Echinoderes dujardinii Claparède, 1863

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 : 12-20

Echinoderes dujardinii Claparède, 1863

Figs 2–4 ; Tables 3–4

l’Echinodère Dujardin 1851: 158, pl. 3, figs 1–4.

Echinoderes Dujardinii Claparède, 1863: 90–92 , pl. 16, figs 7–13.

Echinoderes dujardinii – Higgins 1977a: 4–13, figs 1–12. — Sánchez et al. 2012: 26 [South Galicia].

Non Echinoderes dujardinii – Mari & Morselli 1987: 117. — Sánchez-Tocino et al. 2011: 179–184, figs 1–4, tables 1–2. — Sánchez et al. 2012: 26 [Algeciras, Granada, Murcia, Alicante]. — Ürkmez et al. 2016: 1–8 , figs 2–4.

Emended diagnosis

Echinoderes with short middorsal spines on segments 4 to 8, and lateroventral spines on segments 6 to 9; middorsal spines on segments 7 and 8 might reach posterior margins of their respective segments, but they never extend beyond the margins. Tubes present in lateroventral positions on segments 2 and 5, in lateral accessory positions on segment 8, and in laterodorsal positions on segment 10. Minute glandular cell outlets type 2 in laterodorsal positions on segments 8 and 9; those on segment 9 situated anterior to laterodorsal sensory spots. 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 papillae on segment 6 is crescentic, substructure on segments 7 and 8 is tubular.

Material examined

FRANCE • 18 ♀♀, 24 ♂♂; Roscoff ; 48°43′ N, 003°58′ W; 0 m b.s.l.; 19 Oct. 1973; E. Kozloff leg.; sandy mud (see Higgins 1977a); USNM-53342 . Specimens mounted for LM .

SPAIN – Atlantic north coast of Spain • 1 ♀, 4 ♂♂; Cantabric Sea , outlet of Eo River; F. Pardos leg.; UCM. – Galician Atlantic west coast of Spain • 1 ♀; Arousa ; F. Pardos leg.; UCM • 1 ♂; Vigo ; F. Pardos leg.; UCM. – Andalusian Atlantic south coast of Spain • 3 ♀♀, 1 ♂; Huelva ; F. Pardos leg.; UCM. Specimens mounted for LM .

PORTUGAL • 6 ♀♀, 4 ♂♂; Faro, Ria Formosa ; 37°00′ N, 007°49′ W; 0 m b.s.l.; 21 Oct. 2012; R.C. Neves and M. Herranz leg.; mud with Zostera ; NHMD-616804 to 616807 , NHMD-616822 to 616827 . Specimens mounted for LM .

About 30 specimens from the same locality at Faro were mounted for SEM and stored in the first author’s personal reference collection. Type material was not available. See Table 1 for an overview.

Description

Echinoderes dujardinii was redescribed by Higgins (1977a), but due to the numerous new details (mainly revealed by SEM), reinterpretations of cuticular structures, and considerable changes in terminology over the past 40 years, we are providing a full description of the species.

Adults with head, neck and eleven trunk segments ( Figs 2A , 3 , 4A ). Trunk with nearly equally broad sternal plates on segments 5 to 10 ( Fig. 2A ). Lateral terminal spines slender, from 40% to 55% of trunk length. Secondary pectinate fringe formed as one fringed band near anterior segment margin is present on segments 2 to 10. For complete overview of measurements and dimensions of Portuguese and Spanish populations, see Table 3 . Distribution of cuticular structures, i.e., sensory spots, glandular cell outlets, spines and tubes, is summarized in Table 4.

The head consists of a retractable mouth cone and an introvert ( Figs 3 , 4B ). Three rings of inner oral styles, apparently with five styles in each ring. The external mouth cone armature consists of nine outer oral styles, each consisting of two joined units and arranged as one style anterior to each introvert sector, except the middorsal sector 6; each outer oral style basally flanked by pair of lateral spikes, followed by more basal V-shaped row of fringe tips, and again followed by even more basal brush-like arch of bristles ( Fig. 4B ). The introvert sectors are defined by the ten primary spinoscalids in Ring 01 ( Fig. 3 ). Each primary spinoscalid consists of a basal sheath and a distal end piece with a blunt tip. The sheaths have two distinctively differentiated fringes: a most basal, transverse fringe, and a slightly more distal fringe where the fringe tips bend in a curve near their attachment point, and fuse to the scalid along a longitudinal line, giving the attachment area a conspicuous appearance (see inset Fig. 4B ). 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. The basal sheaths terminate into fine, fringed margins in spinoscalids of Rings 02 to 05, and those of Ring 03 have in addition a basal median spike ( Fig. 4B inset). A ring of short fringes extend around the introvert in between spinoscalid Rings 05 and 06. Ring 06 has only six spinoscalids, located in sectors 1, 3, 5, 6, 7, and 9; ring 06 spinoscalids resemble those in preceding sectors, but are much shorter and with densely haired end pieces. 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 unpaired but centred in sector 1; ring 07 spinoscalids resemble those in preceding sector but are even shorter.

Described sector-wise ( Fig. 3 ), sector 1 has spinoscalids arranged as two double diamonds anterior to a single Ring 7 spinoscalid. 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 in Ring 7. Sectors 5 and 7 also have spinoscalids forming double diamonds, but anterior to an unpaired, lateral spinoscalid. Sector 6 has spinoscalids arranged as two double diamonds.

The neck has 16 placids, measuring 20 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 in the dorsal sectors are composed of a distal part and a slightly broader proximal part, whereas the proximal parts of the ventral trichoscalid plates are much broader. Trichoscalids with trichoscalid plates are present in sectors 2, 4, 5, 7, 8, and 10.

Segment 1 consists of a complete cuticular ring. Sensory spots are located close to the anterior margin in subdorsal, laterodorsal and sublateral positions ( Figs 2B , 4 C–D), and slightly more posterior in ventrolateral positions ( Figs 2C , 4E ); sensory spots are 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 ( Fig. 2 B–C). Dorsal and lateral sides, and posterior half of ventral side, densely covered with cuticular hairs emerging through rounded perforation sites ( Fig. 4 C–D); an anterior W-shaped area on the ventral side is completely devoid of hairs ( Fig. 4E ). 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. Pachycyclus of the anterior segment margin is of medium thickness and not interrupted ( Fig. 2 B–C). Sensory spots are located in middorsal (but slightly laterally displaced), laterodorsal (twin pair) ( Figs 2 B–C, 4C–D) and ventromedial positions ( Fig. 4E ); appearance sensory spots on this and all following segments as those on segment 1, but droplet-shaped. Glandular cell outlets type 1 present in middorsal and ventromedial positions ( Fig. 2 B–C); and quite well-developed tubes present in lateroventral positions ( Figs 2C , 4E ). The segment is densely covered with bracteate hairs. The posterior segment margin is nearly straight; pectinate fringe from middorsal to lateroventral positions with short fringe tips, as on segment 1; fringe tips from lateroventral to ventromedial positions conspicuously longer, and then slightly shorter again between ventromedial positions.

Segment 3, and remaining segments, consisting of one tergal and two sternal plates ( Fig. 2C ). Pachycyclus of the anterior segment margin of medium thickness, and interrupted only at tergosternal junctions. Sensory spots present in subdorsal, laterodorsal ( Fig. 2B ) and sublateral positions. Glandular cell outlets type 1 present in middorsal and ventromedial positions. Bracteate cuticular hairs are densely covering the segment from middorsal to ventromedial positions; paraventral parts densely covered by non-bracteate, hair-like extensions, forming a conspicuous shield-shaped area. Pectinate fringe of posterior margin with slightly longer fringe tips on dorsal and lateral sides, compared to those on preceding segment, and conspicuously long tips in lateroventral to ventromedial positions.

Segment 4 with short acicular spine in middorsal position, not reaching the posterior margin of the segment ( Fig. 4F ); all spines on this segment and until segment 9 with cylindrical proximal part that halfway to the tip begins to taper gradually. Sensory spots present in subdorsal, midlateral ( Figs 2D , 4F ) and ventromedial positions; midlateral sensory spots considerably smaller than all other sensory spots on the animals ( Fig. 4F inset), but they occur consistently in all examined specimens. Glandular cell outlets type 1 present in subdorsal ( Fig. 2D ) and ventromedial positions. Pectinate fringe of posterior segment margin with long fringe tips from middorsal to ventromedial positions, and then very short again between ventromedial positions. Pachycycli and cuticular hairs as on preceding segment.

Segment 5 with short acicular spine in middorsal position ( Fig. 4F ), not reaching the posterior margin of the segment, and well-developed tubes in lateroventral positions ( Figs 2E , 4H ). Sensory spots present in subdorsal, midlateral ( Figs 2D , 4F ) and ventromedial positions. 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 ( Fig. 4F, H ); middorsal spine does not reach the posterior margin of the segment, whereas lateroventral spines reach pectinate fringe. Sensory spots present in paradorsal, subdorsal, midlateral ( Fig. 4F ) and ventromedial ( Fig. 4H ) positions. Females with female papillae with openings, resembling small glandular cell outlets type 2 ( Fig. 4H inset), in ventromedial positions, close to and lateral to sensory spots ( Fig. 4H ); the intracuticular structures of the papillae are crescentic with a small protuberance in the curved part of each structure ( Fig. 2E ). 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 (one specimen with two spines emerging from the same opening) and lateroventral positions ( Figs 2 D–E, 4F, H); middorsal spine does not reach the posterior margin of the segment, whereas lateroventral spines reach pectinate fringe. Females with female papillae as on segment 6, but with openings slightly more anterior and lateral to sensory spots ( Figs 2E , 4H ); the substructure of these papillae differs from those on preceding segment, and forms instead a small intracuticular tube ( Fig. 2E ). 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 ( Figs 2 D–E, 4F, H), both reaching the pectinate fringe of the posterior margin of the segment. Tubes are present in lateral accessory positions ( Fig. 4G ). Minute glandular cell outlets type 2 present in laterodorsal positions, but very close to the midlateral lines ( Figs 2D, F , 4G ). Sensory spots present in paradorsal, subdorsal, and ventrolateral positions. Females with female papillae with same substructure as those on segment 7, but with openings more anterior and closer to midventral line. 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 ( Fig. 4G ), just reaching the posterior margin of the segment. Sensory spots present in paradorsal, subdorsal, laterodorsal (posterior to glandular cell outlet type 2), and ventrolateral positions. Glandular cell outlets type 1 and 2 ( Figs 2F , 4G ) as on preceding segment, but female papillae not present. Paired nephridiopore areas each consists of a small, rounded sieve plate anterior to a single pore that we consider to be part of the nephridial system, present in lateral accessory positions ( Fig. 4G , inset). 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 2 G–H, 4I– J). Sensory spots present in subdorsal (but very close to paradorsal) positions; males furthermore with sensory spots in ventrolateral positions ( Fig. 4I ). 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 ( Fig. 4K ); 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 ( Fig. 2A, G ). Males with three pairs of penile spines ( Figs 2G , 4 I–J); all three penile spines resemble each other, with thicker and rigid proximal parts that taper towards more flexible, distal tips; median penile spines slightly thicker than dorsal and ventral ones. Females with short, thin lateral terminal accessory spines ( Figs 2H , 4K ). Sensory spots present in subdorsal and ventrolateral positions. Glandular cell outlets type 1 present as two longitudinally arranged middorsal ones. The dorsal and most of the ventral side of the segment are densely covered with non-bracteate hair-like extensions. Tergal extensions are well-spaced, short and pointed ( Figs 2 G–H, 4I, K); sternal extensions short, with ventrolateral seta-like tuft of extended fringe tips ( Figs 2H , 4I ).

Figures

Fig. 2. Light micrographs showing overviews and details of Echinoderes dujardinii Claparède, 1863, non-types from Ria Formosa, Faro, Portugal.A–D, F–G. ♂ (NHMD-616804). E, H. ♀ (NHMD-616824). A. Ventral overview. B. Segments 1 to 3, dorsal view. C. Segments 1 to 3, ventral view. D. Segments 4 to 9, dorsal view. E. Segments 5 to 9, ventral view, showing female sexual dimorphism. F. Segments 7 to 10, dorsal view. G. Segments 10 to 11, ventral view, showing male sexual dimorphism. H. Segments 10 to 11, ventral view, showing female sexual dimorphism.

Fig. 3. Diagram of mouth cone (grey area), introvert and placids in Echinoderes dujardinii Claparède, 1863, 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. 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.