Onyx disparamphis sp. n. (Nematoda, Desmodorida) from South Korea with a taxonomic review of the genus

Review of the genus Onyx

Desmodoridae, Spiriniinae. Cylindrical body with broad rounded cephalic region and conical tail. Cuticle thin, fine but distinctly annulated, without lateral differentiation. Amphideal fovea spirally coiled in one to several turns or modified; the fovea often shifted to apical surface of the head. Buccal cavity with long spear-like dorsal tooth directed anteriorly. Terminal pharyngeal bulb mostly elongate, may be double with lens-like thickened internal cuticular lining or the lining not thickened. Numerous midventral precloacal supplementary organs tubular and in most species S-shaped. Tail conical.

Type species, Onyx perfectus Cobb, 1891. Altogether 23 valid species, all marine.

Annotated species list (names of valid species in bold)

1. Onyx adenophorus Blome & Riemann, 1994. Blome & Riemann, 1994: 1486–1488, fig. 2 A–H (males, females, juveniles); Australia, New South Wales, high-energy sandy beach.

2. Onyx balochiensis Nasira, Rehmat & Shahina, 2011. Nasira, Rehmat & Shahina, 2011: 3–4, figs 1 A-F, 2 A-E, 3 A-G, 4 A-H, Table 1 (males, females); Pakistan, Balochistan.

3. Onyx blomei Nguyen Dinh Tu et al., 2011. Nguyen Dinh Tu et al., 2011: 5–7, Table 2; figs 3, 4 (males, female); Vietnam, Ho Chi Min City, Can Gio mangrove forest, subtidal at 0.5 m depth, silt.

4. Onyx brevispiculatum (Inglis, 1963) Armenteros, Ruiz-Abierno & Decraemer, 2014. Inglis, 1963: 537–539, figs 11–15 (as Sigmophora brevispiculata) (male, females); south-west coast of South Africa, 54 m deep, mud. (Armenteros, Ruiz-Abierno & Decraemer, 2014): 24 (transfer to the genus Onyx).

5. Onyx cangioensis Nguyen Dinh Tu et al., 2011. Nguyen Dinh Tu et al., 2011: 4–5, figs 1–2 table 1 (males and females); Vietnam, Ho Chi Min City, Can Gio mangrove forest, subtidal at 0.5 m depth, silt.

6. Onyx cannoni Blome & Riemann, 1994. Blome & Riemann, 1994: 1488–1488, figs 3 A–G, 4 (males, females, juveniles); Australia, New South Wales, high-energy sandy beach.

7. Onyx cephalispiculus Hourston & Warwick, 2010. Hourston & Warwick, 2010: 56–58, fig. 6 A–C, Table 7 (males, females); south-western Australia, subtidal sediment of heterogeneous grain size with low to moderate particulate organic content.

8. Onyx cobbi Nguyen Dinh Tu et al., 2011. Nguyen Dinh Tu et al., 2011: 9–13, figs 7–8, Table 4 (males, females); Vietnam, Ho Chi Min City, Can Gio mangrove forest, subtidal at 0.5 m depth, silt.

9. Onyx dimorphus Gerlach, 1963. Gerlach, 1963: 74, Fig. a–f, Taf. 4 (male, female); Maldives, Fadiffolu-Atoll, coarse sand.

10. Onyx disparamphis sp. n. Present paper.

11. Onyx ferox (Ditlevsen, 1921) Gerlach, 1951. Ditlevsen, 1921: 4–6, Fig. 3 and pl. 1 Figs 2, 10, 11 (as Oistolaimus ferox) (single female); Subantarctic Pacific, Auckland Islands, Carnley harbour, clay. (Gerlach, 1951): 61 (transfer to Onyx). Since the species is up to date known by an only female specimen not fully sexually developed, Onyx ferox is considered here species inquirenda.

12. Onyx litorale (Schulz, 1938) Armenteros, Ruiz-Abierno & Decraemer, 2014. Schulz, 1938: 119–121, Abb. 2 Fig. 12, 13, 14, 15 (as Parachromadora littoralis) (males, females); Amrum Island, North Sea, sandy intertidal zone. Gerlach, 1951: 61 (transfer to Sigmophora). Gerlach, 1951: 73–74, Abb. 7 a–d (as Sigmophora litoralis) (male, female); Amrum Island, North Sea, sandy intertidal zone (despite the description text refers to fig. 7, the legend of the fig. 7 indicates Sigmophora rufum and fig. 6 indicates Sigmophora litoralis; we consider the legend of fig. 6 right since that image corresponds to the text description). Armenteros, Ruiz-Abierno & Decraemer, 2014: 24 (transfer to Onyx).

13. Onyx macramphis Blome & Riemann, 1994. Blome & Riemann, 1994: 1484–1486, Fig. 1 A–G (males, females, juveniles); Australia, New South Wales, high energy sandy beach.

14. Onyx mangrovi Nguyen Dinh Tu et al., 2011. Nguyen Dinh Tu et al., 2011: 17–19, Table 6, Fig. 11, 12 (males, females); Vietnam, Ho Chi Min City, Can Gio mangrove forest, subtidal at 0.5 m depth, silt.

15. Onyx minor Huang & Wang, 2015. Huang & Wang, 2015: 1129–1130, Figs 3, 4 (males, females); Yellow Sea, intertidal sandy sediment.

16. Onyx monstrosum (Gerlach, 1956) Armenteros, Ruiz-Abierno & Decraemer, 2014. Gerlach, 1956: 431–433, fig. 4 a–g (as Sigmophora monstrosum) (males); Bay of Biscay, coastal ground water. Armenteros, Ruiz-Abierno & Decraemer, 2014: 24 (transfer to the genus Onyx).

17. Onyx orientalis Nguyen Dinh Tu et al., 2011. Nguyen Dinh Tu et al., 2011: 8–9, Table 3, Fig. 9, 10 (males); Vietnam, Ho Chi Min City, Can Gio mangrove forest, subtidal at 0.5 m depth; Quang Ninh province.

18. Onyx paradimorphus Nguyen Dinh Tu et al., 2011. Nguyen Dinh Tu et al., 2011: 13–16, Table 5, Fig. 5, 6 (males, females); Vietnam, Ho Chi Min City, Can Gio mangrove forest, subtidal at 0.5 m depth.

19. Onyx perfectus Cobb, 1891. Cobb, 1891: 153–155, figs 4–5, 7–8 (male, female); Mediterranean, Bay of Naples, sand with Amphioxus. Filipjev, 1918: 214–218, Fig. 41 a–e (males, females); Black Sea, sand with Amphioxus. Gerlach, 1963: 73–74, Taf. 3, k–l (male) (as Onyx cf. perfectus); Maldive Islands, 10 m deep, sand. Riemann, 1966: 149–150, Abb. 38 a–h (males, female); North Sea, 9–27 m deep, fine to medium sand. Specimen designated as Onyx cf. perfectus by Gerlach (1963) (Maldive Islands) differs significantly from the original description and redescriptions by much lesser body length (688 µm), a (16), cephalic setae length (8.5 µm) and lesser number of supplementary organs (11), and hence could not be considered as O. perfectus.

20. Onyx potteri Hourston & Warwick, 2010. Hourston & Warwick, 2010: 58–60, figs 7 A–D, Table 8 (male, female, juveniles); western Australia, calcareous sediment at relatively high-energy site.

21. Onyx rizhaoensis Huang & Wang, 2015. Huang & Wang, 2015: 1128–1129, Figs 1, 2 (males, females); Yellow Sea, intertidal sandy sediment.

22. Onyx rugatus Wieser, 1959. Wieser, 1959: 47–48, Fig. 48 a–d (males, females); Pacific coast, of USA, Puget Sound, sandy beach.

23. Onyx sagittarius Gerlach, 1950. Gerlach, 1950: 190–193, Abb. 5 a–e (male, females, juvenile); North Sea, sand. Gerlach, 1953: 562–563 (male, female); Mediterranean, Tyrrhenian Sea, coastal ground water.

24. Onyx septempapillatus Wieser, 1954. Wieser, 1954: 51–52, Fig. 125 a–d (male, females); Chile, littoral, exposed sand.

Description of new species of Onyx

Etymology

The species name reflects strong sexual dimorphism in amphideal fovea outline.

Scale bars 100 µm.

Material examined

Holotype male, 17 paratype males and 13 paratype females are deposited in the National Institute of Biological Resources (South Korea). Inventory numbers of the holotype male is U1-5 r2 sl8, paratype males 1 and 2 are M1-5 r1 sl12, paratype male 3 and paratype female 1 –slide M1-5 r1 sl14, paratype females 2 and 3 –slide M1-5 r2 sl6, paratype males 4, 5 and 6 –slide U0-1 r2 sl15, paratype females 4 and 5 –slide U15-20 r1 sl3.

Type locality

Intertidal zone at coast of Jeju Island, South Korea (33°26′05″N, 126°55′15″E), sandy beach, June 19, 2019.

Description

Males. Body cylindrical, anterior end rounded truncated, tail conical (Figs. 1A, 4A). Cuticle thin, fine but distinctly cross annulated, without a lateral differentiation. Numbers of cuticular annules within 10 µm varies along the body: 14 annules within 10 µm at the level of the long amphideal branch and 18 less distinct annules within 10 µm at the midbody.

Apical region of the cephalic region not annulated but finely longitudinally striated, with sharp border between longitudinal striation and annulation (Figs. 6B, 6C). Inner labial sensilla not evident. Outer labial sensilla as six minute papillae (1–1.5 µm). Four long cephalic setae situated apically and directed anteriorly. There first, anterior crown of eight subcephalic setae located just posterior to the cephalic setae at the level of the anterior margin of cross annulation of the cuticle. The second, posterior, less regular crown of eight subcephalic setae located slightly anterior to the middle point of the long amphideal branch. The subcephalic setae of both crowns and several irregular singular setae in the preneural body region are about equal in length and breadth to one another and to cephalic setae. Other shorter somatic setae are dispersed sparsely along the body. There are cuticular pores distributed along the body; which look like a minute hole in the centre of a smooth circular spot on the cuticle (Fig. 3A, arrow).

Amphids shifted onto the apical area of the cephalic region. Anterior end of the amphideal fovea is located on apical surface close to the mouth opening; the fovea turns dorsally and runs on into the long dorsal arm of the fovea extended far hindward as elongated loop with tight but distinct ridge-like interspace between two arms (Figs. 3A, 3C; 6A–6C).

Somatic cuticle not widened around the mouth. Cheilostoma shaped as a truncate cone with longitudinal rugosity. Long and narrow pharyngostoma armed with a long dorsal tooth provided with a conical pointed cuticular arrowhead (corona). The tooth is adherent dorsally to the pharynx tissue at two thirds of its length. Pharyngostoma is surrounded by inflated pharyngeal tissue with fine transversal striation. Middle part of the pharynx slender; posterior part of the pharynx is formed as an elongate terminal bulb with muscular cross striation. Internal cuticular lining of the bulb with muscular cross striation not thickened and seemingly not modified. Midgut slender, filled with orange pigment inclusions.

No renette found.

Testis singular anterior, outstretched, situated to the left of the intestine in all the male specimens. Spicules paired and equal, short, arcuate, proximally cephalated and distally pointed. Gubernaculum S-shaped and oriented perpendicularly to the longitudinal body axis. Series of 14–19 equal midventral precloacal supplementary organs. Supplements consist of three constituents, (1) surface cuticular pit with cuticularized walls, (2) core within the pit, head of the core bears a longitudinal ridge with a papilla, (3) short internal straight cuticular tube extending from the pit obliquely inward (Figs. 4B, 6D–6E).

Tail conical, with caudal glands and a terminal spinneret. Caudal gland cell bodies hardly discernible, visibility limited within tail, but may have seemingly pushed out to preanal region in some specimens.

Females. Amphideal fovea spirally coiled in three turns and situated entirely on the cephalic apex close to the mouth opening (Figs. 3C, 6C).

Ovaries paired, antidromously reflected, both situated to the left of the intestine in all female specimens studied (Fig. 1B).

Diagnosis

Body length 695–1014 µm, index a 20–40.5, index c’ 2.5–4.34. Cephalic setae 6.5–14.2 µm long. Two subsequent crowns of eight subcephalic setae similar in length to the cephalic ones. Amphideal fovea shows strong sexual dimorphism: in females, the amphideal fovea spirally coiled in three turns and located entirely on the head apex, while in males, the fovea turns dorsally from the aperture on the apex, then extended hindward as elongated loop. Dorsal tooth 27–40 µm along the ventral side. Terminal bulb of the pharynx elongated, 40–60 µm long, with faint internal lining. Spicules arcuate, 33–40 µm long. Midventral precloacal supplementary organs 14–19 in number, consist of flat cap and internal short and almost straight cuticular tubes. Tail conical, c’ 2.4–4.3.

Relationships

Onyx disparamphis sp. n. differs immediately from all other Onyx species by the peculiarly very long loop of the amphideal fovea of males. O. disparamphis shares simple non-double terminal pharyngeal bulb with thirteen other Onyx species (Table 2), among them O. balochinensis, and O. brevispiculatum may show some resemblance in shape of supplementary organs, relatively small and straight, non-sigmoid. O. disparamphis differs from O. balochinensis by smaller body length (690–1014 versus 1240–1640 µm), smaller cephalic setae (6.5–15 versus 17–22 µm), smaller terminal pharyngeal bulb (38–62 versus 84–105 µm in length) and smaller spicules (33–40 versus 45–50 µm). O. disparamphis differs from O. brevispiculatum by also smaller body (695–1014 versus 1800–3300 µm), twice the lower number of supplementary organs (14–19 versus 39) and relatively longer tail (c’ 2.4–4.4 versus 1.2).

Ecological remarks

Onyx disparamphis is a common, but not very numerous species on the Shinyang beach, being the 12th most abundant and comprising 1.6% of total nematode abundance of the beach. O. disparamphis is distributed across the whole intertidal sandy beach from lower to upper horizon, with some increase in numbers at middle and upper horizons. No obvious confinedness to a certain layer in vertical sediment column is observed, evidently because of uniformity of conditions (granulometry) within a sediment depth 0–20 cm.

Microscopic examination of gut content does not reveal any evident particles or identifiable remnants. The intestine of the individuals studied either appear empty or with spherical drops. The long and strong dorsal tooth may protrude from the mouth as it is shown for Onyx sagittarius by Gerlach (1950, Abb. 5c). We suppose that Onyx disparamphis and its congeners could pierce covers of some food items (e.g., protists) and suck out the liquid matter by muscular bulb pumping.

Pictorial key for identification Onyx species

The present pictorial key for identification of 23 valid species of Onyx is constructed based on principles of Platt (1984), who first introduced such keys in marine nematology. The key consists of two components, (1) a set of species icons or pictorial key (Figs. 7–8), and (2) a table of the most important morphometric and numerical characteristics (Table 2). Most valid species are known on both males and females, and only two species, O. monstrosum and O. orientalis are described based only on males. Only males are used for pictures since they provide more distinctly perceiving features (such as amphids) on the head and much more features (such as copulatory and supplementary organs) on the posterior body. The table 2 includes characteristics of only males, because females are not known for two species and data on females are often less complete in comparison with males in other descriptions based on two sexes.

On Figs. 7–8, the heads are arranged in such an order that species having the largest and most conspicuous amphideal fovea are located at the top of the key; by scanning the icons from top to bottom, the amphids and head setae become gradually smaller and shorter.

Spatial distribution of Onyx species

Like most other marine nematode superspecies taxa, the genus Onyx shows a worldwide distribution (Fig. 9); however, most species are confined with warm waters, and none occurs in Arctic and Antarctic (with possible exception O. ferox sp. inq. in Subantarctic). Nine species are recorded in tropical areas (balochiensis, blomei, cangioensis, cobbi, dimorphus, mangrove, orientalis, paradimorphus, perfectus); eight species in subtropical regions (adenophorus, brevispiculatum, cannoni, cephalispiculus, macramphis, perfectus, potteri, sagittarius), nine species in temperate regions (disparamphis, littorale, minor, monstrosum, perfectus, rizhaoensis, rugatus, sagittarius, septempapillatus). Surprisingly, there were no Onyx species recorded along the east coasts of the Americas, but this is likely due to insufficient information on meiofauna in this specific region. A cluster of six co-occuring species within a limited area was found in the CanGio mangrove habitat (South Vietnam) in silty sediment at a depth 0.5 m.

All the Onyx species are confined with coastal shallows, from intertidal zone to upper sublittoral of several tens of meters depth; no species are recorded from the deep sea. The majority of species inhabits coarse sands (16 of 24 species), often on high energy beaches. The remaining eight species were found on silts, most of them (six) in mangrove milieu.