Echinoderes sensibilis Adrianov, Murakami & Shirayama, 2002

Sørensen, Martin V., Goetz, Freya E., Herranz, María, Chang, Cheon Young, Chatterjee, Tapas, Durucan, Furkan, Neves, Ricardo C., Yildiz, N. Özlem, Norenburg, Jon & Yamasaki, Hiroshi, 2020, Description, redescription and revision of sixteen putatively closely related species of Echinoderes (Kinorhyncha: Cyclorhagida), with the proposition of a new species group - the Echinoderes dujardinii group, European Journal of Taxonomy 730, pp. 1-101 : 39-49

Echinoderes sensibilis Adrianov, Murakami & Shirayama, 2002

Figs 11–15 ; Tables 11–12

Emended diagnosis

Echinoderes with short middorsal spines on segments 4 to 8, and lateroventral spines on segments 6 to 9; middorsal spines on posterior segments barely or just reaching the posterior margin of their respective segments. Tubes present in lateroventral positions on segments 2 and 5, and in laterodorsal positions on 10. Minute glandular cell outlets type 2 in midlateral positions on segments 8 and 9. Tergal extensions of segment 11 short, pointed and well-spaced; sternal extensions short, with ventrolateral seta-like tuft of extended fringe tips. Females with ventromedial female papillae resembling glandular cell outlets type 2 on segments 6 to 8; intracuticular substructure of female papillae crescentic on segment 6, and tubular on segments 7 and 8.

Material examined

Holotype

JAPAN • ♂; Honshu Island , Tanabe Bay ; 33°42′12″ N, 135°22′54″ E; 0 m b.s.l.; Mar. 2001; A. Adrianov, C. Murakami and Y. Shirayama leg.; calcareous red algae ( Corallina pilulifera ) in tidal pool; SMBL CM-A-JAP-E04 . Specimen mounted for LM.

Paratypes

JAPAN • 3 ♂♂; same collection data as for holotype; SMBL CM-A-JAP-E01 , CM-A-JAP-E05 and CM-A-JAP-E08 .

Specimens mounted for LM. One specimen was incorrectly identified as female in the original description.

Additional material

JAPAN • 1 ♀; Honshu Island , Tanabe Bay ; 33°41′31″ N, 135°20′10″ E; 0 m b.s.l.; 12 Sep. 2012; H. Yamasaki leg.; detritus and mixed sediment in tidal pool; GenBank: LC557098 ; ICHUM-6127 .

DNA was extracted from this specimen, and cytochrome oxidase subunit 1 was sequenced. The cuticle of the specimen was subsequently recovered and mounted for LM ( ICHUM- 6127).

JAPAN • 3 ♂♂; same collection data as specimen above; personal reference collection of the last author. Specimens mounted for SEM.

Additional specimens from the same locality were collected by C.Y. Chang, mounted for SEM, and stored in the personal reference collection of the first author.

JAPAN • 1 ♀; Okinawa, Sesoko Station ; 26°39′00″ N, 127°51′22″ E; 0 m b.s.l.; 10 Nov. 2016; S. Fujimoto leg.; coarse sand in tidal pool; NHMD-115257 . Specimen mounted for LM .

REPUBLIC OF KOREA • 2 ♂♂; Korean west coast, Wido Island ; 35°36′52″ N, 126°17′01″ E; 0 m b.s.l.; 31 Feb. 2000; J. Lee and Y.H. Song leg.; intertidal macroalgae; NHMD-664200 , NHMD-664201 • 1 ♀, 1 ♂; Jeju Island , Gimnyeong ; 33°33′33″ N, 126°45′16″ E; 0 m b.s.l.; 1 Mar. 2000; C.Y. Chang, J. Lee and Y.H. Song leg.; intertidal macroalgae; NHMD-664202 , NHMD-664203 • 1 ♂; Jeju Island , Udo Islet ; 33°31′03″ N, 126°57′40″ E; 0 m b.s.l.; 3 May 2000; C.Y. Chang and J. Lee leg.; intertidal macroalgae; NHMD-664204 .

All Korean specimens mounted for LM.

HAWAII • 4 ♀♀, 6♂♂; Oahu, Kaneohe Bay, lagoon at Coconut Island , St. MVS-0224-HI-01 (= workshop St. KANM005); 21°26′09″ N, 157°47′18″ W; 0,5 m b.s.l.; 22 May 2017; M. V. Sørensen leg.; subtidal black mud, rich in organic matter; GenBank: MT999943 ; NHMD-662049 to 662058 .

Specimens were mounted for LM. Additional 5 ♀♀, 5 ♂♂ collected at the same station were mounted for SEM and stored in the first author’s personal reference collection. One specimen was picked up for molecular barcoding and a 625 bp long cytochrome oxidase subunit 1 sequence was deposited in GenBank under accession number MT999943 ; the cuticle could not be recovered afterwards, but the specimen used for DNA extraction is shown on Fig. 11 .

HAWAII • 6 ♀♀, 4 ♂♂; Oahu, Kaneohe Bay, He’ia Fish Pond , St. MVS-0229-HI-06 (= St. KANM034); 21°26′05″ N, 157°48′19″ W; 3 m b.s.l.; 24 May 2017; workshop participants leg.; subtidal black mud, very rich in organic matter; NHMD-662059 to 662068 .

Specimens were mounted for LM. Additional 7 ♀♀, 3 ♂♂ collected at the same station were mounted for SEM and stored in the first author’s personal reference collection.

See Table 1 for an overview.

Redescription

Since the present redescription adds several new features to the species, including information on head structures, observations of live material, and significant diagnostic traits, and since the distributional range of the species is extended considerably, we are providing a full description for the species. As much information as possible is based on observations of the type material, but the specimens are partly deteriorated, hence structures such as sensory spots could no longer be observed. Additional information is primary based on examination of topotypes, supplemented with information from Okinawa and Hawaii populations that morphologically agreed completely with the topotypes.

Adults with head, neck and eleven trunk segments ( Figs 11–13 , 14A , 15A ). Glandular cells appear brown-red in live specimens, giving the species a conspicuous longitudinal colour pattern along its trunk ( Fig. 11 ). The colouring fades, and eventually disappears, when the animal is fixed. The trunk appears stout, with nearly equally broad sternal plates on segments 6 to 10 ( Figs 11A, C , 14A ). Segments 1 to 4 were often strongly contracted in fixed specimens. Lateral terminal spines slender, from 40% to 55% of trunk length. For complete overview of measurements and dimensions, see Table 11 . Secondary pectinate fringe present near anterior segment margin on segments 2 to 10, but it is usually covered by the preceding segment. Distribution of cuticular structures, i.e., sensory spots, glandular cell outlets, spines and tubes, is summarized in Table 12.

The head consists of a retractable mouth cone and an introvert ( Figs 13 , 15 B–C). Three rings of inner oral styles present, with five styles in each ring ( Fig. 13 ). The external mouth cone armature consists of nine outer oral styles; bases of outer oral styles each with a V-shaped row of short fringe tips and a central bristle of much longer fringe tips ( Fig. 15B ). The introvert sectors are defined by the ten primary spinoscalids in Ring 01 ( Figs 13 , 15C ). Each primary spinoscalid consists of a basal sheath and a distal end piece with a blunt tip. The sheaths have a well-defined basal, transverse fringe, and a less distinct fringe more distally on their exterior surfaces; fringe tips of the distal fringe attach along a longitudinal line and alternatingly projects to the left and to the right (see inset Fig. 4B for a similar morphology in a different species). End pieces are smooth and flexible. Rings 02 and 04 have 10 spinoscalids and Rings 03 and 05 have 20. All spinoscalids in these rings are well-developed, and consist of a basal sheath and a pointed end piece ( Fig. 15C ). The basal sheaths terminate into fine, fringed margins in spinoscalids of Rings 02 to 05, and those of Rings 03 to 05 have in addition a basal median spike. A ring of short fringes extend around the introvert in between spinoscalid Rings 04 and 05. Ring 06 has only six spinoscalids, located in sectors 1, 3, 5, 6, 7, and 9 ( Fig. 13 ); Ring 06 spinoscalids resemble those in preceding sectors, but without a distinct differentiation into sheath and end piece. Ring 07 also has 6 spinoscalids, located as pairs in sectors 3 and 9, and unpaired but laterally displaced in sectors 5 and 7 (trichoscalids are taking up the space in the opposite side of each sector); Ring 07 spinoscalids resemble those in preceding sector.

Described sector-wise ( Fig. 13 ), sectors 1 and 6 are similar, having spinoscalids arranged as two double diamonds. Sectors 2, 4, 8 and 10 all have spinoscalids arranged as a quincunx, located in between a medial anterior spinoscalid (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 ( Fig. 13 ).

Regular trichoscalids with trichoscalid plates are present in sectors 2, 4, 5, 7, 8, and 10. In addition, a single trichoscalid without trichoscalid plate is present in sector 1 ( Figs 13 , 14H , 15C ). The trichoscalid has the typical furry appearance ( Figs 14H , 15C ), but basally it also has a series of more well-organized pointed denticles.

The neck has 16 placids, measuring 18 µm in length. The midventral placid is broadest, measuring 15 µm in width at its base, whereas all other are narrower, measuring 11 µm in width at their bases. The trichoscalid plates are well-developed; subdorsal and laterodorsal ones are narrow and elongated, and ventromedial ones broadly oval.

Segment 1 consists of a complete cuticular ring. Sensory spots are located near the anterior margin in subdorsal and laterodorsal positions, and slightly more posterior in sublateral and ventromedial positions ( Figs 12 A–B, 14B, 15D–E); sensory spots are large, and rounded to oval, with numerous micropapillae, two pores, and often a cilium emerging from one of the pores. Glandular cell outlets type 1 present in middorsal and lateroventral positions ( Figs 12 A–B, 14B–C, 15D–E); all glandular cells with type 1 outlets on this and following segments with conspicuous brown-red colouring that gets lost during fixation ( Fig. 11 A–B). Dorsal and lateral sides, and posterior half of ventral side, with scattered cuticular hairs emerging through rounded perforation sites. The posterior segment margin is straight around the segment, terminating into a pectinate fringe with short, uniform fringe tips.

Segment 2 consists of a complete cuticular ring. Pachycyclus of the anterior segment margin is of medium thickness and not interrupted ( Figs 11B , 14 A–C). Sensory spots are located in middorsal (but slightly laterally displaced), laterodorsal (twin pair) and ventromedial positions ( Figs 12 A–B, 15D–E); sensory spots on this and all following segments as on segment 1, but slightly smaller. Glandular cell outlets type 1 present in middorsal and ventromedial positions, and quite well-developed tubes present in lateroventral positions ( Figs 12 A–B, 14B–C, 15D–E). The segment is densely covered with bracteate hairs; hair cover slightly thinner between ventromedial sensory spots. The posterior segment margin is nearly straight; pectinate fringe from middorsal to midlateral positions with short fringe tips, as on segment 1; fringe tips from midlateral to ventromedial positions conspicuously longer, and then again very short between ventromedial positions.

Segment 3, 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 ( Figs 11 B–C, 14C). Sensory spots present in subdorsal, laterodorsal and sublateral positions ( Fig. 12 A– B). Glandular cell outlets type 1 present in middorsal and ventromedial positions ( Figs 12 A–B, 14B–C). Bracteate cuticular hairs are densely covering the segment from middorsal to ventromedial positions; paraventral areas densely covered by non-bracteate, hair-like extensions. Pectinate fringe of posterior margin hairs as on preceding segment.

Segment 4 with short acicular spine in middorsal position, not reaching the posterior margin of the segment ( Figs 12A , 14B ). Sensory spots present in subdorsal, midlateral and ventromedial positions ( Fig. 12 A–B); midlateral and ventromedial sensory spots considerably smaller than all other sensory spots in the species, but they occur consistently in all examined specimens. Glandular cell outlets type 1 present in subdorsal and ventromedial positions ( Figs 12 A–B, 14B–C). Pectinate fringe of posterior segment margin with long fringe tips from middorsal to ventromedial positions, and with very short tips between ventromedial positions. Pachycycli and cuticular hairs as on preceding segment.

Segment 5 with short acicular spine in middorsal position, not reaching the posterior margin of the segment ( Figs 12A , 14D ), and well-developed tubes in lateroventral positions ( Figs 12B , 14E ). Sensory spots present in subdorsal, midlateral and ventromedial positions ( Fig. 12 A–B). Glandular cell outlets type 1, pachycycli, pectinate fringe of posterior margin and cuticular hairs as on preceding segment.

Segment 6 with short acicular spines in middorsal and lateroventral positions ( Figs 12 A–B, 14D– E, 14G–H), not reaching the posterior margin of the segment. Sensory spots present in paradorsal, subdorsal, midlateral and ventromedial positions ( Figs 12 A–B, 15G). Females with female papillae in ventromedial positions, close to and lateral to sensory spots ( Figs 12B , 14E , 15H ); openings of papillae resemble small glandular cell outlets type 2 ( Fig. 15H ), and intracuticular substructures each form a semicircle with a small protuberance in the curved part of the structure ( Fig. 14E ). Glandular cell outlets type 1, pachycycli, pectinate fringe of posterior margin and cuticular hairs as on preceding segment.

Segment 7 with short acicular spines in middorsal and lateroventral positions, barely reaching the posterior margin of the segment ( Figs 12 A–B, 14D–E, 15G–I). Females with female papillae as on segment 6, but with openings slightly more anterior and lateral to sensory spots ( Figs 12B , 14E , 15 H–I); the substructure of these papillae differs from those on preceding segment, and forms instead a small intracuticular tube ( Fig. 14E ). Sensory spots, glandular cell outlets type 1, pachycycli, pectinate fringe of posterior margin and cuticular hairs as on preceding segment.

Segment 8 with short acicular spines in middorsal and lateroventral positions, barely or just reaching the posterior margin of the segment ( Figs 12 A–B, 14D–G, 15G, I). Minute glandular cell outlets type 2 present in midlateral positions, but very close to the laterodorsal areas ( Figs 12A , 14G , 15F ). Sensory spots present in paradorsal, subdorsal, midlateral (posterior to glandular cell outlets), ventrolateral positions ( Figs 12 A–B, 15F, I). Females with female papillae similar to those on segment 7, but with

openings slightly more anterior and closer to midventral line ( Figs 12B , 14E , 15I ). Glandular cell outlets type 1, pachycycli, pectinate fringe of posterior margin and cuticular hairs as on preceding segment.

Segment 9 with acicular spines in lateroventral positions, just reaching the posterior margin of the segment ( Figs 12B , 15F ). Sensory spots, glandular cell outlets type 1 and 2 as on preceding segment, but female papillae not present ( Figs 12 A–B, 14F–G, 15F). Small, rounded nephridial sieve plates present in lateral accessory positions. Pectinate fringe of posterior segment margin with uniformly long fringe tips around the segment. Pachycycli and cuticular hairs as on preceding segment.

Segment 10 with well-developed laterodorsal tubes near posterior segment margin ( Figs 12 , 14J , 15 J–L). Sensory spots present in subdorsal (but close to paradorsal) positions ( Figs 12A, C , 15J, L ); males furthermore with sensory spots in ventrolateral positions ( Fig. 12D ). Glandular cell outlets type 1 present as two longitudinally arranged middorsal ones and in ventromedial positions ( Figs 12 , 14I ). The posterior segment margin of the tergal plate is straight, whereas margins of sternal plates are concave and extend midventrally into a point that almost reaches the posterior margin of the terminal segment; fringe tips of pectinate fringe are considerably shorter than those on preceding segments. Pachycycli and cuticular hairs as on preceding segment.

Segment 11 with lateral terminal spines ( Figs 11A , 12 A–B, 14A). Males with three pairs of penile spines ( Figs 12 C–D, 14J, 15K–L); dorsal and ventral penile spines are thin, flexible tubes, whereas the median ones are slightly thicker, conical, and more rigid; females with short, thin lateral terminal accessory spines ( Figs 12 A–B, 14I, 15J). Two pairs of sensory spots present in subdorsal positions and one pair in ventrolateral positions; one pair of subdorsal sensory spots medially on segment, other pair at posterior margin ( Fig. 15J ). Glandular cell outlets type 1 present as two longitudinally arranged middorsal ones and in subdorsal positions, anterior on segment. The dorsal and most of the ventral side of the segment are densely covered with non-bracteate hair-like extensions. Tergal extensions are wellspaced, short and pointed ( Figs 12 , 14 I–J, 15J, L); sternal extensions short, with ventrolateral seta-like tuft of extended fringe tips ( Figs 14J , 15J ).

Notes on habitat and ecology

The specimens collected in Kaneohe Bay, Hawaii, showed a very clear preference for muddy localities, rich in organic matter. They seemed to thrive very well in it, and appeared in high numbers. Especially at the locality in He’ia Fish Pond (St. MVS-0229-HI-06) – an 800 year old fish pond established by isolating a part of the coastal water with a 2 km long lava rock wall – specimens of E. sensibilis occurred in ball-like aggregations composed of detritus, and up to 40 specimens. At low magnification, these balls would just resemble detritus pellets, but by gently opening the ball with a needle, it would appear that the balls mainly consisted of mass aggregated kinorhynchs.

Figures

Fig. 11. Light micrographs showing overviews of live female of Echinoderes sensibilis Adrianov et al., 2002 from Coconut Island, Oahu, Hawaii (USNM-1616695). Note the brown-red glandular cells. DNA was subsequently extracted from the specimen and it is voucher for CO1 barcode sequence, GenBank Acc. number: MT999943.

Fig. 12. Line art illustrations of Echinoderes sensibilis Adrianov et al., 2002. 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.

Fig. 13. Diagram of mouth cone (grey area), introvert and placids in Echinoderes sensibilis Adrianov et al., 2002, showing distribution of inner oral styles (full circles), outer oral styles (diamonds), primary scalids (triangles), spinoscalids (thick 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’.

Fig. 14. Light micrographs showing overviews and details ofEchinoderes sensibilis Adrianovet al., 2002. A–I. ♀. A. ICHUM-6127. B–F, I. NHMD-662049. G. NHMD-662066. H. NHMD-662060. A. Ventral overview. B. Segments 1 to 4, dorsal view. C. Segments 1 to 4, ventral view. D. Segments 5 to 8, dorsal view. E. Segments 5 to 8, ventral view, showing female sexual dimorphism. F. Segments 8 to 10, dorsal view. G. Segments 8 to 9, dorsal view. H. Detail showing ventral trichoscalids and trichoscalid plates. I. Segments 10 to 11, ventral view, showing female sexual dimorphism. J. ♂ (NHMD-662056). Segments 10 to 11, ventral view, showing male sexual dimorphism.

Fig. 15. Scanning electron micrographs showing overviews and details of Echinoderes sensibilis Adrianov et al., 2002. A, D, F–J. ♀ (MVS, personal reference collection). B–C, E, K–L. ♂ (MVS, personal reference collection). A. Ventrolateral overview. B. Mouth cone, ventral view. C. Introvert sectors 1 and 10 (ventral). D. Segments 1 to 2, dorsal view. E. Segments 1 to 2, ventrolateral view. F. Segments 8 to 9, lateral view; insets show glandular cell outlets type 2. G. Segments 6 to 8, dorsal view. H. Segments 6 to 7, ventral view, showing female sexual dimorphism. I. Segments 7 to 8, ventral view, showing female sexual dimorphism. J. Segments 10 to 11, dorsal view, showing female sexual dimorphism. K. Segments 10 to 11, lateral view, showing male sexual dimorphism. L. Segments 10 to 11, dorsal view, showing male sexual dimorphism.

Fig. 4. Scanning electron micrographs showing overviews and details of Echinoderes dujardinii Claparède, 1863. A–B, D, G–H, K. ♀ (MVS, personal reference collection). C, E–F, I–J. ♂ (MVS, personal reference collection). A. Lateroventral overview. B. Head with mouth cone and introvert, ventral view; inset shows detail of primary spinoscalid fringes attaching along a longitudinal line, and the median basal sheath spike of the Ring 03 spinoscalid. C. Segments 1 to 2, dorsal view. D. Segments 1 to 2, lateral view. E. Segments 1 to 2, ventral view. F. Segments 4 to 7, subdorsal view; inset shows the minute midlateral sensory spot on segment 4. G. Segments 8 to 9, lateral view; inset shows detail of sieve plate and lateroventral spine of segment 9.H. Segments 5 to 8, ventral view, showing female sexual dimorphism; inset shows detail of glandular cell outlet type 1, sensory spot and female papillae on left sternal plate of segment 6. I. Segments 10 to 11 ventrolateral view, showing male sexual dimorphism. J. Segments 10 to 11 lateral view, showing male sexual dimorphism. K. Segments 10 to 11 ventral view, showing female sexual dimorphism.