VENUS 76 (1–4): 1–18, 2018 DOI: http://doi.org/10.18941/venus.76.1-4_1Taxonomy of Volutharpa in Japan ©The Malacological Society of Japan1

Contribution to the Knowledge of the of the Japanese of Volutharpa (: )

Tomoyasu Yamazaki1*, Takeshi Sonoda2, Takahiro Nobetsu3 and Seiji Goshima4 1Shellfish Museum of Rankoshi, 1401 Minato-Machi, Rankoshi, Hokkaido 048-1341, Japan 2Tokyo University of Agriculture, 196 Yasaka, Abashiri 099-2493, Japan 3Shiretoko Nature Foundation, 531 Iwaubetsu, Shari 099-4536, Japan 4Graduate School of Fisheries Sciences, Hokkaido University, 3-1-1 Minato-Machi, Hakodate 041-8611, Japan

Abstract: The Recent species of the genus Volutharpa in Japanese and adjacent waters are reviewed based on the morphology of the shell, , penis and , as well as their geographical distribution. The genus is provisionally distinguished from the allied genus based on the differences in the general morphology of the shell. Five operational taxa are recognized, and compared with each other. The morphology of the penis, especially the gonopore, and of the were found to be most valuable in distinguishing species and subspecies within the genus. Radula characters, including the number of cusps, were shown to be variable even within species, and not suitable for species-level classification. Three discontinuous morphotypes were recognized in the shape of the gonopore, and these were considered to represent three species groups: 1) papillary type: ampullacea; 2) triangular type: nipponkaiensis species group comprising nipponkaiensis and limnaeformis; and 3) pointed type: perryi species group comprising perryi and ainos. Furthermore, two taxa in each species group were morphologically distinguished by the condition of the periostracum, and distinguished as subspecies. The subspecific distinction of limnaeformis and ainos are also supported by their allopatric distribution with corresponding nominotypical subspecies. As a result, the genus Volutharpa in Japanese waters is revised to comprise three species and two subspecies.

Keywords: Volutharpa, Buccinidae, taxonomy, morphology, classification

Introduction

Volutharpa is a small genus in the family Buccinidae, and endemic to the North Pacific , from the Yellow Sea and temperate Japanese waters through the Aleutians to Alaska (Yoo, 1976; Golikov, 1980; Min, 2004; Zhongyan, 2004). It has been regarded either as a distinct genus (e.g., Adams, 1860; Dall, 1871; Troschel, 1876; Kobelt, 1883; Tryon, 1886; Yoo, 1976; Tsuchida, 1991; Kwon et al., 1993; Zhongyan, 2004), or as a subgenus of Buccinum (e.g., Adams & Adams, 1858; Thiele, 1931; Golikov, 1980) due to similarities in the external morphology of the soft parts, although most recent authors adopt the former view based on the significant differences in shell morphology (Okutani, 2000; Min, 2004; Kantor & Sysoev, 2006; Bouchet & Fraussen, 2015). There has also been considerable disagreement with respect to species delimitation in Volutharpa. Mörch (1858), who reviewed the genus for the first time, recognized three taxa (V. ampullacea, deshayesiana, and perryi). Nine additional nominal taxa have since been included in the genus, but most of them are regarded by recent authors as synonyms or subspecies of V. ampullacea. Japanese authors (e.g., Habe & Ito, 1980; Higo et al., 1999; Okutani, 2000) have generally recognized two

* Corresponding author: [email protected] 2 T. Yamazaki, et al. valid species, V. ampullacea and V. ainos, with three subspecies in the former, i.e., V. ampullacea perryi, V. a. nipponkaiensis, and V. a. limnaeformis. The separation of these two distinct species was based on the morphology of the periostracum and radula (Habe & Ito, 1980; Okutani et al., 1988). On the other hand, Russian authors recognized only one valid species, V. ampullacea, and regarded all the other taxa as synonyms (Golikov, 1963, 1980; Kantor & Sysoev, 2005, 2006). This discrepancy in the recognition of species may be due to the lack of integrated information on the morphology of both soft and hard parts, including the operculum, penis, and radula, which are considered to be important in the classification of the Buccinidae (Golikov, 1980; Alexeyev & Gornichnykh, 2009; Kosyan & Kantor, 2013). In order to contribute to a comprehensive review of the genus, we examined and compared the morphology of shell, operculum, penis, and radula in detail based on specimens collected from Hokkaido and adjacent waters.

Materials and Methods

Five operational taxa (V. ampullacea, V. nipponkaiensis, V. limnaeformis, V. perryi, and V. ainos) were tentatively recognized based on the identification key shown by Habe (1980), and their morphological characters were examined in detail and compared with each other. Examination of the soft and hard parts was mainly carried out on live-collected specimens from southern Sakhalin, Hokkaido, Honshu, and adjacent waters (Fig. 1), taken between 1982 and 2012.

120° 125° 130° 135° 140° 145° 150° 50°

Tikhaya Sea of Okhotsk Kaneda Bunkichi ° Bay 45 Musashi Utoro Bank Otaru Rausu Akkeshi Kamiiso Usujiri Kushiro Matumae Kojima Mutsu Bay 40° Japan Sea Iwate pref. Jumun-jin, Gangnenung Otsuchi Bay Samcheok Ishikawa pref. Gyeongbuk Tean-Gun Japan 35° Yellow Sea Sagami Bay Goheung-gun Ise Bay Gyeongnam Wakasa Bay Tajima 30° Pacific Ocean

25° Fig. 1. Map showing sampling sites and adjacent locations. Taxonomy of Volutharpa in Japan 3

They were generally fixed and preserved in 99.9% ethanol. The operculum was observed in situ on the epipodium under a stereomicroscope. The size of the shell was measured with a digital caliper (Mitutoyo: CD-15AXW, nearest to ±0.02). The penis was cut off from the head-foot and observed in detail under a stereomicroscope. The radula was extracted from the proboscis, cleaned in 1N NaOH solution, and observed with a scanning electron microscope (Hitachi: S-2300). Additional dry specimens were also examined. Statistical analyses were performed using IBM SPSS Statistics 15.0 (SPSS Inc., IL, USA). Voucher specimens were individually registered and deposited in the Fishery Museum of the Faculty of Fisheries Sciences, Hokkaido University, Japan (HUMZ), or the Shellfish Museum of Rankoshi, Hokkaido, Japan (SMRZ).

Results and Discussion

Evaluation of taxonomic characters Shell: In the size of adult shell, five operational taxa tended to fall into two groups (Fig. 2): smaller (shell length up to 41.81 mm; V. ampullacea, V. nipponkaiensis, V. limnaeformis; Figs 2A–C), and larger (shell length up to 68.04 mm; V. perryi, V. ainos; Figs 2D–E). Furthermore, these two groups also differed in the outline of the shell (Fig. 3): rather high in the smaller group (V. ampullacea, V. nipponkaiensis, V. limnaeformis), and rather low in the larger group (V. perryi, V. ainos). In V. perryi, however, individuals from shallower waters tended to become larger (Fig. 3; northern perryi) than those from deeper waters (Fig. 3; southern perryi). Although the smaller specimens of V. perryi from deeper waters superficially resembles V. ampullacea in the size and shape, these two taxa differ fundamentally in other characters such as the morphology of the operculum, penis, and the periostracum (Table 2). This indicates that the size and shape of shells cannot be regarded as distinguishing characters in themselves. Operculum: Volutharpa species generally possess a vestigial concentric operculum with a terminal nucleus (Figs 4–5), which is missing in some individuals. With regard to the condition of the nuclear part, two distinct types were recognized: one retaining the intact initial part with a round terminal (V. ampullacea, V. nipponkaiensis, and V. limnaeformis; Figs 4A–C), and the other lacking the initial part with a truncated appearance (V. perryi and V. ainos; Figs 4D–E). In addition to the shape, there is a clear difference in the position of the operculum on the epipodium: in the former type, the operculum is situated near the posterior end of the foot (Figs 5A–F), whereas in the latter type it is situated in a more anterior position (Figs 5G–L). The distance from the operculum to the posterior end of the foot in the former type is nearly equal to the length of the operculum in ethanol-fixed specimens (Figs 5A–F), whereas in the latter type it is about twice as the length of operculum (Figs 5G–L). This character is stable in each taxon, and no intermediate conditions were observed. Penis: In the shape of the gonopore, five operational taxa were classified into three discrete types (Fig. 6): 1) papillary (V. ampullacea; Fig. 6A), 2) triangular (V. nipponkaiensis, V. limnaeformis; Figs 6B–C), and 3) pointed (V. perryi, V. ainos). This character is stable within each group, and there was no intraspecific variation. Because the morphology of the external copulatory organ is closely related to reproductive isolation in various groups including gastropods (e.g., Reid, 1996), it is regarded herein as the most important diagnostic character to distinguish species in Volutharpa (Table 2). Radula: The morphology of the radula is generally identical in all the operational taxa, except for the number of cusps on the central and lateral teeth, which is variable even within a taxon (Figs 7–8; Table 1). Radula morphology has widely been accepted as an important diagnostic character to distinguish species of gastropods in general (e.g., Suter, 1907) and also in the Buccinidae (Golikov, 1963, 1980). In the genus Volutharpa, Okutani et al. (1988) regarded the number of cusps on the 4 T. Yamazaki, et al.

Fig. 2. Shells of Volutharpa spp. A. Volutharpa ampullacea, HUMZ M-1797, Shiretoko Peninsula, eastern Hokkaido, SH 22.75 mm. B. Volutharpa nipponkaiensis nipponkaiensis, HUMZ M–1735, off Iwanai, western Hokkaido, SH 41.68 mm. C. Volutharpa nipponkaiensis limnaeformis, HUMZ M-1736, Musashi-Bank, northern Japan Sea, SH 34.98 mm. D. Volutharpa perryi perryi, HUMZ M-1737, Kamiiso, southern Hokkaido, SH 55.37 mm. E: Volutharpa perryi ainos, HUMZ M-1809, off Rausu, western Hokkaido, SH 62.96 mm. Scale = 5 cm. central as a diagnostic character to separate V. ainos (five cusps) from V. ampullacea and V. perryi (six cusps). However, the number of cusps can be variable in buccinid species (Friele, 1879). Volutharpa species have been reported to possess three to seven cusps on each lateral tooth and four to six cusps on the central tooth (Troschel & Thiele, 1868; Tryon, 1881; Habe, 1958; Habe & Sato, Taxonomy of Volutharpa in Japan 5

80 ampullacea N=7 70 nipponkaiensis N=6 limnaeformis N=10 60 )

m 50

40 length ( m l

l 30 e h S 20 northern perryi N=52 10 southern perryi N=4 ainos N=11 0 0 10 20 30 40 50 Shell width (mm) Fig. 3. Relationship between shell length (vertical axis) and shell width (horizontal axis) in Volutharpa spp.

Table 1. Number of cusps on radula teeth recorded in previous studies. Number of cusps on radula Taxa Reference L-L C L-R 3 4 not indicate Habe (1958) not indicate 6 4 Habe & Sato (1972) not indicate 6 4 Habe & Ito (1980) ampullacea 4 6 4 Golikov (1980) 7 6 6 not indicate 6 not indicate Okutani et al. (1988) 3 5 3 Tian et al. (2009) 6 6 6 Troschel & Thiele (1868) perryi 6 6 6 Tryon (1881) not indicate 6 not indicate Okutani et al. (1988) 4 5 4 Habe & Ito (1980) ainos not indicate 5 not indicate Okutani et al. (1988) Abbreviations: L–L, lateral tooth on left; C, central tooth; L–R, lateral tooth on right.

1972; Habe & Ito, 1980; Golikov, 1980), and the present study confirmed this variation even in the same taxon (Figs 7–8; Table 1). It is concluded that radula morphology, including the number of cusps, is not acceptable as a diagnostic character to distinguish species or subspecies in this genus. Periostracum: Five distinct and discontinuous types were recognized in the morphology of the periostracum, i.e., 1) thin, fuzz-like and velvety (Fig. 9A; ampullacea); 2) thick and velvety with many lamellae (Fig. 9B; nipponkaiensis); 3) very thin (Fig. 9C; limnaeformis); 4) thick, film- like and velvety (Fig. 9D; perryi); 5) very thick, rib-like and velvety (Fig. 9E; ainos). Although 6 T. Yamazaki, et al.

Table 2. Taxonomic keys for Volutharpa species and subspecies.

Species ampullacea nipponkaiensis perryi Subspecies ampullacea nipponkaiensis limnaeformis perryi ainos Shell: size (Figs 2) small (SH; up to 41 mm) large (SH; up to 68 mm) Shell: shape (Fig. 3) rather high rather low Operculum: nucleus (Fig. 4) intact lacking Operculum: position (Fig. 5) posterior end of the foot more posterior end of the foot Penis: gonopore (Fig. 6) papillary triangle sharp Radula: cusps number 4, 5-6, 4-5 4-5, 6-7, 4-5 4, 7, 4 5-6, 5-7, 5 4, 5-6, 4 (Figs 7–8, Table 1) thin, fuzz-like thick, many thick, film-like very thick, Periostracum (Fig. 9) very thin velvety holds velvety velvety rib-like velvety Abashiri Off Shiretoko Alask to Musashi Bank Distribution (Southern Sea of Peninsula only eastern Korea Japan Sea only (Japan (See taxonomy) Okhotsk) to (Southern Sea of Peninsula Sea) Yellow Sea Okhotsk)

Fig. 4. Operculum of Volutharpa spp. A. Volutharpa ampullacea, HUMZ M-1820, Shiretoko Peninsula, eastern Hokkaido. B. Volutharpa nipponkaiensis nipponkaiensis, HUMZ M–1803, off Iwanai, western Hokkaido. C. Volutharpa nipponkaiensis limnaeformis, HUMZ M-1830, Musashi-Bank, northern Japan Sea. D. Volutharpa perryi perryi, HUMZ M-1827, Mutsu Bay, northern Japan. E. Volutharpa perryi ainos, HUMZ M-1809, off Rausu, western Hokkaido. Scale = 1 mm. Taxonomy of Volutharpa in Japan 7

Fig. 5. Posterior part of foot of Volutharpa spp. showing the position of operculum. A–B. Volutharpa ampullacea, HUMZ M-1821, Shiretoko Peninsula, eastern Hokkaido. C–D. Volutharpa nipponkaiensis nipponkaiensis, HUMZ M–1804, off Iwanai, western Hokkaido. E–F. Volutharpa nipponkaiensis limnaeformis, HUMZ M-1831, Musashi-Bank, northern Japan Sea. G–H. Volutharpa perryi perryi, HUMZ M-1840, Mutsu Bay, northern Japan. I–L. Volutharpa perryi ainos, HUMZ M-1808 (I–J), HUMZ M-1838 (K–L), off Rausu, western Hokkaido. Scale = 1 cm. the condition of the periostracum can be variable and affected by some environmental factors, this character is consistently stable in each taxon among the material examined, and is therefore regarded as a diagnostic character for the classification of Volutharpa at the species and subspecies level (Table 2). 8 T. Yamazaki, et al.

A ×2

×2

B C ×2

×2 ×2

D E Fig. 6. Penis of Volutharpa spp. A. Volutharpa ampullacea, HUMZ M-1822, Shiretoko Peninsula, eastern Hokkaido. B. Volutharpa nipponkaiensis nipponkaiensis, SMRZ M–7, off Iwanai, western Hokkaido. C. Volutharpa nipponkaiensis limnaeformis, HUMZ M-1832, Musashi-Bank, northern Japan Sea. D. Volutharpa perryi perryi, HUMZ M-1841, Mutsu Bay, northern Japan. E. Volutharpa perryi ainos, HUMZ M-1828, off Rausu, western Hokkaido. Scale = 1 cm.

Recognition of species As discussed above, four morphological characters are accepted to have taxonomical significance, at least to some extent, because of their discontinuous state of condition, i.e., 1) the size and the shape of the shell, 2) the shape and position of the operculum, 3) the shape of the gonophore, and 4) the condition of the periostracum. Among these, the shape of the gonophore can be regarded as the most important taxonomic character, and the taxa treated in this study should accordingly be classified into three distinct species; 1) ampullacea, 2) nipponkaiensis + limnaeformis, and 3) perryi + ainos. Because the oldest name has to be adopted for each taxon, these species should be called Volutharpa ampullacea, V. nipponkaiensis and V. perryi. Volutharpa perryi is also distinguished from the other two species in the morphology and position of the operculum. Among each species, limnaeformis could be distinguished from nipponkaiensis (s.s.) and ainos from perryi (s.s.), respectively, in the morphology of the periostracum. Because these morphotypes are distributed allopatrically with respect to each nominotypical taxon, they Taxonomy of Volutharpa in Japan 9

Fig. 7. Radula of Volutharpa spp. A. Volutharpa ampullacea HUMZ M-1822, Shiretoko Peninsula, eastern Hokkaido. B. Volutharpa nipponkaiensis nipponkaiensis SMRZ M–7, off Iwanai, western Hokkaido. C. Volutharpa nipponkaiensis limnaeformis HUMZ M-1832, Musashi-Bank, northern Japan Sea. D. Volutharpa perryi perryi HUMZ M-1841, Mutsu Bay, northern Japan. E. Volutharpa perryi ainos HUMZ M-1828, off Rausu, western Hokkaido. Scale = A: 200 μm; B–E: 500 μm. are treated herein as geographical subspecies. Accordingly, the northwestern Pacific species of the genus Volutharpa are classified into three species and two subspecies; V. ampullacea, V. nipponkaiensis nipponkaiensis, V. n. limnaeformis and V. perryi perryi and V. p. ainos (Table 2).

Taxonomy

Family Buccinidae Rafinesque, 1815 Genus Volutharpa Fischer, 1856

Type species (by monotypy): Volutharpa deshayesiana Fischer, 1856 [= Bullia ampullacea Middendorff, 1848]. Remarks: Adams (1860) pointed out the similarity of Volutharpa to Buccinum in the external 10 T. Yamazaki, et al.

9 8 A N=7 7

6

5

4

3 L-L C L-R 9 9 8 B N=2 8 C N=6 7 7

6 6

5 5 Cusps number 4 4

3 3 L-L C L-R L-L C L-R 9 9 8 D N=15 8 E N=6 7 7

6 6

5 5

4 4

3 3 L-L C L-R L-L C L-R Fig. 8. Box plot diagrams of number of cusps on radula teeth in Volutharpa spp. Box plots display the median, quartiles and extremes values. A. Volutharpa ampullacea. B. Volutharpa nipponkaiensis nipponkaiensis. C. Volutharpa nipponkaiensis limnaeformis. D. Volutharpa perryi perryi. E. Volutharpa perryi ainos. morphology of the head-foot, and their phylogenetic affinity was supported by subsequent authors (e.g., Golikov, 1980). Some authors (e.g., Thiele, 1931; Golikov, 1980) regarded Volutharpa as a subgenus of Buccinum, while others preferred to retain it as a distinct genus because of its significant morphological peculiarities, such as the distinctly inflated body and vestigial operculum. Furthermore, the operculum in the species of Volutharpa is concentric with a terminal nucleus (Figs 4–5), which is different from the typical concentric type seen in all the other known species in Buccinum (Golikov, 1980). The taxonomy of Volutharpa has been confused, with more than 10 nominal taxa that were mostly described based only on shell morphology. Because the objective of this study was to recognize species, and due to the difficulty in investigating and comparing primary types of all known taxa, we leave a detailed review of the synonymy of each taxon as a future task. Taxonomy of Volutharpa in Japan 11

A

B C

D E Fig. 9. Periostracum of Volutharpa. A. Volutharpa ampullacea, HUMZ M-1797, Shiretoko Peninsula, eastern Hokkaido. B. Volutharpa nipponkaiensis nipponkaiensis, HUMZ M–1735, off Iwanai, western Hokkaido. C. Volutharpa nipponkaiensis limnaeformis, HUMZ M-1736, Musashi-Bank, northern Japan Sea. D. Volutharpa perryi perryi, HUMZ M-1737, Kamiiso, southern Hokkaido. E. Volutharpa perryi ainos, HUMZ M-1809, off Rausu, western Hokkaido. The specimen of each taxon corresponds to the one shown in Fig. 2. Scale = 5 mm.

Volutharpa ampullacea (Middendorff, 1848) (Figs 2A, 4A, 5A–B, 6A, 7A, 9A)

Type locality: Schantar Islands (western Okhotsk Sea). Type material: Syntypes (10 exs.), Zoological Institute, Russian Academy of Science, St. Petersburg, ZIN 25500/29 (not examined). One of the syntypes is illustrated by Kantor & Sysoev (2007: pl. 86, fig. G). Materials examined: 22 specimens. Shallow water in Bunkichi Bay (44°20′01.12′′N, 145°19′00.12′′E), Shiretoko Peninsula, eastern Hokkaido, leg. (collected by) S. Chiba while SCUBA diving on 31 May 2007 (HUMZ M-1797–1799; live collected, preserved as dry specimens) and 19 June 2008 (HUMZ M-1734; live collected, preserved as dry specimen); collected by a cage 12 T. Yamazaki, et al. trap by T. Yamazaki on 14 May 2009 (HUMZ M-1811–1819; live collected, preserved in 99% ethanol) and 20 August 2009 (HUMZ M-1820–1826; live collected, in 99% ethanol). Drifted on the cost of Tikhaya (48°0′48.04′′N, 142°32′14.07′′E), southwest Sakhalin, collected by T. Nobetsu on 19 October 2008 (HUMZ M-1800; dead collected, preserved as dry specimen). Shallow water off Usujiri at a depth of 22 m, southern Hokkaido, collected by S. Awata while SCUBA diving on 16 March 2009 (HUMZ M-1801; dead collected, preserved as dry specimen). Diagnosis: Shell ovate, rather small for genus, thin, from deep purple to deep brown in color, inner deep purple to deep brown (Figs 2A, 3). Periostracum thickened along growth lines, resembling skin of kiwifruit (Figs 2A, 9A). Penis yellowish with irregular black areas on white base, smooth surface, enlarged penile base, and papillary gonopore (Fig. 6A). Foot yellowish with irregular black areas (Figs 5A–B). Operculum thick, deep brown, thickened at end part in adult individuals, and situated near posterior end of foot (Figs 5A–B). Nucleus of operculum intact and situated at posterior terminal (Fig. 4A). Distribution: Japan Sea: Off Jumun-jin, Gangnenung city, middle Korea peninsula, at a depth of 50 m (Min, 2004); Otaru (Ito, 1987). Pacific Ocean: off Kushiro (Yokohira, 1960); off Akkeshi (Habe, 1958; Yamazaki, 2011). Okhotsk Sea: Shantar islands (Middendorff, 1848); Sakhalin (Golikov, 1980; Yamazaki et al., 2016): Kuril Islands, Bering Strait, Alaska, Sitka (Dall, 1871), at depths ranging from 0 to 600 m (Fig. 1). Remarks: Identification of this species is based on the morphology of the shell in comparison with the illustrated syntype (Kantor & Sysoev, 2007: pl. 86, fig. G), and is rather provisional. Syntypes of this nominal taxon are preserved in ethanol with intact soft parts, and it is necessary to examine the morphology of penis to confirm the identification. Adams (1860) regarded V. perryi and V. ampullacea as separate species, and described the morphology of the shell and soft parts including the operculum of the latter based on one specimen collected by dredging in Aniwa Bay, at a depth of 17 fathoms, but did not mention on the penis. Dall (1871) described the morphology of the operculum in detail of the specimens from Sitka, Alaska (as a subspecies V. anpullacea acuminate Dall, 1871), and clearly stated presence of the nucleus at the margin of the operculum, suggesting their conspecificity with the present species. Golikov (1980: fig. 200) illustrated the penis of a specimen from an unspecified locality, and it generally agrees with that of the present material, although he recognized only one species in the genus with all the other nominal taxa as synonyms.

Volutharpa nipponkaiensis nipponkaiensis Habe & Ito, 1980 (Figs 2B, 4B, 5C–D, 6B, 7B, 9B)

Type locality: “Iwashiro” (sic; = Iwanai, see remarks), southern Hokkaido in the Japan Sea. Type material: Although the holotype and two paratypes were cited in the original description (Habe & Ito, 1980) as having been deposited in the National Science Museum, Tokyo [now National Museum of Nature and Science] (NSMT) with the catalog numbers NSMT-Mo 58012 and 58013–4, they are not located in the type collection of the museum. A search in the general collection resulted in the discovery of specimens that completely agree with the holotype (Habe & Ito, 1980: pl. 1, figs 2–3) and the figured paratype from off Rebun Island (Habe & Ito, 1980: pl. 1, fig. 9), not only in morphology but also their measurements (K. Hasegawa, NSMT, personal communication). This probable holotype had been cataloged as “Volutharpa sp.” with the number NSMT-Mo 46625, and the locality was noted just as “the Sea of Japan, collected by Shigetomi Kato” with no more detailed information. According to the registration record for NSMT-Mo 58012, the authors intended to designate another specimen collected from “Iwashiro” as the holotype, but they might have mistakenly photographed and measured (thus designated) the specimen in NSMT-Mo 46625. Accordingly, the type locality of this taxon is here corrected to Taxonomy of Volutharpa in Japan 13 just “the Sea of Japan”. Materials examined: 10 specimens. Off Matsumae Kojima at a depth of 360 m, southern Hokkaido, collected by S. Igarashi on 21 June 1982 (SMRZ M-1, 2; dry specimens); off Kaneda at a depth of 145 m, Rebun Island, northern Hokkaido, collected by gill-net by K. Sasaki on 2 October 2003 (HUMZ M-1735, 1802, 1892–1894; dry specimens); 14 September 2009 (HUMZ M-1803, 1804; in 99% ethanol); off Funadomari at a depth of 100 m, Rebun Island, northern Hokkaido, collected by gill-net by K. Sasaki on 20 September 2010 (SMRZ M-7; in 99% ethanol). Diagnosis: Shell elongate, rather small for genus, thin and dark yellowish in color (Fig. 2B). Periostracum thick and velvety with many lamellae along on growth lines in dry specimens (Figs 2B, 9B). Penis yellowish with wrinkled surface, triangular gonopore (Fig. 6B), and constricted penile base. Foot yellowish, covered by irregular black pigment (Figs 5C–D). Operculum thick, deep brown, with thickened end part in adult individuals, round initial part, and nucleus situated near posterior margin (Figs 2B, 5C–D). Operculum situated at posterior end of foot (Figs 5C–D). Distribution: Endemic to the northeastern Sea of Japan, from Matsumae-Kojima Islet to Rebun Island, excluding the Musashi Bank, at depths from 100 to 360 m, and off Samcheok, middle Korean Peninsula (Min, 2004) (Fig. 1). Remarks: Although the type locality of this taxon was given as “Iwashiro, southern Hokkaido in the Japan Sea” in the original description (Habe & Ito, 1980), “Iwashiro” does not exist as a local name in Hokkaido (Hokkaido Shinbun Press, 1981). The locality was actually Iwanai, southern Hokkaido according to Mr. K. Sasaki (pers. comm., 2008) who provided the authors with the corresponding material. The specimen illustrated as “V. ampullacea morchiana Fischer, 1859” by Min (2004: fig. 641) from eastern middle Korea Peninsula can correctly be identified as V. n. nipponkaiensis based on the size and proportion of the shell, the color of the inner lip and the condition of the periostracum, although examination of the soft parts will be necessary to confirm the identification. The descriptions of “V. a. limnaeformis” and “V. a. morchiana” were erroneously switched in that work.

Volutharpa nipponkaiensis limnaeformis Habe & Ito, 1980 (Figs 2C, 4C, 5E–F, 6C, 7C, 9C)

Type locality: Musashi Bank, the northern part of the Sea of Japan, at depths ranging from 35 to 60 m. Type material: Although the holotype and two measured paratypes were to be deposited in the NSMT under the catalog numbers NSMT-Mo 58015 and 58016–7 (Habe & Ito, 1980), they were not found in the type collection. Specimens probably corresponding to the holotype and one of the measured paratypes were found unregistered in the general collection with the data “Musashi-tai [= Musashi Bank], 20–25 fathoms”, and they were formally cataloged under the appropriate numbers (K. Hasegawa, personal communication). Materials examined: 10 specimens. Musashi Bank at depths ranging from 45 to 50 m, northern Japan, collected by gill-net by Mr. K. Sasaki on 16 October 2002 (HUMZ M-1895; dry specimen); 2 September 2003 (HUMZ M-1736, 1805; dry specimen); 31 July 2009 (HUMZ M-1830–1834; in 99% ethanol); 7 August 2009 (HUMZ M-1835, 1836; dry specimens). Diagnosis: Shell elongate, rather small for genus and lymnaeid-like in shape; thin, brown, with yellowish inner lip (Figs 2C, 9C). Periostracum very thin (Figs 2C, 9C). Penis pale yellowish brown, with wrinkled surface, rather constricted penile base, and triangular gonopore (Fig. 6C). Foot yellowish (Figs 5E–F). Operculum rather thick, yellowish, with nucleus situated near posterior end (Figs 4C, 5E–F). Operculum situated at posterior end of foot (Figs 5E–F). Distribution: Endemic to Musashi Bank, the northeastern Sea of Japan, at depths from 35 to 60 m (Fig. 1). 14 T. Yamazaki, et al.

Remarks: This species has been known only from a very narrow area around the Musashi Bank. Although there have been only a few published records of this species since its original description until the present study (e.g., Higuchi, 2006), it is found in personal and museum collections (e.g., Kawamura and Sakurai collections in NSMT).

Volutharpa perryi perryi (Jay, 1856) (Figs 2D, 4D, 5G–H, 6D, 7D, 9D)

Type locality: Bay of Yedo [= Tokyo Bay]. Type material: Holotype, American Museum of Natural History, AMNH 56084 (Jay Coll. 11906), illustrated by Habe (1977: pl. 2, figs 4–5) and Higo et al. (2001: p. 82, G2826). Materials examined: 59 specimens. Drifted on the cost of Kamiiso, southern Hokkaido, collected by T. Yamazaki on 16 April 1995 (HUMZ M-1737, 1806; dead collected, dry specimen). Mutsu Bay, collected by T. Yamazaki on 10 May 2003 (HUMZ M-1827; live collected, in 99% ethanol) and 14 January 2010 at a depth of 25 m (HUMZ M-1840–1891; live collected, in 99% ethanol). Entrance of Ise Bay collected by S. Kimura on February 2012 at a depth of 10 to 20 m (SMRZ M-3–6; live collected, in 99% ethanol). Diagnosis: Shell ovate, rather large for genus, thin, white with velvety periostracum in dry specimens, with white inner lip (Figs 2D, 9D). Penis yellowish with irregular black blotches on white base, with wrinkled surface, slender penile base, and sharply pointed gonopore (Fig. 6D). Foot yellowish, covered by irregular black film (Figs 5G–H). Operculum thick, slender, deep brown, with thickened end part in adult individuals; initial part situated near posterior end lacking nucleus (Figs 4D, 5G–H). Operculum situated at posterior end of foot (Figs 5G–H). Distribution: East China Sea: Yellow Sea, Bohai Sea (Zhongyan, 2004), off Tean-Gun (Min, 2004). Japan Sea: off Gyeongbuk, off Gyeongnam, off Goheung-gun (Min, 2004), off Tajima (Ito, 1967); Wakasa Bay (Ito, 1990); off Ishikawa prefecture (Ito, 1986); off Otaru (Ito, 1987). Pacific Ocean: Sagami Bay (Kuroda et al., 1971); off Iwate prefecture (Toba, 2009); Otsuchi Bay (Tsuchida, 1991); Mutsu Bay (Ishikawa, 1975). Okhotsk Sea: off Utoro (Sonoda et al., 2010), at depths from 3 to 90 m (Fig. 1). Remarks: The record of this taxon in the Bering Sea (Oldroyd, 1927) may be due to misidentification of V. ampullacea, although this could not be confirmed because of the absence of illustration in the work, and also the lack of material from that area in the present study. The specimen illustrated by Min (2004: fig. 642) as “V. ampullacea limnaeformis Habe & Ito, 1980” can correctly be identified as this subspecies. Specimens collected from the sublittoral zone in temperate waters (e.g., at the entrance of Ise Bay) almost always possess a smaller shell, but they are indistinguishable from ordinary examples in the morphology of the gonopore and periostracum, and thus they are regarded here as a phenotype of this taxon.

Volutharpa perryi ainos Kuroda & Kinoshita, 1956 (Figs 2E, 4E, 5I–L, 6E, 7E, 9E)

Type locality: Off Rausu at a depth of 120–130 fathoms [= 216 to 234 m]. Type material: Kuroda & Kinoshita (1956) did not mention the depository of the holotype. It was not located in the Nishinomiya Shell Museum, where majority of the late Dr. Kuroda’s collection is preserved (Nishinomiya City, 1996), or in other facilities (Nishinomiya City, 1997). Although Tiba & Kosuge (1980) illustrated the “holotype,” the photograph was probably reproduced from the original description, and the specimen is not located in Tiba’s collections in the Rikuzen-Takata City Museum (Mr. K. Kumagai, pers. comm., 2008). Nevertheless this taxon Taxonomy of Volutharpa in Japan 15 can be readily distinguished from other taxa in the genus by its unique shell morphology, and there is no nomenclatural problem. Materials examined: 11 specimens. Off Rausu at depths from 300 to 500 m, collected by gill- net by M. Miyamoto on January 2003 (HUMZ M-1738, 1807, 1896; dry specimens). Off Rausu 817 m at a depth of 356 m, collected by an upwelling pump of deep sea water by T. Nobetsu on 15 October 2008 (HUMZ M-1808; in 99% ethanol); 23 January 2008 (HUMZ M-1809; in 99% ethanol); 12 July 2008 (HUMZ M-1828; in 99% ethanol); 19 August 2008 (HUMZ M-1810; in 99% ethanol); 16 June 2009 (HUMZ M-1838; in 99% ethanol); 20 August 2009 (HUMZ M-1837; in 99% ethanol); 3 September 2009 (HUMZ M-1839; in 99% ethanol); 4 September 2009 (HUMZ M-1829; in 99% ethanol). Diagnosis: Shell ovate, rather large for genus, very thin and white, with white inner lip (Fig. 2E). Periostracum extraordinarily thick, velvety, with 22–27 regular axial folds that are gently sigmoidal in dry specimens (Figs 2E, 9E). Penis yellowish, with wrinkled surface, constricted penile base and sharply pointed gonopore (Fig. 6E). usually eroded (Figs 2E, 5J–L). Foot black in adult individuals (Figs 5I–J), yellowish with irregular black areas in juveniles (Figs 5K–L). Operculum thick, slender, deep brown, with thickened end part, flat initial part; initial part situated near posterior end lacking nucleus (Fig. 4E). Operculum situated at posterior end of foot (Figs 5K–L). Distribution: Endemic to eastern Hokkaido, North Pacific: off Shiretoko Peninsula and adjacent areas at depths ranging from 100 to 900 m (Fig. 1). Remarks: Although Okutani et al. (1988) treated ainos as a distinct species based on the difference in the number of cusps on the central tooth of the radula, this character cannot be regarded as diagnostic as stated in the Discussion (evaluation of taxonomic characters). The present taxon agrees in overall morphology of the soft parts with V. perryi, but is clearly distinguished from the latter by the remarkable difference in shell morphology, especially in the condition of the periostracum.

Acknowledgements

We extend our sincere thanks to Mr. Masaru Kumagai, Rikuzen-Takata Sea and Shell Museum, for his attempt to locate the holotype of Volutharpa perryi ainos and for giving us a useful reference. Dr. Sadao Kosuge also helped us search for the holotype of V. p. ainos. Mr. Koichi Sasaki, Mr. Keisuke Machi, Graduate School of Fisheries Sciences, Hokkaido University, Dr. Satoshi Awata, Usujiri Fisheries Station, Hokkaido University, and Mr. Mitsuo Miyamoto sent us specimens. Dr. Kazunori Hasegawa, National Museum of Nature and Science, Tokyo, Japan, helped us to improve the manuscript. This research was conducted with the financial support of the Japanese Ministry of the Environment for a “Fauna and flora survey of the shallow sea area along the Shiretoko coast,” and of the Tokyo University of Agriculture for a research project on “Ecology and fauna of the coast of the Okhotsk region.”

References

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(Received January 5, 2016 / Accepted April 7, 2018) 18 T. Yamazaki, et al.

日本産モスソガイ属（腹足綱：エゾバイ科）の分類への寄与

山崎友資・園田 武・野別貴博・五嶋聖治

要 約

サハリン～北海道，本州周辺海域から採集された標本に基づいて，モスソガイ属の分類学的再検討を 行った。モスソガイ属は近縁のエゾバイ属の異名として扱われる場合もあるが，貝殻の形態の顕著な違い から，独立した属として扱った。 これまでモスソガイ属は研究者によって 2 種 3 亜種，あるいは 1 種に分類されていた。本研究において は，Habe & Ito（1980）により定義された 5 つの種および亜種タクサを操作上のタクサとして，主に貝殻， 蓋と陰茎の形態，および地理的分布を比較した結果，以下の 3 種群に分類された。なお，歯舌形態は中歯 の歯尖数に個体間変異が多く，本属において，種レベルにおける分類形質として有効ではないことが明ら かとなった。 1）ampullacea 種群：殻は小型，蓋の核は保存されていて丸く，足後縁部の前側に位置し，陰茎の生殖 口は丸みを帯びる。ベーリング海，オホーツク海，日本海，北太平洋広域に分布する。含まれるタクソン は，ampullacea のみ。 2）nipponkaiensis 種群：殻は小型，蓋の核は保存されていて丸く，足後縁部の前側に位置し，陰茎の生 殖口は三角形。日本海，宗谷海峡に分布する。含まれるタクソンは nipponkaiensis と limnaeformis。 3）perryi 種群：殻は大型，蓋の核は欠けていて裁断状，足後縁部のやや前側に位置し，陰茎の生殖口 は鋭く尖る。オホーツク海，日本海，北太平洋広域に分布する。含まれるタクサは perryi と ainos。 同一種群に含まれる nipponkaiensis と limnaeformis，perryi と ainos のそれぞれは，側所的に生息し，貝 殻，特に殻皮の形態から不連続に区別できることから亜種として扱い，モスソガイ属は以下 3 種 2 亜種か ら構成されると結論づけた。 V. ampullacea ampullacea（Middendorff, 1848）ヒメモスソガイ V. nipponkaiensis nipponkaiensis Habe & Ito, 1980 ナガモスソガイ V. nipponkaiensis limnaeformis Habe & Ito, 1980 ウスカワモスソガイ V. perryi perryi（Jay, 1856）モスソガイ V. perryi ainos Kuroda & Kinoshita, 1956 クマモスソガイ ウスカワモスソガイ V. n. limnaeformis Habe & Ito, 1980 のタイプ産地は，北海道南部の岩代 Iwashiro 沖 として記載されたが，北海道には岩代という地名は存在せず，岩内 Iwanai 沖であることが確認できた。し かしながら，ホロタイプの再調査により本タクソンのタイプ産地は詳細地名の特定されない北海道と訂正 される。 本論文で取り扱った標本は全て北海道大学総合博物館分館水産科学館及び，蘭越町貝の館に所蔵されて いる。