Rhiostoma Benson, 1860

Tongkerd, Piyoros, Tumpeesuwan, Sakboworn, Inkhavilay, Khamla, Prasankok, Pongpun, Jeratthitikul, Ekgachai, Panha, Somsak & Sutcharit, Chirasak, 2023, Systematic revision of the snorkel snail genus Rhiostoma Benson, 1860 (Gastropoda, Caenogastropoda, Cyclophoridae) with descriptions of new species, ZooKeys 1142, pp. 1-144 : 1

Genus Rhiostoma Benson, 1860

Rhiostoma Benson, 1860: 96. Pfeiffer 1862b: 45, 46. Blanford 1864: 451. Pfeiffer 1865: 38. Martens 1867: 63. Kobelt and Möllendorff 1897: 115. Kobelt 1902: 176. Kobelt 1911: 754, 755. Gude 1921: 127, 128. Thiele 1929: 100. Wenz 1938: 462. Egorov 2009: 36, 37. Preece et al. 2022: 247.

Pterocyclus [sic] ( Rhiostoma )- Nevill 1878: 262. Fischer 1885: 745.

Type species.

Rhiostoma haughtoni Benson, 1860 by original designation in Benson (1860: 96).

Diagnosis.

Shell small to large, and heliciform to depressed. Detached whorl absent or with short to long detached whorl, curved and descending. Breathing device prominently present with various types (Fig. 1B ). Peristome double; lip thickened and expanded. Shell colour varying from uniform colour to zigzag pattern. Operculum calcareous, cup-shaped, and anticlockwise multispiral with elevated lamella (Figs 2B , 5 ).

Description.

Shell. Shell flattened to heliciform, thick to thin, and widely umbilicate, showing all preceding whorls (Figs 1 , 2 ). Detached whorl absent or present and short to long and/or curved and/or descending. Periostracum thick or thin corneous to brownish and transparent. Shell colour uniformly brownish to purplish and/or with brownish variegated streaks or zigzag patterns. Peristome continuous, double, multi-layered, or sometimes with inconspicuous boundary, and circular; lip thickened and/or slightly expanded. Breathing device located at upper junction of peristome and with form varying by species, i.e., knob, notch, canal, incomplete tube, complete tube, or tubular. Operculum calcareous, cup-shaped, thickened, concave, and inside, anticlockwise multispiral with elevated lamella, lateral fringe straight, and diameter considerably smaller than aperture width.

Radula. Typical taenioglossate teeth arranged in inverted V-shaped row, each transverse row containing 7 teeth (2-1-1-1-2). Central tooth large, symmetrical, and triangular, and with 2-4 well-developed cusps on each side. Lateral and marginal teeth slightly slender, inclining toward central tooth, and with three or four cusps. Shape of teeth and number of cusps on each tooth vary by species.

External features. Examination of many living snails indicates that the body colour varies from blackish to whitish, with or without brown to grey mottled spots spread over the body. This vast variation was present both within and between populations and depended on the age of snails. The internal reproductive organs and the external penis appeared very similar and provided no informative characters for distinguishing species. Therefore, the type species R. haughtoni (Figs 6 , 7 ) and R. housei (Fig. 20 ) were selected as representative species for detailing the external and internal anatomical characters of the genus.

Animal exhibits dark brown to blackish patches and/or mottles scattered on blackish, brownish, or greyish body, faded near mantle cavity (Figs 6 , 20 ). Head with a pair of long cephalic tentacles (ct), each one with a dark eyespot (es) at the outer base; snout (sn) broad and furrowed. The anterior body is short, and on the right side has a genital groove running downwards from the anterior end of the pallial cavity. Posterior body long; foot broad, with longitudinal pedal groove, and operculum (op) attached dorsally to posterior body. Animals are dioecious, the female possessing only a vaginal groove (vg) on the right side (Figs 6C , 20A ); the male has both a long conical external penis (p) on the right side below cephalic tentacle and a sperm groove (sg) passing to tip of the external penis (Figs 6A , 20B ).

Internal features. Kidney (kd) brownish, triangular (Figs 6B , 7A ). Heart (h) located on the left side of the kidney (on the right in the figure), pericardium thin, atrium slightly larger than ventricle. Lung cavity (lc) with large vein (v) and reticulated vessels. Rectum (re) large, bonded with genital apparatus (male prostate gland or female uterus), containing elliptical-shaped faeces (fc) and anteriorly tapering to the anus (an), which opens near mantle collar edge. Ctenidium and osphradium absent. Mantle collar (mc) smooth and slightly thickened. Columellar muscle (cm) broad and thick (Fig. 6A, C ).

Reproductive organs. Testis (te) with branched tubules, bright orange, and occupying ~ 2-3 whorls from the apex (Fig. 6A ). Vas deferens (vd) a thin, straight tube attached to prostate gland at ~ 2/3 of its length proximal to genital opening. Prostate gland (pg) large, long, curved, pale yellowish in colour, and anterior end with a genital opening (go) located close to mantle collar (Fig. 7B ). Sperm groove (sg) narrow, distinct, and connecting to genital opening on right side of snail with tip of penis. External penis (p) with long cylindrical shape but pointed tip and situated posteriorly below cephalic tentacles (Fig. 6A ).

Ovary (ov) bright orange with multilobulated glands embedded within brownish digestive glands (Fig. 6C ). Oviduct (od) a thin tube connecting ovary and uterus near base of seminal receptacle. Bursa copulatrix (bc) peanut-shaped, creamy to whitish in colour, and ~ 1/2 the length of uterus. Seminal receptacle (sr) small, pale orange, and located at the posterior end of the uterus. Uterus (ut) large, long, curved; posterior end rounded, and anterior end tapered, with a genital opening (Fig. 7C ).

Spermatophores of two species, namely R. samuiense and R. furfurosum sp. nov., were examined. They appeared whitish, with a coiled cylindrical shape, and ~ 10 mm long (Fig. 7D ). Anterior part slightly flat with compressed sperm sac, and bearing keels on both sides (see cross-section). The middle part has a swollen sperm sac (rounded in cross-section) and one prominent keel. Posterior part tapered, with a pointed end, and tiny sperm sac.

Distribution.

The genus Rhiostoma seems to have a limited distribution, occurring only in mainland Southeast Asia, including Cambodia, Laos, Myanmar, Thailand, Vietnam, peninsular Malaysia, and southern China ( Benson 1860; Möllendorff 1894; Ancey 1898; Blanford 1902; Kobelt 1902, 1911-1914; Bavay and Dautzenberg 1909a, b; Gude 1921; Tomlin 1932, 1938; Salisbury 1949; Solem 1966). A few shells from Xishuangbanna, Yunnan Province, China, were collected and examined in this study. Within the overall limits of its total geographical distribution (Table 2 ), Rhiostoma occupies a more restricted area than other cyclophorids such as Pterocyclos and Cyclotus . The boundary of the genus is demarcated in the west with the endemic genera Spiraculum and Theobaldius Nevill, 1878 of South Asia; in the north with Ptychopoma and Scabrina Blandford, 1863 of China ( Yen 1939); and in the south, with the dominant and closely related Pterocyclos in Greater Sunda Islands and the Philippines.

Remarks.

The reproductive anatomy of the Cyclophoroidea is little known and reports are scattered (i.e., Sarasin and Sarasin 1899; Weber 1925; Tielecke 1940; Jonges 1980; Kongim et al. 2013a; Sutcharit et al. 2014; Páll-Gergely et al. 2020b). A relatively comprehensive review of genitalic morphology of various cyclophorid genera was published by Tielecke (1940), and includes a brief note (without figures) of only one pterocyclinid species. Tumpeesuwan (2001) examined the reproductive anatomy of various Rhiostoma species and reported that it is relatively conserved, and that the only distinction observed was in the shape of bursa copulatrix in females. The length of the male genital opening of the Rhiostoma tended to be longer than the Pterocyclos . In addition, a well-developed seminal vesicle in male Cyclophorus seems to be the main character distinguishing it from the Rhiostoma and Pterocyclos , which do not have this character (see Weber 1925; Tumpeesuwan 2001). However, the taxonomic importance of the reproductive anatomical characters needs to be verified by further observations from various taxa. Nevertheless, the dissection of cyclophoroidian reproductive organs is difficult due to the indistinct organ boundary and watery or soft texture present in fresh specimens, whereas the ethanol-preserved specimens are far more fragile (S. Panha pers. obs.; Páll-Gergely et al. 2020b).

The following species groupings are mainly based on the similarity in length of their detached whorl and in the shape of their breathing devices (Fig. 8 ). This informal subdivision is composed of four groups, and may assist in species identifications. No formal names or descriptions are provided, only the general characteristics of each group are provided.

Group I: Rhiostoma haughtoni group. This group can be recognised by a short to long detached whorl, and knob- or notch-shaped breathing device (Fig. 1B ). This group is composed of three species: R. haughtoni Benson, 1860; R. samuiense Tomlin, 1932; and R. rhothonotaphrosa Tongkerd & Panha, sp. nov.

Group II: Rhiostoma housei group. Usually having a medium to long detached whorl, and breathing device as an incomplete tube or tubular (Fig. 1B ). This group contains ten species: R. housei (Haines, 1855); R. hainesi Pfeiffer, 1862; R. simplicilabre Pfeiffer, 1862; R. marioni (Ancey, 1898); R. dalyi Blanford, 1902; R. jalorensis Sykes, 1903; R. thachi Huber in Thach, 2018; R. ebenozostera Tongkerd & Panha, sp. nov.; R. lannaense Tongkerd & Tumpeesuwan, sp. nov.; and R. tigrina Tongkerd & Tumpeesuwan, sp. nov.

Group III: Rhiostoma asiphon group. This group is characterised by a short detached whorl, and breathing device as an incomplete tube or notch (Fig. 1B ). There are seven species belonging to this group: R. asiphon Möllendorff, 1893; R. strubelli Möllendorff, 1899; R. abletti Thach, 2016; R. anceyi Tongkerd & Inkhavilay, sp. nov.; R. breviocollar Tongkerd & Tumpeesuwan, sp. nov.; R. furfurosum Tongkerd & Panha, sp. nov.; and R. platymorpha Tongkerd & Tumpeesuwan, sp. nov.

Group IV: Rhiostoma morleti group. The heliciform or flattened shell is generally without a detached whorl (rarely very short) and with a notch- or canal-shaped breathing device. However, some species have a wide canal-shaped breathing device, in which the columellar side is completely attached to the preceding whorl, causing the whorl to appear attached. There are seven species belonging to this group: R. cochinchinensis (Pfeiffer, 1857); R. cambodjense (Morelet, 1875); R. morleti Dautzenberg & Fischer, 1906; R. prestoni Bavay & Dautzenberg, 1909; R. cheliopegma Tongkerd & Tumpeesuwan, sp. nov.; R. gnomus Tongkerd & Panha, sp. nov.; and R. laosense Tongkerd & Inkhavilay, sp. nov.

Figures

Figure 1. Schematic of shell morphology and terminology of the Rhiostoma A apertural view with shell terminology and measurements of coiled-whorl height B breathing device types as recognised in this revision: knob, incomplete tube, notch, canal and tubular C inner peristomal lip variation as recognised in this revision: incision and hole.

Figure 2. Schematic of shell morphology and terminology of the Rhiostoma A apical view with shell terminology and measurements of coiled-whorl width and detached-whorl length B operculum showing side and cross-section views C apertural views showing various shell shapes as recognised in this revision: flattened, discoidal, sub-discoidal and heliciform.

Figure 5. Comparison of breathing device and operculum characteristics among the five genera that closely resemble Rhiostoma. The specimens and opercula represented herein are the type specimen or topotype of the respective type species of each genus; Pterocyclos: P. rupestris Benson, 1832 (lectotype UMZC I. 102070, no locality data), Spiraculum: S. hispidum Pearson, 1833 (specimen NHMUK 1906.4.4.72, from Khasi, Teria Ghat), Rhiostoma: R. haughtoni Benson, 1860 (syntype UMZC I. 103445, from Moulmein), Cyclotus: C. variegatus Pearson, 1833 (specimen NHMUK 1896.6.7.34 - 35, from Palawan), Opisthoporus: Cyclostoma taylorianum Pfeiffer, 1851 = junior synonym of Pterocyclos biciliatum Mousson, 1849 (specimen NHMUK 20210200 for shell, from Basan, Sarawak) and Pterocyclos tener Menke, 1856 (NHMUK ex. Cuming collection for operculum, from Cochin China), and Ptychopoma: Cyclophorus chinensis Moellendorff, 1875 (lectotype SMF 39415, from Lushan bei Kiukiang, China). Red arrows indicate the expansion of outer lip at upper junction of the peristome. Blue arrows indicate breathing tubes (apertural tube in Rhiostoma and sutural tubes in Spiraculum and Opisthoporus).

Figure 6. General anatomy of Rhiostoma haughtoni specimen CUMZ 10048 / 2 from Dhammatat Cave, Myanmar A right side of male testis and external penis and with enlargement of cephalic area B left side of male shows lung cavity and stomach C right side of female shows ovary and vaginal groove, and with enlargement of cephalic area. Abbreviations: bc, bursa copulatrix; cm, columellar muscle; ct, cephalic tentacle; dg, digestive gland; es, eyespot; f, foot; h, heart; kd, kidney; lc, lung cavity; mc, mantle collar; od, oviduct; op, operculum; ov, ovary; p, external penis; pg, prostate gland; sg, sperm groove; sn, snout; te, testis; ut, uterus; vd, vas deferens; vg, vaginal groove.

Figure 7. A-C Internal anatomy of Rhiostoma housei specimen CUMZ 3982 from Tham Sriwilai, Saraburi, A inside view of lung cavity shows an arrangement of the kidney, circulatory system and the terminal part of the digestive tract B male genitalia and C female genitalia D spermatophore of Rhiostoma samuiense specimen CUMZ 4713 from Kanchanadit, Surat Thani with its cross sections showing spermatophore shape in each position. Abbreviations: an, anus; bc, bursa copulatrix; fc, faeces; go, genital opening; h, heart; kd, kidney; mc, mantle collar; od, oviduct; pg, prostate gland; re, rectum; sr, seminal receptacle; ut, uterus; v, vein; vd, vas deferens.

Figure 8. Box-and-whisker plots showing variation in the ratio of detached-whorl width to aperture width in some Rhiostoma species. Boxes show the median, 25 th and 75 th percentiles, whiskers show minimum and maximum observations, and circles show outliers. See text for the explanation of species grouping. 1 = topotype of Rhiostoma samuiense s. s. from Samui Island. 2 = topotype of " Rhiostoma chupingense " from Bukit Chuping, Malaysia. 3 = specimens of " proboscis " morphotype from Surat Thani, Thailand.

Figure 20. Drawing of general anatomy of Rhiostoma housei specimen CUMZ 3982 from Saraburi Province, Thailand. A female B male. Abbreviations: bc, bursa copulatrix;; cm, columellar muscle; ct, cephalic tentacle; dg, digestive gland; es, eyespot; f, foot; fc, faeces; int, intestine; lc, lung cavity; mc, mantle collar; od, oviduct; op, operculum; ov, ovary; p, external penis; pg, prostate gland; sg, sperm groove; sn, snout; te, testis; ut, uterus; vd, vas deferens; vg, vaginal groove.