Research Article
Print
Research Article
A revision of Bithyniidae (Mollusca, Gastropoda) from the Inle Lake Basin, Myanmar
expand article infoLe-Jia Zhang‡§|, Shu-Sen Shu‡§|, Xin-Yuan Song‡§|, Nay Htet Naing‡§|, Thaung Naing Oo, Xiao-Yong Chen‡§|
‡ Southeast Asia Biodiversity Research Institute, Chinese Academy of Sciences, Nay Pyi Taw, Myanmar
§ Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China
| Yunnan International Joint Laboratory of Southeast Asia Biodiversity Conservation, Mengla, China
¶ Forest Department, Ministry of Natural Resources and Environmental Conservation, Nay Pyi Taw, Myanmar

Corresponding author: Xiao-Yong Chen ( chenxy@mail.kiz.ac.cn )

Academic editor: Frank Köhler
© 2025 Le-Jia Zhang, Shu-Sen Shu, Xin-Yuan Song, Nay Htet Naing, Thaung Naing Oo, Xiao-Yong Chen.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Zhang L-J, Shu S-S, Song X-Y, Naing NH, Oo TN, Chen X-Y (2025) A revision of Bithyniidae (Mollusca, Gastropoda) from the Inle Lake Basin, Myanmar. Zoosystematics and Evolution 101(2): 643-660. https://doi.org/10.3897/zse.101.143936
ZooBank: urn:lsid:zoobank.org:pub:C0F8018F-646D-491E-A749-715896CBF713
Open Access

Abstract

Inle Lake, located on the Shan Plateau of Myanmar, is the only ancient lake on the Indochinese Peninsula and a biodiversity hotspot of freshwater fauna with high diversity and endemism, including molluscs. However, recent research on its biodiversity remains limited. Based on morphological, anatomical, and molecular studies, we systematically revise the freshwater snails of the family Bithyniidae from the Inle Lake basin. We provide an updated re-description of four bithyniid species within three genera from the Inle Lake basin, including one new record, Digoniostoma iravadica comb. nov. The endemic genus Parabithynia syn. nov. with one endemic species of Inle Lake, Hydrobioides physcus comb. rev., is considered a synonym of Hydrobioides. Gabbia nana comb. nov. is assigned to Gabbia based on shell morphology and molecular phylogeny. Hydrobioides dautzenbergi stat. rev. from Thailand is recognised as a valid species rather than a synonym of Hydrobioides nassa, which is endemic to Shan State of Myanmar. There are altogether seven bithyniid species recorded from the Inle Lake basin and surrounding area, including four endemic species.

Key Words

Ancient lake, bithyniid snail, phylogeny, radula, Shan State, taxonomy

Introduction

Inle Lake, located on the southern Shan Plateau, is the second largest lake in Myanmar and the only ancient lake on the Indochinese Peninsula, which was formed around 1.5 million years ago; despite its relatively small size (covering about 116 square kilometres) and shallow depth (averaging only two meters), Inle Lake supports remarkable freshwater biodiversity and endemism, similar to other ancient lakes such as Baikal, Tanganyika, and Biwa (Hampton et al. 2018). There are 13 families and 28 genera of fish native to the Inle Lake basin, including 15 endemic species (Kano et al. 2016); 36 species of freshwater molluscs, including 18 endemic species, have been recorded from the Inle Lake basin (Annandale 1918; Annandale and Rao 1925).

Bithyniidae is one of the most common families of freshwater snails in the Inle Lake basin. This diverse and common family of freshwater snails is widely distributed across Africa, Eurasia, and Australia, inhabiting rivers, wetlands, ponds, and lakes. It also includes Helicostoa, the only known group of obligate sessile freshwater snails (Zhang et al. 2024a). Annandale (1918) recorded and described altogether six bithyniid species from the Inle Lake basin and surrounding areas: Hydrobioides turrita (Blanford, 1869) (subfossils from Heho), Hydrobioides nassa (Theobald, 1866), Parabithynia physcus (Annandale, 1918), Hydrobioides avarix Annandale, 1918, Hydrobioides nana Annandale, 1918, and Gabbia alticola (Annandale, 1918). Of these, four species (P. physcus, H. avarix, H. nana, G. alticola) and one genus, Parabithynia Pilsbry, 1928, were considered endemic to the Inle Lake basin. Sawada (2022) revisited Annandale’s historical malacological collection from Inle Lake, kept in the Kyoto University Museum, including the dry-shell specimens of three bithyniid species (H. nassa, P. physcus, G. alticola). However, since the works of Annandale and Rao (Annandale and Rao 1925; Rao 1928), there have been almost no published modern studies and collected records of freshwater snails from the Inle Lake basin or even Shan State.

In July 2024, we conducted comprehensive fieldwork for freshwater fauna in the Inle Lake basin, collecting a diverse assemblage of freshwater molluscs, including bithyniid snails. The present study aims to provide a systematic revision and re-description of bithyniid snails from the Inle Lake basin based on shell morphology, anatomy, and molecular study, after a nearly century-long gap in research on this biodiversity hotspot of freshwater fauna.

Materials and methods

Materials

Seven type specimens of three species (one for Hydrobioides nassa, three for Hydrobioides physcus, three for Hydrobioides avarix) were examined from the Natural History Museum, London (NHMUK). Fieldwork was conducted in the Inle Lake basin from 1 Jul. 2024 to 11 Jul. 2024. The samples of bithyniid snails were collected in five localities (Fig. 1B); the types of habitats included lake, rice field, shallow pond, wetland, and river (details see in Systematic Descriptions). The samples were fixed using 75% ethanol and then preserved in analytical pure ethanol. Additional materials for comparison were collected in Mandalay Region and mountains of Kalaw Township (Shan State) (details see in Systematic descriptions: Hydrobioides nassa, Digoniostoma iravadica). The newly collected specimens are deposited in the Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming (KIZ), and the Southeast Asia Biodiversity Research Institute, Chinese Academy of Sciences, Yezin, Nay Pyi Taw (SEABRI).

Figure 1. 

Collecting sites of bithyniid snails in the Inle Lake basin. A. A map of Myanmar showing the location of Shan State and Inle Lake; B. A red dot (site a to e) showing the collecting sites in the Inle Lake basin, an altitude map modified based on the resources from https://topographic-map.com (license offered by the website builder Guillaume VK); C. Habitat at the site b, Inle Lake; D. Habitat at the site e, rice field; E. Habitat at the site a, shallow pond.

Examination of morphology

The shell height (H) and width (W) were measured with a calliper to a precision of 0.01 mm. The specimens were photographed in a consistent orientation using focus stacking methods with a Nikon® Z5 camera and a Nikon® Nikkor Z MC 105mm f/2.8 VR lens. S. Zerene Stacker 1.04 software was used to do focus stacking. Radulae were extracted through dissection; radulae were cleaned by boiling in 1% NaOH solution for half an hour and rinsed with distilled water. Radulae and operculum were coated with gold before scanning electron microscopy with a Zeiss® Sigma 300 scanning electronic microscope. The male genital structure of the snail was examined during dissection and photographed under a stereomicroscope. The terms used for describing the operculum are according to Zhang and von Rintelen (2021). The newly collected specimens were identified based on the description of shell, radula, male genitalia, and collecting locality provided by Annandale (1918), Rao (1989), and comparisons to type specimens. Abbreviations of radula: ct–central teeth; lt–lateral teeth; imt–inner marginal teeth; omt–outer marginal teeth.

Molecular methods

DNA was extracted from 10–20 mg of foot tissue of each snail using a mollusc-specific CTAB/chloroform 112 extraction protocol (Winnepenninckx et al. 1993). A fragment of the mitochondrial 16S gene was amplified through polymerase chain reaction (PCR) with the following primer pairs: LCO1490, 5ʹ-GGTCAACAAATCATAAAGATATTGG-3ʹ, and COX-B7R, 5ʹ-ACCACCAGCTGGA TCAAAAA-3ʹ (Schultheiß et al. 2011) for COI; 16Sar-L, 5ʹ-CGCCTGTTTATCAAAAACAT-3ʹ, and 16Sbr-H, 5ʹ-CCGGTCTGAACTCAGATCACGT-3ʹ (Palumbi et al. 2002). PCR amplifications were conducted in volumes of 30 μL under the following cycling conditions: an initial denaturing step at 94 °C for 10 min, followed by 35 cycles of 94 °C for 1 min, 50 °C for 1 min (COI) or 52 °C for 30 s (for 16S), and 72 °C for 1 min, with a final extension step of 10 min at 72 °C. The purification and sequencing were conducted by Sangon Biotech.

Sequence and phylogenetic analyses

New sequences of four species have been uploaded to GenBank; 46 sequences of 25 bithyniid species were included in the present study (Suppl. material 1). Amnicola dalli (AY622435) of family Amnicolidae was selected as the outgroup based on Zhang et al. (2024b). Sequences were aligned using MUSCLE as implemented in Geneious (https://www.geneious.com). Genetic distances were calculated using MEGA X (Kumar et al. 2018). GTR+G was suggested as the best-fit model of sequence evolution for our dataset by means of the Akaike and Bayesian information criteria in MEGA X. A Bayesian inference (BI) analysis was performed with MrBayes 3.2.6 (Ronquist et al. 2012) as implemented in Geneious with four independent chains for 5,000,000 generations, sample freq = 1,000, burnin = 25%, and it was confirmed that convergence was reached based on the trace plots generated in Geneious Prime 2020. A maximum likelihood (ML) analysis was conducted with RAxML as implemented in Geneious, with support estimated by 1,000 bootstrap replicates (Kozlov et al. 2019).

Results

Molecular phylogeny

The molecular tree (Fig. 2) reveals that Hydrobioides is not a monophyletic group. Hydrobioides dautzenbergi is the sister group of a clade including species of Hydrobioides, Gabbia, and Digoniostoma. Hydrobioides nassa is the sister species of Hydrobioides physcus. Gabbia nana is a distinct species, clustered with Gabbia pygmaea. Digoniostoma is a highly supported monophyletic group, which is sister to genus Gabbia. Digoniostoma iravadica is a distinct species clustered with the clade including Digoniostoma funiculata, Digoniostoma siamensis siamensis, and Digoniostoma siamensis goniomphalos. Four subfamilies of Bithyniidae (Parafossarulinae, Bithyniinae, Helicostoinae, Mysorellinae) are generally supported by the tree. All the species from the Inle Lake basin belong to the subfamily Mysorellinae.

Figure 2. 

Bayesian inference phylogram based on partial COI and 16S sequences of the selected bithyniid snails, with an emphasis on species from the Inle Lake basin (red star). Numbers above branches are BI posterior probabilities, and numbers underneath branches are ML bootstrap values.

Systematic descriptions

Class Gastropoda Cuvier, 1795

Order Littorinimorpha Golikov & Starobogatov, 1975

Family Bithyniidae Gray, 1857

Subfamily Mysorellinae Annandale, 1920

Hydrobioides Nevill, 1885

Hydrobioides Nevill, 1885: 42.

Paranerita Annandale, 1920: 4.

Parabithynia Pilsbry, 1928, syn. nov.: 108.

Bithynia (Parabithynia) – Popova et al. 1970: 95.

Type species.

Fairbankia turrita Blanford, 1869 (original designation; Myanmar, Irrawaddy River, “Kyoukpong”).

Diagnosis.

Shell medium for the family, solid, aperture lip thickened, outer lip outward extended; penial appendix located in the central of penis, penial appendix slightly shorter than distal part of penis.

Remarks.

According to Molluscabase (2024a), there are six extant valid species assigned to this genus; five species are described from Myanmar, and one species is described from Laos. The type species of this genus is Hydrobioides turrita (Blanford, 1869) with high spiral whorls and an extremely outward extended outer lip (Fig. 3P); its type locality is “Kyoukpong” near the Irrawaddy River in Myanmar (probably referring to Kyouk Pon near Bagan in the Mandalay Region), and it was also collected from Heho near the Inle Lake basin as subfossils (Annandale 1918). However, this species has never been collected again since Annandale (1918). Based on shell characters of Hydrobioides turrita, we consider that the outward extended outer lip is the most important morphological diagnosis character for this genus. Hydrobioides nassa is always considered widely distributed in north to central Thailand, but we consider that the Thai population should be another species (see in remarks of Hydrobioides nassa). We consider that Parabithynia Pilsbry, 1928, should be a synonym of Hydrobioides (see in remarks of Hydrobioides physcus). The molecular study based on 16S and COI does not support Hydrobioides as a monophyletic group (Fig. 2). The taxonomy of this genus needs systematic revision.

Figure 3. 

Shell of Hydrobioides nassa (A–O) and Hydrobioides turrita (P). A–D. NHMUK.1888.12.4.845, Syntype of Bithinia nassa, from Natural History Museum (2014); E–H. KIZ.2400057, Kalaw; I–M, KIZ.2400054 (I–L), 2400055 (M), Inle Lake; N. “Hydrobioides nassa lacustris” from Annandale, 1918; O. “Hydrobioides nassa rivicola” from Annandale, 1918; P. “Bythinea(?) trrita” from Nevill (1881). Scale bars: 1 cm (A–I).

Hydrobioides nassa (Theobald, 1866)

Bithinia nassa Theobald, 1866: 275 (Myanmar, Shan State).

Hydrobioides nassa – Annandale, 1918: 118–120, pl. 13, figs 1–7, pl. 14, figs 4, 4a.

Hydrobioides nassa distoma Annandale, 1918 †: 120, pl. 13, fig. 1 (Myanmar, Shan States, Heho plain).

Hydrobioides nassa lacustris Annandale, 1918: 119, pl. 13, figs 4, 4a, 5, 5a, 7 (Myanmar, Shan States, Inle Lake).

Hydrobioides nassa rivicola Annandale, 1918: 119–120, pl. 13, figs 6, 6a (Myanmar, Shan States, small streams at Thamakan).

Diagnosis.

Shell medium, high spiral whorls, a varix near outer lip, outer lip outward extended.

Material examined.

• 1 syntype (preserved dry), Upper Salwin River, Purchase of W. Theobald, NHMUK.1888.12.4.845; 3 specimens (preserved in ethanol), Shan State, Taunggyi District, Taungpoetgyi, near Tone Lae, river near spring (Fig. 1B. c), 20°29'48.9"N, 96°50'17.5"E, 2 Jul. 2024, Le-Jia Zhang leg., KIZ.2400054–2400056 • 2 specimens (preserved in ethanol), Shan State, Taunggyi District, Nyaungshwe, Inle Lake, floating islands near Intha (Fig. 1B. b), 20°36'33.4"N, 96°54'53.8"E, 3 Jul. 2024, Le-Jia Zhang leg., KIZ.2400057–2400058 • 2 specimens (preserved in ethanol), Shan State, Taunggyi District, Kalaw, river near Nanthe’ Cafe Garden, 20°36'30.6"N, 96°33'55.3"E, 11 Jul. 2024, Le-Jia Zhang leg., KIZ.2400059–2400060.

Description.

Shell (Fig. 3) medium for the family (Table 1), thin but solid, conical, bright yellow or olive grey, with five whorls at adulthood; teleoconch relatively high, smooth, without shoulder, a weak to strong varix structure on the body whorl, close to or directly connected to the outer lip; aperture ovate, lip thickened, nearly half of shell in height, outer lip outward extended; umbilicus covered by inner lip completely.

Table 1.
Download as
CSV
XLSX

Shell measurements of bithyniid snails from the Inle Lake basin.

Species n H W AH W/H AH/H
Hydrobioides nassa 6 7.97 ± 0.76 (6.57–8.87) 5.23 ± 0.49 (4.3–5.69) 4.23 ± 0.35 (3.67–4.57) 0.66 ± 0.01 (0.64–0.69) 0.53 ± 0.03 (0.5–0.57)
Hydrobioides physcus 4 5.94 ± 0.27 (5.52–6.18) 5.19 ± 0.11 (5.08–5.36) 4.02 ± 0.20 (3.75–4.29) 0.88 ± 0.03 (0.84–0.92) 0.68 ± 0.03 (0.64–0.7)
Hydrobioides avarix 2 (6.57–6.7) (4.43–4.48) (3.42–3.48) (0.67) (0.52)
Gabbia nana 9 4.54 ± 0.38 (3.74–5.15) 3.44 ± 0.27 (2.87–3.77) 2.64 ± 0.20 (2.23–2.92) 0.76 ± 0.02 (0.73–0.79) 0.58 ± 0.02 (0.57–0.62)
Digoniostoma iravadica 6 12.06 ± 0.42 (11.42–12.65) 6.91 ± 0.22 (6.55–7.28) 6.22 ± 0.29 (5.82–6.65) 0.57 ± 0.02 (0.55–0.61) 0.52 ± 0.02 (0.48–0.53)

Operculum (Fig. 3E, 4A) calcium, ovate, thin, slightly smaller than aperture, transparent grey; exterior surface smooth, nucleus close to the inner opercular margin; interior surface with wide concentric veins on inner opercular region, nuclear region relatively small, with irregular veins.

Figure 4. 

SEM photo of the opercular inner surface of bithyniid snails from the Inle Lake basin. A. Hydrobioides nassa; B. Hydrobioides physcus; C. Gabbia nana; D. Digoniostoma iravadica. Scale bars: 1 mm.

Penis (Fig. 5A) with a grey penial appendix located in the central of penis, penial appendix slightly shorter than distal part of penis.

Figure 5. 

Male genitalia of bithyniid snails from the Inle Lake basin. A. Hydrobioides nassa; B. Hydrobioides physcus; C. Digoniostoma iravadica. P refers to penis; PA refers to penial appendix.

Radula (Fig. 6) taenioglossate (2 + 1 + 1 + 1 + 2); central tooth upper margin with one broad triangle central cusp and two to three small sharp cusps on either side, lateral margin each with two to three small sharp cusps; lateral tooth with one broad tongue-shape central cusp and three to four small sharp cusps; inner marginal tooth with 14 to 15 small cusps; outer marginal tooth with eight to nine small cusps.

Figure 6. 

SEM photo of the radula of Hydrobioides nassa.

Remarks.

This species can be easily distinguished from other bithyniid snails based on the varix structure near the outer lip. The location of varix can be relatively far from the outer lip (Fig. 3I–M), viz. “Hydrobioides nassa lacustris” (Fig. 3N), mostly found in Inle Lake; the varix also can be directly connected to the outer lip (Fig. 3E–H), viz. “Hydrobioides nassa rivicola” (Fig. 3O), mostly found in rivers. However, there is no clear boundary between these two morphotypes. The syntype is quite similar to the “lacustris “type but much bigger than the newly collected specimens (Fig. 3A–D). This species was considered widely distributed in north to central Thailand. However, “Hydrobioides nassa” from Thailand does not have an obvious varix and an extended outward outer lip, and the molecular analysis has confirmed that the Thailand species is distinct from Hydrobioides nassa from the type locality, Shan State of Myanmar (Fig. 2). Therefore, we consider that Hydrobioides dautzenbergi Walker, 1927, stat. rev. (type locality: Thailand, Chieng Mai) should be a valid species name for the “Hydrobioides nassa” from Thailand. Hydrobioides nassa is probably endemic to Shan State, Myanmar.

Habitat and distribution.

Rivers, ponds, wetlands, and lakes of Shan State, Myanmar.

Values are arithmetic means, standard deviations, maximum and minimum values (in brackets) of shell height (H), shell width (W), and aperture height (AH) of n measured specimens.

Hydrobioides physcus Annandale, 1918, comb. rev.

Hydrobioides physcus Annandale, 1918: 121–122, pl. 13, figs 8, 8a, 9, pl. 14, figs 5, 5a (Myanmar, Shan State, Inle Lake).

Hydrobioides (Paranerita) physcus –Annandale, 1920: 45.

Paranerita physcus – Annandale & Rao, 1925: 115.

Parabithynia physcus – Pilsbry, 1928: 108

Gabbia physcus – Subba Rao, 1989: 78, figs 127–129.

Diagnosis.

Shell medium, low spiral whorls, weak keel on shoulder, outer lip outward extended.

Material examined.

• 3 probable paratypes (preserved dry), Inle Lake, South Shan, Burma. “Ex. India Museum”, NHMUK.20060144; 2 specimens (preserved in ethanol), Shan State, Taunggyi District, Inn Paw Hkon, Inthein, riverbank under Inthein Bridge (Fig. 1B. d), 20°27'35.9"N, 96°50'32.6"E, 1 Jul. 2024, Le-Jia Zhang leg., KIZ.2400061–2400062 • 2 specimens (preserved in ethanol), Shan State, Taunggyi District, Nyaungshwe, Inle Lake, floating islands near Intha (Fig. 1B. c), 20°36'33.4"N, 96°54'53.8"E, 3 Jul. 2024, Le-Jia Zhang leg., KIZ.2400063–2400064.

Description.

Shell (Fig. 7) medium for the family (Table 1), relatively thick, solid, subglobose to globose, white or bright yellow to orange yellow, with four whorls at adulthood; teleoconch low, with a keel on shoulder, forming weak nodules on shoulder with vertical growth lines, two weak additional keels on body whorl; aperture ovate, lip thickened, always more than half of shell in height, outer lip outward extended; umbilicus covered by inner lip completely.

Figure 7. 

Shell of Hydrobioides physcus. A–C. KIZ.2400063, Inle Lake; D. KIZ.2400064, Inle Lake; E–F. KIZ.2400063, Inle Lake; G–I. KIZ.2400063, Inthein; J–K. Probable paratype, NHMUK.20060144, taken by Aimee McArdle, NHMUK Photographic Unit; L. Living animal in aquarium; M. Drawings of the type specimens from Annandale, 1918. Scale bars: 1 cm (A–I).

Operculum (Figs 7A, 4B) calcium, ovate, thin, slightly smaller than aperture, transparent grey; exterior surface smooth, nucleus close to the central of operculum; interior surface with relatively thin outer opercular region, narrow weak concentric veins on the margin of inner opercular region, nuclear region relatively large, with irregular veins and grains.

Penis (Fig. 5B) with a white penial appendix located in the central of penis, penial appendix slightly shorter than distal part of penis.

Radula (Fig. 8) taenioglossate; central tooth upper margin with one broad triangle central cusp and two to three small sharp cusps on either side, lateral margin each with two to three small sharp cusps; lateral tooth with one broad tongue-shape central cusp and two to three small sharp cusps; inner marginal tooth with 10 to 11 small cusps; outer marginal tooth with six small cusps.

Figure 8. 

SEM photo of the radula of Hydrobioides physcus.

Remarks.

This species can be easily distinguished from other bithyniid snails based on the thick subglobose to globose shell with keels and shoulder. It also can be distinguished from H. nassa based on opercular characters and less small cusps on inner and outer marginal teeth. This species is the type species and only extant species of genus Parabithynia Pilsbry, 1928, which is now endemic to Inle Lake. Several fossil species of this genus were reported from China and Russia (Popova 1981; Yu et al. 1978), but the assignment needs a revision. Our molecular study confirms that this species is the sister species of H. nassa, with a close genetic relationship (p distance of 16S: 4.3–4.5%). The similarity in shell (especially the extended outer lip), operculum, and male genital structure also supports that these two species should be placed in one genus. Therefore, we consider that Parabithynia is a synonym of Hydrobioides. Hydrobioides physcus comb. rev. should be re-assigned to its original genus.

Habitat and distribution.

Inle Lake and the big rivers connected to Inle Lake; swamps in Heho, Shan State, Myanmar.

Hydrobioides avarix Annandale, 1918

Hydrobioides avarix Annandale, 1918: pl. 14, figs 1, 2, 2a, 2b, 2c (Myanmar, Shan State, NW shore of Inle Lake, a stream near Fort Stedman, now Maing Thauk).

Material examined.

• 3 probable syntypes (preserved dry), Inle Lake, South Shan, Burma. “Ex. India Museum”, NHMUK.20060143.

Remarks.

We did not discover this species during our fieldwork and only examined three probable syntypes. The detailed descriptions of shell, operculum, radula, and male genitalia of this species have been given by Annandale (1918). This species can be distinguished from Hydrobioides nassa by more inflated whorls and a simple outer lip without the varix structure nearby. It can be distinguished from Gabbia nana comb. nov. based on a larger and thinner shell with less inflated whorls and an operculum, which is much smaller than the aperture. The validity and genus assignment of this species need further study based on fresh specimens.

Gabbia Tryon, 1865

Type species.

Gabbia australis Tryon, 1865 accepted as Gabbia vertiginosa (Frauenfeld, 1862) (type by monotypy; Australia, New South Wales).

Remarks.

This genus is a highly diverse genus with nearly 50 species. Most species were assigned to this genus only based on the morphology of a small globose shell with an inflated body whorl. The taxonomy of this genus needs a systematic revision using molecular methods, especially a large number of species from Australia (including the type species Gabbia vertiginosa).

Gabbia nana (Annandale 1918), comb. nov.

Hydrobioides nana Annandale, 1918: pl. 14, fig. 3 (Myanmar, Shan State, NW shore of Inle Lake, Fort Stedman, now Maing Thauk).

Diagnosis.

Shell small, transparent white to pale yellow, high spiral whorls, inflated body whorl.

Material examined.

• 10 specimens (preserved in ethanol), Shan State, Taunggyi District, Nampan, water in rice field (Fig. 1B. e), 20°28'02.6"N, 96°55'58.1"E, 5 Jul. 2024, Le-Jia Zhang leg., KIZ.2400065–2400075.

Description.

Shell (Fig. 9) small for the family (Table 1), thin but solid, subglobose, transparent white to pale yellow, with four to 4.5 whorls at adulthood; teleoconch relatively high, smooth, without shoulder, body whorl inflated; aperture ovate, lip slightly thickened, always more than half of shell in height; umbilicus covered by inner lip or with narrow slit.

Figure 9. 

Shell of Hydrobioides avarix. A–F. Probable syntypes, NHMUK 20060143, taken by Aimee McArdle, NHMUK Photographic Unit; G–H. Drawing of the type specimens of Hydrobioides avarix from Annandale, 1918. Scale bars: 1 cm (A–F).

Operculum (Figs 9A, F, 4C) calcium, ovate, thin, slightly bigger than aperture, transparent grey; exterior surface smooth, nucleus close to inner opercular margin; interior surface with weak concentric growth lines and small grains on inner opercular region.

No fresh male specimen discovered.

Radula (Fig. 10) taenioglossate; central tooth upper margin with one long triangle central cusp and three small sharp cusps on either side, lateral margin each with three small sharp cusps; lateral tooth with one long triangle central cusp and four small sharp cusps; inner marginal tooth with 16 to 17 small cusps; outer marginal tooth with nine small cusps.

Figure 10. 

Shell of Gabbia nana. A–D. KIZ. 2400065, Nampan; E. KIZ. 2400066, Nampan; F. KIZ. 2400067, Nampan; G. Living animal in aquarium; H. Drawing of the type specimens of Hydrobioides nana from Annandale, 1918. Scale bars: 1 cm (A–F).

Remarks.

This species is assigned to Gabbia based on its morphology of a small globose shell with an inflated body whorl and its close relationship with Gabbia pygmaea in the molecular phylogeny (Fig. 2). It cannot be assigned to Hydrobioides since this species lacks an outward extended outer lip. It can be distinguished from Gabbia pygmaea (Preston, 1908) (type locality: Myanmar, Thayet) based on its higher spiral whorls and white to pale yellow shell.

Habitat and distribution.

Only known from the wetlands and small creeks in the Inle Lake basin.

Digoniostoma Annandale, 1920

Digoniostoma Annandale, 1920 in Annandale & Seymour Sewell (1920): 103–104; Starobogatov, 1970: 26; Izzatullaev, 1982: 336–340; Rao, 1989: 79–80; Ng & Tan, 2024: 154–155.

Bithynia (Digoniostoma) – Brandt, 1974: 58; Ramakrishna, 2007: 118–122; Glöer & Bössneck, 2013: 137–156.

Bithynia – Molluscabase, 2024b: synonym.

Type species.

Paludina cerameopoma Benson, 1830 (original designation).

Diagnosis.

Shell large for the family, thin and fragile, inner lip straight, base of peristome angled, umbilicus open, usually with a keel around; penial appendix located close to the base of penis, penial appendix much shorter than distal part of penis.

Remarks.

This genus is always considered as a subgenus or even a synonym of Bithynia by some recent studies, e.g., Glöer and Bössneck (2013) and Molluscabase (2024b). However, the molecular study has confirmed that Digoniostoma from South and Southeast Asia is a distinct group and not closely related to Bithynia, mainly from Europe. Morphologically, this genus also can be easily distinguished from other bithyniid groups based on large shell with base of peristome angled and open umbilicus with a keel around. Molecular, morphological, and distributional evidence all support that Digoniostoma is a valid genus. There are 11 species and subspecies assigned to this genus based on molecular evidence and former morphological studies: Digoniostoma cerameopoma (Benson, 1830); Digoniostoma funiculata (Walker, 1927), stat. nov.; Digoniostoma kashmirense (G. Nevill, 1885); Digoniostoma lithoglyphoides Nesemann & Sharma, 2007; Digoniostoma oxiana Izzatullaev, 1982; Digoniostoma pulchella (Benson, 1836); Digoniostoma iravadica (Blanford, 1869); Digoniostoma siamensis siamensis (Lea, 1856), stat. nov.; Digoniostoma siamensis goniomphalos (Morelet, 1866) stat. nov.; Digoniostoma textum Annandale, 1921; Digoniostoma truncatum (Eydoux & Souleyet, 1852). The taxonomy of Digoniostoma species, especially the species from India, should be revised.

Digoniostoma iravadica (Blanford, 1869), comb. nov.

Bithynia iravadica Blanford, 1869: 446 (Myanmar, Mandalay, Ava, swamp, and river); Molluscabase, 2021: taxon inquirendum.

D. iravadica – Rao, 1989: no description or remarks, only figures with ambiguous genus assignment and species name, figs 122–123.

Diagnosis.

Shell big, thin, high spiral whorls, thin outer lip, base of peristome angled, umbilicus narrow and deep, penial appendix about one-third of distal part of penis in length.

Material examined.

• 7 specimens preserved in ethanol, Shan State, Taunggyi District, Shwenyaung, Taung Lay Lone, a shallow pond in the north of town (Fig. 1B. a), 20°44'56.7"N, 96°53'59.4"E, 6 Jul. 2024, Le-Jia Zhang leg., KIZ.2400076–2400082 • 1 dry shell specimen, Mandalay Region, Meiktila, Wundwin, Seywa, dry pond near road, 21°14'15.2"N, 95°50'27.7"E, 29 Jun. 2024, Le-Jia Zhang leg., KIZ.2400083.

Description.

Shell (Fig. 11) relatively large for the family (Table 1), thin and fragile, high conical, pale olive green to grey, with 5.5 whorls at adulthood; teleoconch high, relatively smooth but with very fine grid-like micro-structure, without shoulder; aperture ovate, nearly half of shell in height, outer lip thin, inner lip straight, base of peristome angled; umbilicus narrow and deep, always open obviously, with a keel around.

Figure 11. 

SEM photo of the radula of Gabbia nana.

Operculum (Figs 11A, G, 4A) calcium, ovate, thin, slightly smaller than aperture, transparent grey; exterior surface smooth, with obviously concentric growth lines, nucleus close to the inner opercular margin; interior surface with many vermicular veins covering most parts of inner opercular region, and a few concentric veins on the margin of inner opercular region.

Penis (Fig. 5C) with a white penial appendix located close to the base of penis, penial appendix about one-third of distal part of penis in length.

Radula (Fig. 12) taenioglossate; central tooth upper margin with one long triangle central cusp and four small sharp cusps on either side, lateral margin each with three small sharp cusps; lateral tooth with one long triangle central cusp and four small sharp cusps; inner marginal tooth with 10 to 11 small cusps; outer marginal tooth with 10 small cusps.

Figure 12. 

Shell of Digoniostoma iravadica. A–D. KIZ.2400076, Shwenyaung, dyed brown by the minerals; E–F. KIZ.2400077, Shwenyaung; G–J. KIZ.2400078, Shwenyaung; K. Micro-structure on shell surface; L–M. Figure from Rao (1989). Scale bars: 1 cm (A–J).

Remarks.

This species can be distinguished from other Digoniostoma species based on high spiral whorls, fine grid-like micro-structure shell surface, narrow umbilicus, and very long distal part of the penis. The molecular study also confirms the validity of this species. The radula of Digoniostoma iravadica has the central cusp with a different shape and a larger number of small sharp cusps on both the central tooth and the lateral tooth, compared to that of Hydrobioides species from Inle Lake.

Figure 13. 

SEM photo of the radula of Digoniostoma iravadica.

Habitat and distribution.

Rivers, swamps, and shallow ponds in central Myanmar (Mandalay, Meiktila, Taunggyi).

Discussion

Ancient lakes are widely recognised as important refuges and evolutionary centres for aquatic fauna. As the only ancient lake on the Indochinese Peninsula, Inle Lake supports a high diversity of bithyniid snails. The five bithyniid species examined in the present study are all endemic to Myanmar, with three species (Hydrobioides physcus, Hydrobioides avarix, and Gabbia nana) restricted to the Inle Lake basin and nearby region (Heho). We did not find two tiny bithyniid species endemic to the Inle Lake basin, viz. Hydrobioides avarix and Gabbia alticola (Annandale 1918). Based on the original description and the type specimens figured by Sawada (2022), we considered Gabbia alticola a valid endemic species. With altogether four endemic bithyniid species, the Inle Lake basin appears to have the highest known endemicity of Bithyniidae worldwide, surpassing Lake Skadar and Lake Trichonis of the Balkan Peninsula, each with three endemic bithyniid species (Glöer et al. 2007). In total, including the newly recorded Digoniostoma iravadica, seven bithyniid species have been recorded from the Inle Lake basin. Our study confirms the continued existence of four species and provides the first molecular-based revision of the bithyniid fauna from the Inle Lake basin.

Our multi-method study has significantly improved the taxonomy of bithyniid snails. Hydrobioides nassa has long been considered a common species in northern to central Thailand (Brandt 1974; Kulsantiwong et al. 2013; Bunchom et al. 2021). However, all previous studies did not compare the Thai population to the population from the type locality, Shan State of Myanmar. Our present study confirms that the true Hydrobioides nassa from Shan State can be clearly distinguished from the Thai “Hydrobioides nassa” based on shell morphology and molecular phylogeny. The molecular tree has revealed that the Thai “Hydrobioides nassa” is not even closely related to Hydrobioides nassa, and the sister species of Hydrobioides nassa is Hydrobioides physcus, endemic to Inle Lake. Therefore, we reintroduce the name Hydrobioides dautzenbergi for the Thai species, though its genus assignment requires further study due to the polyphyletic condition of Hydrobioides (Fig. 2). Genus Parabithynia with the type species Hydrobioides physcus is considered a synonym of Hydrobioides based on strong evidence of molecular study and morphology. Digoniostoma should be a valid genus based on molecular, morphological, and distributional evidence.

The present study on Bithyniidae represents the first part of our systematic survey and study of freshwater snails from the Inle Lake basin. As an important biodiversity hotspot of freshwater fauna, Inle Lake is increasingly threatened by human activities (Iwai et al. 2022). Further research on other freshwater snails from the Inle Lake region will enhance our understanding of the biodiversity and evolution of freshwater snails in this ancient plateau lake and provide valuable insights for the conservation of Inle Lake.

Acknowledgements

We thank Daw Khin Pa Pa Shwe (Forestry Research Institute, Nay Pyi Taw, Myanmar), Thinnsu Tin (SEABRI), Phyo Htet Zaw (SEABRI), Nyein Chan Kyaw for their help in conducting fieldwork and collecting specimens, Cai-Xin Liu (SEABRI) for helping in taking photos, Jon Ablett (NHMUK), Andreia Salvador (NHMUK), and Aimee McArdle (NHMUK) for helping in examining and taking photos of the type specimen, and Guillaume VK for providing resources for the map. We thank Zhijia Gu (Platform for Plant Multi-dimensional Imaging and Diversity Analysis, Kunming Institute of Botany, CAS) for the SEM technical support. This work was funded by the Southeast Asia Biodiversity Research Institute, CAS (Grant No. Y4ZK111B01), Transboundary Cooperation on Biodiversity Research and Conservation in Gaoligong Mountains (Grant No. E1ZK251), and Yunnan Province Science and Technology Department (Grant No. 202203AP140007).

References

  • Annandale N (1920) Materials for a generic revision of the freshwater gastropod molluscs of the Indian Empire. Part III. The Freshwater Genera of Hydrobiidae. Records of the Indian Museum 22: 1–6. https://doi.org/10.26515/rzsi/v22/i1/1921/163524
  • Annandale N, Seymour Sewell RB (1920) Progress report on a Survey of the freshwater gastropod molluscs of the Indian Empire and of their trematode parasites. Indian Journal of Medical Research 8(1): 93–124.
  • Blanford WT (1869) Descriptions of new land and freshwater molluscan species collected by Dr. John Anderson in Upper Burma and Yunnan. Proceedings of the Zoological Society London 37(1): 444–450. https://doi.org/10.1111/j.1469-7998.1869.tb07354.x
  • Brandt RAM (1974) The non-marine aquatic Mollusca of Thailand. Archiv für Molluskenkunde 105: 1–423.
  • Bunchom N, Saijuntha W, Pilap W, Suksavate W, Vaisusuk K, Suganuma N, Agatsuma T, Petney TN, Tantrawatpan C (2021) Genetic variation of a freshwater snail Hydrobioides nassa (Gastropoda: Bithyniidae) in Thailand examined by mitochondrial DNA sequences. Hydrobiologia 848: 2965–2976. https://doi.org/10.1007/s10750-019-04013-2
  • Glöer P, Albrecht C, Wilke T (2007) Enigmatic distribution patterns of the Bithyniidae in the Balkan Region (Gastropoda: Rissooidea). Mollusca 25(1): 13–22.
  • Hampton SE, McGowan S, Ozersky T, Virdis SG, Vu TT, Spanbauer TL, Kraemer BM, Swann G, Mackay AW, Powers SM, Meyer MF, Labou SG, O’Reilly CM, DiCarlo M, Galloway AWE, Fritz SC (2018) Recent ecological change in ancient lakes. Limnology and Oceanography 63(5): 2277–2304. https://doi.org/10.1002/lno.10938
  • Izzatullaev Z (1982) Molluscs of the family Bithyniidae (Gastropoda, Pectinibranchia) in the Middle Asia. Zoologicheskiy Zhurnal 61(1): 336–340.
  • Kano Y, Musikasinthorn P, Iwata A, Tun S, Yun LKC, Win SS, Matsui S, Tabata R, Yamasaki T, Watanabe K (2016) A dataset of fishes in and around Inle Lake, an ancient lake of Myanmar, with DNA barcoding, photo images and CT/3D models. Biodiversity Data Journa 4: e10539. https://doi.org/10.3897/BDJ.4.e10539
  • Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A (2019) RAxML-NG: a fast, scalable and 1495 user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35(21): 4453–4455. https://doi.org/10.1093/bioinformatics/btz305
  • Kulsantiwong J, Prasopdee S, Ruangsittichai J, Ruangjirachuporn W, Boonmars T, Viyanant V, Pierossi P, Hebert PDN, Tesana S (2013) DNA barcode identification of freshwater snails in the family Bithyniidae from Thailand. PLoS One 8(11): e79144. https://doi.org/10.1371/journal.pone.0079144
  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular biology and evolution 35(6): 1547. https://doi.org/10.1093/molbev/msy096
  • Nevill G (1881) New or little-known Mollusca of the Indo-Malayan fauna. Journal of the Asiatic Society of Bengal 50(2): 125–167.
  • Nevill G (1885) Hand List of Mollusca in the Indian Museum, Calcutta. Part II. Gastropoda. Prosobranchia-Neurobranchia (contd.). Office of Superintendent of Government Printing: Calcutta.
  • Ng TH, Tan SK (2024) The Family Bithyniidae Gray, 1857 (Gastropoda: Truncatelloidea) in Peninsular Malaysia and Singapore. Tropical Natural History 24: 153–163. https://doi.org/10.58837/tnh.24.1.262922
  • Palumbi SR, Martin A, Romano S, McMillan WO, Stice L, Grabowski G, MacMillan WO (2002) The Simple Fool’s Guide to PCR. University of Hawaii Press, Honolulu.
  • Pilsbry HA (1928) Paranerita Annandale, 1920. The Nautilus 41(3): 108.
  • Popova SM (1981) Kaynozoyskaya kontinental’naya malakofauna yuga Sibiri i sopredel’nykh territoriy [The Cenozoic continental malacofauna of Southern Siberia and adjacent territories]. Nauka, Moskva.
  • Popova SM, Devyatkin YV, Starobogatov YI (1970) Mollyuski kyzylgirskoy svity Gornogo Altaya [Molluscs of the Kyzylgir Formation of the Altay Mountains]. Nauka, Moskva.
  • Ramakrishna AD (2007) Handbook on Indian Freshwater Molluscs. Zoological Survey of India, Pune.
  • Rao S (1989. Handbook of Freshwater Molluscs of India. Zoological Survey of India: Calcutta.
  • Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61(3): 539–542. https://doi.org/10.1093/sysbio/sys029
  • Schultheiß R, Wilke T, Jørgensen A, Albrecht C (2011) The birth of an endemic species flock: demographic history of the Bellamya group (Gastropoda, Viviparidae) in Lake Malawi. Biological Journal of the Linnean Society 102(1): 130–143. https://doi.org/10.1111/j.1095-8312.2010.01574.x
  • Starobogatov YI (1970) Molluscan fauna and zoogeographic zonation of continental freshwater bodies of the world. Nauka Publishers, Leningrad.
  • Theobald W (1866) Notes on a collection of land and freshwater shells from the Shan States. – Collected by F. Fedden, Esq., 1864–65. Journal of the Asiatic Society of Bengal 34(2): 273–279.
  • Yu W, Mao XL, Chen ZQ, Huang LS (1978) Early Tertiary gastropod fossils from the coastal region of Bohai. Paleontological and Geological Research Institute, Nanjing.
  • Zhang LJ, von Rintelen T (2021) The neglected operculum: a revision of the opercular characters in river snails (Caenogastropoda: Viviparidae). Journal of Molluscan Studies 87(2): eyab008. https://doi.org/10.1093/mollus/eyab008
  • Zhang LJ, Shi ZA, Chen ZY, von Rintelen T, Zhang W, Lou ZJ (2024a) Rediscovery and systematics of the enigmatic genus Helicostoa reveals a new species of sessile freshwater snail with remarkable sexual dimorphism. Proceedings of the Royal Society B 291: 20231557. https://doi.org/10.1098/rspb.2023.1557
  • Zhang L.J, Bernardes SC, Meng K, von Rintelen T (2024b) A new family of freshwater snails with Cretaceous origin from Yunnan, China. Zoological Journal of the Linnean Society 202(1): zlae117. https://doi.org/10.1093/zoolinnean/zlae117

Supplementary material

Supplementary material 1 

Supplementary data

Le-Jia Zhang, Shu-Sen Shu, Xin-Yuan Song, Nay Htet Naing, Thaung Naing Oo, Xiao-Yong Chen

Data type: xlsx

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Download file (11.27 kb)
login to comment