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Systematic Revision of the Subgenus Luchuhadra (Pulmonata: Camaenidae: Satsuma) Occurring in the Central Ryukyu Archipelago

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Systematic Revision of the Subgenus Luchuhadra (Pulmonata: Camaenidae: Satsuma) Occurring in the Central Ryukyu Archipelago VENUS 66 (3-4): 127-145, 2008 Systematic Revision of the Subgenus Luchuhadra (Pulmonata: Camaenidae: Satsuma) Occurring in the Central Ryukyu Archipelago Yuichi Kameda* and Makoto Kato Graduate School of Human and Environmental Studies, Kyoto University, Yoshida-Nihonmatsu- cho, Sakyo, Kyoto 606-8501, Japan;* [email protected] Abstract: Satsuma (Luchuhadra) largillierti is an arboreal land snail endemic to Okinawa Island, Japan, and its extensive geographic variation in shell morphology has long caused taxonomic confusion. A recent molecular phylogenetic study demonstrated that S. largillierti and the two species endemic to Okinoerabu Island, S. erabuensis and S. sooi, are more correctly re-organized into two species that are anatomically and genetically distinct. To confirm the taxonomic status and nomenclature of these species, we examined the available type materials and corresponding descriptions. We suggest that the above species be treated as S. eucosmia and S. largillierti, that S. sooi become a synonym of S. largillierti, and that S. erabuensis is reduced to a subspecies of S. eucosmia. We also present revised morphological descriptions of the four Luchuhadra species that range from Iheya Island off Okinawa Island to the Miyako Islands, which are here confirmed as distinct based on both morphological and molecular data. Keywords: discriminant analysis, genital morphology, Satsuma amanoi, Satsuma hemihelvus, Satsuma iheyaensis, Satsuma omoro Introduction The subgenus Luchuhadra (Camaenidae: Satsuma) is an arboreal group of land snails endemic to the middle Ryukyu Archipelago in the southwestern part of Japan. Luchuhadra currently consists of 11 extant species (Minato, 1988), which are regarded as having largely distinct morphologies (Minato, 1976, 1980, 1982a, 1984, 1987; Azuma, 2000). Among them, Satsuma largillierti exhibits great variation in shell shape, shell color pattern, and anatomy, which has raised speculation concerning the specific status of different varieties (Chinen, 1977; Azuma, 1982, 1995; Azuma, 2000; Minato, 1995). Kameda et al. (2007) performed genetic and morphometric analyses on these snails and found that S. largillierti and the two species endemic to Okinoerabu Island, S. erabuensis and S. sooi, compose two distinct biological species, Group E and L, that do not agree with the current circumscriptions (Fig. 1). Satsuma largillierti was divided into two morphologically and genetically distinct species with largely allopatric distributions (Fig. 2). In addition, our genetic analysis and morphometric reassessment did not support the separation of S. erabuensis and S. sooi, except for the shell shape of S. erabuensis. Thus we concluded that these two species should be included in one of the two cryptic species of S. largillierti (Kameda et al., 2007). Here we aim to reassess the specific status of the S. largillierti species complex (including S. sooi and S. erabuensis). We also present revised morphological descriptions of the four related species distributed from Iheya Island to the Miyako Islands. Institutional abbreviations: ANSP, Academy of Natural Sciences, Philadelphia; NC, Nishinomiya Shell Museum; NSMT, National Museum of Nature and Science, Tokyo. 128 Y. Kameda & M. Kato S. sororcula S. adelinae S. shigetai S. tokunoshimana S. iheyaensis S. amanoi S. eucosmia (including S. erabuensis) S. largillierti (including S. sooi) S. omoro S. hemihelvus outgroup Fig. 1. Phylogenetic relationships among Luchuhadra species based on mitochondrial COI sequences (redrawn from Kameda et al., 2007). Materials and Methods Sampling To reaffirm the morphological circumscription of the Luchuhadra species, we sampled snails from all currently recognized species. In total, we obtained 398 adult Luchuhadra snails. The sampling sites and sample sizes are shown in Appendix. Four species from Amami-Oshima and Tokunoshima Islands, S. sororcula, S. adelinae, S. shigetai and S. tokunoshimana, are not discussed in this paper because our preliminary analysis of morphology and genetic data indicates that their specific status may require further investigation. Some of the specimens used in this study were deposited in the NSMT, and others have been retained in the collection of the first author. Classification of type specimens Satsuma largillierti, S. erabuensis and S. sooi are clustered in two distinct lineages, Group E and L, each of which is further subdivided into five (Eb, Ef, Eg, Es, and Ee [= S. erabuensis]) and eight (Lh, Li, Lk, Lm, Lu, Ly, Lz, and Y [= S. sooi]) well-supported subgroups (Kameda et al., 2007). According to Minato (1988), six names have been given to this species group: Helix largillierti Pfeiffer, 1849, Helix immaculata Adams & Reeve, 1850, Ganesella largillierti var. eucosmia and var. zacosmia Pilsbry, 1895, Satsuma erabuensis Minato, 1978, and Satsuma sooi Minato, 1982. To confirm the nomenclature of this species complex, we examined the type materials of G. largillierti var. eucosmia and var. zacosmia, S. erabuensis, and S. sooi. We also examined the type material of S. yoronjimana, a fossil species from Yoron Island, because it is possible that this species belongs to one of the two groups, E or L. Discriminant analysis was used to determine to which group each type series corresponds. The analysis was performed using the CANDISC procedure of SAS software (SAS Institute). The following characters were measured from either digital or printed images: shell height, shell width, spire height, spire width, aperture height, aperture width, and inner lip length. Because shell measurements cannot be used to confidently distinguish species (Kameda et al., 2007), we also considered the angularity of the periphery and color pattern. The assignment of H. largillierti and H. immaculata were based on Systematic Revision of the Subgenus Luchuhadra 129 A Lh B Eb Ly Li Lk Ly Eg Lm Li Ef Lu Lz Es 10km Fig. 2. Distributions of Satsuma largillierti (A) and S. eucosmia eucosmia (B) on Okinawa Island. The shaded regions represent the distributions of mitochondrial subgroups within each species. See text for abbreviated codes applied to subgroups. the original descriptions because we were unable to locate the type material. Systematics Family Camaenidae Pilsbry, 1895 Genus Satsuma Adams, 1868 Subgenus Luchuhadra Kuroda & Habe, 1949 Satsuma (Luchuhadra) largillierti (Pfeiffer, 1849) (Figs. 3A-D, 5A-B) Helix largillierti Pfeiffer, 1849: 78-79; Tryon, 1887: 218, pl. 50 fig. 45-46. Helix immaculata Adams & Reeve, 1850: 62, pl. 16, fig. 5. Eulota (Euhadra) largillierti: Gude, 1900: 77. Satsuma (Luchuhadra) largillierti: Habe, 1955: 221-222, fig. 5; Minato, 1988: 145. Luchuhadra largillierti: Kuroda, 1960: 48; Kuroda, 1963: 46. Luchuhadra adelinae: Chinen, 1977: 134, pl. 3, fig. 18 (non Ganesella adelinae Pilsbry, 1901). Satsuma sooi Minato, 1982a: 188, 190-191, pl. 1, fig. 4. Satsuma (Luchuhadra) sooi: Minato, 1987: 38, pl. 2, figs. 3-4; Minato, 1988: 146; Yukita, 2003: 78, 161. 130 Y. Kameda & M. Kato A B C D E F G H I J K L 10 mm Fig. 3. Shells of the Luchuhadra species. A-D. Satsuma largillierti; A, subgroup Lz (Kameda Collection [KC] No. 2854), this individual agree well with the description of Pfeiffer (1849); B, subgroup Li (KC No. 2366); C, subgroup Ly (KC No. 3833); D, subgroup Lu (NSMT-Mo 73960). E-G. S. eucosmia eucosmia; E, lectotype of Satsuma eucosmia eucosmia (ANSP 70803); F, lectotype of Ganesella largillierti var. zacosmia Pilsbry, 1895 (ANSP 70802); G, specimen without bands (KC No. 2389). H. S. eucosmia erabuensis (lectotype, ANSP 89996). I. S. iheyaensis (NSMT-Mo 73940). J. S. amanoi (NSMT- Mo 73939). K. S. omoro (NSMT-Mo 73942). L. S. hemihelvus (NSMT-Mo 73933). A B ps ap ps ap ep ep C a D a ps b ps b ep ep Fig. 4. The external and internal structures of the penis sheath and the appendix of the penis of Satuma eucosmia eucosmia (A, B) and S. omoro (C, D). In S. omoro, the small projection (a) is usually regarded as the appendix of the penis. The thick part between the projection and epiphallus (b) has been considered as a part of the epiphallus, but the internal structure is similar to that of the appendix of the penis in S. e. eucosmia. See text for letters indicating anatomical parts. Systematic Revision of the Subgenus Luchuhadra 131 Satsuma (Luchuhadra) yoronjimana Azuma & Azuma, 1990: 198-200. Luchuhadra sooi: Azuma, 1995: 212-213, pl. 74, fig. 629. Luchuhadra yoronjimana: Azuma, 1995: 213, pl. 74, fig. 631. Type material: Not located. Type locality: Liew-Kiew (= Ryukyu). Original description: “T. perforata, subtrochiformis, tenuis, sublaevigata, diaphana, albida; spira conica, obtusiuscula; anfr. 5½ vix convexiusculi, ultimus peripheria obsolete angulatus; apertura obliqua, rotundato-lunaris; perist. simplex, margine dextro breviter expanso, basali subincrassato, columellari dilatato, reflexo, umbilicum angustissimum semiegente. -Diam. maj. 22, min. 20, alt. 17 mill. (Coll. Phillipi.)”. Redescription: The shell is small- to large-sized for Luchuhadra, approximately 15-29 mm in diameter. The size of the shell and the angularity of the periphery show a high degree of geographic variation. The spire is tall, but the shell height seldom or never exceeds the diameter. The number of whorls is 5.5-6.5. The protoconch consists of two whorls. The shell surface is smooth, pale or yellowish-white without bands, or occasionally with light brown to black bands at the periphery, sutures, and umbilicus. A few individuals exhibit two color bands at the periphery. The aperture is roundly
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