Enigmaticolus inflatus, Zhang & Zhang & Chen, 2020

Zhang, Shuqian, Zhang, Suping & Chen, Hao, 2020, Enigmaticolus inflatus sp. nov., a new buccinid species from a methane seep area in the South China Sea (Gastropoda: Neogastropoda), Zootaxa 4728 (3), pp. 385-389 : 385-389

Enigmaticolus inflatus sp. nov. ( Figures 1 , 2 )

Type specimens. Holotype MBM 286512 , height: 79.2 mm, width: 46.4 mm, 22°07′N 119°17′E, 1119 m deep, August 2018 ; Paratype MBM286513 , one specimen, height: 83.3 mm, width: 50.0 mm, collected with the holotype at the type locality .

Both type specimens were fixed in 99.5% ethanol with soft parts, and deposited in the Marine Biological Museum of Chinese Academy of Sciences ( MBMCAS), Qingdao, China.

Type locality. A deep-sea methane seep site in South China Sea (22°07′N 119°17′E), at a depth of 1119 m. The entire seep field is dominantly colonized by Bathymodiolus platifrons Hashimoto & Okutani, 1994 (Mytilidae) and Shinkaria crosnieri Baba & Williams, 1998 ( Munidopsidae ) associated with polynoid worms, gastropods, and shrimps.

Etymology. The name refers to its remarkable inflation of shell.

Description. Shell ( Figs 1 A–D) medium-sized for genus (length to 83.3 mm), ovate-conic, thick. Colour reddish brown. Periostracum adherent, thin, dark brown in colour. Spire small, relatively low, the last whorl large. Siphonal canal short, broad, open, anterior end with a prominent incision. Protoconch and upper whorls lost, with only last four whorls remaining. Suture narrow, deep. Teleoconch whorl roundly inflated, subsutural area slightly constricted. Spiral sculpture with fine, indistinct trace of grooves, becoming slightly developed on shell base; axial sculpture limited to some weakly recurved growth lines. Aperture large, ovate, inner surface shining pinkish brown, outer lip not thickened; columellar lip strongly callused. Callus raised and slightly reflected, forming a chink between columellar lip and the last whorl. Fasciole well developed.

Operculum ( Fig 1D ). Corneous, elongately ovate, nucleus apical.

Radula ( Fig 1E ). Rachidian teeth with three cusps. Two lateral cusps slightly stronger than the middle one, elevated from basal plate, forming a narrow concavity. The rightmost cusp with a small secondary cusp. Basal plate roughly rectangular, strongly concave along anterior edge. Lateral teeth with two strong cusps, outer one longer, but slightly thinner than inner one.

Soft parts ( Fig 2 ). Preserved animal whitish to yellowish in general. Foot large, fleshy, anterior end with opening of pedal gland. Head large, tentacles contracted, stout, cylindrical, with large black eyes near bases. Penis large, broad, laterally compressed, distal end truncated with a small, digitate seminal papilla. Mantle edge broadly thickened, with narrow, reddish brown patches along its margin. Ctenidium large, three times as wide as the osphradium, twice as long as osphradium. Siphon broad, short, muscular. Proboscis in inverted position folded into the rhynchocoel, nearly 40 mm in length, thick-walled, occupying entire rhynchocoel. Proboscis retractor muscles numerous, arranged in two lateral symmetrical bundles. These retractor muscles attached the proboscis to roof, lateral and basal walls of rhynchodaeum.

Remarks. Based on shell morphology and molecular information from COI, the new species can clearly be assigned to the genus Enigmaticolus . To date, the genus includes three species: Enigmaticolus monnieri Fraussen, 2008 from western Indian Ocean ( Mozambique Channel), E. marshalli Fraussen & Stahlschmidt, 2016 (Kermadec Ridge, New Zealand) and E. voluptarius Fraussen & Stahlschmidt, 2016 ( New Caledonia) from the southwestern Pacific’), bathymetrically ranging from 704 m to 1026 m.

Enigmaticolus inflatus sp. nov. most resembles E. marshalli Fraussen & Stahlschmidt, 2016 in overall shell shape. From the new species, however, E. marshalli differs in having a more slender shell with prominent spiral sculpture over the entire surface, narrow axial ribs on the subsutural slope, and a distinct subsutural concavity. Two undescribed species from East China Sea, reported as Enigmaticolus sp. 1 and Enigmaticolus sp. 2 by Fraussen & Stahlschmidt (2016) may represent the geographically closest congeners to E. inflatus sp. nov. Enigmaticolus sp. 1 somewhat resembles the new species in general shell shape, but differs in having a much more slender shell. In addition, E. inflatus sp. nov. may be confused with Thermosipho desbruyeresi ( Okutani & Ohta, 1993) , a species from hydrothermal vents, in having a similar shell shape with reduced spiral sculpture. T. desbruyeresi , however, has a smaller adult shell with different proportions, and a shorter siphonal canal.

Molecular analyses. Sequencing and phylogenetic methods follow that of Zhang & Zhang (2017). The length of the obtained COI sequence is 658 bp. The Neighbor-joining (NJ) tree ( Fig 3 ) was reconstructed using available COI sequences from this study and GenBank. The alignment of COI had a total 636 bp, without insertions and deletions. The NJ tree shows that E. inflatus sp. nov. falls into Enigmaticolus in which, together with E. monnieri Fraussen, 2008 , it forms a well-supported sister clade to Thermosipho auzendei ( Warén & Bouchet, 2001) . The pairwise distance between the new species and E. monnieri is only 0.3–0.6%. Typically, the interspecific pairwise differences between COI sequences of marine gastropods is above 3% ( Meyer & Paulay 2005). Morphologically, however, E. monnieri can be clearly separated from E. inflatus sp. nov. in having a slender shell with developed axial ribs, and a more distinct subsutural constriction. In addition, the penis in E. monnieri seems to be more slender with a pointed distal end (see Kantor et al. 2013).

Deep-sea cold seeps are in general thought to be harsh (e.g. high pressure, high toxicity, and low oxygen) but very stable (e.g. cooler temperature, rich food supply) environments for growth of organisms. From this point of view, the members of the seep-associated genus Enigmaticolus , as top predator, may live in such environment with a complex genetic adaptation. In the process of adaptation, the mtDNA evolution may be subjected to an ecosystem-specific selection pressure, which results in a slowdown or generally low rate of COI evolution in E. inflatus sp. nov. and E. monnieri . This may explain why the genetic distances of COI is so minimal between these two species.

The two species are quite different, not only in shell morphology, but also in external anatomy and radula features, indicating that there should be sufficient generic diversity and evolutionary depth to generate such morphological differences. This requires further study to find the relevant genes. In addition, only two specimens are available in the present study, which could not provide enough statistic information for a thorough comparison. Clearly, larger sample sizes, both from type locality of E. inflatus sp. nov. and E. monnieri , are needed for further analysis and comparisons.

Figures

FIGURE 1. Enigmaticolus inflatus sp. nov. A–C. holotype MBM 286512, 79.2 mm; D. paratype MBM 286513, 83.3 mm; E. Radula of holotype.

FIGURE 2. Soft parts of Enigmaticolus inflatus sp. nov., holotype MBM 286512. A. Right view, B. left view, and C. apical view of the head-foot; D. Dorsal view of the proboscis. Abbreviations. (cep.t) cephalic tentacle; (cm) columellar muscle; (ct) ctenidium; (e) eye; (f) foot; (me) mantle edge; (os) osphradium; (p) penis; (pg) pedal gland; (pr) proboscis; (prr) proboscis retractors; (rm) retractor muscle; (s) siphon; (sp) seminal papilla.

FIGURE 3. Neighbour-joining tree for Enigmaticolus and related genera based on available COI sequences from this study and Gen- Bank. Numbers above branches indicate the bootstrap values. (MN102347 is the GenBank accession number for the COI sequence of Enigmaticolus inflatus sp. nov.)