Two new species of Echinoderes (Kinorhyncha: Cyclorhagida) from the Gulf of Mexico

Sørensen, Martin V.; Landers, Stephen C.

doi:10.3389/fmars.2014.00008

ORIGINAL RESEARCH article

Front. Mar. Sci., 27 May 2014
Sec. Marine Evolutionary Biology, Biogeography and Species Diversity
Volume 1 - 2014 | https://doi.org/10.3389/fmars.2014.00008

Two new species of Echinoderes (Kinorhyncha: Cyclorhagida) from the Gulf of Mexico

Martin V. Sørensen¹^*

Stephen C. Landers²

¹Geogenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark
²Department of Biological and Environmental Sciences, Troy University, Troy, AL, USA

Comprehensive sampling of meiofauna along the northern continental slope in the Gulf of Mexico has revealed a diverse kinorhynch fauna of undescribed species. The present contribution includes the description of two new species of the cyclorhagid genus Echinoderes. Echinoderes augustae sp. nov. is recognized by the presence of acicular spines in middorsal positions on segments 4–8, and in lateroventral positions on segments 6–9, tubes in lateroventral positions on segments 2–5, midlateral positions on segment 4, and in sublateral positions on segment 8. It furthermore has glandular cell outlets type 2 in subdorsal positions of segment 2, a middorsal protuberance-like extension from the intersegmental border between segments 10 and 11, and conspicuously short and stout lateral terminal spines. Echinoderes skipperae sp. nov. has acicular spines in middorsal positions on segments 4, 6, and 8, and in lateroventral positions on segments 8 and 9, tubes in sublateral and ventrolateral positions on segment 2, in lateroventral positions on segment 5, in lateral accessory positions on segment 8, and in laterodorsal positions on segment 10. The species can furthermore be recognized by its conspicuously well-developed pachycycli at the anterior segment margins of segments 2 to 10, and margins of sternal plates facing the midsternal junctions of segments 3 to 10.

Introduction

The meiobenthic invertebrate group Kinorhyncha can be found in the oceans throughout the world, but even though these animals have been known for more than 150 years, only slightly more than 200 species are described today, and sampling efforts to obtain more information about their biodiversity have been scattered and random, to say the least. The US East Coast is considered as relatively well-sampled, primarily due to the efforts of Robert P. Higgins (Higgins, 1964a,b, 1965, 1977, 1990; Higgins and Fleeger, 1980), as well as other more recent initiatives (Sørensen, 2007; Sørensen et al., 2005, 2007; Herranz and Pardos, 2013; Herranz et al., 2014), but even in this regard, the sampling areas have to a great extent been determined by location of field stations and coincident sampling opportunities. More coordinated sampling, with a focus on the kinorhynch fauna and distribution specifically, has within the last two decades been carried out in the waters around in the Iberian Peninsula in Southwest Europe (Pardos et al., 1998; G^aOrdóñez et al., 2008; Sánchez et al., 2011, 2012, 2014; Herranz et al., 2012; Sørensen et al., 2012a). This work has extended our knowledge about kinorhynch diversity significantly, and at the taxonomic level it has been a major contribution. However, despite the numerous samplings and hours spend analyzing the results, the information is still too incomplete to point out any general patterns in the kinorhynch community structures, species distribution, sediment preferences, etc. An almost parallel example can be found in a third rather well-examined region, namely the waters around the Korean Peninsula. Through a series of recent contributions our knowledge about the East Asian kinorhynch fauna has increased greatly (Sørensen et al., 2010a,b,c, 2012a,b, 2013; Lundbye et al., 2011, Sánchez et al., 2013; Thomsen et al., 2013), but a closer examination of the recordings of each species leaves no clear picture about their actual distributional ranges or eventual habitat preferences.

Currently, our information about the Gulf of Mexico kinorhynch fauna is extremely scarce, and limited to a single published recording by Chitwood (1951), who reports the finding of Echinoderes steineri from Aransas Bay near Corpus Christi, Texas. Shirley (2009) furthermore cites a personal communication of John Fleeger, who reports the finding of an Echinoderes species resembling Echinoderes coulli at near-shore localities in Louisiana. In 2007 an extensive meiofauna survey was initiated in the northern Gulf of Mexico (Landers et al., 2012). From 2007–2009 meiofauna were collected on National Ocean and Atmospheric Administration (NOAA) research vessels along the United States' continental shelf from Mexico to the Florida Keys. Following the Deepwater Horizon oil spill disaster in 2010, this research has received funding from the Gulf of Mexico Research Initiative (GoMRI) to continue the meiobenthic surveys in the Northern Gulf. Currently the collections have resulted in hundreds of meiobenthic samples and have provided a unique opportunity to get detailed information about the meiofaunal and specifically kinorhynch communities along the rim of the continental shelf.

The present study is the first in a series of contributions that focuses on the kinorhynch fauna collected during the NOAA cruises beginning in 2007. Currently about 22 different species—most of them new to science—have been identified. Even though sampling continues, we have now sufficient information to present the first results of the taxonomic studies, and in the following we are describing two of the more abundant species. The new taxa belong to the specious genus Echinoderes. Both of them are highly characteristic in their morphology, which makes them easy to recognize, even for the non-specialist.

Materials and Methods

Samples were collected from 2007 to 2012 on the NOAA ships Gordon Gunter and Pisces, in conjunction with the National Marine Fisheries Service Laboratory in Pascagoula, Mississippi. Specimens for the present study originate from 16 stations distributed across the United States' Gulf of Mexico continental shelf (see Figure 1 and Table 1 for details about sampling and positions). Sediment samples were collected using a box corer (WildCo©) or a Shipek^® sediment grab.

FIGURE 1

Figure 1. Map showing the sampling locations in the Gulf of Mexico. Station numbers are given for each collection site.

TABLE 1

Table 1. Summary of data on stations, species identities, and accession numbers.

The samples were fixed immediately in 5–10% formalin, and kinorhynchs were subsequently extracted by Ludox centrifugation (Burgess, 2001). After sorting under a dissecting microscope, the specimens were stored in isopropanol until prepared for light microscopy (LM) or scanning electron microscopy (SEM) examination. Specimens for LM were dehydrated through a graded series of glycerin, mounted in Fluoromount G, mounted between two cover glasses and attached to a plastic H-S slide with glyceel. They were examined and photographed with an Olympus BX51 microscope, equipped with an Olympus DP20 camera and a drawing tube. Line art illustrations were based on camera lucida drafts of mounted specimens that subsequently were scanned and drawn in Adobe Illustrator CS5. Measurements were made with Cell^∧D software. All dimensions reported in the tables are based on LM measurements. If a dimension mentioned in the text is estimated from SEM images, this is indicated clearly. Specimens for SEM were primarily examined in Copenhagen, and were dehydrated through a series of alcohol, critical point dried, mounted on aluminum stubs, sputter coated with a platinum/palladium mix, and examined with a JEOL JSM-6335F Field Emission scanning electron microscope.

The type material is deposited at the Natural History Museum of Denmark and at the Smithsonian Institution, National Museum of Natural History. Even though it has been common practice up to now, allotypes are not designated, because they do not have a name-bearing function according to the International Code of Zoological Nomenclature (see ICZN, 1999).

Systematics

Order Cyclorhagida Zelinka, 1896
Family Echinoderidae Bütschli, 1876
Genus Echinoderes Claparède, 1863

Echinoderes augustae sp. nov.

Type material

Holotype, adult female, collected from mud on October 25, 2012, at station 084 (Figure 1), at 85 m depth near the rim of the continental Shelf, east of the Mississippi River Delta (28°58′51.02″N 088°59′56.47″W), mounted in Fluoromount G, deposited at the Natural History Museum of Denmark, under accession number ZMUC KIN-705. Paratypes include nine specimens mounted in Fluoromount G (seven specimens deposited at the Natural History Museum of Denmark under accession numbers ZMUC KIN-706 to KIN-712, and two specimens deposited at the Smithsonian Institution, National Museum of Natural History under accession numbers USNM 1231476-1231477) and 16 specimens mounted for SEM (accession numbers ZMUC KIN-713 to KIN-729), deposited at the Natural History Museum of Denmark. Paratypes originate from eight stations near the rim of the continental shelf, from site 033 in the west (southeast of Galveston, Texas) to site 163 in the east (southwest of Tampa, Florida). The species was furthermore recorded from four additional stations, but these specimens were either lost, had incomplete collection information or are included in S. Landers' personal reference collection. See Figure 1 for localities and Table 1 for detailed station data.

Diagnosis

Echinoderes with acicular spines in middorsal positions on segments 4 to 8, and in lateroventral positions on segments 6 to 9. Tubes present in lateroventral positions on segments 2 and 5, midlateral positions on segment 4, and in sublateral positions on segment 8; males furthermore with tubes in laterodorsal positions on segment 10. Large glandular cell outlets type 2 in subdorsal positions of segment 2. A conspicuous middorsal protuberance-like structure extends from the intersegmental border between segments 10 and 11. Tergal extensions of segment 11 short and triangular. Lateral terminal spines conspicuously short and stout. Males with three penile spines, females with short, and thin lateral terminal accessory spines.

Etymology

The species is named after Augusta Bork Larsen in appreciation of her help and assistance examining the new species.

Description

Adults with head, neck, and 11 trunk segments (Figures 2A,B, 4A,F, 5A). The trunk of the species appears relatively broad and stout in its anterior end, but tapers from segment 7 toward its much slimmer hind end. Its lateral terminal spines appear conspicuously short and stout. 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.

FIGURE 2

Figure 2. Line art illustrations of Echinoderes augustae sp. nov. (A) Female, dorsal view. (B) Female, ventral view. (C) Male, segments 10 to 11, dorsal view. (D) Male, segments 10 to 11, ventral view.

TABLE 2

Table 2. Measurements from light microscopy of adult Echinoderes augustae sp. nov. (in μm), including number of measured specimens (n), and standard deviation (SD).

TABLE 3

Table 3. Summary of nature and location of sensory spots, glandular cell outlets, tubes and spines arranged by series in Echinoderes augustae sp. nov.

The head consists of a retractable mouth cone and an introvert (Figures 3, 5B,C). The pharynx terminates into a pharyngeal crown, and rings of inner oral styles are present, but their exact number and arrangement could not be determined. The external mouth cone armature consists of nine outer oral styles that alternate in size between slightly smaller and slightly larger ones (Figure 5B), arranged as one style anterior to each introvert sector, except the middorsal sector 6 (Figure 3). A structure with laterally folded margins is located at the base of each style. The structure has three distally bifurcated spikes located at its base, and a pair of lateral spikes that insert more anterior (Figure 5B). More posterior on the mouth cone, large elongated diamond-shaped elements are present in between the bases of each of the outer oral styles. Each element has a basal fringe with short, densely set fringe tips. Posterior to introvert sector 6, where the style is missing, the element is triangular, rather than diamond-shaped, and the tips in the median part of the fringe are considerably longer and extend almost to the tip of the triangle (Figure 5B).

FIGURE 3

Figure 3. Diagram of mouth cone (gray area), introvert, and placids in Echinoderes augustae sp. nov., showing distribution of outer oral styles, scalids, and trichoscalids. Table shows the scalid arrangement by sector; single-lined boxes mark quincunxes, double-lined boxes mark “double diamonds.”

The introvert sectors are defined by 10 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 5C). The basal sheaths have several long extensions that form transverse fringes, whereas the end pieces vary between some smooth parts, and some parts with longitudinal wrinkles. Rings 02 and 04 have 10 spinoscalids and Ring 03 has 20 (Figure 3). All spinoscalids in these rings consist of a basal sheath and an end piece. The basal sheaths terminate into fringed margins. Ring 03 spinoscalids furthermore have a median spike anterior to their attachment points (Figure 5C). Ring 05 has 20 spinoscalids that are composed as those in the preceding rings, but with shorter end pieces though. A ring of short fringes appear to extend around the introvert in between spinoscalid rings 04 and 05 (Figure 5C). Rings 06 and 07 have only 6 spinoscalids each (Figure 3). These scalids are considerably shorter than those in the more anterior rings, their basal sheaths have serrulated margins, and the end pieces are wrinkled. Additional scalids are found even more posterior on the introvert. These scalids are very short and appears to consist of partly fused fringe-like extensions, leaving the impression that they might be reduced trichoscalids, even though they do not attach to a trichoscalid plate (Figures 5C,D). These putative reduced trichoscalids are located in sections 3, 5, 6, 7, and 9 (Figure 3). It was not possible to confirm the eventual presence of a similar reduced trichoscalid in section 1, but its presence would be expected from the general symmetry patterns in the introvert. Well-developed trichoscalids, attached to trichoscalid plates, are present in sectors 2, 4, 5, 7, 8, and 10 (Figures 3, 4B, 5C). Described sector-wise, sectors 1 and 6 are similar, having spinoscalids arranged as two double diamonds (the only difference between the sections is the reduced trichoscalid, present posteriorly in section 6 but with its presence unconfirmed for section 1). Sectors 2, 4, 8, and 10 all have spinoscalids arranged as a quincunx, located in between a medial anterior spinoscalid and a trichoscalid plate. The remaining sectors, 3, 5, 7, and 9 are almost identical, having a set of double diamonds located anterior to a pair of Ring 07 spinoscalids and a pair of reduced trichoscalids. However, in sectors 5 and 7, one Ring 07 spinoscalid and one reduced trichoscalid are missing, due to the presence of a trichoscalid plate that takes up space (Figure 3).

FIGURE 4

Figure 4. Light micrographs showing overviews and details of trunk morphology in Echinoderes augustae sp. nov. (A–E) and (G,H) female holotype (ZMUC KIN-705); (F,I). Male paratype (ZMUC KIN-710); (J) non-type female. (A) Ventral overview. (B) Partly retracted head, neck and segments 1 to 2, dorsal view. (C) Neck and segments 1 to 3, ventral view. (D) Segments 3 to 6, dorsal view. (E) Segments 3 to 6, ventral view. (F) Dorsal overview. (G) Segments 8 to 9, focusing on sublateral tubule on segment 8. (H) Segments 6 to 8, ventral view. (I) Segment 10, dorsal view, showing middorsal protuberance, and male morphology. (J) Segment 11, ventral view, showing female morphology. Abbreviations: gco1/2, glandular cell outlet type1/2; ltas, lateral terminal accessory spine; lts, lateral terminal spine; lvt, lateroventral tube; mds, middorsal spine; mvp, midventral placid; pam, pachycyclus markings or loops; pe, penile spine; pl, placid; pr, protuberance; slt, sublateral tube; te, tergal extension; tr, trichoscalid; trp, trichoscalid plate.

FIGURE 5

Figure 5. Scanning electron micrographs of Echinoderes augustae sp. nov. (A) Female paratype (ZMUC KIN-719); (B–G). female paratype (ZMUC KIN-729); (H–I). and (K) male paratype (ZMUC KIN-725); (J,L). female paratype (ZMUC KIN-721). (A) Lateral overview. (B) Mouth cone, dorsal view, anterior to introvert section 6. (C) Introvert, showing introvert section 7 in the center. (D) Detail of introvert section 7, showing reduced trichoscalid. (E) Segments 1 to 2, dorsal view. (F) Segments 2 to 4, lateral view. (G) Detail of segments 8 to 9, showing sublateral tubule and sieve plate. (H) Detail showing middorsal sensory spot on segment 2. (I) Detail showing middorsal area, anterior to spine, on segment 4. Note the pore fields of the glandular cell outlets (marked with dashed line) that appear extremely indistinct in s.e.m. (J) Detail showing middorsal protuberance-like structure emerging between segments 10 and 11. (K) Segment 11, dorsal view of male. (L) Segment 11, dorsal view of female. Abbreviations: fr, fringe; gco2, glandular cell outlet type 2; ld, laterodorsal sensory spot; ldt, laterodorsal tube; ltas, lateral terminal accessory spine; lts, lateral terminal spine; ml, midlateral sensory spot; mlt, midlateral tube; oos, outer oral styles; pd, paradorsal sensory spot; pe, penile spine; pr, protuberance; psp, primary spinoscalid; sd, subdorsal sensory spot; sec x, introvert sector followed by sector number; si, sieve plate; slt, sublateral tube; sp x, spinoscalid followed by ring number; tr(r), trichoscalid (reduced); te, tergal extension.

The neck has 16 placids, measuring 11 μm in length. The midventral placid is broadest (Figures 2B, 4C), measuring 13 μm in width at its base, whereas all other are narrower (Figures 2A, 4B), measuring 7 μm in width at their bases. The trichoscalid plates are well-developed, with the ventral pair (Figure 4C) being broader (13 μm in width) than the two dorsal pairs (8 μm in width) (Figure 4B).

Segment 1 consists of a complete cuticular ring (Figures 2A,B, 4A–C,F, 5A,E). Sensory spots are located near the anterior segment margin in subdorsal and laterodorsal positions (Figure 5E), and more posteriorly in ventromedial positions (Figure 2B). The sensory spots are small and rounded. Glandular cell outlets type 1 are present in middorsal and lateroventral positions (Figures 2A,B, 4B). In light microscopy the subcuticular glandular cells appear like a row of light refracting granules (Figure 4B). The light refracting granules are arranged as a vertical row in the middorsal position, whereas those in the lateroventral positions form transverse rows. Cuticular hairs emerge through rounded perforation sites, and are scattered around the segment. On the dorsal side (Figure 5E), the hairy area extends to a position just posterior to the sensory spots, whereas the anterior half of the segment is without hair on the ventral side. Posteriorly, the hair areas are limited by the intersegmental joint line. The segment terminates into a pectinate fringe with well-developed fringe tips.

Segment 2 consists of a complete cuticular ring, with tubes (ca. 14 μm from s.e.m.) located in lateroventral positions (Figures 2B, 4C). Pachycyclus of the anterior segment margin of regular thickness, but with a pair of notches in its posterior margin in paraventral positions (Figure 4C). Sensory spots are located in middorsal, laterodorsal (two pairs but not twin pairs), and ventromedial positions, and glandular cell outlets type 1 in ventromedial positions (Figures 2A,B, 4C). Glandular cells are arranged as an oblique cluster of light refracting granules. Sensory spots on this and the following segments are extremely small (Figure 5H), and appear as a few (ca. 8) micropapillae arranged in a circle around a central pore, that eventually has an emerging cilium. A pair of relatively large glandular cell outlets type 2 is located in subdorsal positions (Figures 2A, 4B, 5E,F). Secondary pectinate fringe present on anterior part of segment, consisting of thin, flexible fringe tips. On this and all following segments, the cuticular hairs are bracteate. They are distributed around the segment, more densely than on the preceding segment, forming a uniform covering between the secondary fringe and the intersegmental joint line on the dorsal side of the segment, whereas hairs on the ventral side are missing in the ventromedial areas. Pectinate fringe of posterior margin as on preceding segment.

Segment 3, and remaining segments, consisting of one tergal and two sternal plates (Figures 2A,B, 4A,C,E,F). Pachycycli of the anterior segment margin of regular thickness, but forming two small loops at the anteromedial corners of the sternal plates (Figures 4C,E). Segment with sensory spots in subdorsal and sublateral positions, and glandular cell outlets type 1 in middorsal and ventromedial positions (Figures 4D,E, 5F). Light refracting granules in middorsal glandular cell form a transverse rod, whereas those in the ventromedial positions form obliquely arranged clusters on this and the following seven segments. Cuticular hairs evenly distributed over tergal plate, between secondary fringe and intersegmental joint line, whereas hairs on the sternal plates are arranged in rectangular patterns covering the ventrolateral and ventromedial areas. Paraventral areas are completely hairless. Posterior segment margin straight, with pectinate fringe as on preceding segment.

Segment 4 with acicular spine in middorsal position (Figures 2A, 4D), and a pair of tubes (ca. 17 μm from s.e.m.) in midlateral positions (Figures 2A, 5F). Sensory spots not present. Glandular cell outlets type 1 present in paradorsal and ventromedial positions (Figures 4D,E). Light refracting granules in paradorsal glandular cell form obliquely arranged clusters on this and the following five segments. All glandular cells appear very distinct in LM (Figure 4D), whereas the pore fields at their outlets are almost impossible to visualize with SEM (Figure 5I). Pachycycli, secondary fringe, pectinate fringe of posterior margin, and cuticular hairs as on preceding segment.

Segment 5 with acicular spine in middorsal position and tubes (ca. 13 μm from s.e.m.) in lateroventral positions (Figures 2A,B, 4D,E). Sensory spots present in subdorsal, midlateral, and ventromedial positions. Glandular cell outlets type 1 present in paradorsal and ventromedial positions. Loop-like structures in the anteromedial corners of the sternal plates appear less distinct than on the two preceding segments (Figure 4E). Secondary fringe, pectinate fringe of posterior margin and cuticular hairs otherwise as on preceding segment.

Segments 6 and 7 are identical, with acicular spines in middorsal and lateroventral positions (Figures 2A,B, 4H). Sensory spots present in paradorsal, subdorsal, midlateral and ventromedial positions, and glandular cell outlets type 1 in paradorsal and ventromedial positions. Pachycycli without loops in the anteromedial corners of the sternal plates (Figures 4E,H). Secondary fringe, pectinate fringe of posterior margin and cuticular hairs as on preceding segment.

Segment 8 with acicular spines in middorsal and lateroventral positions and tubes (ca. 16 μm from s.e.m.) in sublateral positions (Figures 2B, 4G, 5G). Sensory spots present in paradorsal and subdorsal positions only, and glandular cell outlets type 1 in paradorsal and paraventral positions. Pachycycli, secondary fringe, pectinate fringe of posterior margin, and cuticular hairs as on preceding segment.

Segment 9 without middorsal spine, but with acicular spines in lateroventral positions (Figures 2A,B). Sensory spots present in paradorsal, subdorsal, midlateral, and ventrolateral positions. A pair of minute sieve plates is located in sublateral positions (Figure 5G). Glandular cell outlets, pachycycli, secondary fringe, and pectinate fringe of posterior margin as on preceding segment, whereas fewer cuticular hairs are present in middorsal and paradorsal positions.

Segment 10 with laterodorsal tubes near posterior segment margin in males (ca. 11 μm from s.e.m.) (Figures 2C, 5K); tubes are not present in females (Figure 5L). A prominent protuberance-like structure emerges in a middorsal position from the intersegmental joint between segments 10 and 11 (Figures 4I, 5J–L). The structure appears cone-shaped in LM (Figure 4I), whereas SEM shows that it is a tuft of hair-like cuticular extensions that basally are overlapped by a small, elongate cuticular plate (Figure 5J). Sensory spots present in subdorsal and ventrolateral positions, and glandular cell outlets type 1 as two middorsal ones and one pair in paraventral positions. Light refracting granules in the middorsal glandular cells form vertical clusters, whereas those of the paraventral glands are obliquely arranged. Cuticular hairs are slightly shorter than those on preceding segments, and on the tergal plate, hairs are lacking in two laterodorsal bands. The hair covering of the sternal plates is basically as on the preceding segments. The posterior segment margin of the tergal plate is straight, whereas the margins of the sternal are concave. Fringe tips in pectinate fringe of posterior margin are well-developed.

Segment 11 with lateral terminal spines (Figures 2, 4J, 5K,L). Lateral terminal spines are rather short (around 10% of trunk length) but very stout. Females with thin and short lateral terminal accessory spines (Figures 4J, 5K), and males with three pairs of penile spines (Figures 2C,D, 4I, 5K): Dorsal and ventral penile spines are long (26–29 μm from SEM) and relatively flexible, whereas the medial one is shorter (ca. 14 μm from SEM), more rigid, with a slightly swollen basal part that tapers distally. Apparently a middorsal glandular cell is present, and has its outlet through a pore field on the cuticular plate of the protuberance-like structure that emerges between segments 10 and 11. Sensory spots are present in paradorsal (Figure 5J) and ventromedial positions, the latter near the margins of the sternal extensions. The mid- to subdorsal areas of the tergal plate are densely covered with minute filiform cuticular extensions (Figure 5K), whereas the remaining parts of the tergal plate and the sternal plates are completely smooth. Tergal extensions are rather short and triangular, whereas sternal extensions are even shorter and broadly rounded.

Notes on diagnostic and taxonomic features

Echinoderes augustae sp. nov. is easily recognized, even under a low power dissecting microscope, by its short, but really stout lateral terminal spines. Species of Echinoderes come with lateral terminal spines of varying lengths that typically lie within a range of 20–80% of the trunk length. Only few species have shorter lateral terminal spines that get down near the LTS/TL index around 10% as found in E. augustae sp. nov., but even some of these species, e.g., E. aquilonius (Higgins and Kristensen, 1988) and E. coulli (Higgins, 1977) (see Higgins, 1977; Higgins and Kristensen, 1988) still have the typical thin, needle-shaped spines that differ significantly from the stout ones found in E. augustae sp. nov.

The presence of short and stout lateral terminal spines resembling those in E. augustae sp. nov. is restricted to only six other species: E. abbreviatus (Higgins, 1983) from Belize, E. brevicaudatus (Higgins, 1966) from the Red Sea, E. cavernus (Sørensen et al., 2000) from an Australian submarine cave, E. hwiizaa (Yamasaki and Fujimoto, 2014) from Okinawa, E. obtuspinosus (Sørensen et al., 2012b) from the Korean West Coast and E. ulsanensis Adrianov and Malakhov, 1999 from Ulsan at the Korean East Coast (see Higgins, 1966, 1983; Adrianov and Malakhov, 1999; Sørensen et al., 2000, 2012b; Yamasaki and Fujimoto, 2014). Echinoderes augustae sp. nov. can be distinguished from these six species by its possession of midlateral tubes on segment 4 and sublateral tubes on segment 8. None of the six species have tubes in these positions, and only E. abbreviatus has tubes on segment 8, but these are located in lateral accessory positions. However, since especially the midlateral tubes on segment 4 can be difficult to visualize with light microscopy, some additional differential characters are convenient. Even without examining the tubes on segments 4 and 8, E. abbreviatus and E. hwiizaa are easily distinguished from E. augustae sp. nov. because E. abbreviatus has middorsal spines on segments 4, 6, and 8 only, whereas E. hwiizaa has no middorsal spines at all (Higgins, 1983; Yamasaki and Fujimoto, 2014). Echinoderes ulsanensis also stands out, because it lacks ventrolateral tubes on segment 5 and lateroventral spines on segment 6 (Adrianov and Malakhov, 1999). Of the remaining three species, E. brevicaudatus and E. cavernus have conspicuously short middorsal spines that do not extend beyond on the posterior margin of the segments where they attach (Higgins, 1966; Sørensen et al., 2000). Furthermore, none of them have glandular cell outlets type 2 on the second trunk segment, as found in subdorsal positions on segment 2 in E. augustae sp. nov. (no glandular cell outlets type 2 have been reported from E. brevicaudatus, and E. cavernus only has a single pair, located in midlateral positions on segment 9). The last species with short and stout lateral terminal spines, E. obtuspinosus, resembles E. augustae sp. nov. in several ways. The middorsal spines are still shorter, but yet closer, to the dimensions we find in E. augustae sp. nov., and in sublateral position of segment 8, it has a glandular cell outlet type 2, that could be confused with the attachment point of the tube found in E. augustae sp. nov. The key to distinguish E. obtuspinosus from E. augustae sp. nov. is the structures on segment 2 in the two species. Whereas E. augustae sp. nov. has glandular cell outlets type 2 in subdorsal positions only, and a pair of tubes in lateroventral positions, E. obtuspinosus has no tubes on this segment, but has instead four pairs of glandular cell outlets, situated in subdorsal, laterodorsal, sublateral, and ventrolateral positions (Sørensen et al., 2012b). These differences alone, make it easy to differentiate between the species.

Another unusual and noteworthy structure in E. augustae sp. nov. is the middorsal protuberance-like structure that emerges from the intersegmental junction between segments 10 and 11. Such a structure is, if not unique, then at least rather rare among species of Echinoderes. A search through the literature, available specimens and unpublished photos, revealed only a single recording of something similar, namely in E. eximus (Higgins and Kristensen, 1988) (see Figure 48 in Higgins and Kristensen, 1988). Light microscopical re-examinations of paratypes of E. eximus confirmed that the species apparently has a large, tubular structure emerging middorsally between segments 10 and 11, but SEM of specimens (photos kindly provided by Jonas Thormar) could unfortunately not confirm the nature of this structure, because the examined specimens were strongly contracted so only the distal, fringed part of the structure could be observed.