DOI: http://doi.org/10.18941/venus.77.1-4_45 Short Notes ©The Malacological Society of Japan45

Short Notes

A New Species of Mucronalia (: ) Parasitizing the Ophiocomid Ophiomastix mixta in Japan

Tsuyoshi Takano1,2*, Hayate Tanaka3,4 and Yasunori Kano2 1Meguro Parasitological Museum, 4-1-1 Shimomeguro, Meguro, Tokyo 153-0064, Japan; *[email protected] 2Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japan 3Graduate School of Science, The University of Tokyo, 7-3-1, Hongo, Bunkyo, Tokyo 113-0033, Japan 4National Museum of Nature and Science, 4-1-1 Amakubo, Tsukuba, Ibaraki 305-0005, Japan

Gastropods of the family Eulimidae Over 30 species have been described in this , (: ) are parasites of largely based on the presence of a mucronate apex or including all five classes of the a calloused inner (e.g., Pease, 1860; Habe, 1974). phylum, namely Asteroidea, Crinoidea, Echinoidea, However, Warén (1980a) has transferred more Holothuroidea and Ophiuroidea (Warén, 1984). than half of them to other eulimid genera such as The Eulimidae contain numerous extant and extinct Echineulima Lützen & Nielsen, 1975, Hypermastus species (Bouchet et al., 2002; Lozouet, 2014), but Pilsbry, 1899 and Melanella Bowdich, 1822 or to many remain to be described (Warén, 1984). This the cerithioid family Pelycidiidae (see Ponder & has led to a number of recent publications on eulimid Hall, 1983: fig. 1C; Takano & Kano, 2014). Some systematics that aim at a better understanding of ten described species remain in Mucronalia, all their ecological, morphological and species diversity of which bear the mucronate apex, parietal callus (e.g., Matsuda et al., 2010, 2013; Dgebuadze et and curved outer lip of the shell (Warén, 1980a). al., 2012; Souza & Pimenta, 2014; Nekhaev, 2016; The spiral bands may be present or absent, with Takano et al., 2017). Mucronalia lepida Melvill, 1906 and Mucronalia Mucronalia A. Adams, 1860 is a poorly oxytenes Melvill, 1904 as examples of colorless known genus of the Eulimidae inhabiting shallow species. Shell color and color pattern are consistent subtidal to bathyal waters in temperate to tropical within each eulimid species, whereas variation exists regions worldwide. The type species of the genus, among congeneric species (Warén, 1984). The genus Mucronalia bicincta A. Adams, 1860, has been Risso, 1826, for example, includes species collected only as empty shells from 40–150 m with and without spiral bands (Bouchet & Warén, depths along the coasts of Honshu and Kyushu 1986). Islands, Japan (A. Adams, 1860; Hori & Matsuda, Among the species of Mucronalia sensu Warén 2017), and thus no ecological, anatomical or genetic (1980a), host information is available for only two information is available for the species (Warén, species (Warén, 1980a; Hori & Matsuda, 2017). 1980a). The shell of M. bicincta is characterized by Both are ectoparasites of brittle stars: Mucronalia (1) a cylindrical outline, (2) a height of up to 9 mm, exilis A. Adams, 1862 on Amphioplus laevis (Lyman, (3) a “mucronate” apex with a projecting protoconch 1874) in the Amphiuridae and Ophioplocus sp. in and a nearly planispiral first whorl of the teleoconch, the Hemieuryalidae; Mucronalia trilineata Warén, (4) brownish spiral bands on the teleoconch whorls, 1980 on Ophiarachnella septemspinosa (Müller (5) an aperture with a parietal callus, and (6) a & Troschel, 1842) in the Ophiodermatidae. Warén strongly curved outer lip with its most protruding (1980a, 1984) has hence speculated that all their part at 2/3 of aperture height from the suture (Warén, congeners depend on Ophiuroidea, conforming 1980a, 1984; Hori & Matsuda, 2017: pl. 103, fig. 5). to the general rule that eulimids in a single genus http://zoobank.org/urn:lsid:zoobank.org:pub:121AB97A-BDCE-498F-B010-EB3844323078 46 VENUS 77 (1–4), 2019 or a terminal clade parasitize hosts of the same Systematics class. We herein describe a new species of Mucronalia Family Eulimidae Philippi, 1853 from the ophiocomid brittle star Ophiomastix Genus Mucronalia A. Adams, 1860 mixta Lütken, 1869, collected shallow subtidally Type species: Mucronalia bicincta A. Adams, in Manazuru, Kanagawa, Japan. Type specimens 1860, by monotypy. and their hosts have been deposited in the National Museum of Nature and Science, Tokyo (NSMT) and Mucronalia alba n. sp. Meguro Parasitological Museum (MPM). (Figs 1–7)

Figs 1–5. Mucronalia alba n. sp. and its host Ophiomastix mixta. 1. Oral view of O. mixta (Om1), showing attachment site of holotype (arrowhead) and egg masses (em). Live-taken photograph in bottom left box. 2. Paratype 2 on arm of another host (Om2) with egg masses. Arrowhead denotes attachment site of Paratype 1. 3. Shell of holotype, apertural and lateral views. Arrowheads indicate growth pause scars. 4. Close-up view of protoconch and first teleoconch whorl of holotype (arrowhead for boundary). 5. Shell of Paratype 1, apertural view. Short Notes 47

Type locality: Kotogahama, Manazuru, Kanagawa, columellar lip straight, thick, tilted at 20° from Honshu Island, Japan (35°08′54″N, 139°08′57″E). coiling axis of in holotype; parietal Type material: Holotype NSMT-Mo 79008 and callus thin but present, colorless; basal lip round two paratypes MPM Coll. No. 21461, all collected and inflated (Fig. 3). Umbilicus absent. Protoconch from the type locality on 1 August 2015, found of slightly more than 2 whorls, pupiform, glassy, attached to the ventral side of the arms of translucent with brownish tinge, tilted at 10° from Ophiomastix mixta living under stones at depths of teleoconch axis; exposed part 210 μm wide and 250 1–2 m (Figs 1, 2). The two paratypes were found on μm high (Figs 4, 6). thin, yellowish. the same arm of another host (Table 1). Eyes black; reddish-purple contents of esophagus Etymology: The name refers to the translucent visible through shell (Fig. 3, apertural view). white shell without color bands. Holotype and Paratype 2 accompanied by several Diagnosis: Shell slender for genus, conical, egg masses of < 1 mm diameter (Figs 1, 2). Each translucent white with no spiral bands. Teleoconch mass contained eggs or trochophores or veligers at whorls asymmetrically convex, irregularly increasing same stage of development. in diameter. Growth pause scars distinct, irregularly Distribution: In addition to the type locality, this spaced, slightly brownish. Aperture oblong-ovate; species has been collected from Misaki, Kanagawa columellar lip straight, tilted at 20° from coiling axis (35°10′N, 139°37′E) and Tateyama, Chiba (35°00′N, of body whorl. 139°50′E), all on the Pacific coast of central Honshu. Description: Shell conical with mucronate apex, The specimens from the latter two localities were up to 5.5 mm high, thin but not fragile, translucent identified by the authors from photographs provided white. Teleoconch of up to 6.6 asymmetrically by M. Okanishi and S. Tsuzuki (pers. comm.). convex whorls, irregularly increasing in diameter; Remarks: The generic position of the present growth pause scars distinct, somewhat brownish, new species is readily determined by its mucronate situated at 3.6, 5.6 and 6.3 whorls in holotype (Fig. apex, the parietal callus and the curved outer lip of 3), each accompanied by slight change of coiling the aperture. Furthermore, the ectoparasitic mode axis (Fig. 7); growth lines numerous and faint. of life on ophiuroids (Figs 1, 2) conforms to the Aperture oblong-ovate; outer lip simple, curved, concept of Mucronalia as interpreted by Warén with most protruding part at half of aperture height; (1980a, 1984). Ophioarachnicola biformis Warén, 1980, the monotypic species of the genus, also parasitizes ophiuroids and shows some resemblance to certain Mucronalia in shell form (Warén, 1980b: 287, figs 24, 25), but its straight apical slopes suggest a distant relationship. Mucronalia alba n. sp. differs from all congeners, including the type species M. bicincta, in having a colorless, conical shell with asymmetrically convex whorls. Its shell profile resembles those of M. exilis (another species of the genus from temperate waters Figs 6, 7. Line drawings of M. alba n. sp. 6. Apex of in Japan) and M. trilineata (Queensland, Australia), holotype from same angle with Fig. 4, showing boundary between protoconch and teleoconch but the latter two species are characterized by the (arrowhead). 7. Growth pause scar at 3.3 whorls of presence of brownish spiral bands on the teleoconch teleoconch in Paratype 1 (arrowhead). whorls. The shape of the aperture is also different,

Table 1. Shell measurements of three specimens of Mucronalia alba n. sp.

Shell Shell Number of Specimen Voucher Host Preservation height width teleoconch whorls Holotype NSMT-Mo 79008 Om1 5.5 mm 2.0 mm 6.6 Dry Paratype 1 MPM Coll. No. 21461 Om2 3.1 mm 1.4 mm 4.5 Pure ethanol Paratype 2 MPM Coll. No. 21461 Om2 c. 4 mm* 1.7 mm > 5* Pure ethanol

*Specimen preserved in situ on host and exact measurements unavailable (see Fig. 2). 48 VENUS 77 (1–4), 2019 with the columellar lip tilted 20° in M. alba or almost (1944), a preliminary molecular phylogeny of perpendicular in M. exilis and M. trilineata (Warén, the family shows its position within the hyper- 1980a; Hori & Matsuda, 2017). The three species diverse, holothuroid-parasitic genus Melanella (T. further differ in their habitat and host characteristics. Takano, unpublished data). Its shell morphology also The new species attaches by the proboscis to the arm warrants the reallocation of “Mucronalia lactea” to of Ophiomastix mixta on a subtidal rocky bottom. the latter genus (see e.g., Hori & Matsuda, 2017: Mucronalia exilis parasitizes Amphioplus laevis and pl. 99 for similar shells). The species name lactea, Ophioplocus sp. on soft bottoms at depths of 10 to however, seems to be preoccupied in Melanella 50 m (Hori & Matsuda, 2017). Mucronalia trilineata by another species by the same author. Melanella is known to attach to Ophiarachnella septemspinosa lactea (A. Adams in Sowerby II, 1854) was in tropical coral reefs (Warén, 1980a). originally described under Eulima, whereas its Three described species of Mucronalia bear colorless, conical shell with impressed sutures and colorless shells without spiral bands. These include strong growth pause scars with intervals of ca. M. lepida and M. oxytenes, both described from 340° (A. Adams, 1854: 799, pl. 169, fig. 2) closely a depth of 285 m in the Gulf of Oman, Indian resembles the shells of some other Melanella [e.g., Ocean, and M. involuta Carpenter, 1865 from M. martinii (A. Adams in Sowerby II, 1854); see Mazatlan, Mexico, East Pacific. The former two Warén, 1984: fig. 22] as suggested in Higo et al. can be discriminated from M. alba n. sp. in having (1999). We therefore propose a new replacement broader shells with less rounded whorls (Melvill, name, Melanella tanabensis, for Mucronalia lactea 1904: pl. 10, fig. 13; Melvill, 1906: pl. 7, fig. 8). A. Adams, 1864 (p. 91) after its type locality The last species is much smaller; its holotype, with (Tanabe Bay, Wakayama, Japan; see Warén, 1980a: more than five teleoconch whorls, measures 2.7 mm 203). The same would be the case with Melanella in height (Carpenter, 1865; see also Keen, 1968: variabilis (Schepman & Nierstrasz, 1914) n. comb., 407, text-fig. 36). Finally, two other congeners, M. originally described as Mucronalia from Zanzibar bizonula Melvill, 1906 from the Gulf of Oman and Archipelago, East Africa. It is similar to Melanella M. exquisita Sowerby III, 1915 from Sri Lanka, tanabensis in shell morphology and parasitizes are readily distinguishable from the new species in the same host, Patinapta ooplax (Schepman & having cylindrical shells with brownish spiral bands Nierstrasz, 1914: pl. 28, figs 22–41; Warén, 1980a: (Sowerby III, 1915: 214, text-fig; Melvill, 1906: 203). Combined morphological and ecological pl. 8, fig. 31). None of the five species have been comparisons for other species will help disentangle collected on a host (Carpenter, 1865; Melvill, 1904, the evolutionary histories and classification of 1906; Sowerby III, 1915; Warén, 1980a). Mucronalia, Melanella, Hypermastus and numerous Hori & Matsuda (2017: pl. 103) showed two other genera of the family Eulimidae. more species without spiral bands as congeneric taxa: “Mucronalia” subula A. Adams, 1864 and Acknowledgements: We are grateful to Dr. “Mucronalia lactea” A. Adams, 1864. However, Masanori Okanishi (Misaki Marine Biological their shell morphology or parasitic ecology does Station, The University of Tokyo) and Mr. Shoji not fit the concept of Mucronalia as interpreted Tsuzuki (Chiba Prefecture) for providing photographs by Warén (1980a, 1984). The shell of “M.” subula of the new species. Invaluable comments were has straight apical slopes and a straight outer lip made by Dr. Anders Warén (Swedish Museum of of the aperture, which rather support a position in Natural History) and an anonymous reviewer for the the echinoid-parasitic genus Hypermastus (Warén, improvement of the manuscript. 1980a; Warén & Crossland, 1991). The conchological features of “Mucronalia References lactea” do not outright reject the current generic position. However, this species lives in the coelom Adams, A. 1849–1855. Monographs of the genera of the synaptid sea cucumber Patinapta ooplax (von Eulima, Niso, Leiostraca, Obeliscus, Marenzeller, 1881) on tidal flats in the western part Pyramidella and Monoptygma. In: Sowerby, G. B. II (ed.), Thesaurus Conchyliorum, or of mainland Japan (Habe, 1944; Hori & Matsuda, Monographs of Genera of Shells, vol. 2, pp. 2017). Although Warén (1980a) had placed it in 439–899, pls 92–186. Hypermastus, probably without having seen the Adams, A. 1860. On some new genera and species host information provided in Japanese by Habe of from Japan. The Annals and Short Notes 49

Magazine of Natural History, Zoology, Botany, new species of Hemiliostraca (Caenogastropoda: and Geology, ser. 3 5: 299–303. Eulimidae) from Japan and Taiwan. Venus 71: Adams, A. 1864. On the Japanese species of 163–174. Leiostraca. Journal of the Proceedings of the Melvill, J. C. 1904. Descriptions of twenty-eight Linnean Society 7: 84–91. species of Gastropoda from the Persian Gulf Bouchet, P. & Warén, A. 1986. Revision of the and Gulf of Oman, and Arabian Sea, dredged northeast Atlantic bathyal and abyssal by Mr. F. W. Townsend, of the Indo-European Aclididae, Eulimidae, Epitoniidae (Mollusca, Telegraph Service, 1900–1904. Proceedings of Gastropoda). Bollettino Malacologico, the Malacological Society of London 6: 158– Supplemento 2: 299–576. 169. Bouchet, P., Lozouet, P., Maestrati, P. & Heros, V. Melvill, J. C. 1906. Descriptions of twenty-one 2002. Assessing the magnitude of species Gastropoda and one scaphopod from the richness in tropical marine environments: Persian Gulf and Gulf of Oman, dredged by exceptionally high numbers of molluscs at a Mr. F. W. Townsend, 1902–1904. Proceedings New Caledonia site. Biological Journal of the of the Malacological Society of London 7: Linnean Society 75: 421–436. 69–80. Carpenter, P. P. 1865. Diagnoses of new species and Nekhaev, I. O. 2016. A new species of endoparasitic new genus of mollusks, from the Reigen mollusc from the Arctic (Gastropoda: Mazatlan Collection; with an account of Eulimidae). Journal of Conchology 42: 73–78. additional specimens presented to the British Pease, W. H. 1860. Descriptions of forty-seven new Museum. Proceedings of the Zoological Society species of shells from the Sandwich Islands, in of London 1865: 268–273. the collection of Hugh Cuming. Proceedings of Dgebuadze, P. Y., Fedosov, A. E. & Kantor, Y. I. the Zoological Society of London 28: 431–438. 2012. Host specificity of parasitic gastropods of Ponder, W. F. & Hall, S. J. 1983. Pelycidiidae, a new the genus Annulobalcis Habe, 1965 (Mollusca, family of archaeogastropod molluscs. The Gastropoda, Eulimidae) from crinoids in Nautilus 97: 30–35. Vietnam, with descriptions of four new species. Schepman, M. M. & Nierstrasz, H. F. 1914. Zoosystema 34: 139–155. Parasitische und kommensalistische Mollusken Habe, T. 1944. The Japanese species of the genus aus Holothurien. Reise in Ostafrika in den Mucronalia. Venus (Japanese Journal of Jahren 1903–1905 mit mittein der Hermann Malacology) 13: 311–313. (in Japanese) und Elise geb. Heckmann Wentzel-Stiftung Habe, T. 1974. Five new gastropodous species ausgeführt von Professor Dr. Alfred Voeltzkow, parasitic to the Japanese echinoderms. Venus Wissenschaftliche Ergebnisse 4: 383–416. (Japanese Journal of Malacology) 32: 117– Souza, L. S. & Pimenta, A. D. 2014. Fusceulima and 123. Halielloides (Gastropoda: Eulimidae) in the Higo, S., Callomon, P. & Goto, Y. 1999. Catalogue southwestern Atlantic, with descriptions of two and Bibliography of the Marine Shell-Bearing new species of Fusceulima. Zoologia 31: 621– Mollusca of Japan. 749 pp. Elle Scientific 633. Publications, Osaka. Sowerby, G. B. III. 1915. Descriptions of five new Hori, S. & Matsuda, H. 2017. Eulimidae. In: species of Mollusca of the genera Drillia, Okutani, T. (ed.), Marine Mollusks in Japan, Marginella, Apicalia, Plesiotrochus, and the Second Edition, pp. 142–151, 823–832. Ringicula, all from Ceylon; also notes on the Tokai University Press, Hiratsuka. genus Plesiotrochus. Proceedings of the Keen, A. M. 1968. West American mollusk types at Malacological Society of London 11: 213–216. the British Museum (Natural History) IV. Takano, T. & Kano, Y. 2014. Molecular phylogenetic Carpenter’s Mazatlan Collection. The Veliger investigations of the relationships of the 10: 389–439. echinoderm-parasite family Eulimidae within Lozouet, P. 2014. Temporal and latitudinal trends in (Mollusca). Molecular the biodiversity of European Atlantic Cenozoic Phylogenetics and Evolution 79: 258–269. gastropod (Mollusca) faunas. A base for the Takano, T., Warén, A. & Kano, Y. 2017. Megadenus history of biogeographic provinces. Carnets de atrae n. sp., an endoparasitic eulimid gastropod Géologie 14: 273–314. (Mollusca) from the black sea cucumber Matsuda, H., Uyeno, D. & Nagasawa, K. 2010. A Holothuria atra Jaeger (Aspidochirotida: new species of Hypermastus (Prosobranchia: Holothuriidae) in the Indo-West Pacific. Eulimidae) associated with Echinodiscus Systematic Parasitology 94: 699–709. tenuissimus (Echinoidea: Astriclypeidae) from Warén, A. 1980a. Revision of the genera Thyca, off Okinawa, Japan. Venus 69: 17–23. Stilifer, Scalenostoma, Mucronalia and Matsuda, H., Uyeno, D. & Nagasawa, K. 2013. Two Echineulima (Mollusca, Prosobranchia, 50 VENUS 77 (1–4), 2019

Eulimidae). Zoologica Scripta 9: 187–210. 原殻がつまみ状に突出すること，殻口内唇に滑 Warén, A. 1980b. Descriptions of new taxa of 層を有すること，また外唇は中央部が突出し横か Eulimidae (Mollusca, Prosobranchia), with Mucronalia notes on some previously described genera. らみると大きく曲がることから， 属の Zoologica Scripta 9: 283–306. 一種であると判断された。殻は本属としては細く Warén, A. 1984. A generic revision of the family 塔型，最大 5.5 mm，白色半透明である。後成殻は Eulimidae (Gastropoda, Prosobranchia). 6.6 巻，螺層は時に非対称に膨れ，螺塔は成長に伴 Journal of Molluscan Studies, Supplement 13: 1–96. い不規則に太くなる。外唇縁痕は不定期に現れ， Warén, A. & Crossland, M. R. 1991. Revision of 僅かに褐色を呈する。殻口は細長い卵型。軸唇は Hypermastus Pilsbry, 1899 and Turveria Berry, まっすぐで，体層の軸から 20° 傾く。原殻は淡い 1956 (Gastropoda: Prosobranchia: Eulimidae), 褐色。 two genera parasitic on sand dollars. Records of the Australian Museum 43: 85–112. 本種の殻形は，同じく日本に産するヤセフタオ ビツマミガイ M. exilis と，オーストラリアのクイー (Accepted September 20, 2018) ンズランドから記載された M. trilineata に似る。一 方これら 2 種は殻に褐色の色帯を有し，また軸唇 の傾きが弱い。オマーンをタイプ産地とする M. lepida と M. oxytenes，メキシコ西岸の M. involuta 神奈川県真鶴町より採取された はいずれも本種と同様白色の殻をもつが，前 2 種 M. アカクモヒトデに寄生する は殻が太く螺層の膨らみが弱い点で，また involuta は本種と比してはるかに小型である点で区 ハナゴウナ科の 1 新種 別される。タイプ種であるフタオビツマミガイ M. bicincta，オマーンに産する M. bizonula，スリラン 髙野剛史・田中 颯・狩野泰則 カの M. exquisita は，色帯のある円筒形の殻をもつ 点で本種と明瞭に異なる。 要 約 上述の種のほか，コガタツマミガイ“M.” subula やヒモイカリナマコツマミガイ“M. lactea”が ハナゴウナ科 Eulimidae の腹足類は，棘皮動物を Mucronalia 属として扱われることがある。しかし 宿主とする寄生者である。同科の Mucronalia 属は ながら，前者は殻口外唇が湾曲せず，カシパンヤ 形態および生態情報に乏しいグループで，タイプ ドリニナ属 Hypermastus に含めるのが妥当である。 種のフタオビツマミガイ M. bicincta は生貝での採 後者は，殻形態，寄生生態および予察的な分子系 集報告がなされていない。Warén（1980a）による 統解析（髙野，未発表）により，セトモノガイ属 殻形態に基づく属の概念では，つまみ状の原殻， Melanella の一種であると考えられた。しかしなが 内唇滑層，ならびに中央部の突出した外唇を有す ら，Eulima lactea A. Adams in Sowerby II, 1854 が同 ることが重要視されている。また 2 既知種がクモ じ Melanella に所属すると考えられるため，ヒモイ ヒトデ寄生性であることが知られており，これが カリナマコツマミガイに対する lactea A. Adams, 本属貝類に共通の生態とみなされている。本報で 1864 は主観新参ホモニムとなる。そこで，ヒモイ は，神奈川県真鶴町の潮下帯より採取されたアカ カリナマコツマミガイに対する代替名として クモヒトデ Ophiomastix mixta の腕に外部寄生する Melanella tanabensis を提唱した。東アフリカのザ Mucronalia 属の 1 新種を記載した。 ンジバル諸島産で，同じくヒモイカリナマコに内 部寄生する“Mucronalia” variabilis もセトモノガイ Mucronalia alba n. sp. オビナシツマミガイ（新種・ 属に含めるのが妥当と考えられ，本論文で属位を 新称） 変更した（Melanella variabilis n. comb.）。