Research Article
Print
Research Article
A new genus of river snails, Dalipaludina (Gastropoda, Viviparidae), endemic to the Yunnan Plateau of SW China
expand article infoLe-Jia Zhang‡, Li-Na Du§, Thomas von Rintelen‡
‡ Museum für Naturkunde, Leibniz, Institut für Evolutions und Biodiversitätsforschung, Berlin, Germany
§ Guangxi Normal University, Guilin, China

Corresponding author: Le-Jia Zhang ( lejia.zhang@mfn.berlin )

Academic editor: Frank Köhler
© 2023 Le-Jia Zhang, Li-Na Du, Thomas von Rintelen.
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, Du L-N, von Rintelen T (2023) A new genus of river snails, Dalipaludina (Gastropoda, Viviparidae), endemic to the Yunnan Plateau of SW China. Zoosystematics and Evolution 99(2): 285-297. https://doi.org/10.3897/zse.99.102586
ZooBank: urn:lsid:zoobank.org:pub:6856760F-3F9E-4B27-8AC2-B59D25845F67
Open Access

Abstract

A new genus of viviparid snail, Dalipaludina gen. nov., from the Yunnan Plateau of China is described within an integrative taxonomic framework based on data from the mitochondrial COI marker and morphology. Dalipaludina can be distinguished from all other viviparid genera by a unique combination shell, operculum and radula characters. Four species are assigned here to the new genus, Dalipaludina delavayana comb. nov., Dalipaludina oxytropoides comb. nov., Dalipaludina occidentalis comb. nov., and Dalipaludina pyramidella comb. nov., and one species is newly assigned to Margarya, Margarya dianchiensis comb. nov. The four species of Dalipaludina are allopatrically distributed in shallow water lentic habitats at high altitude regions of the Yunnan Plateau.

Key Words

High altitude, lentic habitat, phylogeny, taxonomy

Introduction

River snails (Viviparidae) are widely distributed freshwater gastropods that are found on all continents except for Antarctica and South America. The oldest fossil record of Viviparidae can be traced back to the mid Jurassic. About 28 extant genera and 125 to 150 extant species of this family worldwide are currently recognised (Van Bocxlaer and Strong 2019). China is the country with the highest biodiversity of Viviparidae, harbouring two subfamilies (Bellamyinae Rohrbach, 1937; Viviparinae J. E. Gray, 1847), 13 genera (Amuropaludina Moskvicheva, 1979; Angulyagra Rao, 1931; Anularya Zhang & Chen, 2015; Cipangopaludina Hannibal, 1912; Filopaludina Habe, 1964; Idiopoma Pilsbry, 1901; Margarya G. Nevill, 1877; Mekongia Crosse & P. Fischer, 1876 Rivularia Heude, 1890; Sinotaia F. Haas, 1939; Tchangmargarya He, 2013; Ussuripaludina Zatravkin & Bogatov, 1987; Viviparus Montfort, 1810), and at least 40 species (Liu et al 1995; Zhang et al. 2015; Van Bocxlaer et al. 2017).

The Yunnan Province of China, which covers an area of only 394,000 km2, harbours nine genera (Angulyagra; Anularya; Cipangopaludina; Filopaludina; Idiopoma; Margarya; Mekongia; Sinotaia; Tchangmargarya) including three endemic ones (Anularya; Margarya; Tchangmargarya) and at least 24 species including 14 endemic ones of Viviparidae (Liu et al 1995; Zhang et al. 1997; Zhang et al. 2015). While it is the region with the highest diversity of Viviparidae at both the genus and species level not only in China but also worldwide, recent studies (Du et al. 2011; Zhang et al. 2015; Zhang 2017) have revealed that the diversity of Viviparidae in Yunnan is still underestimated. Based on an integrative study combining molecular and morphological data, we here revise the taxonomy of several viviparid species from the Yunnan Plateau, and describe a new genus. The phylogeny and ecology of the new genus, as well as conservation aspects, are discussed.

Materials and methods

Material

Type specimens of three Viviparidae species from Yunann kept in the Institute of Zoology, Chinese Academy of Sciences, Beijing (IZCAS), the Kunming Natural History Museum of Zoology, Kunming (KIZ), and the Museum of Comparative Zoology at Harvard University, Cambridge (MCZ), as well as other specimens in Museum für Naturkunde, Berlin (ZMB), have been examined. From 2011 to 2022, altogether 19 lakes of Yunnan and the surrounding aquatic habitats, including rivers, creeks, springs and wetlands, have been surveyed (Fig. 1A). Newly collected fresh samples of the species belonging to the new genus were collected by Le-Jia Zhang and Jiao-Wei Ning from 2018 to 2022 in northwest Yunnan (Fig. 1B–D). The newly sampled material is stored in ZMB and the private collection of Le-Jia Zhang (ZLJ) Jiao-Wei Ning (NJW).

Figure 1. 

Collecting sites and habitats of Dalipaludina gen. nov. in Yunnan, China. A. Map of Yunnan Province showing 19 surveyed lakes (adapted from Zhang et al. 2015), study area in northwest Yunnan highlighted in blue, where Dalipaludina species were found during surveys; B. Map of study area in northwest Yunnan, star–Dalipaludina oxytropoides, triangle–Dalipaludina occidentalis, square–Dalipaludina delavayana, circle–Dalipaludina pyramidella; altitude of each collecting site is given; C. Environment of one collecting site of Dalipaludina oxytropoides in Lake Lugu; D. Environment of one collecting site of Dalipaludina occidentalis in an unnamed pond in Lijiang.

Examination of morphology

Shell height (H) and width (W) of only mature and complete specimens were measured with a caliper to a precision of 0.1 mm (Table 1). The morphometric data of Dalipaludina oxytropoides kept in ZMB are from Wiese et al. (2022). The specimens were photographed in a consistent orientation using a Sony alpha 7R 4 camera. Radulae and embryonic shells were extracted through dissection; radulae were cleaned by boiling in 1% NaOH solution for half an hour and rinsed with distilled water. Radulae and embryonic shells were coated with gold before scanning electron microscopy with a Zeiss EVO LS10 scanning electronic microscope. The terms used for describing the operculum are according to Zhang and von Rintelen (2021).

Table 1.
Download as
CSV
XLSX

Shell measurements of Dalipaludina species. Values are arithmetic means (mm).

Species H W W/H
Dalipaludina delavayana (n=25) 58.30 ± 8.30 38.30 ± 5.27 0.70 ± 0.04
Dalipaludina oxytropoides (n=91) 44.60 ± 5.78 32.30 ± 3.82 0.70 ±0.04
Dalipaludina occidentalis (n=27) 50.17 ± 4.17 41.00 ± 2.38 0.82 ±0.05
Dalipaludina pyramidella (n=30) 47.86 ± 7.06 41.34 ± 5.48 0.87 ± 0.05

DNA extraction and amplification

DNA was extracted from the foot tissue of eight individuals (10–20 mg of each individual), using a mollusc-specific CTAB/chloroform extraction protocol (Winnepenninckx et al. 1993). A fragment of the mitochondrial cytochrome c oxidase subunit I (COI) gene was amplified through polymerase chain reaction (PCR) with the following primer pair: LCO1490, 5′-GGTCAACAAATCATAAAGATATTGG-3′ and COX-B7R, 5′-ACCACCAGCTGGATCAAAAA-3′. (Schultheiß et al. 2011) PCR amplifications were conducted in 25 μl volumes under the following cycling conditions: initial denaturing step at 94 °C for 10 min, followed by 30 cycles of 94 °C for 1 min, 50 °C for 1 min, and 72 °C for 1 min, with a final extension step of 10 min at 72 °C. The purification and sequencing were conducted by Macrogen Europe, Amsterdam, Netherlands.

Phylogenetic analysis

Eight new DNA sequences (from eight individuals of two Dalipaludina species) have been uploaded to GenBank (accession numbers and museum voucher numbers, see Suppl. material 1). Additionally, three sequences of Dalipaludina oxytropoides published by Wiese et al. (2022) and sequences of 17 different genera of the subfamily Bellamyinae (Suppl. material 1) published by Stelbrink et al. (2020) and Hirano et al. (2019a) were downloaded from GenBank; Viviparus viviparus of the subfamily Viviparinae was selected as outgroup based on Stelbrink et al. (2020).

Sequences were aligned using MUSCLE as implemented in Geneious Prime 2020 (https://www.geneious.com). Genetic distances were calculated using MEGA X (Kumar et al. 2018). The dataset was tested in MEGA X for the best-fit model of sequence evolution by means of the Akaike and Bayesian information criteria; GTR+G+I was suggested as the best-fitting nucleotide substitution model. This model was employed in a maximum likelihood (ML) analysis conducted by RAxML as implemented in Geneious Prime 2020, with support estimated by 1,000 bootstrap replicates, and a Bayesian inference (BI) analysis performed with MrBayes 3.2.6 (Ronquist et al. 2012) as implemented in Geneious Prime 2020 with four independent chains for 5,000,000 generations, samplefreq = 1,000, burnin = 25%, and confirmed that convergence was reached based on the trace plots generated in Geneious Prime 2020.

Results

Genetic differentiation and phylogeny

COI p-distances between species of Dalipaludina are 1.81% to 3.98%; the p-distances between Dalipaludina and its closest relative, viz. the Cipangopaludina/Margarya complex, are 9.22%–14.98%, while p-distances within the Cipangopaludina/Margarya complex are 0–9.31%.

The phylogenetic trees reconstructed by BI and ML based on COI are highly congruent, therefore only the BI tree is shown (Fig. 2). The new genus Dalipaludina is monophyletic and distinct from all other included genera of Viviparidae. The three sequenced species of Dalipaludina are each recovered as monophyletic as well. Dalipaludina occidentalis is the sister species of Dalipaludina delavayana, and Dalipaludina oxytropoides is sister to both. Dalipaludina is the sister clade of a clade formed by the Cipangopaludina/Margarya complex, Celetaia, Ussuripaludina, Hetergen, Torotaia, Anularya and Sinotaia.

Figure 2. 

The BI tree based on cytochrome c oxidase subunit I (COI) showing the phylogenetic position of Dalipaludina gen. nov. within Viviparidae. Numbers above branches are ML bootstrap values/BI posterior probabilities.

Systematics

Family Viviparidae J.E. Gray, 1847

Subfamily Bellamyinae Rohrbach, 1937

Dalipaludina Zhang, gen. nov.

https://zoobank.org/6817CC4A-D98A-4D33-B890-49C91F64A1E5

Type species

Paludina delavayana Heude, 1889.

Etymology

“Dali” refers to the ancient Dali Kingdom (大理国) mostly situated in modern Yunnan, China; “paludina” refers the assignment to Viviparidae. The recommended Chinese name is “理田螺”.

Diagnosis

Shell large, thin but solid; apex acute; teleoconch whorls with strong keel at suture, above suture relatively smooth or with several weak spiral threads or strong spiral cords, many thin and weak spiral threads on base; umbilicus narrow, sometimes bordered by a keel; exterior surface of operculum rather smooth, inner opercular region relatively small, nuclear region of operculum smooth, sometimes with small grains; outer marginal tooth with 9 to 11 small sharp cusps.

Comparative remarks

Dalipaludina gen. nov. resembles Cipangopaludina (widely distributed in East Asia), Ussuripaludina Zatravkin & Bogatov, 1987 (endemic to Far East), Heterogen Annandale, 1921 (endemic to Japan and Korea), and Torotaia Haas, 1939 (endemic to Philippines, Sulawesi and New Guinea). It differs from Cipangopaludina, Ussuripaludina, Heterogen and Torotaia by having one strong keel at the suture, a shell base with many thin and weak spiral threads, a narrow umbilicus sometimes bordered by a keel, and operculum characters. The molecular phylogeny supports that Dalipaludina is distinct from Cipangopaludina, Ussuripaludina, Heterogen and Torotaia. The location of the testis in male Dalipaludina specimens in the mantle cavity supports the classification of this genus in the subfamily Bellamyinae. There are four known species of Dalipaludina.

Distribution

This genus is endemic to the lakes or ponds in northwest to northeast Yunnan, China.

Dalipaludina delavayana (Heude, 1889), comb. nov.

Paludina delavayana Heude, 1889: 47 (“lacu Ta-li fou”, Lake Erhai).

Sinotaia delavayana – Qian et al. 2014.

Material examined

2 syntypes, IZCAS-FG-492553, IZCAS-FG-492554; 1 paratype, MCZ-Mala-167342; 8 specimens in ZMB, collected by Le-Jia Zhang from around 0.5 to 1 metres depth in the north shore of Lake Cibi in Augest 2018, 2 specimens in ZMB, collected by Jiao-Wei Ning from around 1 to 2 metres depth in Lake Haixihai; 17 specimens in NJW, collected by Jiao-Wei Ning from around 1 to 2 metres depth in Lake Cibi.

Description

Shell (Fig. 3A–H) large, conical, thin, greenish yellow to dark olive in colour; up to six whorls at adulthood, including one relatively smooth protoconch whorl, apex acute, spire high; each teleoconch whorls with one strong keel at suture, above suture smooth or with many weak spiral threads, sometimes with additional two to three stronger cords, base of shell with many thin weak spiral threads, weak spiral cords and threads with short periostracal hairs; aperture ovate, less than half of shell in height, lip thin and simple, umbilicus narrow, sometimes bordered by a keel.

Figure 3. 

Shell and operculum of Dalipaludina delavayana. A–C. Specimen collected from Lake Cibi, ZMB Moll. 122707; D, E. Varieties collected from Lake Cibi, ZMB Moll. 122707; F. specimen collected from Lake Haixihai,LJZ; G. Paratype MCZ-Mala-167342, photo taken by Alana Rivera, Museum of Comparative Zoology, Harvard University, President and Fellows of Harvard College; H. Syntype IZCAS-FG-492554, photo taken by Kaibaryer Meng, Institute of Zoology, Chinese Academy of Sciences; I. Exterior (left) and interior (right) surface of operculum. Scale bar: 1 cm, B–H with the same scale bar of A.

Operculum (Fig. 3I) corneous, ovate, rather thin, yellow, with reddish brown nuclear region, exterior surface of operculum rather smooth, inner opercular region relatively small, nuclear region smooth.

Radular (Fig. 7A, B) central tooth with one broad central denticle and with four small sharp cusps on either side; lateral tooth with one broad central denticle and four small sharp cusps on either side; inner marginal tooth with one broad central denticle and three small sharp cusps on either side; outer marginal tooth with 10 to 11 small sharp cusps.

Remarks

This species differs from the other Dalipaludina species by having a larger shell with a higher spiral. It may be difficult to distinguish from the smooth form of Dalipaludina oxytropoides from Lake Lugu based on morphology. However, this species is not recorded from Lake Lugu, and can be distinguished from D. oxytropoides based on differences in COI gene sequences. The recommended Chinese name of this species is “德拉维理田螺”.

Habitat and distribution

shallow water area with sandy and muddy bottoms in Erhai, Cibi and Haixihai, Yunnan, China.

Dalipaludina oxytropoides (Heude, 1889), comb. nov.

Paludina oxytropoides Heude, 1889: 176 (‘lacu prope Tchao-tong’ = lake near Zhaotong City,Yunnan Province, China).

Vivipara oxytropoides – Kobelt 1909: 128.

Margarya sp. – Du et al. 2012: 45.

Margarya oxytropoides – Zhang et al. 2015: 777; Wiese et al. 2022.

Material examined

2 syntypes, IZCAS-FG-492586, IZCAS-FG-492587; 1 paratype, MCZ-Mala-167343; 91 specimens in ZMB, collected by Frank Riedel from around 1 to 6 metres depth in all over the Lake Lugu in September and October 2014; 5 specimens in ZMB, collected by Le-Jia Zhang from 1 metre depth in the east shore of Lake Lugu in April 2022.

Description

Shell (Fig. 4A–H) large, conical, thin, greenish yellow to dark brown in colour; up to six whorls at adulthood, including one relatively smooth protoconch whorl, apex acute; each teleoconch whorls with one strong keel at suture, above suture with many rather weak spiral threads, sometimes with additional two to three strong cords, base of shell with many thin weak spiral threads, weak spiral cords and threads with short periostracum setae; aperture ovate, less than half of shell in height, lip thin and simple, umbilicus narrow, sometimes bordered by a keel.

Figure 4. 

Shell and operculum of Dalipaludina oxytropoides. A–C. Specimen collected from Lake Lugu, ZMB.Moll. 250844; D–F. Varieties collected from Lake Lugu,ZLJ; G. Syntype IZCAS-FG-492587 from a lake in Zhaotong, Yunann, photo taken by Kaibaryer Meng, Institute of Zoology, Chinese Academy of Sciences; H. Paratype MCZ-Mala-167343 from a lake in Zhaotong, Yunann, photo taken by Alana Rivera, Museum of Comparative Zoology, Harvard University, President and Fellows of Harvard College; I. Exterior (left) and interior (right) surface of operculum. Scale bar: 1 cm, B–F, H–I with the same scale bar of A.

Operculum (Fig. 4I) corneous, ovate, thin to relatively thick, yellow to reddish brown, with darker coloured nuclear region, exterior surface of operculum rather smooth, inner opercular region relatively small, nuclear region smooth or with small grains.

Radular (Fig. 7C, D) central tooth with one broad central denticle and three to four small sharp cusps on either side; lateral tooth with one broad central denticle and three to four small sharp cusps on either side; inner marginal tooth with one broad central denticle and four small sharp cusps on either side; each outer marginal tooth with 10 to 11 small sharp cusps.

Remarks

This species has the most variable shell within Dalipaludina. The form with strong cords of this species can be easily distinguished from the other Dalipaludina species. It used to be considered as a species of Margarya with a distribution in Lake Dianchi as well (Zhang et al. 2015). However, the COI-based phylogeny showed that “Margarya oxytropides” from Dianchi is not a species of Dalipaludina, but indeed a member of the Cipangopaludina/Margarya complex. The syntypes of Paludina oxytropoides Heude, 1889 from Zhaotong in Northeast Yunnan show a strong keel at the suture, two strong keels above the suture, a relatively smooth shell base with many weak spiral keels, and a narrow umbilicus with a keel around it. It is distinct from the “Margarya oxytropides” from Lake Dianchi but quite similar to the strongly keeled form of D. oxytropoides from Lake Lugu. Meanwhile, the shell morphology of “Margarya oxytropides” from Lake Dianchi matches the description and figure of Cipangopaludina dianchiensis Zhang, 1990 endemic to Lake Dianchi (Zhang 1990). Therefore, instead of D. oxytropoides, “Margarya oxytropides” from Lake Dianchi is here recognised as Margarya dianchiensis (Zhang, 1990) comb. nov. Paludina oxytropoides Heude, 1889 is reclassified as a member of Dalipaludina. The recommended Chinese name of this species is “尖龙骨理田螺”.

Habitat and distribution

shallow to medium-depth water area with sandy bottoms in Lake Lugu, Yunnan/Sichuan, China; lakes in Zhaotong, Yunnan, China.

Dalipaludina occidentalis (Annandale, 1924), comb. nov.

Lecythoconcha malleata f. occidentalis Annandale, 1924: 415 (“Ho-ching and Shihku”, Heqing County and Shigu town, Lijiang City, Yunnan, China).

Viviparus occidentalis – Yen 1942.

Material examined

8 specimens in ZMB, collected by local fishermen from 3 to 5 metres depth in the south shore of Lake Jianhu. February 2020; 4 specimens in ZMB, collected by Le-Jia Zhang from 0.5 metres depth in an unnamed pond on the Sheshan hill in Lijiang City in April 2022; 19 specimens in NJW, collected by Jiao-Wei Ning from Lake Jianhu.

Description

Shell (Fig. 5A–G) large, broadly conical or sub globose, thin, olive to dark brown in colour; up to six whorls at adulthood, including one relatively smooth protoconch whorl, apex acute; teleoconch whorls inflated, occasionally shouldered, with one strong keel at suture, above suture with many weak spiral threads, sometimes with additional two to three stronger cords, base of shell with many thin weak spiral threads, weak spiral threads and cords with short periostracum setae; aperture ovate, slightly less than half of shell in height, lip thin and simple, umbilicus narrow, sometimes bordered by akeel.

Figure 5. 

Shell and operculum of Dalipaludina occidentalis. A–C. Specimen collected from Lake Jianhu, ZMB.Moll. 122712; D, E. Varieties collected from Lake Jianhu, ZMB.Moll. 122713; F. Sub-adult collected from Lake Jianhu, ZMB.Moll. 122713; G. Original figure of the type specimen in Annandale, 1922; H. Exterior (left) and interior (right) surface of operculum. Scale bar: 1 cm, B–F with the same scale bar of A.

Operculum (Fig. 5H) corneous, ovate, rather thin, yellow, with red nuclear region, exterior surface of operculum rather smooth, inner opercular region relatively small, nuclear region smooth.

Radular (Fig. 7E, F) central tooth with one broad central denticle and four small sharp cusps on either side; lateral tooth with one broad central denticle and four small sharp cusps on either side; inner marginal tooth with one broad central denticle and four small sharp cusps on either side; outer marginal tooth with 9 to 10 small sharp cusps.

Remarks

This species differs from the other species of Dalipaludina by having rather inflated, shouldered whorls. Annandale (1924) presented a photo of the type specimen. The shell morphology and COI phylogeny of the specimens collected from an unnamed pond in Lijiang City, which is very close to the type locality, confirm that this species should be assigned to Dalipaludina. The recommended Chinese name of this species is “滇西理田螺”.

Habitat and distribution

Shallow ponds with muddy bottoms and abundant aquatic plants in Lijiang City, Yunnan, China; Shallow to medium-depth water area with muddy bottoms in Lake Jianhu, Jianchuan County, Yunnan, China.

Dalipaludina pyramidella (Du, Yang & Chen, 2011), comb. nov.

Trochotaia pyramidella Du, Yang & Chen, 2011: 85–89 (Yousuo village of Er-Yuan County, Yunnan, China).

Material examined

Holotype , KIZ-DLN20100035; 19 paratypes, KIZ-DLN20100036 to KIZ-DLN20100054; 3 specimens in ZMB, 7 specimens in NJW, collected by Jiao-Wei Ning from 1 metre depth in the ponds of Yousuo Village, Eryuan County.

Description

Shell (Fig. 6A–D) large, conical, thin, greenish brown to brown in colour; up to six whorls at adulthood, including one relatively smooth protoconch whorl, apex acute, spire low; each teleoconch whorls with one strong keel at suture, above suture smooth, with two rings of short periostracum setae, base of shell smooth, with many rather thin weak spiral threads; aperture ovate, almost half of shell in height, lip thin and simple, umbilicus narrow, sometimes bordered by a keel.

Figure 6. 

Shell and operculum of Dalipaludina pyramidella. A–C. Specimen collected from Eryuan County, ZMB.Moll. 122714; D. Varieties collected from Eryuan County, ZMB Moll. 122714; E. Exterior (left) and interior (right) surface of operculum. Scale bar: 1 cm, B–D with the same scale bar of A.

Operculum (Fig. 6E) corneous, ovate, rather thin, yellow or orange, with red nuclear region, exterior surface of operculum rather smooth, inner opercular region relatively small, nuclear region smooth.

Radular (according to Du et al. 2011) central tooth with one broad central denticle and three to four small sharp cusps on either side; lateral tooth with one broad central denticle and four small sharp cusps on either; inner marginal tooth with one broad central denticle and two small sharp cusps on either side; outer marginal tooth with 9 small sharp cusps.

Figure 7. 

SEM photo of the radula and the protoconch of Dalipaludina species. A, B. Radula of Dalipaludina delavayana, A-ZMB.Moll. 181719, B-ZMB.Moll. 122707; C, D. Radula of Dalipaludina oxytropoides, ZMB.Moll. 250844; E, F. Radula of Dalipaludina occidentalis, ZMB.Moll. 122713. Abbreviations: ct–central teeth; lt–lateral teeth; imt–inner marginal teeth; omt–outer marginal teeth. Scale bars: 100 µm.

Remarks

This species differs from the other species of Dalipaludina by having a relatively smooth shell with lower spire. Du et al. (2011) assigned this species to Trochotaia mainly based on the strongly keeled shell with lower spire. However, characters of the operculum, embryonic shells, the reduced number of cusps on the outer marginal teeth (9 in D. pyramidella vs 14–16 in Trochotaia trochoides) and the distribution in Yunnan strongly support its assignment to Dalipaludina. Species of Trochotaia have a very different operculum according to Zhang and von Rintelen (2021). This species is also quite similar to Cipangopaludina miyagii Kuroda, 1941 endemic to Kaohsiung, S Taiwan, China. It can be distinguished from C. miyagii by having a thinner shell, a shell base with many rather thin weak spiral threads, and a narrowly open umbilicus with a keel around it. The recommended Chinese name of this species is “塔形理田螺”.

Habitat and distribution

shallow ponds with muddy bottoms and aquatic plant Ottelia acuminata (Gagnep.) in Yousuo Village, Eryuan County, Yunnan, China.

Discussion

The molecular and morphological data strongly support that four endemic viviparid species from Yunnan, formerly classified as species of Cipangopaludina, Sinotaia, Margarya or Trochotaia, should be assigned to a new genus described here: Dalipaludina. The former genus-level classification of these species was primarily based on shell morphology (Du et al. 2011; Qian et al. 2014). However, the shell morphology of freshwater snails can be quite similar due to convergence even between different genera. One remarkable example is the case of three highly sculptured but phylogenetically distinct viviparid genera (Margarya, Tchangmargarya and Anularya) endemic to the plateau lakes of Yunnan (Zhang et al. 2015). Our study has confirmed once again the importance of using an integrative approach in generic classification. In additional to shell characters, the operculum and radula, especially the cusps on the outer marginal teeth, provide important data for genus-level taxonomy of Viviparidae as well. The species-level phylogeny solely based on COI has been considered problematic in Viviparidae (Hirano et al. 2019b). However, at the genus level, it does not seem to be a big problem here (Fig. 2). Our BI tree based on partial COI sequences is broadly consistent with the genus-level topology for the Bellamyinae derived from an analysis of multiple genes in Stelbrink et al. (2020), suggesting that Dalipaludina likely falls into clade A of Bellamyinae proposed by Stelbrink et al. (2020).

Four species of Dalipaludina can be differentiated based on shell morphology. The scatter plot (Fig. 8) shows that D. delavayana has a larger and taller shell; D. pyramidella and D. occidentalis both have a lower spire, and D. pyramidella can be distinguished from D. occidentalis based on its less inflated whorls and comparatively smooth shell surface. The COI phylogeny has supported the reciprocal monophyly of the three sequenced species. The populations of D. occidentalis from two localities roughly 50 km apart cluster togther in the tree, without obvious geographic structuring (Fig. 2). The keeled, shouldered form of D. occidentalis (Fig. 5E) cannot be differentiated from the smooth form based on p-distance or phylogeny of COI as well. Moreover, the four species of Dalipaludina have allopatric distributions (Fig. 1B), and we have yet to find any lake or pond with more than one Dalipaludina species. Based on these results derived from morphological, molecular, and distribution data, we believe that there are four valid species of Dalipaludina.

Figure 8. 

Comparison of Dalipaludina species with respect to parameters H (in mm) and W/H.

Intraspecific diversity of shell morphology varies among the four species. Dalipaludina delavayana and D. pyramidella both display a relatively low intraspecific diversity; morphological diversity within D. occidentalis is higher; and that of D. oxytropoides is by far the highest within the genus. An integrative study combining morphometrics and a COI phylogeny of D. oxytropoides from Lake Lugu (“Margarya oxytropoides” in Wiese et al. 2022) showed that it should be considered a single, but highly variable species. We have also observed many intermediate forms in this species.

In contrast to the other three endemic genera of Viviparidae from Yunnan (Margarya, Tchangmargarya and Anularya) mostly found in medium-depth to deep water (Zhang et al. 2015), Dalipaludina displays a preference for shallow water. In addition to large lakes like Lake Lugu or Jianhu, Dalipaludina also can be found in small shallow ponds, such as the artificial ponds for farming the aquatic vegetable Ottelia acuminata in Eryuan County (D. pyramidella) and an unnamed small pond on the top of Sheshan Hill in Lijiang (D. occidentalis). D. oxytropoides and D. delavayana are also more common in shallow water areas than in deeper water. However, Dalipaludina is only found in lentic environments. It has never been found in rivers or any other lotic environment.

The lowest altitude where we have found Dalipaludina species is in Eryuan County, around 1974 m a.s.l., and one historical record of D. oxytropoides in Zhaotong County from ~1920 m a.s.l. (Heude 1886); Lake Lugu harbouring D. oxytropoides is ~2698 m a.s.l., which is the highest altitude record of Viviparidae (Fig. 1B). Among the other three viviparid genera endemic to Yunnan Plateau, only Margarya is found within a similar but smaller altitudinal range (1886–2192 m a.s.l), while Tchangmargarya (1770–1907 m a.s.l.) and Anularya (1284–1721 m a.s.l.) inhabit a relatively lower altitude with no overlap with that of Dalipaludina. Viviparids from elsewhere in the world occur at much lower altitudes. In conclusion, Dalipaludina displays an adaptation to the shallow lentic environment in high altitude regions, and occurs at the highest altitude of any viviparid.

With the discovery of the new genus Dalipaludina, the Yunnan Plateau now harbours four endemic genera of Viviparidae, confirming again that it is the most important diversity hotspot of Viviparidae in the world. However, almost all of these species are threatened by human activities such as overharvesting, pollution, and habitat destruction (Yang et al. 2004; Zhang et al. 2015). D. pyramidella nearly disappeared from its only known site, the ponds in Eryuan County, during our recent surveys in 2021; the present population of D. oxytropoides in Lake Lugu has declined dramatically compared to that in the 1990s according to local fishermen. Most endemic viviparid species of Margarya, Tchangmargarya and Anularya are on the national Red List of China (Wang and Xie 2005), and one species Margarya melanioides Nevill, 1877 is a Class 2 species under state protection in the latest List of State Key Protected Wild Animals of China in 2021. Since all four Dalipaludina species are restricted to just one or two lakes or several small ponds, specific conservation measures should be applied urgently for each species based on more detailed population biology and ecology studies. The phylogeny based on genomic data, such as data from exon capture method, can also improve our understanding of the evolution of these rare species endemic to the plateau lentic environment.

Acknowledgments

The authors thank Jiao-Wei Ning from Yuxi, Yunnan and Hong-Quan Xiang (Yuxi Agriculture Agricultural Technology College) for collecting specimens, Bernhard Schurian (Museum für Naturkunde, Berlin) for help with photography, Kaibaryer Meng (Institute of Zoology, Chinese Academy of Sciences, Beijing), Adam Baldinger and Alana Rivera (Museum of Comparative Zoology at Harvard University, Cambridge) for providing the important type specimens for study.

References

  • Annandale TN (1924) Zoological results of the Percy Sladen Trust Expedition to Yunnan under the leadership of Professor J.W. Gregory, F.R.S., 1922. Aquatic gastropod molluscs. Journal and Proceedings of the Asiatic Society of Bengal, New Series 19(9): 399–422.
  • Du LN, Chen XY, Yang JX, Aldridge DC (2012) A survey of Molluscan compositions in four plateau lakes, Northwest Yunnan [In Chinese]. China. Journal of Hydroecology 33: 44–49.
  • Heude PM (1886) Notes sur les mollusques terrestres de la vallée du fleuve Bleu. Mémoires Concernant l’Histoire Naturelle de l’Empire Chinois 1: 1–188.
  • Hirano T, Saito T, Tsunamoto Y, Koseki J, Prozorova L, Do VT, Matsuoka K, Nakai K, Suyama Y, Chiba S (2019a) Role of ancient lakes in genetic and phenotypic diversification of freshwater snails. Molecular Ecology 28(23): 5032–5051. https://doi.org/10.1111/mec.15272
  • Hirano T, Saito T, Tsunamoto Y, Koseki J, Ye B, Do VT, Miura O, Suyama Y, Chiba S (2019b) Enigmatic incongruence between mtDNA and nDNA revealed by multi-locus phylogenomic analyses in freshwater snails. Scientific Reports 9(1): e6223. https://doi.org/10.1038/s41598-019-42682-0
  • Kobelt W (1909) Systematisches Conchylien-Cabinet von Martini und Chemnitz. Die Raublungenschnecken (Agnatha). Zweite Abtheilung: Streptaxidae und Daudebardiidae. Bauer & Raspe, Nuremberg, 128 pp.
  • 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. https://doi.org/10.1093/molbev/msy096
  • Liu YY, Zhang WZ, Wang YX (1995) Distribution of the Viviparidae from China (Mollusk: Gastropoda) [In Chinese].Transactions of the Chinese Society of Malacology 5–6: 8–16.
  • Qian ZX, Fang YF, He J (2014) A conchological review of Bellamyinae (Gastropoda: Viviparidae) of China. Shell Discoveries 1(3): 3–12.
  • 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
  • Stelbrink B, Richter R, Köhler F, Strong EE, van Bocxlaer B, Albrecht C, Hauffe T, Page TJ, Aldridge DC, Bogan AE, Du LN, Manuel-Santos MR, Marwoto RM, Shirokaya AA, von Rintelen T (2020) Global diversification dynamics since the Jurassic: Low dispersal and habitat-dependent evolution explain hotspots of diversity and shell disparity in river snails (Viviparidae). Systematic Biology 69(5): 944–961. https://doi.org/10.1093/sysbio/syaa011
  • Van Bocxlaer B, Strong EE (2019) Viviparidae Gray, 1847. In: Lydeard C, Cummings KS (Eds) Freshwater Mollusks of the World: A Distribution Atlas. Johns Hopkins University Press, Baltimore, 43–50.
  • Van Bocxlaer B, Strong EE, Richter R, Stelbrink B, Von Rintelen T (2017) Anatomical and genetic data reveal that Rivularia Heude, 1890 belongs to Viviparinae (Gastropoda: Viviparidae). Zoological Journal of the Linnean Society 182(1): 1–23. https://doi.org/10.1093/zoolinnean/zlx014
  • Wang S, Xie Y (2005) China Species Red List (Vol. III). Invertebrates. Higher Education Press, Beijing, 299–306.
  • Wiese R, Harrington K, Hartmann K, Hethke M, von Rintelen T, Zhang HC, Zhang LJ, Riedel F (2022) Can fractal dimensions objectivize gastropod shell morphometrics? A case study from Lake Lugu (SW China). Ecology and Evolution 12(3): e8622. https://doi.org/10.1002/ece3.8622
  • Yen TC (1942) A review of Chinese gastropods in the British Museum. The Journal of Molluscan Studies 24(5–6): 170–289.
  • Zhang L (1990) A new species of genus Cipangopaludina from Dianchi Lake in Yunnan Province, China. Acta Zootaxonomica Sinica 15(1): 25–27. [In Chinese]
  • Zhang LJ (2017) A new species of freshwater snail Tchangmargarya (Gastropoda: Viviparidae) endemic to a vanished small lake in Yunnan, China. Molluscan Research 37(4): 252–257. https://doi.org/10.1080/13235818.2017.1323369
  • 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 NG, Hao TX, Wu CY, Chen YX, Zhang W, Li JK, Zhang Y (1997) Primary investigation of freshwater Gastropoda in Yunnan Province. Studia Marina Sinica 39(2): 15–26. [In Chinese]
  • Zhang LJ, Chen SC, Yang LT, Jin L, Köhler F (2015) Systematic revision of the freshwater snail Margarya Nevill, 1877 (Mollusca: Viviparidae) endemic to the ancient lakes of Yunnan, China, with description of new taxa. Zoological Journal of the Linnean Society 174(4): 760–800. https://doi.org/10.1111/zoj.12260

Supplementary material

Supplementary material 1 

Accession numbers and museum voucher numbers

Le-Jia Zhang, Li-Na Du, Thomas von Rintelen

Data type: table (excel document)

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 (11.97 kb)
login to comment