Research Article
Research Article
The genus Erhaia (Gastropoda, Truncatelloidea, Amnicolidae), with a new species from Bhutan
expand article infoEdmund Gittenberger§, Choki Gyeltshen|, Björn Stelbrink
‡ GiMaRIS, Sassenheim, Netherlands
§ Naturalis Biodiversity Center, Leiden, Netherlands
| National Biodiversity Centre, Thimphu, Bhutan
¶ Justus Liebig University Giessen, Giessen, Germany
Open Access


The distribution of the five Erhaia (Gastropoda, Truncatelloidea, Amnicolidae) species that are diagnosed by both morphological and molecular data is combined with several records of less completely diagnosed nominal Erhaia species. The resulting distribution pattern is summarized in a map and is discussed herein. Erhaia norbui sp. nov. is described from Bhutan on the basis of shell morphology and two mitochondrial DNA barcoding markers. A molecular phylogeny is presented for the five Erhaia species for which molecular data are available, three of which form a separate clade and are from Bhutan.


16S, Bhutan, China, COI, Erhaia, India, Nepal, taxonomy


The genus Erhaia Davis & Kuo, 1985 (Gastropoda, Truncatelloidea, Amnicolidae), as it is accepted in the literature at present (Gittenberger et al. 2020 and literature therein), is distributed over an area covering nearly 3.500 km from west to east, from northern India and Nepal to eastern China. Comparable to its European counterpart Bythinella Moquin-Tandon, 1856 (Gastropoda, Truncatelloidea, Bythinellidae), which is known from an even larger area measuring nearly 4.000 km from west to east, from Spain to western Russia and Ukraine (Boeters 1998; Vinarski and Kantor 2016), it exemplifies a radiation, in which some species occur syntopically, that may have evolved in a non-adaptive fashion (see Gittenberger 1991; Wilke et al. 2010). However, the lack of data does not allow for a more fundamental discussion here.

Both Erhaia and Bythinella species occur in the clear waters of springs and brooklets. Despite their large ranges, suggesting relatively easy dispersal mechanisms, i.e., low barriers to gene flow, both genera show a high degree of allopatric speciation. This is illustrated by the occurrences in Bhutan, where four species, including the one described as new below, are known only from a single locality. At one locality, two of these species occur syntopically. Three Erhaia species are reported from the Latipur and Kavre districts in the province of Bagmati in Nepal (Nesemann et al. 2007); two of them are known from one locality only, where they occur together with the third species, which has been reported from four additional localities, thus from six in total. A taxonomic revision is needed to clarify whether the Chinese species have similar small ranges and syntopic occurrences.

The shells of species in these two genera are more or less slender ovoid and less than 5 mm high. They show a conspicuous transition in height-width ratio from protoconch to teleoconch. The protoconch shell is valvatiform, as for example in fully grown freshwater snails of the species Valvata cristata O.F. Müller, 1774 (Gastropoda, Valvatoidea, Valvatidae) (Glöer 2019: 196, fig. 244), whereas the teleoconch is not, therefore the shells have an obliquely flattened apical part. The adaptive significance of this, if any, is unknown. Fully grown valvatiform or planispiral shells occur in several species of minute spring snails (e.g. Hershler and Longley 1986; Beran et al. 2014). Apart from their general shape, shells of Erhaia vary more than those of Bythinella and may have character states that do not occur in that genus, viz. a spiral microsculpture and one or more lamellae inside the shell.

Material and methods

Using the literature, we compiled distributional records for 22 nominal species (and a single undetermined individual from China) that are currently classified more or less convincingly in Erhaia (Fig. 1). Many of these taxa were originally classified in Bythinella or Pseudobythinella Liu & Zhang, 1979 (Gastropoda, Truncatelloidea, Bythinellidae) (not Pseudobythinella Melville, 1956). A taxonomic revision, which is beyond the scope of the present study and is also currently not possible given the lack of molecular data for many species, may indicate that some nominal taxa are synonyms. The original descriptions of all taxa mentioned here are included in the References. Following Davis et al. (1985) and Davis and Rao (1997), we excluded so-called Bythinella taxa described from Japan. Coordinates for each species were obtained from the source publication or were estimated based on the locality information provided therein (Table 1). Distribution maps were generated using QGIS 3.10.5 (QGIS Development Team 2000).

Table 1.

Distribution of Erhaia species with coordinates (sorted from west to east) either provided by the source publication or estimated based on the locality information therein.

Species Coordinates
E. norbui spec. nov. 27°22'33.0"N, 89°17'15.0"E
E. jannei Gittenberger & Stelbrink in Gittenberger et al., 2020 27°18'43.0"N, 89°36'10.0"E
E. pelkiae Gittenberger & Gyeltshen in Gittenberger et al., 2020 27°18'43.0"N, 89°36'10.0"E
E. wangchuki Gittenberger, Sherub & Stelbrink, 2017 27°26'17.6"N, 90°11'18.9"E
E. nainatalensis Davis & Rao, 1997 29°23'00.0"N, 79°30'00.0"E
E. banepaensis Nesemann & S. Sharma in Nesemann et al., 2007 27°00'00.0"N, 85°00'00.0"E
E. chandeshwariensis Nesemann & S. Sharma in Nesemann et al., 2007 27°00'00.0"N, 85°00'00.0"E
E. sugurensis Nesemann, Shah & Tachamo in Nesemann et al., 2007 27°00'00.0"N, 85°00'00.0"E
E. daliensis Davis & Kuo in Davis et al., 1985 25°45'00.0"N, 100°06'00.0"E
E. kunmingensis Davis & Kuo in Davis et al., 1985 24°40'00.0"N, 102°35'00.0"E
E. lii (Kang, 1985) [also in Kang, 1986] 30°00'00.0"N, 110°00'00.0"E
E. shimenensis (Liu, Zhang & Chen, 1982) 30°00'00.0"N, 110°00'00.0"E
E. triodonta (Liu, Wang & Zhang, 1991) 29°58'00.0"N, 110°15'00.0"E
E. wantanensis (Kang, 1983a) 30°04'00.0"N, 110°26'00.0"E
E. robusta (Kang, 1986) 29°52'18.8"N, 110°32'54.5"E
E. wufungensis (Kang, 1983a) 30°12'00.0"N, 110°41'00.0"E
Erhaia sp. [Liu et al. 2014: Table 5] 25°44'16.0"N, 110°43'07.0"E
E. hubeiensis (Liu, Zhang & Wang, 1983) 31°10'00.0"N, 110°50'00.0"E
E. chinensis (Liu & Zhang, 1979) 30°00'00.0"N, 111°00'00.0"E
E. liui (Kang, 1985) 30°00'00.0"N, 111°00'00.0"E
E. tangi (Cheng, Wu, Li & Lin, 2007) 26°08'00.0"N, 117°40'00.0"E
E. jianouensis (Liu & Zhang, 1979) 26°58'00.0"N, 118°33'00.0"E
E. gongjianguoi (Kang, 1983b) 30°00'00.0"N, 120°00'00.0"E
Figure 1. 

Distribution of Erhaia species across Asia.

In a spring area in Bhutan (Fig. 2), several specimens of a minute snail species were discovered and collected by Sangay Norbu. Based on this material, Erhaia norbui sp. nov. is described here. Photographs of the holotype (Fig. 3) were made using a Wild MS-26 binocular camera set-up. Shells of two paratypes (Figs 4, 5), which were used for a molecular analysis and thus could not be saved, were photographed with a Keyence VHX-2000 digital microscope system (Keyence Corp., Itasca, IL, USA). Additional paratypes were kept as dry shells.

Figure 2. 

Habitat of E. norbui sp. nov. at the type locality. Photo by Mr. Sangay Norbu.

The DNA lab work and phylogenetic analyses were identical to those described in Gittenberger et al. (2020). For the phylogenetic analyses, a reduced dataset including both mitochondrial markers, COI and 16S rRNA, was used. Uncorrected genetic p-distances for COI and 16S rRNA between the species from Bhutan were calculated using MEGA X 10.1.7 (Kumar et al. 2018).

Figures 3–5. 

Erhaia norbui sp. nov. from the type locality, district Haa, Uesu, Naychu, ca. 2700 m a.s.l. 3 holotype, NBCB 1239 (H = 2.3 mm) and paratypes used for DNA analyses (4 UGSB 25956, H = 1.5 mm 5 UGSB 25957, H = 1.8 mm). Scale bar: 1 mm.

The following abbreviations are used: B = shell breadth; H = shell height; NBCB = National Biodiversity Centre, Serbithang, Thimphu, Bhutan; RMNH = National Biodiversity Center Naturalis, Leiden, The Netherlands.


Superfamily Truncatelloidea Gray, 1840

Family Amnicolidae Tryon, 1863

Erhaia Davis & Kuo in Davis et al., 1985

Type species by original designation

Erhaia daliensis Davis & Kuo in Davis et al., 1985.


Pseudobythinella Liu & Zhang, 1979. Not Melville, 1956. Type species by original designation: Pseudobythinella jianouensis Liu & Zhang, 1979.


Shell ovoid to elongate ovoid or conical, smooth or with spiral microsculpture on the proto- and/or teleoconch. Apex conspicuously and more or less obliquely flattened. Aperture varying from ovoid-elliptical to circular; its palatal side curved and gradually passing into the basal side. Peristome continuous, attached at the parietal side or more or less protruding. Umbilicus minute or closed. Parietal part of the aperture smooth or with a lamella; columella smooth or with 2 spiral lamellae.


Molecular data, which are available for only a limited number of the amnicolid species, are inconclusive regarding the status of Erhaia versus Akiyoshia Kuroda & Habe, 1954 Gastropoda, Truncatelloidea, Amnicolidae) (see also the more comprehensive phylogenetic reconstruction in Gittenberger et al. 2020). No DNA data are known for the type species of these nominal taxa, i.e., E. daliensis Davis & Kuo, 1985 and A. uenoi Kuroda & Habe, 1954. Furthermore, the species that are generally called Erhaia jianouensis (Liu & Zhang, 1979) and Akiyoshia kobayashii Kuroda & Habe, 1958 are sister species (Fig. 7) that should be congeneric by definition. At present, their ranges in China and Japan, respectively, have been decisive for the generic classification. Pending additional data that can help solve this problem convincingly, we opted to still use the current, contradictory nomenclature (see also notes under E. norbui sp. nov.).


The genus Erhaia was initially reported from a wide range in southern China, where it has been recorded with various species from the provinces of Yunnan, Sichuan, Guangxi, Hubei, Hunan, and Fujian (Davis et al. 1985; Davis and Kang 1995; Davis and Rao 1997; Wilke et al. 2000, 2001; Liu et al. 2014). Regarding its occurrence in Japan, see foregoing notes. One species was described from northern India (Davis and Rao 1997), three additional species were described from Nepal (Nesemann et al. 2007), and, most recently, three species were described from Bhutan (Gittenberger et al. 2017, 2020). Here, we describe a fourth species from Bhutan and present, for the first time, a map of all known records of the genus (see Fig. 1 and Table 1). As usual, it is unknown where snails may have been looked for in vain and thus our distribution maps (Figs 1, 6) may represent human sampling activity rather than the real range of Erhaia. Contrary to Gittenberger et al. (2020), in the absence of DNA data, we refer to E. chandeshwariensis Nesemann & S. Sharma, 2007 as a species closely related to E. nainatalensis Davis & Rao, 1997. The shells cannot be distinguished, but the type localities are over 600 km apart, which makes conspecificity unlikely in Erhaia. Remarkable facts are the allopatric distribution and diversification in this genus in general, the syntopic occurrence of E. jannei Gittenberger & Stelbrink, 2020 and E. pelkiae Gittenberger & Gyeltshen, 2020 in Bhutan (Fig. 6), and that of E. banepaensis Nesemann & S. Sharma, 2007 with either E. chandeshwariensis or E. sugurensis Nesemann, Shah & Tachamo, 2007 in Nepal (Fig. 5).

Figure 6. 

Distribution of Erhaia species described for Bhutan. Note that E. jannei and E. pelkiae were found to occur syntopically.

Erhaia norbui sp. nov.

Figs 2, 3–5, 6

Material examined

Holotype. (Fig. 4) Bhutan • District Haa, Uesu, Naychu, ca. 2700 m a.s.l.; 27°22'33"N 89°17'15"E; Sangay Norbu leg. 2020 (NBCB 1239).

Paratypes. (Figs 56) 3 shells (NBCB 1240), 2 shells (RMNH.MOL.511432).


Shell pale greyish, large for the genus (H > 2 mm), with a globular body whorl and a roundish aperture.


Shell obliquely ovoid, with 3½–3¾ regularly convex whorls that are separated by a deep suture; clearly higher than broad; pale greyish with fine irregular growth lines and some blackish-brown periostracal ridges, one of which runs from the apertural columellar border into the umbilicus. Aperture nearly circular in fully grown specimens, with a continuous, free peristome that is thickened, not reflected; with a minute umbilicus. Protoconch encrusted in all specimens; teleoconch without spiral sculpture.

Measurements of shells with thickened apertural border (n = 6): H 2.3–2.6 mm, B 1.6–1.8 mm. Holotype 2.3×1.7 mm.

Shells of E. jannei, which are most similar in shape, are yellowish-brown and a little narrower, with the aperture slightly compressed laterally. The other Bhutanese Erhaia species known, i.e., Erhaia pelkiae and E. wangchucki Gittenberger, Sherub & Stelbrink, 2017, are smaller, i.e. H < 2 mm and H < 2.2 mm, respectively; their shells are less pale, of an elongated ovoid shape and with an elliptical aperture in E. pelkiae, or conical shape with a piriform aperture in E. wangchucki.


(Fig. 2). The species was found in spring water among abundant watercress. The annual temperature of the water is 9–12 °C, with pH of 7–8.5 and 6.5 mg/l oxygen.

Molecular data

(Fig. 7). Both of the individuals (paratypes) that we analyzed genetically shared an identical haplotype for both COI (GenBank acc. no.: OM135616) and 16S rRNA (GenBank acc. no.: OM135244). The uncorrected genetic p-distances between E. norbui sp. nov. vs. E. jannei and E. wangchuki were 3.97% and 5.19%, respectively, for COI, and 1.42% and 1.22%, respectively, for 16S rRNA.

Figure 7. 

Maximum likelihood tree reconstructed with RAxML BlackBox (Stamatakis et al. 2008; GTR+G substitution model for each partition and 100 bootstrap replicates) based on the COI and 16S rRNA dataset of Liu et al. (2014) and Guan et al. (2008), with new data in red. Numbers on branches denote bootstrap values > 50.


The three Erhaia species from Bhutan form a highly supported clade, with Erhaia sp. from China as the sister-group. Interestingly, the species called E. jianouensis, from China, and Akiyoshia kobayashii, from Japan, form the highly supported sister-group of the remaining Erhaia species (see foregoing notes for Erhaia). For additional notes regarding the truncatelloidean gastropods of N. India, Nepal, Bhutan, and S. China, in particular the species of Erhaia, see also Gittenberger et al. (2020).


The epithet norbui refers to Mr. Sangay Norbu, who discovered this species.


We would like to thank Dr Tashi Y. Dorji, Program Director of the NBC, and Ms Sangay Dema (NBC) for their support and guidance during this project. We are particularly grateful to Mr Sangay Norbu (Manager/Livestock Production Officer, Bhutan Livestock development Corporation, Haa, Bhutan), who discovered and collected the species described here as E. norbui sp. nov. We also thank both Jonathan Ablett, The Natural History Museum, London, UK, and Bernhard Hausdorf, Leibniz Institute for the Analysis of Biodiversity Change, Hamburg, Germany, for constructive remarks, and the staff members of the Library of Naturalis Biodiversity Center (Leiden) for their bibliographic assistance.


  • Boeters HD (1998) Mollusca: Gastropoda: Rissooidea. Süsswasserfauna von Mitteleuropa 5 (1–2): i–ix, 1–76.
  • Cheng Y-Z, Wu X-P, Li L-S, Lin C-X (2007) A new species of Pseudobythinella (Mesogastropoda, Pomatiopsidae) from China. Acta Zootaxonomica Sinica 32(4): 896–899.
  • Davis GM, Kang ZB (1995) Advances in the Systematics of Erhaia (Gastropoda: Pomatiopsidae) from the People’s Republic of China. Proceedings of the Academy of Natural Sciences of Philadelphia 146: 391–427.
  • Davis GM, Rao S (1997) Discovery of Erhaia (Gastropoda: Pomatiopsidae) in northern India with description of a new genus of Erhaiini from China. Proceedings of the Academy of Natural Sciences of Philadelphia 148: 273–299.
  • Davis GM, Kuo Y-H, Hoagland KE, Chen P-L, Yang H-M, Chen D-J (1985) Erhaia, a new genus and new species of Pomatiopsidae from China (Gastropoda: Rissoacea). Proceedings of the Academy of Natural Sciences of Philadelphia 137: 48–78.
  • Gittenberger E, Leda P, Wangchuck J, Gyeltshen C, Stelbrink B (2020) The genera Erhaia and Tricula (Gastropoda, Rissooidea, Amnicolidae and Pomatiopsidae) in Bhutan and elsewhere in the eastern Himalaya. ZooKeys 929: 1–17.
  • Glöer P (2019) The freshwater gastropods of the West-Palaearctis. Volume I. Fresh- and brackish waters except spring and subterranean snails. Identification key, anatomy, ecology, distribution. Published by the author, Hetlingen, Germany, 399 pp.
  • Hershler R, Longley G (1986) Phreatic hydrobiids (Gastropoda: Prosobranchia) from the Edwards (Balcones fault zone) Aquifer region, south-central Texas. Malacologia 27(1): 127–172.
  • Kang Z-B (1983a) A new genus and three new species of the family Hydrobiidae (Gastropoda: Prosobranchia) from Hubei province, China. Oceanologia et Limnologia Sinica 14(5): 499–505. [In Chinese and English]
  • Kang Z-B (1983b) Two new molluscan hosts for Paragonimus skrjabini. Oceanologia et Limnologia Sinica 14(6): 536–541. [In Chinese and English]
  • Kang Z-B (1985) Description of a new species of Bythinella from China. Acta Hydrobiologica Sinica 9(1): 84–88. [In Chinese and English]
  • Kang Z-B (1986) Descriptions of eight new minute freshwater snails and a new and rare species of land snail from China. Archiv für Molluskenkunde 117(1–3): 73–91.
  • 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): 1547–1549.
  • Liu L, Huo G-N, He H-B, Zhou B, Attwood SW (2014) A phylogeny for the pomatiopsidae (Gastropoda: Rissooidea): a resource for taxonomic, parasitological and biodiversity studies. BMC Evolutionary Biology 14: e29.
  • Liu Y-Y, Zhang W-Z (1979) On new genus and species of freshwatersnails harbouring cercariae of lung flukes from China. Acta Zootaxonomica Sinica 4(2): 132–136.
  • Liu Y-Y, Wang Y-X, Zhang W-Z (1991) On the freshwater molluscs in the area of Sanxia Reservoir. Acta Zootaxonomica Sinica 16(1): 1–14.
  • Liu Y-Y, Zhang W-Z, Chen C-E (1982) Pseudobythinella shimenensis, sp. nov., a new aquatic Paragonimus cercariae carrying snail from Hunan province. Acta Zootaxonomica Sinica 7(3): 254–256.
  • Liu Y-Y, Zhang W-Z, Wang Y-X (1983) On three new freshwater snails from China. Acta Zootaxonomica Sinica 8(4): 366–369.
  • Nesemann H, Sharma S, Sharma G, Khanal SN, Pradhan B, Shah DN, Tachamo RD (2007) Class Gastropoda. In: Nesemann H, Sharma S, Sharma G, Khanal SN, Pradhan B, Shah DN, Tachamo RD (Eds) Aquatic invertebrates of the Ganga river system (Mollusca, Annelida, Crustacea, 57–102.
  • Vinarski MV, Kantor YI (2016) Analytical catalogue of fresh and brackish water molluscs of Russia and adjacent countries. A.N. Severtsov Institute of Ecology and Evolution of Russian Academy of Sciences, Moscow, 544 pp.
  • Wilke T, Davis GM, Gong X, Liu H-X (2000) Erhaia (Gastropoda: Rissooidea): phylogenetic relationships and the question of Paragonimus coevolution in Asia. The American Journal of Tropical Medicine and Hygiene 62: 453–459.
  • Wilke T, Benke M, Brändle M, Albrecht C, Bichain JM (2010) The neglected side of the coin: non-adaptive radiations in spring snails (Bythinella spp.). In: Glaubrecht M (Ed.) Evolution in action: 551–578. Springer, Berlin, Heidelberg.
  • Wilke T, Davis GM, Falniowski A, Giusti F, Bodon M, Szarowska M (2001) Molecular systematics of Hydrobiidae (Mollusca: Gastropoda: Rissooidea): testing monophyly and phylogenetic relationships. Proceedings of the Academy of Natural Sciences of Philadelphia 151: 1–21.[0001:MSOHMG]2.0.CO;2
login to comment