Echinoderes shahmaranae, Sørensen & B & B & B, 2021

Sørensen, Martin V., B, Maria Herranz, B, Fernando Pardos & B, Furkan Durucan, 2021, Kinorhynchs from sandy coastal habitats in Turkey, with the description of a new pan-Mediterranean species of Echinoderes (Cyclorhagida: Echinoderidae), Turkish Journal of Zoology 45 (7), pp. 526-549 : 529-537

Echinoderes shahmaranae sp. nov.

Figures 2A–2D , 3 , 4A–4I , 5A–5M, Tables 2–3

urn:lsid:zoobank.org:act:C423CEF8-D5B2-4B5E-99B3-510FD89F7F14

Synonymy: Echinoderes sp. 3 – Herranz 2009: pp. 37-42, Figures 13–14, Tables 10–11. Echinoderes sp. 3 – Herranz 2014: p. 25, Table 2.1.

Diagnosis: Echinoderes with long middorsal spines on segments 4, 6, and 8, with middorsal spine on segment 8 reaching at least the terminal segment; lateroventral spines present on segments 6 to 9. Tubes present in subdorsal and ventrolateral positions on segment 2, lateroventral positions on segment 5, lateral accessory positions on segment 8, and in laterodorsal positions on 10; laterodorsal tubes show sexual dimorphism. Very well-developed sublateral glandular cell outlets type 2 present on segment 2. Dorsal glandular cell outlets type 1 with following pattern on segments 1 to 9: middorsal on segments 1 to 3, 5 and 7, and paradorsal on segments 4, 6 and 8 to 9. Conspicuous strong bristles present in paraventral positions on segment 3 to 6. Tergal extensions form elongate triangular tips, with a minute tooth on each inferior margin. Females with lateral terminal accessory spines, and very minute laterodorsal tubes on segment 10. Males with well-developed laterodorsal tubes on segment 10; dorsal and ventral penile spines slender and tubular, while median penile spines are very stout and triangular.

Etymology: The species is named after the mythological creature Shahmaran (in Turkish Şahmeran) - ‘queen of serpents’ and half woman half serpent, known from Anatolian folklore ( Figure 1 , inset).

Material examined: Holotypic male, collected on Station 9 during SCUBA by F. Durucan on Sept. 13, 2019 from medium coarse sand at 8 m depth, near Fethiye, Muğla, Turkey (36.60251°N, 29.03095°E), ( Table 1, Figure 1 ); mounted in Fluoromount G between two cover slips attached to a plastic H-S slide, and deposited at the Natural History Museum of Demark under catalogue number NHMD-872854. Paratypes, three males and one female, same collection and mounting data as holotype, deposited under catalogue numbers NHMD-872855 to 872858. Additional material includes four males and one female with same collection and mounting data as holotype, mounted for SEM and stored in the first author’s personal reference collection. In addition, two males and one female, were collected with a Higgins meiobenthic dredge by F. Pardos on March 24, 1999 from fine sand at 30 m depth, near Blanes, Spain (41.657°N, 02.7995°E); mounted in Fluoromount G on glass slides, and deposited in the personal reference collection of F. Pardos. These three specimens are referred to as Echinoderes sp. 3 in the theses of Herranz (2009, 2014) .

Description: Long and slender adults with head, neck and eleven trunk segments ( Figures 2A–2B , 3 , 4A , 5A–5B). Single row of secondary pectinate fringe with pointed teeth present near anterior segment margin of segments 2 to 10. Sexual dimorphism restricted to segments 10 and 11 ( Figure 2C–2D ). For complete overview of measures and dimensions, see Table 2. Distribution of cuticular structures, i.e. sensory spots, glandular cell outlets, spines and tubes, is summarized in Table 3.

The head consists of a retractable mouth cone and an introvert ( Figure 3 ). Inner oral styles of mouth cone could not be examined. The external mouth cone armature consists of nine outer oral styles; bases of outer oral styles each flanked with a pair of short spikes; two central, distally bifurcated bristles are present more posteriorly (Figure 5C). A short transverse fringe is present at the base of the bifurcated bristles. The introvert sectors are defined by the ten primary spinoscalids in Ring 01 ( Figure 3 ). Each primary spinoscalid consists of a basal sheath and a distal end piece with a blunt tip (Figure 5D). The sheaths have, described from proximal towards distal parts: seven to nine transverse rows with extremely minute fringes; four long (two lateral and two central) fringe tips extending from the most distal transverse row; five similar (two lateral and three central), but slightly more distal long fringe tips; numerous long fringe tips marking the distal margin of the sheath. End pieces are flexible, and smooth except for very fine denticle-like hairs. Rings 02 and 04 have 10 spinoscalids and Rings 03 and 05 have 20 ( Figures 3 and 5D). All spinoscalids in these rings are well-developed, and consist of a basal sheath and a pointed end piece. The basal sheaths of Ring 02 spinoscalids have long fringes along their distal margins, whereas those of Ring 03 have shorter margin fringe tips, and a central spike-like tip on the proximal part of the sheath. The basal sheaths of Ring 04 spinoscalids have short marginal fringe tips, and proximally paired hand-like structures, resembling a wrist with 5-6 finger-like fringes. Basal sheaths of Ring 05 are short and have very short marginal fringes. Ring 06 has

Figure 5. Scanning electron micrographs showing overviews and details of Echinoderes shahmaranae sp. nov. (A) Lateral overview. (B) Ventral overview. (C) Mouth cone, ventral view. (D) Introvert section 5 (subdorsal); insert shows close-up of fringes on basal sheath of primary spinoscalids. (E) Segments 1 to 2, lateral view. (F) Segment 2, dorsal view. (G) Segments 1 to 2, ventral view. (H) Segments 4 to 5, dorsal view. (I) Segments 5 to 6, lateral view. (J) Segments 5 to 6, ventral view. (K) Segments 10 to 11, laterodorsal view, showing female sexual dimorphism. (L) Segment 8, lateral view. (M) Segments 10 to 11, laterodorsal view, showing male sexual dimorphism. Abbreviations: lat, lateral accessory tube; ldss, laterodorsal sensory spot; ldt, laterodorsal tube; ltas, lateral terminal accessory spine; lts, lateral terminal spine; lvs, lateroventral spine; lvt, lateroventral tube; mdgco1, middorsal glandular cell outlet type 1; mds, middorsal spine; mdss, middorsal sensory spot; mlss, midlateral sensory spot; oos, outer oral styles; pdgco1, paradorsal glandular cell outlet type 1; pdss, paradorsal sensory spot; pe, penile spines; pvb, paraventral bristles; psp, primary spinoscalid; sdss, subdorsal sensory spot; sdt, subdorsal tube; slgco2, sublateral glandular cell outlet type 2; sp, spinoscalid followed by introvert ring number; te, tergal extension; tr, trichoscalid; vlt, ventrolateral tube; vmss, ventromedial sensory spot.

only six spinoscalids, located in sectors 1, 3, 5, 6, 7, and 9; they resemble those in preceding sectors, but without the distinct differentiation into sheath and end piece. Ring 07 has 7 spinoscalids, located as pairs in sectors 3 and 9, unpaired but laterally displaced in sectors 5 and 7 (trichoscalids are taking up the space in the opposite side of each sector), and centrally unpaired in sector 1; ring 07 spinoscalids appear very simplified, and resemble thin fringes rather than actual scalids.

Described sector-wise ( Figure 3 ), sectors 1 and 6 are very similar, having spinoscalids arranged as two double diamonds; however, sector 1 has one additional central spinoscalid in Ring 07, whereas sector 6 has spinoscalids in Rings 02 to 06 only. Sectors 2, 4, 8 and 10 all have spinoscalids arranged as a quincunx, located in between an anterior spinoscalid in Ring 02 and a trichoscalid plate. Sectors 3 and 9 have spinoscalids forming double diamonds anterior to a pair of spinoscalids. Sectors 5 and 7 also have spinoscalids forming double diamonds, but anterior to an unpaired, lateral spinoscalid; the lateral spinoscalid is unpaired because a trichoscalid plate takes up the space in the opposite side of the sector. Regular trichoscalids with trichoscalid plates are present in sectors 2, 4, 5, 7, 8, and 10.

The neck has 16 placids, measuring 12 µm in length. The midventral placid is broadest, measuring 10 µm in width at its base, whereas all other are narrower, measuring 7 µm in width at their bases. The trichoscalid plates are well-developed, subdorsal and laterodorsal ones narrow and elongated, and ventromedial ones hat-shaped.

Segment 1 consists of a complete cuticular ring ( Figures 2A–2B , 4B–4C , 5E–5G). Sensory spots are located in subdorsal, laterodorsal and ventromedial positions; subdorsal ones are located on the anterior 1/3 of the segment, but not at the anterior margin; laterodorsal and ventromedial ones are located centrally on segment; sensory spots on this and following nine segments are very small and rounded, and sometimes flanked by at least one, but typically two long cuticular hairs. Glandular cell outlets type 1 present in middorsal and sublateral positions. Dorsal and lateral sides with a few cuticular hairs emerging through rounded perforation sites; ventral side nearly hairless. The posterior segment margin is straight around the segment, terminating into a pectinate fringe with very short, uniform fringe tips.

Segment 2 consists of a complete cuticular ring ( Figures 2A–2B , 4B–4C , 5E–5G). Pachycyclus of the anterior segment margin is of medium thickness and uninterrupted. Tubes are located in subdorsal and ventrolateral positions. Sensory spots are located in middorsal, laterodorsal and ventromedial positions. Large glandular cell outlets type 2 present in sublateral positions. Glandular cell outlets type 1 present in middorsal and ventromedial positions. Bracteate cuticular hairs are present on the dorsal and lateral sides of the segment, and arranged in four more or less welldefined transverse rows; the hairs in the posteriormost row are conspicuously longer than those in anterior ones; ventral side with one transverse row of short hairs, and disorganized patches with longer hairs in ventrolateral to ventromedial positions. The posterior segment margin is nearly straight; pectinate fringe with uniform tips, slightly longer than those on preceding segment.

Segment 3 ( Figures 2A–2B , 4B–4C ), and remaining segments, consisting of one tergal and two sternal plates. Pachycyclus of the anterior segment margin of medium thickness, and interrupted only at tergosternal junctions. Sensory spots present in subdorsal and sublateral positions. Glandular cell outlets type 1 present in middorsal and ventromedial positions. Cuticular hairs as on preceding segment, but in addition with a pair of paraventral patches each with three long, thick and highly conspicuous bristle-like hairs ( Figures 2B and 4C ; but see also 4E and 5J). Pectinate fringe of posterior margin hairs as on preceding segment.

Segment 4 ( Figures 2A–2B , 4D , 5H) with long acicular spine in middorsal position, extending to or even beyond the posterior margin of segment 6. Sensory spots not present. Glandular cell outlets type 1 present in paradorsal and ventromedial positions. Cuticular hair patterns, inclusive paraventral patches with stiff bristle-like hairs, as on preceding segment. Pachycycli and pectinate fringe of posterior margin as on preceding segment.

Segment 5 ( Figures 2A–2B , 4D–4E , 5H–5J) with tubes in lateroventral positions. Sensory spots present in subdorsal and ventromedial positions. Glandular cell outlets type 1 present in middorsal and ventromedial positions. Pectinate fringe of posterior segment margin slightly longer than those on preceding segment. Pachycycli and cuticular hairs, inclusive paraventral patches with stiff bristle-like hairs, as on preceding segment.

Segment 6 ( Figures 2A–2B , 4D, 4F , 5I–5J) with long acicular spine in middorsal position, extending to or even beyond the posterior margin of segment 8; additional acicular spines also present in lateroventral positions. Sensory spots present in paradorsal, midlateral and ventromedial positions. Glandular cell outlets type 1 present in paradorsal and ventromedial positions. Pachycycli, pectinate fringe at posterior segment margin, and cuticular hairs, inclusive paraventral patches with stiff bristle-like hairs, as on preceding segment.

Segment 7 ( Figures 2A–2B , 4D, 4F ) with acicular spines in lateroventral positions. Sensory spots present in subdorsal, midlateral and ventromedial positions. Glandular cell outlets type 1 present in middorsal and ventromedial positions. Cuticular hair patterns as on preceding segment, but without the paraventral patches with stiff bristle-like hairs; midventral to paraventral areas instead covered with minute bracteate hairs. Pachycycli and pectinate fringe of posterior segment margin as on preceding segment.

Segment 8 ( Figures 2A–2B , 4F–4G , 5L) with long acicular spine in middorsal position, extending to or beyond the terminal segment; additional acicular spines present in lateroventral positions, and tubes in lateral accessory positions. Sensory spots present in paradorsal positions. Glandular cell outlets type 1 present in paradorsal and ventromedial positions. Pachycycli, pectinate fringe of posterior segment margin and cuticular hairs as on preceding segment.

Segment 9 ( Figures 2A–2B , 4G , 5K) with acicular spines in lateroventral positions. Sensory spots present in paradorsal, subdorsal, and ventrolateral positions. Glandular cell outlets type 1 present in paradorsal and ventromedial positions. Nephridial sieve plates could not be observed in any specimens. Pachycycli, pectinate fringe of posterior segment margin and cuticular hairs as on preceding segment.

Segment 10 ( Figures 2 , 4H–4I , 5K, 5M) with tubes in laterodorsal position, inserting on posterior part of segment, but not at the posterior segment margin; tubes in females extremely short, only 2–3 µm ( Figures 2A and 5K), not even reaching the posterior segment margin; tubes in males about 11 µm and extending well beyond posterior segment margin ( Figures 2C and 5M). Sensory spots present in subdorsal and ventrolateral positions. Glandular cell outlets type 1 present as two longitudinally arranged middorsal ones and in ventromedial positions. The posterior segment margin of the tergal plate is straight, whereas margins of sternal plates are deeply concave; fringe tips of pectinate fringe are shorter and thinner than those on preceding segments. Cuticular hairs as middorsal and ventromedial patches of short bracteate hairs, and patches with longer hairs in midlateral to ventromedial areas. Pachycycli as on preceding segment.

Segment 11 with lateral terminal spines ( Figures 2 , 4H–4I , 5K, 5M). Males with three pairs of penile spines; dorsal and ventral penile spines are thin, flexible tubes, and ventral one (ca. 27 µm in length) is considerably longer than the dorsal one (ca. 17 µm in length), whereas the median penile spine is short, but very stout and triangular, and with distal longitudinal furrows; females with short, thin lateral terminal accessory spines. Sensory spots present in paradorsal positions. Segment basically without hairs, except for inferior surfaces of tergal extension that are densely covered with nonbracteate hair-like extensions. Tergal extensions are well-spaced, triangular and pointed, with small tooth at inferior margin; sternal extensions shorter, and triangular to rounded.

Notes on diagnostic characters: Echinoderes shahmaranae sp. nov. is very easily distinguished from all known congeners, since the combined spine, tube and glandular cell type 2 distribution is unique for this species.

The arrangement of cuticular structures on segment 2 is in itself an easy way to distinguish E. shahmaranae sp. nov. from most other echinoderids. The presence of tubes in subdorsal and ventrolateral positions, combined with sublateral glandular cell outlets type 2 are only shared with five other species. This combination is described from Echinoderes rociae Pardos et al., 2016a and E. brevipes Cepeda et al., 2019 (see Pardos et al., 2016a; Cepeda et al., 2019), and reexaminations carried out during the preparation for the virtual identification key of Yamasaki et al. (2020) revealed the same character combination in E. abbreviatus Higgins, 1983 . However, these three Caribbean species are characterised by having very short and stout lateral terminal spines ( Higgins, 1983; Pardos et al., 2016a; Cepeda et al., 2019), and cannot possibly be confused with E. shahmaranae sp. nov.

Another species with similar arrangement of cuticular structures on segment 2 is the Portuguese E. reicherti Neves et al., 2016 , but with its single and relatively short middorsal spine, located on segment 4 ( Neves et al., 2016), it cannot be confused with E. shahmaranae sp. nov. either. The fifth species with a similar arrangement on segment 2 is the Caribbean species E. intermedius SØrensen, 2006. The species was originally described as having three pairs of tubes on segment 2 ( SØrensen, 2006), but Pardos et al. (2016a) redescribed it and clarified that cuticular structures on segment 2 included subdorsal and ventrolateral tubes, and sublateral glandular cell outlets type 2 – same arrangement as in the new species. E. intermedius is therefore the species that shows closest resemblance with the new species, but it differs by having lateral accessory tubes on segments 6 and 7, as well as laterodorsal tubes on segment 8.

Another diagnostic character of interest is the strong bristle-like hairs in paraventral positions. In the new species, these bristle-like hairs always appear in groups of three on each sternal plate, from segments 3 to 6. The hairs are very conspicuous in both LM and SEM ( Figures 4E–4F , 5J), and especially SEM demonstrates that the bristle-like hairs are more than twice as thick as any other bracteate cuticular hair in the animal. This presence of paraventral hairs is a character that has obtained very limited attention in previous echinoderid descriptions. Interestingly though, such bristle-like hairs also seem to be present to the two last mentioned species above, E. reicherti and E. intermedius . This character trait, its occurrence among echinoderids, and potential phylogenetic implications will be addressed further in the Discussion below.

3.2. New records of Echinoderes gerardi Higgins, 1978

Material examined: The species was abundant, and it appeared at all stations in this study (see Table 1 for station data). All specimens mounted for LM are deposited at NHMD (see Table 1 for catalogue numbers), and all SEM specimens are stored in the reference collection of the first author.

Notes on morphology, habitat and distribution: The examined specimens followed the emended species diagnosis proposed by SØrensen et al. (2020). This study demonstrated that E. gerardi and E. dujardinii Claparède, 1863 show very close resemblance, and mostly can be distinguished by the shorter, and somehow lanceolate, middorsal spines in E. gerardi . The results of SØrensen et al. (2020) also indicated that E. gerardi seemed to have a Mediterranean distribution, whereas E. dujardinii is East Atlantic/West European. The specimens examined in the present study agree with this, both in terms of morphology and distribution. SØrensen et al. (2020) furthermore suggested that E. gerardi and other species of the E. dujardinii group seem to be very opportunistic in terms of habitat/substrate choice. This is also supported by the present study, where specimens of E. gerardi were found in a range of substrates, from fine- to medium coarse sand, as well as Neptune grass and coralline red algae.

Echinoderes gerardi appears to be a very common species throughout the Mediterranean, and besides its type locality in Tunisia ( Higgins, 1978), it has been found in Spain (identified as E. dujardinii ( Sánchez-Tocino et al., 2011, Sánchez et al., 2012) but see SØrensen et al. (2020)), Sicily (Dal Zotto and Todaro, 2016), and at several localities around Turkey, inclusive the coast of Antalya ( SØrensen et al., 2020), the Aegean coast ( Sönmez et al., 2016, SØrensen et al. 2020) and Black Sea coast (identified as E. dujardinii ( Ürkmez et al., 2016) but see SØrensen et al. (2020)). The present study stresses that E. gerardi seems to be one of the most common kinorhynch species around Turkey, and we can probably expect to find it throughout the Turkish coastline. The species’ morphology is already well-documented (see SØrensen et al., 2020), thus we find it redundant to provide further photo documentation in the present contribution.

Figures

Figure 1. Map showing all kinorhynch reports from Turkey, including species reported in the present contribution (species names appear with flags marking the sampling localities) and previously reported species (superscript number after species names refers to bibliographic references: 1) Ürkmez et al., 2016;2) Sönmez et al., 2016; 3) Yıldız et al., 2016; 4) Yamasaki et al., 2018;5) Yamasaki and Durucan, 2018;6) SØrensen et al., 2020). Inset: Shahmaran, the Anatolian serpent queen; source: Wikimedia.

Figure 2. Line art illustrations of Echinoderes shahmaranae sp. nov. (A) Female, dorsal view. (B) Female, ventral view. (C) Segments 10 to 11 in male, dorsal view. (D) Segments 10 to 11 in male, ventral view. Abbreviations: lat, lateral accessory tube; ldt, laterodorsal tube; ltas, lateral terminal accessory spine; lts, lateral terminal spine; lvs, lateroventral spine; lvt, lateroventral tube; mdgco1, middorsal glandular cell outlet type 1; mds, middorsal spine; mlss, midlateral sensory spot; pdgco1, paradorsal glandular cell outlet type 1; pe, penile spines; pvb, paraventral bristles; sdss, subdorsal sensory spot; sdt, subdorsal tube; slgco1/2, sublateral glandular cell outlet type 1/2; slss, sublateral sensory spot; vlss, ventrolateral sensory spot; vlt, ventrolateral tube; vmss, ventromedial sensory spot.

Figure 3. Diagram of mouth cone (grey area), introvert and placids in Echinoderes shahmaranae sp. nov., showing distribution of inner oral styles (full circles), outer oral styles (diamonds), primary scalids (triangles), spinoscalids (fat open circles), and trichoscalids (stars), with positions of trichoscalid plates and placids indicated. Table shows the scalid arrangement by sector; single-lined boxes mark quincunxes, double- lined boxes mark “double diamonds”.

Figure 4. Light micrographs showing overviews and details of (A–H) male holotype, NHMD-872854, and (I) female paratype, NHMD- 872856, of Echinoderes shahmaranae sp. nov. from Fethiye, Turkey.(A) Ventral overview.(B) Segments 1 to 3, dorsal view. (C) Segments 1 to 3, ventral view. (D) Segments 4 to 8, dorsal view. (E) Segment 5, ventral view. (F) Segments 6 to 8, ventral view. (G) Segments 8 to 10, dorsal view. (H) Detail of segments 10 to 11, dorsal view, showing male sexual dimorphism. (I) Segments 10 to 11, ventral view, showing female sexual dimorphism. Abbreviations: lat, lateral accessory tube; ldt, laterodorsal tube; ltas, lateral terminal accessory spine; lts, lateral terminal spine; lvs, lateroventral spine; lvt, lateroventral tube; mds, middorsal spine; pdgco1, paradorsal glandular cell outlet type 1; pe, penile spine; pvb, paraventral bristles; sdtu, subdorsal tubes; slgco2, sublateral glandular cell outlet type 2; te, tergal extensions; vlt, ventrolateral tubes.