Ophiomyxa xispa Ordines & Ramírez-Amaro & Calero & Farriols & Massutí 2024, sp. nov.

Ophiomyxa xispa sp. nov. Ordines, Calero & Ramírez-Amaro

Figures 2 and 3

Type material. Holotype. CBB-UIB 100485, Ses Olives seamount, Mallorca Channel, Balearic Islands, western Mediterranean (38°57.38′N, 02°00.87′E) 235-263 m depth, rock dredge, R/V Ángeles Alvariño, Cruise INTEMARES- A22B_0718, St. 18, Francesc Ordines, 28 July 2018.

Comparative material. Ophiomyxa serpentaria: Senckenberg am Meer, German Centre for Marine Biodiversity Research in Hamburg (DZMB-HH) 61037 (one specimen), Reykjanes Ridge (60°14.86′N, 29°08.274′W) 718 m, ROV, R/V Maria S. Merian, Cruise IceAGE, St. 67-6, 13 July 2018. DZMB-HH 61728 and DZMB-HH 61729 (one specimen each), Reykjanes Ridge (60°14.25′N, 29°06.89′W) 644 m, ROV, R / V Maria S. Merian, Cruise IceAGE, St. 188-6, 1 August 2018. DZMB-HH 61728, Reykjanes Ridge (60°14.25′N, 29°06.89′W) 644 m, ROV, R / V Maria S. Merian, Cruise IceAGE, St. 188-6, 1 August 2018. Zoological collections of the Marine Zoology Laboratory at University of Vigo (LZM-UV) 7430 (three specimens), Morocco (35º15'31''N, 6º35'01''W), 874 m, bottom trawl, R / V Vizconde de Eza, Cruise Maroc-0411, St. MO-04, 14 November 2004. LZM-UV 16697 (one specimen), Western Sahara (26º15'48''N, 15º09'32''W), 843 m, bottom trawl, R / V Vizconde de Eza, Cruise Maroc-0511, St. MO 179, 10 December 2005. LZM-UV 6702 (one specimen), Western Sahara (26º12'42''N, 15º27'44''W), 1311 m, bottom trawl, R / V Vizconde de Eza, Cruise Maroc-0511, St. MO 184, 12 December 2005. LZM-UV 16725 (one specimen), Western Sahara (26º06'50''N, 15º26'49''W), 847 m, bottom trawl, R / V Vizconde de Eza, Cruise Maroc-0511, St. MO 185, 12 December 2005. LZM-UV 7624 (one specimens), Western Sahara (25º44'01''N, 15º56'01''W), 805 m, bottom trawl, R / V Vizconde de Eza, Cruise Maroc-0611, St. MO 281, 10 December 2006. LZM-UV 18008 (one specimens), Guinea Bissau (10º22'50''N, 17º19'08''W), 895 m, bottom trawl, R / V Vizconde de Eza, Cruise Bissau-0810, St. BS 156, 14 November 2004. Ophiomyxa pentagona: Centre Balear de Biodiversitat-Universitat de les Illes Balears (CBB-UIB) 100026 (one specimen), south Formentera, Balearic Islands, western Mediterranean (38°35.21′N, 01°26.51′E) 54 m depth, bottom trawl, R / V Miguel Oliver, Cruise MEDITS_ES_2023, St. 263, Francesc Ordines, 19 August 2023. CBB-UIB 100487 (one specimen), Menorca Channel, Balearic Islands, western Mediterranean (39°40.58′N, 03°32.12′E) 60 m depth, beam trawl, R/V Ángeles Alvariño, Cruise CANAL0419, St. 20, Francesc Ordines, 28 March 2019.

Etymology. The species name xispa is the name of the first author’s dog and also is the word in Catalan for spark, which alludes to the bright white spots on the brown background of the disk.

Diagnosis. The specimen is identified as belonging to the family Ophiomyxidae and genus Ophiomyxa due to the following combination of characters: disk, oral area, arms and arm spines covered by integument; radial shields very small (about 1/8 the disk diameter); broad infradental and oral papillae with serrated edge; second oral tentacle pore opens inside the mouth.

The specimen can be distinguished from the rest of Ophiomyxa species by the combination of the following characters: interradial marginal plates absent; arm spines 3; two thin, transparent and completely perforated dorsal arm plates on each segment, arranged longitudinally on the arm axis; ventral arm plates heptagonal, separated by lateral arm plates; disk integument full of transparent rounded scales and few scattered perforated ossicles; disk brown, covered with abundant scattered bright white spots.

Description. Disk diameter 6.1 mm with slightly indented interradial margins. Disk covered with thin smooth integument, transparent so it is possible to distinguish the jaws from the dorsal side (Figure 2A, B). The integument is full of thin transparent rounded scales, their diameter ranging from 150 μm to 210 μm, as well as some scattered perforated ossicles of diameter 140 to 160 μm and each bearing 5–12 perforations (Figures 2C and 3A). The integument also covers, but doesn’t obscure, the oral and adoral shields, the base of the oral plates, the arms and the arm spines. Radial shields small, about 0.4 mm in length (1/8 the disk radius) and 0.2 mm in width, barely visible through integument. No series of interradial marginal plates, but 2–4 perforated plates appear at the base of the arms between the radial shields. Genital slits short, 0.7 mm long, barely reaching the end of the 2 nd arm segment, ending 1 mm before the disk margin (Figure 2D). Adradial and abradial genital scales visible. Abradial genital scale almost in touch proximally with a comma-shaped plate partially overlapped by the oral shield (Figure 2D), the space in between filled with 1–3 small perforated plates.

Arms are approximately 38 mm long and 1 mm wide at the base. The ventral and lateral arm plates are barely visible through the integument in the live individual, whereas the dorsal arm plates are completely obscured. Once the individual was preserved in pure ethanol all arm plates were visible. The lateral arm plates are in contact ventrally from the second segment (Figure 2E), and are moderately extended dorsally. Dorsal arm plates are thin, delicate, transparent and completely perforated. They appear on the first two proximal segments as a continuous plate, with an ill-defined shape; from the third, each segment bears two plates, a proximal one nearly rounded but with very irregular margins, and a distal one larger also with irregular margins and nearly semicircular, the rounded edge oriented distally, with sides almost reaching the lateral arm plates (Figure 2F and 3B). Ventral arm plates heptagonal, with similar length and width, and separated by the lateral arm plates; on proximal segments they measure about 0.6 mm long and 0.55 mm wide; proximally they are sharply pointed whereas the distal end presents a deep notch (Figure 2E and 3C); all angles sharp. The 1 st ventral plate with similar shape and proportions than the rest but with rounded angles (Figure 2E). Each lateral arm plate bears three spines positioned laterally, with the middle spine at the lateral midline, some segments bearing only two spines per side. The spines are serrated (Figure 2G) and all three very similar in length. Proximally and midway down the arm they measure 0.5–0.6 mm in length (about equal or slightly less than the length of a segment) and 0.1 mm in width, then decreasing gradually to around 0.2 mm in length (about half the length of a segment) and 0.05 mm in width, at the tip of the arms, where the spines are hooked at the last segments. There is only one spine on the arm segments within the disk. No tentacle scales. Second oral tentacle pore opens inside the mouth.

Oral shields nearly triangular with rounded lateral angles, about two times wider than long. Adoral shields wide, nearly trapezoid-shaped with the proximal edge in contact with the oral plates but not touching each other, leaving a gap between adoral and oral shields and the oral plates (Figure 2D). Oral plates about 0.5 mm long and 0.2 mm wide. At each oral plate there are one infradental papillae and 1–3 lateral oral papillae. The infradental papillae is glassy, 1.5 higher than wide, with rounded serrated edge. The lateral oral papillae are smaller than the infradental, more triangular, about 3 times higher than wide, with serrated edge (Figure 2D). Dental plates bear three teeth, the ventralmost and the middle one similar to the infradental papillae (in two of the jaws not as serrated), the innermost about 2.5 higher than wide. Adoral shield spine pointed, well visible (Figure 2D).

Colour. Live specimen (Figure 2A): Dorsal surface of disk is brown, covered with abundant scattered bright white spots. The ventral disk surface is more transparent, appearing darker due to the stomach wall, and without or only with one white spot in each interradial space. Arms are orange dorsally and ventrally with tube feet a transparent white. Oral and adoral shields and oral plates and base of oral papillae orange. Preserved specimen (Figure 2B): the orange colour faded away completely and these parts appearing now white or transparent. The brown colour of the disk is now yellowish with white spots completely preserved and still standing out on the background.

Genetics and phylogeny. A fragment of 603 base pairs (bp) of the COI mitochondrial gene was sequenced. The nucleotide frequencies were T = 27.53, C = 27.03, A = 26.87 and G = 18.57. In general, high values of genetic distance as well as a high number of base pairs differences were detected between Ophiomyxa species, the average of both indices was of 17.6% and 106 pb differences. The new species Ophiomyxa xispa sp. nov. showed the closest genetic distance to O. stimpsonii (8.5% and 51 bp differences; Table 1). This genetic distance was among the closest interspecific distances observed of all the analyzed Ophiomyxa species. Closest distances were only found between O. vivipara and O. serpentaria (3.4% and 20 bp differences), O. tumida and O. brevicauda (5.6% and 34 bp differences) and O. crinita and O. bengalensis (7.3% and 44 bp differences). The phylogenetic reconstruction based on the COI fragment clearly separated O. xispa sp. nov. from the rest of species, and showed two main clades within the genus Ophiomyxa: one including O. xispa sp. nov., O. stimpsonii, O. neglecta, O. bengalensis, and O. crinita, and another including O. serpentaria, O. vivipara, O. anisacantha, O. brevirima, O. australis, O. flaccida, O. pentagona, O. brevicauda and O. tumida (Figure 4). Ophiomyxa stimpsonii appeared as the phylogenetically closest species to O. xispa sp. nov. Likewise, the species with a closer interspecific distance showed a closer phylogenetic relationship (Figure 4).

Ecology. The holotype was collected from a rocky bottom on the margin of Ses Olives seamount summit and the beginning of its upper flank. The rock dredge sample was mainly composed by coarse biogenic sand with mud and fragments of limestone crusts, with several sponges and brachiopods, as well as the bivalve Asperarca nodulosa (O.F. Müller, 1776) and the decapods crustaceans Plesionika edwardsii (Brandt, 1851) and Plesionika narval (Fabricius, 1787), all of them characteristic of rocky bottoms. The Ophiomyxa specimen was hidden inside a small crevice in one of the rock fragments (Figure 5). Despite a thorough sampling of the Mallorca Channel seamounts rocky and sedimentary bottoms (Figure 1), we have not recovered any other specimen of this species so far. However, high abundances of ophiuroids were detected in this area, particularly from sedimentary bottoms (Ordines et al. 2019; Massutí et al. 2022). So far, the species seems to be restricted to rocky bottoms.

Remarks. Ophiomyxa xispa sp. nov. is distinguished from O. pentagona, the only Ophiomyxa species recorded so far from the Mediterranean, by the number of arm spines (3 vs. 4–5, respectively), the shape of the ventral arm plates (as long as wide vs. 1.5–1.6 times wider than long, respectively; Figures 2E, 3C and 6A), and the shape and arrangement of dorsal arm plates: two plates, a proximal one nearly rounded, and a distal one larger nearly semicircular in O. xispa sp. nov. vs. two dorsal arm plates with triangular shape, about twice as wider as long, one on each side of the midline of the arm, where they are in contact; these plates are also in contact with the lateral arm plates (Figures 2F, 3B and 6B, C, D).

Our species morphologically resembles the subgroup of Ophiomyxa species characterised by the absence of a row of marginal interradial plates. The species with this character were previously distinguished as the genus Ophiodera Verrill, 1899, who differentiated it from Ophiomyxa mainly by the following characteristics (Verrill 1899; 1900): rudimentary marginal disk scales and absence of the disk-scales proximal to the radial shields, no upper arm plates, and, three or four arm-spines enclosed in cuticle. Verrill (1899) designated O. serpentaria as the type species for Ophiodera, and hence this genus is not currently accepted, as Mortensen (1927) considered it a synonym of Ophiomyxa. This synonymy was ignored by A. H. Clark when describing O. punctata as a member of Ophiodera (A.H. Clark 1952). Other species originally described as Ophiodera include O. compacta and O. neglecta, whereas O. stimpsonii was transferred to Ophiodera by Verrill (1900). The description of all these species fits within Ophiodera, with no interradial marginal scales or at least lacking the scales proximal to the radial shields as is the case for O. stimpsonii (Verrill 1900), no dorsal arm plates and 3–4 arm spines (rarely five in O. punctata and four proximally but five distally in O. compacta). Ophiomyxa bengalensis, described previously to the description of the genus Ophiodera, also shares the main differentiating characters of this genus and lacks interradial marginal plates, dorsal arm plates and has 3 arm spines (Koehler 1897). Finally, O. anisacantha H.L. Clark, 1911, originally described as Ophiomyxa, and O. crinita, have no interradial marginal plates and 3 (O. crinita) or 3–4 (O. anisacantha) arm spines, but both with dorsal arm plates present (Clark 1911; Franklin and O’Hara 2008).

Within Ophiodera and related species, our species morphologically resembles the most to O. anisacantha, O. bengalensis, O. crinita, O. neglecta and O. serpentaria, due to the combination of the absence of interradial marginal plates and the presence of three arm spines. However, it is easily distinguished by the shape and number of dorsal arm plates. Dorsal arm plates are small, fragmented (3–4 fragments) and only present in the proximal of the arm in O. bengalensis (Mortensen 1933a), and also presents the disk covered by rounded granulations (Koehler 1897). Ophiomyxa serpentaria was described as lacking dorsal arm plates (Lyman 1883; Mortensen 1927; Paterson 1985), but Mortensen (1933b) re-described this species, reporting the presence of one thin and transparent, regularly perforated large dorsal arm plate with semicircular shape in each segment, the rounded side oriented distally. This dorsal arm plates could also be observed in the sequenced individuals DZMB-HH 61037 (GenBank ID: ON341503) and DZMB-HH 61728 (GenBank ID: ON341511). Furthermore, O. serpentaria has ventral arm plates widely in contact (Mortensen 1927) vs. separated in our species. Ophiomyxa anisacantha has two larger dorsal arm plates on each segment, one on each side of the midline of the arm, where they are in touch, and a variable number of smaller plates proximally, connecting with the larger plates of the previous segment (Clark 1911). Ophiomyxa crinita has a large rhombic dorsal arm plate accompanied by three smaller ones, one overlaying the proximal edge of the large one and two proximal, one on each side of the arm midline (Franklin and O’Hara 2008). Ophiomyxa neglecta has a pair of large dorsal arm plates, one on each side of the arm midline which are not in contact but the space between them is filled by smaller plates (Koehler 1922). Moreover, among all these species, the presence of ossicles has only been reported for three of them, O. crinita and O. neglecta, both with C-shaped ossicles, in the stomach wall, and in the disk and arms integument, respectively, and O. serpentaria, with bone-shaped ossicles in the disk integument (Mortensen 1933b). We have not detected this type of ossicle in our species, but instead we record the presence of perforated plates in the disk integument, similar to those present in some holothurians.

The phylogenetic clade in which O. xispa sp. nov. is included in one group gathering species with an Indian Ocean (O. bengalensis and O. crinita) or western Pacific Ocean distribution (O. neglecta) (Koehler 1897, 1904; Franklin & O’Hara 2008), and another group including O. stimpsonii, distributed in the Caribbean Sea (western Atlantic Ocean) (Verrill 1899), and O. xispa sp. nov., so far only known from the Mediterranean. Paradoxically, the geographically closer species O. serpentaria and O. pentagona, distributed in the north eastern Atlantic Ocean and north eastern Atlantic Ocean and Mediterranean Sea, respectively (Mortensen 1927; Tortonese 1965), belong to the other detected phylogenetic clade, which also includes species distributed in the Caribbean (O. tumida, O. brevicauda, O. flaccida, the latter also southwards at least to Brazil) (Say 1825; Lyman 1883; Verrill 1899; Gondim et al. 2013), the western Pacific Ocean (O. australis, O. brevirima, O. anisacantha) and the south Atlantic Ocean (O. vivipara) (Studer 1876; Mortensen 1936). Besides the widespread distribution of the representatives of the two clades, so far, we have not been able to detect distinctive consistent morphological traits allowing to discern among them.