Introduction
Gastropods of the family Eulimidae (Caenogastropoda: Vanikoroidea) are parasites of all five extant classes of Echinodermata: Asteroidea (sea stars), Crinoidea (feather stars and sea lilies), Echinoidea (sea urchins), Holothuroidea (sea cucumbers), and Ophiuroidea (brittle stars; Warén, Reference Warén1983a). At least 14 eulimid genera are known to contain ophiuroid-parasitic species. These genera include Ersilia Monterosato, 1872, Eulima Risso, 1826, Fuscapex Warén, Reference Warén1981, Fusceulimoides Takano, Kano, Mogi and Okanishi, Reference Takano, Kano, Mogi and Okanishi2023, Hemiliostraca Pilsbry, 1917, Mucronalia A. Adams, 1860, Ophieulima Warén and Sibuet, Reference Warén and Sibuet1981, Ophioarachnicola Warén, Reference Warén1980, Ophiolamia Warén and Carney, 1981, Punctifera Warén, Reference Warén1981, Pyramidelloides G. Nevill, 1885, Sticteulima Laseron, 1955, Stilapex Iredale, 1925, and Vitreolina Monterosato, 1884 (Warén, Reference Warén1980, Reference Warén1981, Reference Warén1983a, Reference Warén1983b; Bouchet and Warén, Reference Bouchet and Warén1986; Dgebuadze, Reference Dgebuadze2014; Takano et al., Reference Takano, Kano, Mogi and Okanishi2023).
The genus Ophieulima consists of parasites of deep-sea ophiuroids (Warén and Sibuet, Reference Warén and Sibuet1981). Only two named and one undescribed species have been reported from bathyal depths as extant taxa (Warén, Reference Warén1981; Warén and Sibuet, Reference Warén and Sibuet1981). The type species, Ophieulima minima (Dall, 1927), inhabits the Atlantic Ocean and Mediterranean, 452–2140 m deep, parasitizing Ophiactis abyssicola (M. Sars, 1861) of Ophiactidae (Warén and Sibuet, Reference Warén and Sibuet1981; Bouchet and Warén, Reference Bouchet and Warén1986; Hoffman et al., Reference Hoffman, van Heugten and Lavaleye2011; Romani et al., Reference Romani, Bartolini, Giusti and Sbrana2014; Souza et al., Reference Souza, Pimenta and Barros2021). Its shell is characterized by (1) a conical shape with convex teleoconch whorls, (2) a length of up to 3 mm, (3) many fine growth lines and up to two strong growth pause scars on the teleoconch, (4) a solid and twisted columella, (5) a sculpture of oblique incised line segments, and (6) a brownish transparent protoconch with ca. 3 whorls (Warén and Sibuet, Reference Warén and Sibuet1981; Romani et al., Reference Romani, Bartolini, Giusti and Sbrana2014; Souza et al., Reference Souza, Pimenta and Barros2021; but see Remarks below). Other notable characters of the species include the lack of pigmented eyes and the radula (a tongue-like feeding apparatus of the Mollusca), presence of the operculum, separate sexes, and sexual dimorphism with the female of 2.5–3 mm in shell length and the male of 1–1.5 mm (Warén and Sibuet, Reference Warén and Sibuet1981; but see O'Reilly, 2016: figure 24 for the presence of pigmented eyes).
Another extant species, Ophieulima fuscoapicata Warén, Reference Warén1981, was reported from off Kermadec Islands of New Zealand, 1189–1225 m deep, parasitizing Ophiactis profundi Lütken and Mortensen, 1899 (Warén, Reference Warén1981). Ophieulima fuscoapicata morphologically resembles to the type species but differs in having a smaller aperture and irregular spiral sculpture of the shell, and a protoconch of 3.9 whorls (Warén, Reference Warén1981). In addition, an undescribed species has been known from off Gabo Is., Victoria, Australia, 400–438 m deep, without host information (Warén, Reference Warén1981). This species is seemingly characterized by a relatively small aperture (Warén, Reference Warén1981).
Two fossil species were also described under this genus. Ophieulima antecessor Lozouet, Reference Lozouet1999 was reported from the Upper Oligocene deposits of Aquitaine, southwestern France (Lozouet, Reference Lozouet1999). Its shell is characterized by a more globose outline than the three extant taxa, 2.45 mm in length and 1.65 mm in width, a large, inflated body (ultimate) whorl, and a protoconch of only two whorls (Lozouet, Reference Lozouet1999). The other fossil species, Ophieulima lobilloensis Landau and Mulder, Reference Landau and Mulder2022, was described from the Lower Piacenzian (upper Pliocene) deposits of Estepona, southwestern Spain (Landau and Mulder, Reference Landau and Mulder2022). This species possesses an elongate ovate shell of 1.4 mm in length and 0.82 mm in width, with a large, pyriform aperture occupying 50% of total length and a pupiform protoconch of >2.5 whorls (Landau and Mulder, Reference Landau and Mulder2022).
Here, we describe Ophieulima yoshiharai n. sp. as a new extant species of the genus from central Japan, parasitic on Ophiactis dyscrita H. L. Clark, Reference Clark1911. This is the first record of the genus from Japanese waters and even from the North Pacific Ocean.
Materials and methods
Six individuals of the brittle star Ophiactis dyscrita were collected from off Jogashima Is., Miura, Kanagawa, Japan (256–343 m deep; R/V Rinkai-Maru St. 2) on 24 June 2010 using a 0.5 m biological dredge. A parasitic snail of Eulimidae was found on one of the six brittle stars, attaching to the lateral side of the disc (Figure 1); the snail and host were directly preserved in 99% ethanol. The preserved specimens were observed and identified under a stereoscopic microscope by referring to previous taxonomic studies (Warén, Reference Warén1981, Reference Warén1983a; Warén and Sibuet, Reference Warén and Sibuet1981 for snail, and Clark, Reference Clark1911; Matsumoto, Reference Matsumoto1917 for brittle star). Unfortunately, tissue clipping for molecular works was impossible without breaking the shell for the present snail specimen. Voucher material was deposited in the National Museum of Nature and Science, Tokyo (NSMT).
Ophieulima yoshiharai n. sp.: (1) holotype NSMT-Mo 79481 in situ on host brittle star Ophiactis dyscrita; (2) holotype, apertural and lateral views; (3) close-up view of protoconch. Arrow denotes demarcation line between protoconch and teleoconch. Distinct scar exists at 2.3 whorls from apex or 1.2 whorls from demarcation line. Scale bars: (2) 500 μm; (3) 200 μm.
Results
The newly collected snail was identified as a species of Ophieulima based on its conchological characters including (1) a small, conical shape with convex teleoconch whorls, (2) many fine growth lines and some strong growth pause scars on the teleoconch, (3) a well-developed, twisted columella, and (4) a multispiral, brownish transparent protoconch (Figures 2, 3; see Warén and Sibuet, Reference Warén and Sibuet1981). We describe it as Ophieulima yoshiharai n. sp.
Superfamily Vanikoroidea Gray, 1840
Family Eulimidae Philippi, 1853
Genus Ophieulima Warén and Sibuet, Reference Warén and Sibuet1981
Ophieulima yoshiharai n. sp.
(Figures 1–3)
http://zoobank.org/AF229D6A-AAE1-4F6D-9FC8-F0A2A07B4880
Type specimen
Holotype NSMT-Mo 79481, found attached to lateral side of host's disc, preserved in 99% ethanol together with host ophiuroid.
Type locality
Off Jogashima Is., Miura, Kanagawa, Japan (35°07.12–07.28′ N, 139°33.72–33.21′ E; 256–343 m deep), sandy bottom.
Type host
Ophiactis dyscrita H. L. Clark, Reference Clark1911 (Echinodermata: Ophiuroidea: Amphilepidida: Ophiactidae).
Etymology
After Mr. Toshiyuki Yoshihara, the owner of the Meguro Beer Pub SCENT, who continuously encouraged the study of the first author.
Diagnosis
Ophieulima species with a slender shell with its length 2.1 times larger than width. Body whorl and shell aperture small for genus, occupying 70% and 39% of total length, respectively. Protoconch multispiral with 3.5 whorls.
Description
Holotype NSMT-Mo 79481: Shell minute, 1.57 mm high, 0.73 mm wide, white translucent, thin but not fragile, conical with 5.6 whorls (Figure 2). Protoconch conical, multispiral, brownish transparent with 3.5 whorls; a distinct scar present at 2.3 whorls from apex; exposed whorls 480 μm high, slightly convex, smooth (Figure 3). Teleoconch whorls 2.1, bearing many fine growth lines and slightly curved, irregularly spaced strong growth pause scars, which are situated at 0.1, 0.6, 0.8, 0.9, 1.2 and 1.7 whorls from demarcation line between teleoconch and protoconch. Body whorl occupies 70% of total shell height. Aperture wide, semicircular, 0.62 mm in height and 0.51 mm in width; outer lip simple, prosocline, arced in lateral view, with its most protruding part at 1/4 of aperture height from suture (Figure 2); parietal wall and columellar lip join in a straight line; columellar callus well developed, twisted, extended outward near round base. Operculum yellowish transparent, thin. Pigmented eyes present.
Remarks
Table 1 summarizes morphological and ecological differences among extant Ophieulima species. Ophieulima yoshiharai n. sp. has the slenderest shell among them, with the length of 2.1 times larger than width. Shell length/width ratio ranges 1.5–1.9 in the other known extant species including the type species O. minima. The new species has a protoconch of 3.5 whorls, which is more coiled than that of the type species (2.7–3 whorls according to previous studies) and less than O. fuscoapicata (3.9 whorls). However, it should be noted that the protoconch of O. minima apparently has up to 3.7 whorls (see Souza et al., Reference Souza, Pimenta and Barros2021: figure 19F, G). As in the present new species, one or two distinct scars, which might be confused with the demarcation line between the protoconch and teleoconch, exist on the protoconch at 0.8–1.2 whorls from the demarcation line. Further verification is required for the protoconch morphology of O. minima. The presence or absence of pigmented eyes might exist within the genus. Warén and Sibuet (Reference Warén and Sibuet1981) noted that ‘no eyes can be seen’ in O. minima, whereas this may be attributable to damage by long-term storage. Two pigmented eyes are visible through the shell in O'Reilly's (2016: figure 24) fresh material. Pigmented eyes are also present in O. yoshiharai n. sp. and O. fuscoapicata.
Morphological and ecological features of extant Ophieulima species, referred by Warén (Reference Warén1981), Warén and Sibuet (Reference Warén and Sibuet1981), Hoffman et al. (Reference Hoffman, van Heugten and Lavaleye2011), Romani et al. (Reference Romani, Bartolini, Giusti and Sbrana2014), O'Reilly (2016) and Souza et al. (Reference Souza, Pimenta and Barros2021)
*Including values measured by authors from figures in previous studies.
The extant species of Ophieulima also have different geographical and bathymetric distributions. The type species habitats 450–2100 m deep in the Atlantic Ocean. The two Pacific species have been recorded around 1200 m of Kermadec Islands and 420 m of Australia, respectively (Table 1). Ophieulima yoshiharai n. sp., collected from 256 to 343 m in this study, thus represents the shallowest record of the genus. On the other hand, the hosts of Ophieulima species have so far been restricted to ophiuroids of the ophiactid genus Ophiactis (Table 1). The three named species have mostly been found attached to the lateral and/or dorsal sides of the host's disc (Warén, Reference Warén1981; Warén and Sibuet, Reference Warén and Sibuet1981; Bouchet and Warén, Reference Bouchet and Warén1986; but see O'Reilly, 2016: table 6), suggesting their similar parasitic ecology.
Ophieulima yoshiharai n. sp. is easily distinguished from the two fossil species. Ophieulima antecessor has a much more globose shell with a protoconch of only 2 whorls (Lozouet, Reference Lozouet1999). Its paucispiral protoconch infers this fossil species is phylogenetically distinct from, or even totally unrelated to, the extant species of the genus. Ophieulima lobilloensis differs from the new species in having an elongate ovate profile of the shell and a large, pyriform aperture occupying 50% of total shell length (Landau and Mulder, Reference Landau and Mulder2022).
Discussion
In this study we reported the eulimid genus Ophieulima from the North Pacific Ocean for the first time and described O. yoshiharai n. sp. as the third extant species of the genus. Given a few previous occurrence records (Warén, Reference Warén1981; Warén and Sibuet, Reference Warén and Sibuet1981; Bouchet and Warén, Reference Bouchet and Warén1986; Hoffman et al., Reference Hoffman, van Heugten and Lavaleye2011; Romani et al., Reference Romani, Bartolini, Giusti and Sbrana2014; O'Reilly, 2016; Souza et al., Reference Souza, Pimenta and Barros2021) and low prevalence (1.4% for O. minima; see O'Reilly, 2016), the species of Ophieulima are rare, while the genus possibly has a global distribution. Their minute sizes and deep-sea habitats may have also been making it difficult to discover Ophieulima species.
Morphological and ecological traits do not provide a clear suggestion for the phylogenetic position of Ophieulima. Warén (Reference Warén1983a) has proposed a systematic hypothesis that eulimid species in closely related genera parasitise echinoderms of a single class. Molecular phylogenetic study of Eulimidae have confirmed that the host's class rather than shell shape tends to reflect intrafamilial relationships (Takano and Kano, Reference Takano and Kano2014; Takano and Goto, Reference Takano and Goto2021). However, ophiuroid-parasitic species were recovered as polyphyletic groups with Fusceulimoides distantly related to Eulima + Hemiliostraca + Pyramidelloides (Takano and Goto, Reference Takano and Goto2021; Takano et al., Reference Takano, Kano, Mogi and Okanishi2023). Species of Eulima, Hemiliostraca, and Pyramidelloides have a brownish protoconch, whereas the protoconch of Fusceulimoides is white (Warén, Reference Warén1983a, Reference Warén1983b; Takano et al., Reference Takano, Kano, Mogi and Okanishi2023; T. Takano, pers. obs.). The presence of a brownish protoconch is a possible synapomorphy for the former three genera and Ophieulima, suggesting their close phylogenetic kinships.
The presence or absence of the radula also accords well with the eulimid phylogeny (Takano and Kano, Reference Takano and Kano2014). All radula-less species analysed so far have been recovered as a robust clade, except for species of the highly modified endoparasitic genus Asterophila Randall and Heath, 1912 (Takano and Kano, Reference Takano and Kano2014; Takano and Goto, Reference Takano and Goto2021). Asterophila was found to be sister to the radula-bearing genus Niso Risso, 1826 (see Warén, Reference Warén1983a), indicating the radula has been lost multiple times in the evolutionary history of Eulimidae (Takano and Goto, Reference Takano and Goto2021). Among ophiuroid-parasitic eulimids above, species of Eulima, Hemiliostraca, and Pyramidelloides possess the radula (Warén, Reference Warén1983a; Reference Warén1983b). The anatomy of Fusceulimoides has not been investigated, while this genus is nested in the radula-less clade and thus probably lacks the radula (Takano et al., Reference Takano, Kano, Mogi and Okanishi2023). In this view, the absence of the radula in the type species O. minima (Warén and Sibuet, Reference Warén and Sibuet1981) suggests its close affinity to Fusceulimoides. Other radula-less genera parasitic to ophiuroids include Stilapex and Vitreolina (Warén, Reference Warén1983a); Bouchet and Warén (Reference Bouchet and Warén1986) pointed a conchological similarity between Ophieulima and Stilapex. As discussed above, Ophieulima may be closely related to Eulima, Hemiliostraca, and Pyramidelloides and in that case the absence of the radula is an apomorphic condition of Ophieulima. Molecular phylogenetic analysis might answer this complicated systematic issue.
Data availability
The data supporting the findings of this study are available within the article.
Acknowledgements
We are grateful to B.M. Landau for providing literature on a fossil species of Ophieulima. Invaluable comments were provided by L. Hoffman, Y. Kano, and L.S. Souza for the improvement of the manuscript.
Author contributions
TT conducted morphological observation of the new species and prepared the manuscript. HK and MO collected the specimens, identified the host ophiuroid, revised drafts, and gave final approval for publication.
Financial support
This work was supported by JSPS KAKENHI grant no. 23K14257.
Competing interests
None.
Ethical standards
Not applicable.
