Semisulcospira niponica ( Smith, 1876 )

Sawada, Naoto & Fuke, Yusuke, 2023, Diversification in ancient Lake Biwa: integrative taxonomy reveals overlooked species diversity of the Japanese freshwater snail genus Semisulcospira (Mollusca: Semisulcospiridae), Contributions to Zoology 92 (1), pp. 1-37 : 20-24

Semisulcospira niponica ( Smith, 1876)

( table 2 , supplementary table S1 ; figs. 8A–K, Q –AN, 12A–G)

Melania niponica Smith, 1876: 123–124 (part); Martens, 1877: 116 (exact taxonomic account uncertain; TAU); Brot, 1877: 338–339, pl. 34, figs 10 (part); Kobelt, 1879: 131, pl. 19, figs 5–7 , 10 –14 (part); Pilsbry, 1902: 119; Iwakawa, 1919: 82 (part; TAU); Annandale, 1916: 45, pl. 3, fig. 3A (part).

Melania biwae Kobelt, 1879: 132–133 , pl. 19, fig. 9 ; Pilsbry, 1902: 120.

Melania (Melanoides) niponica – Nevill, 1884: 264 (TAU).

Melania (Semisulcospira) niponica – Boettger, 1886: 8.

Melania nipponica – De Elera, 1896: 335.

Semisulcospira niponica – Kuroda, 1929: 186, 189, pl. 5, figs 32–33 (part); Fukuoka, 1933: 114, 117, fig. 5 ; Kajiyama & Habe, 1961: 167; Kuroda, 1962: 86 (part; TAU); Kuroda & Habe, 1965: 57 (part); Habe & Kosuge, 1967: 28, pl. 11, fig. 22 (part); Davis, 1969: 243–246, pl. 4, figs 1–3 ; Watanabe, 1984: fig. 3b–d, f–h (part); Watanabe, 1989: 11–13, 47, figs 10 , 27, 28 (part); Köhler, 2016: fig. 4O, P .

Melanoides (Semisulcospira) niponicus – Mori, 1936: 229–230; Mori, 1937: 37–38, fig. 1 .

Hua? niponica – Kira, 1954: 127, pl. 63, fig. 1 .

Biwamelania niponica – Habe, 1978: 94; Nishino & Tanida, 2018: 56, 251 (part).

Biwakomelania niponica – Habe, 1984: 305.

Semisulcospira (Biwamelania) niponica – Matsuoka, 1985: 190; Nishino, 1991: 9–10, unnumbered figures (part); Urabe, 2007: 80, fig. 1A ; Kihira, et al., 2009: 24–25, unnumbered figure (part); Miura et al., 2019: fig. S1f ; Nishino, 2021: 621.

Semisulcospira nipponica – Higo & Goto, 1993: 97; Goto & Poppe, 1996: 204.

Semisulcospira (Biwamelania) niponica (nodose type) – Watanabe & Nishino, 1995: 17–18, fig. 5b (part).

Material examined: Voucher specimens: Lectotype: NHM 1875.11.24.11/1, adult shell, sex undetermined, collected from Lake Biwa in central Honshu Island , Japan in 1875 by Charles Wycliffe Goodwin. Paralectotypes: NHM 1875.11.24.11/2, 1875.11.24.11/3, 2 adult shells, sex undetermined, collected with lectotype. SMF 29151, 1 adult shell, sex undetermined, collected from Lake Biwa in 1874 by Johannes Justus Rein. KUZ Z3959 14 males, KUZ Z3766, 15 females, collected from Otsu Port on 23 June 2020 by Naoto Sawada .

Additional materials:KUZ Z4091, 15 females, KUZ Z4092, 1 male, collected from Oura Port on 28 November 2021; KUZ Z4093,15 females, KUZ Z4094, 15 males, collected from Nagahama Port on 28 November 2021; KUZ Z4095, 12 females, KUZ Z4096, 5 males, collected from Iso on 24 January 2021; KUZ Z4097, 8 females, collected from Kitakomatsu Port on 28 November 2021; KUZ Z4098, 1male, collected from Kitakomatsu Beach on 9 January 2022; KUZ Z4099, 15 females, KUZ Z4100, 10 males, collected from Katata Port on 28 November 2021; KUZ Z4101, 15 females, KUZ Z4102, 10 males, collected from Nango on 28 November 2021.

Amended diagnosis: Viviparous semisulcospirid. Adult shell medium sized [SH 27.7 ± 2.9 (mean ± SD) (female), 23.8 ± 2.1 (male) mm; BWL 17.3 ± 1.6, 14.8 ± 1.3 mm], nearly triangular (SA 23.2 ± 2.7, 22.7 ± 2.6 degrees); color in black or brackish brown background; outer lip of aperture hardly swell (ASL 0.06 ± 0.04, 0.09 ± 0.04 mm); 3.3 ± 1.0, 3.2 ± 0.9 BCN; 13.1 ± 2.1, 11.8 ± 1.9 distinct, longitudinal ribs slightly to moderately nodulated on penultimate whorl; 4.2 ± 0.8, 3.9 ± 0.8 SCN; 1.6 ± 0.1, 1.7 ± 0.1 ASR; 2.9 ± 0.3, 3.0 ± 0.3 WER. Embryonic shell medium sized, with distinct nodes on surface; color in black background or beige background with 3 brown or black bands.

Lectotype designation: One syntype, NHM 1875.11.24.11/1 ( fig. 8A–C ), was chosen as the lectotype for S. niponica in this study because the specimen possesses 15 longitudinal ribs and 3 spiral cords on the body whorl, which correspond to the values in the original description. The other two syntypes, NHM 1875.11.24.11/2 ( fig. 8D ) and NHM 1875.11.24.11/3 ( fig. 8E ) have 6 or 7 spiral cords on the body whorls and were described as a variation of the species ( Smith, 1876).

Description: Lectotype, NHM 1875.11.24.11/1 ( fig. 8A–C ): AH 9.1 mm, AL 9.3 mm, ASR 1.62, AW 5.7 mm, BCN 2, BWL 15.4 mm, NL 0.04 mm; PWL 5.5 mm, RN 15, SA 22.1 degrees, SCN 3, SH 22.1 mm, SW 9.9 mm, TWL 4.6 mm, WN 3.25. Shell nearly triangular; suture hardly undulating; whorl sides slightly convex; outer lip of aperture hardly swell; longitudinal ribs distinct, almost straight, oblique, prominently nodulated in penultimate to body whorl; apex of shell eroded; shell color partly faded, colored brown in body to penultimate whorl, blackish brown in remaining whorls, without color band; without operculum.

Paralectotypes: NHM 1875.11.24.11/2 ( fig. 8D ): AH 5.9 mm, AL 5.2 mm, BCN 3, BWL 10.3 mm, FWL 3.0 mm, NL 0 mm, PWL 4.1 mm, SA 11.3 degrees, SCN 7, SH 17.0 mm, SW 6.1 mm, TWL 3.6 mm, WER 1.97; WN 3.25 ; shell greatly elongated; suture moderately undulating; whorl sides moderately convex; swell of outer lip of aperture absent; longitudinal ribs indistinct, moderately curved, oblique, crossed by prominent spiral cords in penultimate to body whorl; apex of shell eroded; shell color partly faded, colored blackish brown background; aperture chipped; without operculum. NHM 1875.11.24.11/3 ( fig. 8E ): AH 6.3 mm, AL 6.1 mm, ASR 1.62, AW 3.8 mm, BCN 3, BWL 10.9 mm, FWL 2.5 mm; PWL 4.2 mm, SA 17.7 degrees, SCN 6, SH 17.2 mm, SW 6.8 mm, TWL 3.2 mm, WER 2.49; WN 3.25 ; shell elongated; suture moderately undulating; whorl sides slightly convex; swell of outer lip of aperture absent; sculpture distinct, slightly curved, vertical, ribbed longitudinally in penultimate whorl, ribs partly nodulated in body whorl; apex of shell eroded; shell color partly faded, colored beige background; aperture slightly chipped; without operculum .

Variation: Adult shells ( fig. 8G–I, Q, T, X , AA, AD, AF, AI, AL): Holotype of S. biwae, SMF 291511: AH 9.6 mm, AL 9.9 mm, ASR 1.53, AW 6.4 mm, BCN 3, BWL 15.7 mm, PWL 5.3 mm, RN 11, SA 25.6 degrees, SCN 3, SH 21.6 mm, SW 10.9 mm, TWL 4.1 mm, WN 3.25 ; shell nearly triangular; suture hardly undulating; whorl sides moderately convex; outer lip of aperture slightly swell; longitudinal ribs distinct, almost straight to slightly curved, prominently nodulated in penultimate to body whorl; apex

of shell largely eroded; shell colored beige in lower half of body whorl, brown in remaining whorls, without color band; without operculum.

Newly collected specimens: Measurements and counts shown in table 2 and supplementary table S1 . Shell near thick to slightly elongated triangular; suture hardly to slightly undulating; whorl sides slightly convex; outer lip of aperture hardly to slightly swell; longitudinal ribs on penultimate whorl distinct, almost straight to slightly curved, oblique, slightly to prominently nodulated by spiral cords, rarely spiral cords alone on penultimate whorl; sculptures often ribbed on upper whorls, granulated in lower whorls; shell colored black or brackish brown in

Downloaded from Brill.com 08/29/2023 02:12:56AM

via free access background, sometimes several indistinct brown band on lower part of each whorl.

Operculum ( fig. 8R, U, Y , AB, AE, AG, AJ, AM): 5.5–8.5 mm in long diameter; nearly egg-shaped subcircular, paucispiral, comprising around 3 whorls; nucleus subcentral.

Embryonic shells ( fig. 8S, W, Z , AC, AH, AK, AN): Measurements and counts shown in table 2 and supplementary table S1 . Shell globose; suture prominently depressed by discrepancy in adjacent whorls; nodes remarkable, on central part of whorls; keels weak, on lower part of whorls; shell colored black background or beige background with 3 brown or black bands on upper and lower part of each whorl and on basal part of shell.

Radulae ( fig. 12A–G ): Taenioglossa consisting of rachidian in single, lateral teeth, interior and exterior marginal teeth in double row. Rachidian roughly triangular, with large central denticle and 2–3 minor pointed triangular cusps on each side. Lateral teeth with large central denticle, 2–3 inner and outer pointed cusps. Central denticle tip of rachidian and lateral teeth mostly flat, rarely pointed; central denticle of rachidian approximately regular triangular, about 2.5 to 6.0 times longer than other triangular cusps; central denticle of lateral teeth irregular triangular, about 1.5 to 4.0 times longer than other triangular cusps. Interior and exterior marginal teeth spoon-shaped, with 4–6 rounded denticles.

Reproductive organs: Female: Long narrow oviduct, entering near seminal receptacle with long protrusions. Ventral edge of spermatophore bursa with curved sperm gutter, extending toward mantle cavity. Brood pouch on dorsal side of spermatophore bursa, inflated dorsally, separated into many cells, including eggs and embryos; eggs and embryos radially developing from base of brood pouch near seminal receptacle and embryos in anterior or dorsal cells more developed.

Male: Gonad consisting of testes, vas deferens, and prostate without penis. Posterior ventral part of inflated prostate with deep groove, forming U-shape in transverse section. Anterior prostate narrowly opening to mantle cavity.

Distribution and ecology: Semisulcospira niponica is one of the most widespread species in Lake Biwa ( Watanabe & Nishino, 1995; fig. 5b, S . (B.) niponica nodose). The species was discovered in eight localities in this study and is most widely distributed in the S. niponica -group ( fig. 1 ). Semisulcospira niponica mainly inhabits coastal shallow rocky areas and on concrete blocks around harbours at 0–1 m, while it is rarely found on small rocks in shallow sandy areas (e.g., Kitakomatsu Beach and Iso). This species was found with S. watanabei at Kitakomatsu Port and occurred with other Lake Biwa species: S. habei at Oura Port, Nagahama Port, Kitakomatsu Beach, Otsu Port; S. dilatata Watanabe & Nishino, 1995 at Iso; S. decipiens at Otsu Port.

Remarks: One of paralectotypes of S. niponica (NHM 1875.11.24.11/2) was identified as S. decipiens by the small SA and shell surface with longitudinal ribs and spiral cords following Davis (1969) and Watanabe and Nishino (1995). The other paralectotype (NHM 1875.11.24.11/3) was similar to S. habei in the middle SA and had a moderately convex shell with shell surface sculptures. A note “+ v. minor ” was added to the label of the type lot ( fig. 8F ). As Urabe (2007) discussed the name-bearing types of S. niponica cannot be a type specimen of S. niponica var. minor ( Brot, 1883) . The taxonomic account of the latter species was established based on specimens collected from Taiwan. The three species included in the type lot of S. niponica are indigenous to Lake Biwa.

Semisulcospira niponica resembles S. watanabei sp. nov. in shell outline shape and outer lip of the aperture, which hardly undulates. However, the former species tends to possess granulated longitudinal ribs on the shell surface, and this tendency is stronger where both species coexist ( fig. 7 ). Semisulcospira niponica also represents a greater value of BWL, RN, SA, and SHE than S. watanabei sp. nov. Semisulcospira niponica can be discriminated from other congeners with its blackish triangular adult shell and few longitudinal ribs and spiral cords, and globose embryonic shells with several brown bands (supplementary fig. S1 ).

Figures

FIGURE 1 Map of Lake Biwa (A) and Oura Bay (B) showing 15 sampling localities:blue, Semisulcospira niponica; green, S.fuscata; purple, S.watanabei sp.nov.; red, S.nakanoi sp.nov.; orange, S.salebrosa sp.nov; black, putative hybrid between S.fuscata and S.watanabei sp.nov.

FIGURE 2 Schematic drawings representing shell measurements of Semisulcospira species in this study. A, Spire angle (SA) and aperture swell length (ASL) of adult shell. B–D, Criteria for types of sculptures

FIGURE 3 Results of principal components analysis based on 738 SNPs conducted for five Semisulcospira species. A, Principal component (PC) 1 vs PC2.B, PC2 vs PC3. C, PC3 vs PC4. D, PC4 vs PC5

FIGURE 4 Results of ADMIXTURE analysis based on 738 SNPs conducted for five Semisulcospira species.Bar colours of the species in K = 5 correspond to the colour coding in fig.3

FIGURE 5 Phylogenetic relationships of five Semisulcospira species estimated by the Neighbor-Net reconstructed based on uncorrected p-distances of 738 SNPs

FIGURE 6 Map of Lake Biwa indicating geographical variation in the frequency of sculpture types in the adult females of five Semisulcospira species.Colours of locality names correspond to the colour coding in fig.1

FIGURE 7 Results of Random Forest analyses conducted for five Semisulcospira species. Euclidean distances generated from proximities among individuals are plotted. A, Female.B, Male

FIGURE 8 Shells of Semisulcospira niponica and S. fuscata. A–F,Lectotype (A–C), NHM 1875.11.24.11/1, paralectotypes (D, E), NHM 1875.11.24.11/2,1875.11.24.11/3 and the label of S.niponica (F). G–K.Holotype of S.biwae, SMF 291511.L–P, Holotype of S.fuscata, LBM 13-1. Q–S, S.niponica from Oura Port, KUZ Z4091.T–W, S.niponica from Nagahama Port, KUZ Z4093.X–Z, S.niponica from Iso, KUZ Z4095. AA–AC, S.niponica from Kitakomatsu Port, KUZ Z4097. AD–AE, S.niponica from Kitakomatsu Beach, KUZ Z4098.AF–AH, S. niponica from Katata Port, KUZ Z4099.AI–AK, S. niponica from Otsu Port, KUZ Z3766.AL–AN, S.niponica from Nango, KUZ Z4101.AO–AQ, S.fuscata from Lake Yogo, KUZ Z4103. AR–AT, S.fuscata from Oura, KUZ Z4105.AU–AX, S.fuscata from Nihonmatsu, KUZ Z4107.AY–BA, Putative hybrid between S.fuscata and S.watanabei sp. nov.from Nihonmatsu, KUZ Z4140.A–E, G–I, L–N, Q, T, X, AA, AD, AF, AI, AL, AO, AR, AU, AY, Adult shell.R, U, Y, AB, AE, AG, AJ, AM, AP, AS, AW, AZ, Operculum.S, W, Z, AC, AH, AK, AN, AQ, AT, AX, BA, Embryonic shell. F,J, K, O, P, Label. Scale bars: 10 mm (A–E, G–I, L–N,Q, R, T,U, X,Y,AA, AB, AD–AG, AI, AJ, AL, AM, AO, AP, AR, AS, AU, AW, AY, AZ), 1 mm (S, W,Z, AC, AH, AK, AN, AQ, AT, AX, BA). Newly collected specimens (Q–BA) were treated with 3% sodium hypochlorite

FIGURE 9 Shells of Semisulcospira watanabei sp. nov.A–G, Holotype, KUZ Z4109. H–J, Paratype, KUZ Z4110.K–L, Paratype, KUZ Z4114.M–N.Specimen from Oura, KUZ Z4117.O–Q, Specimen from Nihonmatsu, KUZ Z4118.R–T, Specimen from Horikiri Port, KUZ Z4120.A–C, H, K, M, O, R, Adult shell.A–C, H, O, R, Female.K, Male. M, Juvenile.D, I, L, N, P, S, Operculum. E–G, J, Q,T, Embryonic shell. Scale bars: 10mm (A–D, H–I, K–L, M–N, O–P, R–S), 1 mm (E–G, J, Q, T). All specimens were treated with 3% sodium hypochlorite

FIGURE 10 Shells of Semisulcospira nakanoi sp. nov. A–G,Holotype, KUZ Z4122.H–J, Paratype, KUZ Z4125. K–L, Paratype, KUZ Z4126.M–Q, Specimens from Onoe Port, KUZ Z4129, Z4130.A–C, H, K, M, P, Adult shell. A–C, H, M, Female.K, P,Male.D, I, L, N, Q, Operculum.E–G, J, O, Embryonic shell.Scale bars: 10 mm (A–D, H–I, K–L, M–N, P–Q), 1 mm (E–G, J, O). All specimens were treated with 3% sodium hypochlorite

FIGURE 12 Radulae of Semisulcospira species.A–G, Semisulcospira niponica: A, Oura Port, KUZ Z4091; B, Nagahama Port, KUZ Z4093; C, Iso, KUZ Z4095; D, Kitakomatsu Port, KUZ Z4097; E, Katata Port, KUZ Z4099; F, Otsu Port, KUZ Z4101; G, Nango, KUZ Z4103.H–J, Semisulcospira fuscata: H, Lake Yogo, KUZ Z4103; I, Oura, KUZ Z4105; J, Nihonmatsu, KUZ Z4107.K–L, Semisulcospira watanabei sp. nov.:K, Kitakomatsu Port, KUZ Z4115;L, Horikiri Port, KUZ Z4120.M–N, Semisulcospira nakanoi sp. nov.: M, Onoe Port, KUZ Z4129;N, Chikubu-shima Island, KUZ Z4127.O–P, Semisulcospira salebrosa sp. nov.:O, Take-shima Island, KUZ Z4138;P, Shiraishi-jima Island, KUZ Z4136.Scale bars:100 Μm