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Gastropoda: Buccinidae) 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 Taxonomy of the Japanese Species of Volutharpa (Gastropoda: Buccinidae) 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, operculum, penis and radula, as well as their geographical distribution. The genus is provisionally distinguished from the allied genus Buccinum 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 periostracum 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 Ocean, 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 animal 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 tooth as a diagnostic character to separate V.
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