the nearest millimetre on the dorsal side of each specimen -from the base of one arm to the opposing disc side in the inter-radius.
Imaging was obtained using a Nikon DS-Fi2 digital camera mounted on a motorized Nikon SMZ25 stereo microscope.The images were computerized using the NIS-Elements Microscope Imaging Software, which included the Extended Depth of Focus (EDF) functionality.

Table 1 (continued).
Ossicles from the new species Astrodendrum juancarlosi sp.nov.were isolated by immersion in sodium hypochlorite (NaOCl).Subsequently they were washed with ethanol 96% and deionized water, and air-dried.Dried ossicles were mounted on SEM stubs using double-sided conductive tape.Finally, the ossicles were sputter-coated with gold-palladium and examined with a JEOL JEM 2010 F SEM and digitally photographed.
The station data where Euryalida were collected, including date, zone, start and end coordinates and depths, as well as the species recorded in each station are summarized in Table 1.
The samples collected during these cruises were labelled ("survey"-XXXX) and sent to the zoological collections of the Marine Zoology Laboratory at University of Vigo, Spain (LZM-UV), for conservation and curation.Type material of the new species was deposited in the Nacional Natural Sciences Museum of Madrid (MNCN).Besides, paratypes were deposited in the zoological collections of the Marine Zoology Laboratory at University of Vigo, Spain (LZM-UV), in the Collection of Marine Fauna from the Oceanographic Centre of Málaga of the Spanish Institute of Oceanography, Spain (CFM-IEOMA) and the Natural History Museum of the University of Santiago de Compostela, Spain (MHN-USC).

Distribution
Asteronyx loveni Müller & Troschel, 1842 is a circumglobal species, widely distributed across the three major oceans (Indian, Pacific and Atlantic).In the Atlantic Ocean, it has been recorded on both sides: in the West Atlantic, from North USA to West Indies (Hernández-Herrejón et al. 2008), and in the East Atlantic, from Norway (Döderlein 1911) to South Africa (Mortensen 1933).It also has a wide bathymetric distribution, ranging from 100 to 4721 m (Smirnov et al. 2014).
We collected the species at eleven stations from Western Sahara, Mauritania and Guinea-Bissau waters, between 902 and 1862 m.

Remarks
This is a deep-sea-water species generally associated with gorgonians and pennatularians (Mortensen 1927).Our specimens were always associated with pennatularians Distichoptilum gracile Verrill, 1882 and Anthoptilum murrayi Kölliker, 1880.Living colour of the species is cream or pinkish orange, more intense in the central part of the disc.The innermost arm spine much larger than the other spines and a hooked arm spine at the tip of the arm are the most distinctive characteristic for this species.

Distribution
Asteroschema inornatum Koehler, 1906 is considered as an endemic species for the Northeast Atlantic (Paterson 1985).The species was recorded from the Reykjanes Ridge and Mid-Atlantic Ridge, south-Fig.5. Map from the study area with the location of the stations where specimens of Asteroschema inornatum Koehler, 1906 were collected during the ten surveys off Northwest Africa.
We collected the species at six stations located off Western Sahara, between 1004 and 1593 m, normally associated with gorgonians.

Remarks
The records in waters of Western Sahara extend the geographical distribution of the species to the south and represent the first report of A. inornatum in African waters.Our record at 1004-1031 m depth (Stn MO172) also increase its bathymetric range to shallower waters.Living colour of the species is orange pink and grayish in the interadial areas of the disc. Genus

Distribution
Ophiocreas oedipus Lyman, 1879 has a wide geographical distribution in warm and temperate waters.It has been recorded in the Indo-Pacific area (New Zealand to Japan) (Koehler 1904;Clark 1911;Baker 1980;McKnight 1993), between 350 (material deposited in MNHN) and 1994 m (Koehler 1904).In the Atlantic Ocean, it was reported from Ascension Island between 756 and 778 m (Lyman 1882), Madeira from 1500 to 1968 m (Koehler 1909) and from several Northwest Atlantic seamounts (Mosher & Watling 2009;Cho & Shank 2010).
We collected this species at only four stations in Western Sahara, between 909 and 1755 m depth, representing the first record on West African continental margin.

Remarks
Ophiocreas oedipus and Asteroschema inornatum are very similar species.Nevertheless, they can be distinguished chiefly by several characters.In A. inornatum, both dorsal and ventral surfaces are more densely covered by granules, even in juveniles.However, the dorsal granulation on the disc seems to be a slightly variable character in O. oedipus, with different densities of coverage among specimens.Radial shields are quite parallel and aligned with the arms in A. inornatum, giving continuity between the disc and arms; however, in O. oedipus, the radial shields are divergent -closer in the proximal part -and with a marked ridge, forming a border between the disc and arms.Finally, in O. oedipus, the tooth line (not the ventral-most teeth) is truncated, while that of A. inornatum is more pointed.Besides, we found other slight differences between the species: genital slits are smaller and triangular-shaped in A. inornatum and longer and parallel in O. oedipus.In both species, oral papillae are granule-shaped, but these papillae are bigger in A. inornatum.Moreover, in O. oedipus, the arms have well-marked ridges, mostly proximally, and the proximal segments are widened dorsally, creating a median groove along the arm.However, A. inornatum does not have a well-marked ridge, but some specimens show the medial groove along the arm.According to Paterson (1985), these grooves can be related to gonadal development.Living colour of the species is orange-pink with purple hues on the dorsal part, dark underparts, almost black.This species was found, sometimes in large numbers, living on Acanthogorgiidae gorgonians.Family Gorgonocephalidae Ljungmanm, 1867 Genus Astrodendrum Döderlein, 1911 Astrodendrum juancarlosi sp.nov.urn:lsid:zoobank.org:act:ECD0622E-6FAF-4C72-B102-F1B94D8ECBFBFigs 3E-F, 7-9

Diagnosis
Species with small granule-like external ossicles, ending in a crystalline point, covering the dorsal and lateral interradial areas of the disc.Ventral disc areas and arms covered by domed granule-like external ossicles without any crystalline point.Two or three terminal projections on each arm spine; one secondary teeth on each valve.

Etymology
The specific epithet 'juancarlosi' was chosen as a tribute to Mr Juan Carlos Calero, father of the first author.

Description (holotype)
DISc.Five-lobed in shape, slightly excavated inter-radially (Fig. 8A), with no peripheral calcareous plates on rim.Radial shields tumid, long (almost raising the centre of disc) and narrow, which is deeply sunken (Fig. 8C).Radial shields completely concealed by external ossicles, bar-shaped, as wide proximally as distally, but more separated distally, converging towards centre of disc.Distally, radial shields end on enlarged, slightly concave and oval-shaped plate covered by minute granules (Fig. 8C-D).Dorsal disc covered by small granule-like external ossicles (Fig. 8A, C-D), each one ending in terminal crystalline point.At edge of disc, ossicles more densely packed and without crystalline point (Fig. 8C), and bigger in size between radial shields (Fig. 8C-D).Ossicles concealing radial shields similar to those from dorsal disc but more densely packed.Ventral inter-radial areas densely covered by mosaic of small irregular flat plates with granule-like external ossicles without terminal point.Oral shield, adoral shield, oral plates, along edge of mouth frame and ventral arm plates more densely covered by similar external ossicles.Mouth frame sunken (Fig. 8E).Interradial surface of lateral disc covered by external ossicles similar but smaller than those covering dorsal disc.Two large genital slits on each interradius running almost vertically along first five or six brachial segments after first fork (Fig. 8F).Conical external ossicles with terminal crystalline point more developed on adradial edge of genital slits.One oval-shaped and well-developed madreporite located just outside mouth frame (Fig. 8E).Both, tooth and oral papillae spiniform, especially larger apical ones.Mouth and infradental papillae form continuous series along mouth frame (Fig. 8E).Teeth varying in position and size, being irregular in outline and more or less irregularly disposed.ARMS.Arms branching, with first fork before disc margin and second one located at margin.Nevertheless, in smaller specimens (juvenile), first fork located on margin of disc.Arms tapering gradually towards tips, completely covered, both, dorsally and ventrally, by domed granule-like external ossicles (Fig. 9A); these granules somewhat bigger than disc ones and without any crystalline point.Dorsal side of arms carry pedicellarial bands along whole arms.Valves with one secondary tooth downwardly curved (Fig. 9C).Some sunken transverse furrow between segments, giving arms an annulated appearance.Indication observed of median furrow along arm (Fig. 8G).Ventral side of arms with noticeable transverse naked furrows between segments until second fork; afterwards, furrows become smaller, disappearing after third fork.First two pores without arm spine.Arm spines beginning at third pair of pores with only one small spine at third and fourth pair of pores, two arm spines (sometimes one) afterwards and three arm spines (sometimes two) after second fork.Arm spines short and wide, ending in two or three hyaline points (Fig. 9F).Vertebrae streptospondylous (Fig. 9G-K).
coloUR.Living specimens showing varying colours, from creamish-pink to dark orange and brown to gray (Fig. 3E-F) with clear ventral part; preserved specimens are white.
oSSIclE MoRpHoloGy.External ossicles on dorsal surface of disc, including radial shields, are granuleshaped and ending in a crystalline point (Fig. 9A).Baseplates oval-shaped with three to five tubercleshaped articulations for pedicellarial (Fig. 9D).External ossicles on baseplates granule-like shaped, approximately 200 µm in length and 100 µm in height (Fig. 9B).Valves with single inner tooth downwardly directed, and reticular structure (Fig. 9C).Lateral arm plates long, bar-like, with tuberculous stereom, spines placed in external lobe of plate (Fig. 9E).Arm spines ovoid-shaped with two or three small projections, not transforming into hook-shaped spines on distal portion (Fig. 9F).Vertebrae with hourglass-shaped streptospondylous articulations (Fig. 9G-K).Branching vertebra wider and with two surfaces for articulation.

Distribution
This species has been recorded in the Northwest African coast, from the Western Sahara to Guinea-Bissau waters.Its bathymetric distribution ranges between 47 and 797 m.

Remarks
The genus Astrodendrum was established by Döderlein (1911) for Gornocephalus sagaminus Döderlein, 1902.He realised that all species that belong to Gorgonocephalus Leach 1815 are characterised by the presence of a well-developed belt of calcareous plates at the margins of the disc.However, species of Astrodendrum have no ring of calcareous plates at the rim.Additionally, the arm spines appear before the first fork, as in Gorgonocephalus; however, in Astrodendrum Döderlein, 1911, these arm spines are much smaller, hardly reaching ⅓ of the segment length, and their number is reduced: with three (or rarely four) on each side.Taxonomic studies dealing with this genus are scarce, and we have only found a revision of the genus recently published by Okanishi & Fujita (2018).According to these authors, the genus is characterised by having five branching arms, with less than six segments before the first fork; lack of calcareous plates on the edge of the disc margin; variously shaped external ossicles or no ossicles on the disc; a madreporite placed on the innermost part of the interradial lateral disc; and valves from the dorsal arms with one secondary tooth.
In addition to the shape, size and arrangement of external ossicles -widely used as an important specific taxonomic character (Baker 1974(Baker , 1980;;McKnight 2000) - Okanishi and Fujita (2018) included the possibility of the lack of external ossicles (as in the case of A. laevigatum), and they also proposed three new taxonomic characters to distinguish species of Astrodendrum: • absence / presence of bulges on lateral ridges of proximal portion of arm • number of terminal projections of arm spines on proximal portion of arm • number of secondary teeth of hook-shaped arm spines on distal portion of the arm The main morphological features of all known species of Astrodendrum, including A. juancarlosi sp.nov., are summarized in Table 2.
Astrodendrum spinulosum differs from the rest of species by the presence of bulges on lateral ridges of proximal portion of the arm.
The new species here described, also differs from A. spinulosum by the number of terminal projections of arm spines on the proximal portion of the arm (three in the case of the new species and one in A. spinulosum).In addition, A. spinulosun has cone-shaped external ossicles, while A. juancarlosi sp.nov.has granule like ossicles ending in a crystalline point at the dorsal surface of the disc.
Astrodendrum juancarlosi sp.nov. is more similar to A. elingamita in the shape of the ventral coverage and the lack of a scale in the first tentacle pore.Nevertheless, A. elingamita has the first fork in the margin of the disc, while it is located before the margin in our species.The polygonal plates of the ventral covering are closer in the A. elingamita than in our specimen.Our specimens also differ from A. elingamita by having one type of dome-shaped granules with 1-2 hyaline terminal points rather than two smooth types.Astrodendrum sagaminum differs from Astrodendrum juancarlosi sp.nov. in also having two types of granules and naked arms and ventral disk.
Astrodendrum capense has several medium-sized conical tubercles along the radial shields; it also has some smaller conical tubercles along the inter-radial disc margin, both ending in small thorns.Moreover, the disc is closely covered with minute and smooth plates.
Astrodendrum galapagense has a dorsal coarse armament on the disc and arms.The external ossicles on the aboral disc are plate-shaped at periphery and conical at center, both slightly in contact, while on the oral surface has a few small widely scattered granules, except in the ventral interbrachial areas.
Astrodendrum laevigatum is covered by a thin, transparent, soft and perfectly smooth tegument without any granules or spines.According to the description of this species in the literature, there are some doubts about the inclusion of this species in the genus Astrodendrum.We consider necessary to review the type material before we can reach a conclusion on this issue.Therefore, in this paper we follow Okanishi & Fujita (2018) and keep the species within the genus Astrodendrum.
Finally, our specimen has marked rectangular furrows that are absent in the rest of the species of Astrodendrum.Even though Mortensen (1933) described the underside of the arms of A. capense as flat and without any grooves, he pointed out that this "may be an indication of a transverse furrow between the segments from the first forking onwards" (Mortensen 1933: 286).

Distribution
This species has an Indo-Pacific distribution.It has been recorded in South Africa from Cape Province to East London (Mortensen 1933), the Indonesian region (Döderlein 1927) and Flinders Islands (Bass Strait, Australia) (Clark 1916); its bathymetric range extends from 182 (Clark 1916) to 860 m (Clark & Courtman-Stock 1976).
Our material was recorded in one station in Guinea-Bissau waters, between 902 and 908 m.This material is the same as that reported by Calero et al. (2018).

Description
The dorsal side of disc covered by a skin with some scattered tubercles, ending in some small thorns.The same type of tubercles were found on the marginal belt of plates.
Radial shields long and bar-shaped, nearly reaching the centre of the disc (Fig. 11A).They are almost completely covered by tubercles similar to those from the interradial areas but slightly bigger (Fig. 11C).
The ventral interradial areas are almost fully covered by small granules.
Plates of the oral frame swollen and obscured by a thick skin.Oral shields with some scattered small granules.There is a cluster of slender apical papillae flanked on each side by smaller oral papillae.
Arms also covered by a skin concealing the plates.First pair of tentacle pores outside the mouth edge, without arm spines.Two arm spines from the second to fifth or sixth pores; afterwards, from the first fork on, three spines.Arm spines are small, less than one arm segment, and with some thorny ends.
First fork within the edge of the disc.Dorsally, arms covered by flat granules, and with a longitudinal median furrow (Fig. 11F).Pedicellarial bands along the arms, appearing from the first segments.

Remarks
Even though the single specimen collected was badly damaged, the presence of the main distinctive features of Gorgonocephalus pustulatum (H.L. Clark, 1916), like the number of spines (max.4), disc coverage (sparse and low tubercles) or the thin peripheral ring, legitimate our identification to species level.
Our finding in Guinea-Bissau represents the first record of G. pustulatum in the Tropical East Atlantic Ocean, extending its geographical distribution to the north, from south Africa to Guinea-Bissau.This station also represents the deepest record for this species (908 m).

Discussion
Twelve species belonging to the order Euryalida have been identified along the East Atlantic.The Euryalida fauna from this region is mainly composed by Atlantic species (9 species), with a minor component of widely distributed species (Fig. 12).The latter group includes Asteronyx loveni with Fig. 10.Map from the study area with the location of the stations where specimen of Gorgonocephalus pustulatum (H.L. Clark, 1916) was collected during the ten surveys off Northwest Africa.Further five species are Amphi-Atlantic (Astrodia tenuispina (Verrill 1884), Astrochele lymani Verrill, 1878, Gorgonocephalus arcticus Leach, 1819, Gorgonocephalus eucnemis Müller & Troschel, 1842 and Gorgonocephalus lamarckii (Müller & Troschel, 1842)) and the remaining four are exclusively Eastern Atlantic species.
Among these Atlantic species, seven species (the five Amphi-Atlantic species, Asteroschema inornatum and Gorgonocephalus caputmedusae (Linnaeus 1758)) are distributed throughout the Boreal and / or Lusitanian Provinces.
Astrospartus mediterraneus (Risso, 1826) is a common species in the Mediterranean Sea, and has also been reported in the Atlantic from Portugal and Morocco (Tortonese 1985).However, despite the great sampling effort deployed during our surveys in Northwest Africa, we have not found this species in the region.
Euryalida fauna from NW Africa seems to have a higher affinity to warm-temperate regions, while most of species know from the Eastern Atlantic have a cool-temperate affinity.
During this study, only five species of Euryalida have been collected.Among them, three species have a wide distribution, where Asteronyx loveni seems to be circum-global, and Gorgonocephalus pustulatum and Ophiocreas oedipus have been reported from scattered localities in warm-temperate waters from the Atlantic and Indo-Pacific oceans.Only Asteroschema inornatum shows a clear affinity to the borealtemperate fauna of the East Atlantic, with records from the Reykjanes Ridge to the Western Sahara.Finally, the new species Astrodendrum juancarlosi sp.nov.has only been found from the Western Sahara to Guinea Bissau.
Our results leave the question about the boundary between the Tropical East Atlantic and the Lusitania Provinces unresolved.Traditionally, this boundary has been established at Cape Vert (Senegal) by Briggs (1974Briggs ( , 1995) ) but at Cape Juby (north of Western Sahara) by Briggs & Bowen (2012), in their proposal of realignment of marine biogeographic provinces mainly based on fish distributions.Our study area, which falls within the CCLME region, is characterised by a mix of tropical and warm temperate waters (Pelegrí et al. 2017), where the turnover between warm temperate and tropical biotas occurs somewhere along the Mauritanian-Senegalese margin ( van Soest 1993).This question can be illustrated by Asteroschema inornatum, with a Boreal-Lusitanian distribution, whose southern limit of distribution is located in the Western Sahara (present paper), but also by Ophiocreas oedipus, whose Atlantic distribution stretches from Ascension Island (Lyman 1882) to Madeira (Koehler 1909).Calero (2017) and Calero et al. (2017) showed that in NW Africa other groups of Ophiuroidea seem to have a higher affinity with Atlantic-Mediterranean fauna (Boreal-Lusitanian Provinces), and similar results were obtained by Gil 2017;Gil & Ramil 2017;Gil et al. 2020.Nevertheless, in the same region other invertebrates, like decapod crustaceans (Matos-Pita 2015) and molluscs (Castillo 2017), display a clear affinity with the Tropical East Atlantic fauna but not with those of the Lusitania and Boreal Provinces.These different biogeographical affinities along NW Africa seems related with different dispersal strategies displayed by the benthic fauna (Matos-Pita 2015; Calero et al. 2017;Castillo 2017;Gil & Ramil 2017).However, their tolerance to different environmental conditions should also play a key role in the geographic distribution of marine species (Boero & Bouillon 1993), particularly in transition areas, such as the CCLME region.

Fig. 1 .
Fig. 1.Map from the study area with the location of the 1298 bottom trawling stations carried out during the ten surveys off Northwest Africa.

Fig. 2 .
Fig. 2. Map from the study area with the location of the stations where specimens of Asteronyx loveni Müller & Troschel, 1842 were collected during the ten surveys off Northwest Africa.

Fig. 6 .
Fig. 6.Map from the study area with the location of the stations where specimens of Ophiocreas oedipus Lyman, 1879 were collected during the ten surveys off Northwest Africa.

Fig. 7 .
Fig. 7. Map from the study area with the location of the stations where Astrodendrum juancarlosi sp.nov.were collected during the ten surveys off Northwest Africa.

Fig. 12 .
Fig. 12. Distribution of the main biogeographic components of species of Euryalida Lamarck, 1816 identified along the East Atlantic.
-IEOMA = Collection of Marine Fauna from the Oceanographic Centre of Málaga of the Spanish

Table 2
(continued on next page).Key features for species of Astrodendrum Döderlein, 1911 mainly based on the original descriptions; references included in the Table indicated different sources."-" means no data.