©The Malacological Society of Japan DOI: http://doi.org/10.18941/venus.78.3-4_119 Short Notes September 25, 2020119

Short Notes

Systematic Relocation of Chrystella kajiyamai Habe, 1961 to the Eulimid (: )

Tsuyoshi Takano1*, Shouji Tsuzuki2 and Yasunori Kano3 1Meguro Parasitological Museum, 4-1-1 Shimomeguro, Meguro, Tokyo 153-0064, Japan; *[email protected] 253-17 Oyumi, Chiba, Chiba 260-0813, Japan 3Atmosphere and Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japan

The genus Chrystella Laseron, 1956 is a group of family (superfamily Vanikoroidea), in little-known gastropods in the family Pickworthiidae sharing a small, colorless high-conical teleoconch (superfamily ; see Takano & Kano, with strong spiral ribs (Warén, 1983; see e.g., 2014; Bouchet et al., 2017). These gastropods have Hedley, 1899: g. 72; Laseron, 1956: g. 111). been reported only as empty shells from intertidal Eulimids are exclusive parasites of , to bathyal waters in tropical and subtropical regions with specializing in brittle stars worldwide (Le Renard & Bouchet, 2003; Santos & (Warén, 1983, 1984; Takano & Kano, 2014). Their França, 2008; Moolenbeek & Mussai, 2010). The similar teleoconch morphologies led Warén (1983) type of the genus, C. islandica Laseron, to suggest a close relationship between Chrystella 1956, was described from an incomplete shell from and Pyramidelloides and Ponder (1985) to regard Christmas Island of Australia (Laseron, 1956). the former as a subgenus of the latter in the family Eight extant species are currently placed in Eulimidae. The protoconch morphology, however, Chrystella according to MolluscaBase (2020a). dismisses such a generic or familial assignment. Their shells are characterized by 1) a small size, with Protoconchs in the Eulimidae, including those of a height of ca. 2 mm, 2) a high conical shape, 3) lack Pyramidelloides, are smooth conical or pupiform of coloration, 4) strong spiral ribs on teleoconch without having a strong surface sculpture or deep whorls, 5) a developed keel at the periphery, and 6) sutures (e.g., Warén, 1983: gs 66–68). a more or less circular with a thickened “Crystella” kajiyamai Habe, 1961 (= Chrystella (e.g., Laseron, 1956; Bouchet & Le Renard, 1998; kajiyamai Habe, 1961; see Nomenclature below) is a Santos & França, 2008). The protoconch of the type species for which information on the protoconch has species, C. islandica, has never been reported, while been lacking to date. Its holotype, from Kakeroma C. nckhi (Hedley, 1899) with a similar teleoconch Island in southwestern Japan, is an empty shell of bears a distinctly sculptured protoconch with convex 2.2 mm height with a broken (Habe, 1961: whorls (Hedley, 1899; Bouchet & Le Renard, text- g. 3; Higo et al., 2001: g. G1948). The 1998). These teleoconch and protoconch characters original assignment of the species to Chrystella was combined justify the current assignment of the genus thus made on the basis of teleoconch characteristics to Pickworthiidae (Bouchet & Le Renard, 1998; Le including strong spiral ribs (Habe, 1961: text- g. Renard & Bouchet, 2003). Pickworthiid snails are 3). This generic position has been maintained by known to inhabit submarine caves, crevices and subsequent authors (e.g., Warén, 1983; Higo & similar cryptic voids in shallow subtidal waters Goto, 1993; MolluscaBase, 2020a), whereas Le (Kase & Hayami, 1992; Kase, 1998; Takano & Renard & Bouchet (2003) did not include the Kano, 2014). species in their checklist of pickworthiid taxa Some species of Chrystella also resemble with no comment. Japanese authors have placed Pyramidelloides miranda (A. Adams, 1861), the the species (and the genus Chrystella) either in type species of Pyramidelloides Nevill, 1884 in the Eulimidae (Higo et al., 1999, 2001; Hori, 2000) or 120 VENUS 78 (3–4), 2020 in Pickworthiidae (Hasegawa, 2017), apparently by Remarks: This genus comprises three described following Ponder (1985) or Bouchet & Le Renard species: B. striolata (= Subeulima lamberti (1998), respectively. We herein propose placing C. Soubervie, 1875), B. kajiyamai (Habe, 1961) and B. kajiyamai in the eulimid genus Bacula H. Adams morisyuichiroi (Habe, 1968). See below for details. & A. Adams, 1863 based on a newly collected shell with an intact protoconch. We also conduct Bacula kajiyamai (Habe, 1961) n. comb. a brief taxonomic review of the species of Bacula (Fig. 1) and provide circumstantial evidence that they are ectoparasites on ophiuroid echinoderms. Crystella kajiyamai [sic; = Chrystella]: Habe, 1961: 271, 273, text- g. 3; Ekawa, 1985: 8, pl. 2, g. Systematics 23; Ekawa, 1993: 96, g. 91; Higo & Goto, 1993: 86; Héros et al., 2007: 219. Superfamily Vanikoroidea Gray, 1840 Chrystella kajiyamai — Warén, 1983: 293; Hori, Family Eulimidae Philippi, 1853 2000: 363, pl. 180, g. 81; Hasegawa, 2017: 800, pl. 67, g. 7; Kitagawa, 2017: g. 047-06. Genus Bacula H. Adams & A. Adams, 1863 Pyramidelloides (Chrystella) kajiyamai — Higo et al., 1999: 184. Bacula H. Adams & A. Adams, 1863: 18. Type Pyramidelloides kajiyamai — Higo et al., 2001: 56, species: Bacula striolata H. Adams & A. Adams, g. G1948. 1863: 18, 19, by monotypy. Subeulima Soubervie, 1875: 296. Type species: Nomenclature: The generic name “Crystella” Subeulima lamberti Soubervie, 1875: 296 in Habe (1961) is, given his reference to the (subjective junior synonym of Bacula striolata), type species of Chrystella (as “Crystella islandica by monotypy. Laseron”), most certainly a lapsus calami and an “incorrect subsequent spelling” (see International

Fig. 1. Bacula kajiyamai (Habe, 1961) n. comb. from Zamami, Okinawa Islands, Japan, NSMT-Mo 79123. A. Apertural, lateral and abapertural views of shell. B. Protoconch. Arrowhead indicates protoconch–teleoconch boundary. Short Notes 121

Code of Zoological Nomenclature, ICZN, Article eulimid genera as Bacula, Risso, 1826, 33.3). The species name kajiyamai is deemed to Pilsbry, 1917 and Pyramidelloides have been proposed in combination with the correct (e.g., Habe, 1968; Warén, 1980, 1983). These spelling of the generic name Chrystella (ICZN, contrast with the markedly sculptured protoconch Article 11.9.3.2). of the pickworthiid genus Chrystella (see Bouchet Type specimen: Holotype NSMT-Mo 39838 in & Le Renard, 1998: g. 15.101I; Santos & França, the National Museum of Nature and Science, Tokyo 2008: g. 2; Moolenbeek & Mussai, 2010: g. (see Habe, 1961: text- g. 3; Higo et al., 2001: 56, 3). The presence of the incremental lines on the g. G1948) from Kakeroma Island, Amami Islands, teleoconch further corroborates the af nity of C. Kagoshima Prefecture, Japan. kajiyamai to Eulimidae (see below). Material examined: NSMT-Mo 79123, an empty We herein transfer C. kajiyamai to the eulimid shell sorted by one of the authors (ST) from shallow genus Bacula H. Adams & A. Adams, 1863, based subtidal sediment off Zamami Island, Kerama, on its conchological resemblance to the type Okinawa Prefecture, Japan, 26°15′N, 127°18′E, at a species B. striolata H. Adams & A. Adams, 1863. depth of 3 m, July 1, 2016. Somewhat confusingly, however, B. kajiyamai does Distribution: Japan: Wakayama, Honshu not look very similar to the “holotype” ( = probable Island (Higo et al., 1999); islands of Amami and syntype) of B. striolata from “China Sea” (NHMUK Okinawa (see above). New Caledonia, Southwest 1878.1.28.68 in the Natural History Museum, Paci c: Grand Récif de Koumac, Expedition London). This “holotype” is a 7.7-mm high shell MONTROUZIER, Stn. 1316, 20°40′S, 164°11′E, with many spirals but without a carinated periphery 12–55 m deep, October 1993 (SMNH-50835 in (Warén, 1984: g. 48). It represents, however, an Swedish Museum of Natural History, photograph immature condition of a large species, as exempli ed courtesy of A. Warén; Héros et al., 2007). by the holotype of Subeulima lamberti Soubervie, Redescription: Shell slender, straight, conical, 1875 from New Caledonia, southwest Paci c. The 3.8 mm high and 1.3 mm wide, solid (Fig. 1A). holotype shell of the latter nominal taxon has a Teleoconch colorless with 9.2 whorls. Each whorl height of 23 mm and a strongly carinated periphery, bears up to six spiral ribs, which are more numerous whereas its upper whorls are nearly identical to the on later whorls; uppermost rib strongest, knobby on “holotype” of B. striolata (Warén, 1984: 74, gs third to sixth whorls and smooth on later whorls, 203, 204). The genus Subeulima and S. lamberti as largely overlapping peripheral keel of preceding its type species were therefore synonymized under whorl. First two whorls also with ne axial and spiral Bacula and B. striolata, respectively, in the seminal threads, forming grid pattern. Incremental lines generic revision of the family Eulimidae by Warén or growth pause scars distinct, irregularly spaced, (1984: 32). situated at 0.8, 1.4, 2.2, 2.7, 3.4, 4.1, 5.0, 6.0, 6.9 Bacula kajiyamai shows an even stronger and 8.0 whorls. Body whorl occupies 30% of shell resemblance to B. morisyuichiroi (Habe, 1968), the height; periphery forms strong rib-like keel with only other known species of the genus. The latter four ne spiral cords on undersurface; base slightly species was originally described from Amami- convex with six spiral ribs. Aperture small, oblong- Oshima Island, southwestern Japan and later ovate; interrupted by posterior notch; outer reported from elsewhere in the western Paci c (e.g., lip curved in lateral view with its most protruding Savazzi & Sasaki, 2004: g. 1E as B. striolata; part at position of peripheral keel; columellar callus Sasaki, 2008: g. 10H; Tröndlé & Boutet, 2009; very thick. Umbilicus closed. Protoconch with ca. Hori & Matsuda, 2017: pl. 106, g. 11). Although 3 slightly convex whorls, pupiform, smooth, glassy, B. morisyuichiroi at maturity develops the peripheral translucent with brown tinge, slightly tilted from keel into a much stronger, wing-like structure and coiling axis of teleoconch; exposed part 420 µm high the depression of the columellar base into a deep and 280 µm wide; apertural outer lip or demarcation umbilicus (Habe, 1968: text- g. 1), the two species line with teleoconch distinct, opisthocline (Fig. 1B). look very similar in the comparison of the rst Remarks: The present species has a smooth, seven or eight teleoconch whorls. The smooth, pupiform protoconch with a brown tinge (see pupiform protoconch with a brown tinge also exists Fig. 1B; the same is seen in the photograph in B. morisyuichiroi (TT, personal observation). of SMNH-50835 from New Caledonia). Very An alternative position of B. morisyuichiroi in similar protoconchs have been reported for such the heterobranch family Pyramidellidae has been 122 VENUS 78 (3–4), 2020 suggested based on the examination of the holotype be homologous with the also knobby uppermost (Warén, 1984: 32), but the holotype (NSMT-Mo spiral of Pyramidelloides miranda, the type of the 49863) bears the incremental lines on the teleoconch genus (Warén, 1983: gs 57–59). These lines of whorls that con rm the eulimid af nity of the circumstantial evidence suggest an ectoparasitic species (Habe, 1968: 58; see also Higo et al., 2001: mode of life on brittle stars for all species of Bacula. 59, g. G2083). As a side note, the genus Teretianax Iredale, A marked difference between the present species 1918 includes eulimid species with two strong and the other two congeners is a straight (B. spiral keels on the teleoconch and thus approaches kajiyamai) or a right-curved (B. striolata and B. Pyramidelloides and Bacula in appearance (see morisyuichiroi) of the teleoconch. The shells Warén, 1984: g. 205; Ponder, 1985: g. 150C, D; of the latter two species have incremental scars that Faber, 1990: gs 10–12). Some consider Teretianax are perfectly periodical and synchronized between a subgenus or a junior synonym of Pyramidelloides whorls, ca. 1.1 whorls from each other, aligned in apparently with this resemblance in mind (Ponder, a single oblique line on the spire (Warén, 1984: g. 1985; Faber, 1990; MolluscaBase, 2020b). However, 204; Savazzi & Sasaki, 2004: g. 1E; Sasaki, 2008: the type [T. suteri (W. R. B. Oliver, 1915)] and other g. 10H). These incremental scars are associated species of Teretianax bear a colorless protoconch with a growth hiatus, subsequent thickening of the with only two whorls (e.g., Warén, 1983: gs 78, aperture and slight changes to the axis of coiling, 79; Ponder, 1985; g. 150E; Hori & Matsuda, hence the right-curved spire (see Savazzi & Sasaki, 2017: pl. 107, g. 2), potentially suggesting a 2004: 89; Webster & Vermeij, 2017: 739). On the distant relationship to Pyramidelloides or Bacula. other hand, incremental scars appear irregularly Teretianax and Pyramidelloides seem to differ also in B. kajiyamai, with intervals of 0.5–1.1 whorls, in the presence or absence of the radula. A probable resulting in the straight spire of the species. Some lack of a radula and a snout has been noted for T. authors had considered the presence or absence pagoda Powell, 1926 (Warén, 1983; Ponder, 1985), of the curvature an important enough criterion for a species conchologically similar to the type T. the generic separation of Eulimidae (see Souza & suteri (see Ponder, 1967: pl. 11, g. 1). On the other Pimenta, 2019 for review). However, the spacing hand, a ptenoglossate radula is present in all species of the incremental lines and shape of the spire may of Pyramidelloides, Eulima and Hemiliostraca vary among closely related species (e.g., Hori & examined so far (Warén, 1983, 1984; no information Matsuda, 2017: pls. 98, 99 for spp.) and available for Bacula). Given that the radula might even among intraspeci c specimens (Warén, 1984: have been lost only once in the evolutionary history 18), potentially reecting their adaptive responses of the Eulimidae (Takano & Kano, 2014), it seems to varying selective pressures in a short evolutionary safe to regard Teretianax as a valid, independent timescale (see Savazzi & Sasaki, 2004; Webster & genus with an unknown host preference. Vermeij, 2017). There is no information available to date on the Acknowledgements: Our special thanks go to parasitic ecology or host for the genus Dr. A. Warén (SMNH) for sharing his beautiful Bacula. Previous studies have shown, however, that photographs of New Caledonian eulimids and for his eulimid species in a single genus and closely related continuous support and encouragement. Invaluable genera exploit hosts of the same echinoderm class comments were also provided by an anonymous (Warén 1984; Takano & Kano, 2014; Takano et al., reviewer, to whom we are most grateful. 2018). It is noteworthy that the species of Bacula share the same protoconch characters (pupiform, References smooth and brownish) with such ophiuroid- parasite groups as Eulima, Hemiliostraca and Adams, H. & Adams, A. 1863. Descriptions of ve Pyramidelloides (see above). The shells of Bacula new genera of . The Annals and particularly resemble those of Pyramidelloides in Magazine of Natural History; Zoology, Botany, and Geology 3 (11): 18–20. sharing a strongly sculptured teleoconch, which Bouchet, P. & Le Renard, J. 1998. Family is rather rare in the entire Eulimidae (Warén, Pickworthiidae. In: Beesley, P. L., Ross, G. J. 1984; Savazzi & Sasaki, 2004). The uppermost B. & Wells, A. (eds), Fauna of Australia, spiral rib of B. kajiyamai is knobby in the early Mollusca: The Southern Synthesis, vol. 5, pp. teleoconch whorls (Fig. 1A) and this might even 739–741. CSIRO Publishing, Melbourne. Short Notes 123

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Biodiversity 49: 425–442. クリンツボの所属変更（ハナゴウナ Takano, T. & Kano, Y. 2014. Molecular phylogenetic investigations of the relationships of the 科：オドリオネジニナ属） echinoderm-parasite family Eulimidae within (Mollusca). Molecular 髙野剛史・都築章二・狩野泰則 Phylogenetics and Evolution 79: 258–269. Takano, T., Itoh, H. & Kano, Y. 2018. DNA-based identi cation of an echinoderm host for a deep- 要 約 sea parasitic snail (Gastropoda: Eulimidae). Molluscan Research 38: 212–217. Tröndlé, J. & Boutet, M. 2009. Inventory of marine クリンツボは，鹿児島県加計呂麻島の打上げ死 molluscs of French Polynesia. Atoll Research 殻をタイプ標本とする微小な巻貝で，後成殻の螺 Bulletin 570: 1–87. 肋および周縁角の特徴から Chrystella 属の新種 C. Warén, A. 1980. Descriptions of new taxa of Eulimidae (Mollusca, Prosobranchia), with kajiyamai Habe, 1961（リソツボ科）として記載さ notes on some previously described genera. れた。同属は現在ソビエツブ科（オニノツノガイ Zoologica Scripta 9: 283–306. 上科）に含まれ，世界で 8 種が知られるが，いず Warén, A. 1983. An anatomical description of れも生貝の報告がなく内部形態の情報を欠く。ク Alder with remarks on and a revision of Pyramidelloides Nevill (Mollusca, リンツボも破損した死殻として報じられるのみで Prosobranchia, Eulimidae). Zoologica Scripta あった。 12: 273–294. 今回，沖縄県座間味島の潮下帯から本種の新鮮 Warén, A. 1984. A generic revision of the family Eulimidae (Gastropoda, Prosobranchia). な死殻を採集し，その原殻が細長い蛹型，約 3 階， Journal of Molluscan Studies, Supplement (13): 殻表平滑で薄い褐色を帯びていることを初めて明 1–96. らかにした。これらの特徴は Chrystella の諸種を含 Webster, N. B. & Vermeij, G. J. 2017. The varix: むソビエツブ科貝類のものと明らかに異なり， evolution, distribution, and phylogenetic clumping of a repeated gastropod innovation. Bacula オドリオネジニナ属，Pyramidelloides レイ Zoological Journal of the Linnean Society 180: シツボ属，Hemiliostraca クテンハナゴウナ属， 732–754. Eulima ハナゴウナ属の諸種を含む一部のハナゴウ ナ科貝類に近似する。本種の後成殻にみられる外 (Accepted March 19, 2020) 唇縁痕もハナゴウナ科に広く共有される特徴であ り，螺肋および周縁角の形状とあわせて，本種を オドリオネジニナ属に所属変更した。なお，「オド リオネジニナ属」は元来 Subeulima Soubervie, 1875 に対する和名であるが，Bacula H. Adams & A. Adams, 1863 がその古参シノニムとされている。 オドリオネジニナ属は，タイプ種 B. striolata （= Subeulima lamberti）オドリオネジニナ，B. morisyuichiroi クリンオドリオネジニナ，Bacula kajiyamai クリンツボの 3 種からなる。前 2 種では 外唇縁痕が約 1.1 巻き毎に刻まれ，螺塔は強く右に 曲がるが，クリンツボの外唇縁痕は不規則に生じ 螺塔はまっすぐである（なお，これらの特徴はハ ナゴウナ科の属内で比較的変化しやすい）。いずれ の種についても寄生生態に関する知見はないが， 原殻・後成殻の類似から，上記レイシツボ属，ク テンハナゴウナ属，ハナゴウナ属の諸種と同様， クモヒトデ類を宿主とする外部寄生者である可能 性が高い。