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Research Article
Two new genera and three new species of exceptionally rare and endemic freshwater mussels (Bivalvia, Unionidae) from the Mekong Basin
expand article infoEkgachai Jeratthitikul‡, Chirasak Sutcharit§, Pongpun Prasankok|
‡ Mahidol University, Bangkok, Thailand
§ Chulalongkorn University, Bangkok, Thailand
| Suranaree University of Technology, Nakhon Ratchasima, Thailand

Corresponding author: Pongpun Prasankok ( prasankok@sut.ac.th )

Academic editor: Matthias Glaubrecht
© 2024 Ekgachai Jeratthitikul, Chirasak Sutcharit, Pongpun Prasankok.
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: Jeratthitikul E, Sutcharit C, Prasankok P (2024) Two new genera and three new species of exceptionally rare and endemic freshwater mussels (Bivalvia, Unionidae) from the Mekong Basin. Zoosystematics and Evolution 100(4): 1333-1345. https://doi.org/10.3897/zse.100.130929
ZooBank: urn:lsid:zoobank.org:pub:4D6C62E4-224B-4AB5-A251-AA7ABEE66D74
Open Access

Abstract

Two new genera and three new species of freshwater mussels in the tribe Pseudodontini (Bivalvia, Unionidae) are described from the Mekong Basin in Thailand based on an integrative taxonomic study involving morphology and multi-locus phylogenetic analyses (mitochondrial COI and 16S, and nuclear 28S genes). The monotypic genus, Lannanaia kokensis gen. et sp. nov., presents unique features of being rather compressed, sub-trigonal in outline with short and high shell, and with a distinct posterior wing. Another new genus, Isannaia gen. nov., is characterized by having a thin and moderately inflated shell, with rhomboidal to ovate outline. It includes two lineages that are genetically separated by 3.54% uncorrected COI p-distance, and are herein described as I. fortunata sp. nov. and I. occultata sp. nov. Phylogenetic analyses further revealed that these two new genera were nested within a clade of subtribe Pseudodontina, and with pairwise uncorrected COI p-distance to other genera ranging from 11.42 to 15.66%. Based on the present data, Lannanaia gen. nov. is known only from the Kok River in the north of Thailand, whereas the two species of Isannaia gen. nov. are restricted to tributaries of the Mekong River in the northeast of Thailand. The discovery of rare and probably endemic freshwater mussels in the Mekong Basin thus again highlights the importance of this region among freshwater biodiversity hotspots of the world.

Key Words

Freshwater mussels, Indochina, Mekong Basin, multi-locus phylogeny, new taxa, Thailand

Introduction

Freshwater mussels in the family Unionidae represent the most diverse group among bivalves that have evolved to live in freshwater environments, with more than 750 extant representatives described worldwide, excluding Antarctica and South America (Graf and Cummings 2021). They are particularly diverse in East Asia, which hosts approximately 40% of all described species (Graf and Cummings 2021). The region is thus considered one of the most important global hotspots of freshwater mussel diversity, alongside North America, due not only to its high species richness but also to the notable endemism (Zieritz et al. 2018; Graf and Cummings 2021), highlighting the need for comprehensive research and conservation efforts. Examples of this endemism include more than one hundred species that are restricted to a single river basin (e.g., Bolotov et al. 2020, 2023; Konopleva et al. 2021; Pfeiffer et al. 2021; Jeratthitikul et al. 2022; Jeratthitikul and Sutcharit 2023; Kongim et al. 2023), as well as cases at the subfamily level, such as Modellnaiinae, which is exclusively distributed in the Mun River, a tributary of the Mekong River Basin in Thailand (Brandt 1974).

The tribe Pseudodontini, which currently contains around 48 extant species in nine genera, has been considered one of the endemic freshwater mussel groups occurring in Southeast Asian limnetic drainage systems (Bolotov et al. 2023, and references therein). Members of this tribe share characteristics such as the presence of V-shaped fossette at the posterior end of the hinge structure on the inner side of the shell and the reduction or absence of lateral teeth (Lopes-Lima et al. 2017). Recent multilocus phylogenetic approaches suggest that Pseudodontini consists of two well-defined clades that are biogeographically separated along the Salween-Mekong border. The subtribe Indopseudodontina is endemic to the western Indochina Subregion from Ayeyarwady to Salween basins, whereas the subtribe Pseudodontina (= Pilsbryoconchina Bolotov, Vikhrev & Tumpeesuwan in Bolotov et al. 2017b) is mainly distributed in the Chao Phraya and Mekong basins, with some taxa found to the east and southeast of the Salween-Mekong border (Bolotov et al. 2023). The Indopseudodontina currently consists of five species in one genus, Indopseudodon Prashad, 1922, whereas the Pseudodontina currently comprises 43 species in eight genera (Bolotov et al. 2023). These genera are recovered as well-defined clades in phylogenetic analyses (e.g., Jeratthitikul et al. 2021b; Bolotov et al. 2023; Konopleva et al. 2023).

Many Pseudodontini species exhibit restricted ranges and specialized habitat preferences, making them particularly vulnerable to extinction (i.e., Bolotov et al. 2020, 2023; Jeratthitikul et al. 2021b, 2022; Konopleva et al. 2021, 2023; Jeratthitikul and Sutcharit 2023). This susceptibility mirrors the global trend observed in other unionid species, which have experienced a significant decline in diversity over recent decades (Lopes-Lima et al. 2018; Aldridge et al. 2023).

A recent freshwater mollusc survey along the Mekong River and its tributaries in Thailand has yielded enigmatic specimens that were initially identified as belonging to the Pseudodontini. However, these specimens could not be attributed to any known genera and demonstrated evolutionary distinctiveness through multi-locus phylogenetic analyses. Consequently, they are formally described as two new genera and three new species in this study.

Material and methods

Specimen sampling and morphology examination

Animal use protocol was approved by the Faculty of Science, Mahidol University Animal Care and Use Committee, SCMU-ACUC (MUSC65-013-606).

Specimens of freshwater mussels were collected by hand from three tributaries of the Mekong River in Thailand, including 1) Kok River, Chiang Rai Province, northern Thailand; 2) Thuai River, Nakhon Phanom Province, northeastern Thailand, and 3) Yang Stream in Udon Thani Province, a tributary of Lam Pao River, Chi Basin, northeastern Thailand. Specimens were subjected to euthanization by the two-step method recommended by AVMA (AVMA 2020). In brief, the specimens were put in a container with freshwater, and then 95% (v/v) ethanol was added gradually, starting at a concentration of about 5% (v/v), until the foot and adductor muscles fully relaxed. The anesthetized specimens were subsequently fixed in 70% (v/v) ethanol. Soft bodies were then separated from the shells. Small pieces of foot tissues were cut and preserved in 95% (v/v) ethanol for further molecular analyses. The remaining soft parts were preserved in 70% (v/v) ethanol, while the shells were kept as dry specimens. Holotypes and paratypes of the new taxa are deposited in the Mahidol University Museum of Natural History, Department of Biology, Faculty of Science, Mahidol University, Bangkok, Thailand (MUMNH).

Shell morphology was examined based on shell shape, shell outline, shell size, shape and position of the umbo, hinge plate dentition, and muscle attachment scars. Shell dimensions were measured for shell length, height, and width using a digital Vernier caliper (±0.1 mm). Anatomical characteristics of soft parts (i.e., excurrent and incurrent aperture, labial palps, and gills) were also examined under a stereomicroscope.

Molecular analysis

Whole genomic DNA was extracted from the dissected foot tissues using a DNA extraction kit for animal tissue (NucleoSpin Tissue Extraction Kit, Macherey-Nagel, Germany) according to the manufacturer’s instructions. Fragments from the mitochondrial cytochrome c oxidase subunit-I gene (COI), the mitochondrial large ribosomal subunit rRNA gene (16S rRNA), and the nuclear 28S large ribosomal subunit rDNA gene (28S rRNA) were amplified and sequenced using primers LoboF1 and LoboR1 for COI (Lobo et al. 2013), 16sar-L-myt and 16Sbr-H-myt for 16S rRNA (Lydeard et al. 1996), and C1 and D2 for 28S rRNA (Jovelin and Justine 2001). Polymerase chain reaction (PCR) was conducted using a T100™ thermal cycler (BIO-RAD) with a final reaction volume of 30 μL (15 μL EmeraldAmp GT PCR Master Mix, 1.5 μL each primer, 10 ng template DNA, and distilled water up to 30 μL total volume). PCR conditions and processes were as follows: 94 °C for 3 min; 35 cycles of 94 °C for 30 s, annealing for 60 s (46 °C for COI and 16S rRNA, and 58 °C for 28S rRNA), 72 °C for 90 s, and a final extension at 72 °C for 5 min. Amplified PCR products were purified using MEGAquick-spinTM plus (Fragment DNA purification kit), and sequenced in both directions by an automated sequencer (ABI prism 3730XL). Contigs of forward and reverse sequences were edited and assembled using MEGA11 v. 11.0.13 (Tamura et al. 2021), and confirmed by visual inspection. The sequences obtained in this study have been uploaded in the GenBank Nucleotide sequence database under accession numbers OR987588–OR987596 for COI, OR987514–OR987522 for 16S rRNA, and OR987523–OR987531 for 28S rRNA (Suppl. material 1).

Phylogenetic analyses

The dataset for phylogenetic analyses includes haplotypes from nine individuals of the new taxa, along with 42 species from all other genera in the tribe Pseudodontini as the ingroup, and some representative taxa from other tribes (i.e., Schepmaniini, Gonideini, Chamberlainiini, Rectidentini, Contradentini, Ctenodesmini, and Lamprotulini) as the outgroup (Suppl. material 1). Apart from the newly obtained sequences in this study, these sequences were from a series of previously published studies that are available on the GenBank database (Huang et al. 2013; Pfeiffer and Graf 2015; Zieritz et al. 2016, 2020, 2021b; Bolotov et al. 2017a, 2017b, 2020, 2023; Lopes-Lima et al. 2017; Jeratthitikul et al. 2019, 2021a, 2021b, 2022; Konopleva et al. 2019, 2021, 2023; Froufe et al. 2020; Jeratthitikul and Sutcharit 2023; Kongim et al. 2023). The sequences were aligned for each gene separately by ClustalW algorithm using MEGA11, and later all three gene alignments were joined into one concatenated data matrix. The final concatenated alignment was divided into five partitions (3 codons of COI + 16S rRNA + 28S rRNA). The best-fit substitution model for each partition was determined using PartitionFinder2 v. 2.3.4 (Lanfear et al. 2017) under the corrected Akaike Information Criterion (AICc). Phylogenetic analyses were performed using the online CIPRES Science Gateway (Miller et al. 2010). The maximum likelihood (ML) phylogenetic tree was reconstructed in IQ-TREE v. 2.2.2.7 (Minh et al. 2020) with 10,000 replicates of ultrafast bootstrap analysis (UFBoot) to assess topology bootstrap support (BS; Hoang et al. 2018). The Bayesian Inference (BI) phylogenetic analysis was performed in MrBayes v. 3.2.7 (Ronquist et al. 2012). Four Monte Carlo Markov Chains of 10,000,000 generations were run with sampling every 1,000 generations. The resulting effective sample sizes were > 200 for all parameters. A clade of obtained phylogenetic trees was considered well supported when the ultrafast BS was ≥ 95% and Bayesian bipartition posterior probability (bpp) was ≥ 0.95 (San Mauro and Agorreta 2010; Hoang et al. 2018).

Genetic distance between pairs of genus/species clades recovered from the phylogenetic analysis was also estimated as uncorrected p-distance of COI gene sequences, using MEGA11.

Results

Phylogenetic analysis and genetic distances

Phylogenetic trees were estimated from a concatenated alignment of 1,935 bp (660 bp of COI, 500 bp of 16S rRNA, and 775 bp of 28S rRNA), and with the best-fit substitution model GTR+I+G for the first codon of COI, 16S rRNA, and 28S rRNA; GTR+I for the second codon of COI; and GTR+G for the third codon of COI. Both ML and BI analyses resulted in a highly congruent tree topology. Therefore, only the best ML tree from IQ-TREE is presented in Fig. 1.

Figure 1. 

Maximum likelihood (ML) tree of freshwater mussels in subfamily Gonideinae based on 1,935-bp concatenated alignment dataset of COI and 16S rRNA mitochondrial genes, and 28S rRNA nuclear gene. The numbers on nodes represent the bootstrap support (BS) from the ML analysis and the bipartition posterior probability (bpp) from the BI analysis, and are shown as ML/BI. Scale bar indicates the branch length.

The tree topology showed clear monophyly of the Pseudodontini with high BS and bpp (BS = 100%, bpp = 1). All Pseudodontini genera were recovered as highly supported clades (BS = 98–100%, bpp = 0.99–1). Among these genus-level clades, specimens from the Kok River, northern Thailand, were recovered as a monophyletic clade (BS = 100%, bpp = 1). This clade was nested with the monotypic genus Songkhlanaia Konopleva et al., 2023 with high support (BS = 99%, bpp = 0.99), and a deep divergence of 11.42% uncorrected COI p-distance (Table 1). Specimens of the unknown freshwater mussels from northeastern Thailand were recovered as two well-supported species-level clades (BS = 99–100%, bpp = 0.98–0.99). Each clade contained specimens from a single locality, and differed from each other by 3.54% uncorrected COI p-distance. The two were grouped into a genus-level clade with high support (BS = 100%, bpp = 1), and then nested with the clade of Pilsbryoconcha Simpson, 1900, but without significant support (BS = 73%, bpp = 0.58). Nevertheless, in terms of genetic similarity, this group of freshwater mussels from northeastern Thailand showed the closest genetic similarity to Namkongnaia Jeratthitikul et al., 2021, with an uncorrected COI p-distance of 11.77%.

Table 1.
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Mean genetic distances (uncorrected p-distance: %±SD) based on 660 bp COI gene fragment sequences among genera of the tribe Pseudodontini (below diagonal), and between species within each genus (in bold).

1 2 3 4 5 6 7 8 9 10 11
1. Lannanaia gen. nov. n/a
2. Isannaia gen. nov. 15.40 ± 0.17 3.08 ± 0.15
3. Namkongnaia 14.27 ± 0.40 11.77 ± 0.39 5.38
4. Pseudodon 14.01 ± 0.77 13.80 ± 0.76 11.04 ± 1.02 7.03 ± 3.14
5. Bineurus 13.61 ± 0.47 13.86 ± 0.72 11.58 ± 0.70 11.91 ± 0.59 4.14 ± 1.25
6. Thaiconcha 15.66 ± 0.13 14.55 ± 0.36 12.04 ± 0.27 13.44 ± 0.56 11.59 ± 0.52 3.26 ± 0.67
7. Sundadontina 13.38 ± 0.95 13.72 ± 0.71 11.79 ± 0.77 12.46 ± 1.01 12.24 ± 1.19 12.96 ± 1.44 9.92 ± 3.20
8. Nyeinchanconcha 12.72 ± 0.00 13.49 ± 0.27 11.34 ± 0.08 12.58 ± 0.53 11.13 ± 0.88 12.89 ± 0.40 10.54 ± 0.52 n/a
9. Pilsbryoconcha 12.74 ± 0.94 14.21 ± 0.99 12.09 ± 0.80 12.13 ± 1.38 11.41 ± 0.95 12.57 ± 0.95 12.44 ± 1.34 11.54 ± 0.98 8.98 ± 1.57
10. Songkhlanaia 11.42 ± 0.00 13.12 ± 0.29 10.28 ± 0.32 11.18 ± 0.56 10.67 ± 0.62 12.67 ± 0.07 11.73 ± 1.56 11.26 ± 0.00 11.17 ± 0.79 n/a
11. Indopseudodon 13.76 ± 1.59 15.02 ± 0.66 12.11 ± 0.49 13.07 ± 0.80 12.70 ± 0.96 13.47 ± 0.54 13.31 ± 0.66 12.64 ± 1.12 12.46 ± 0.98 11.72 ± 0.86 9.29 ± 3.21

These two newly discovered genus-level clades showed unique conchological characteristics distinguishable from other genera in the Pseudodontini (see taxonomic account below). Therefore, they are herein described as Lannanaia kokensis gen. et sp. nov. for the clade from northern Thailand and Isannaia gen. nov. for the clade from northeastern Thailand. The two species-level clades of the latter genus are described as new species: I. fortunata sp. nov. for the clade from the Thuai River and I. occultata sp. nov. for the clade from Yang Stream, Chi Basin.

The Pseudodontini is further grouped into two larger clades with high support (BS = 99–100%, bpp = 1), corresponding to the currently accepted subtribe classification (e.g. Bolotov et al. 2023). The clade of the Indopseudodontina contained only one genus, Indopseudodon. In contrast, the clade of the Pseudodontina contained ten genera, including the two genera newly described in this study. However, the phylogenetic relationship among genera within the Pseudodontina was still uncertain, except for Bineurus Simpson, 1900, Thaiconcha Bolotov et al., 2020, Nyeinchanconcha Bolotov et al., 2020, and Sundadontina Bolotov et al., 2020, which were grouped into a strongly supported clade (BS = 100%, bpp = 0.99), and a clear sister relationship between Songkhlanaia and Lannanaia gen. nov. (BS = 99%, bpp = 0.99). Pairwise genetic distances as expressed by uncorrected COI p-distance among genera in Pseudodontina ranged from 10.28% in Songkhlanaia versus Namkongnaia to 15.66% in Lannanaia gen. nov. versus Thaiconcha, and with an average of 12.50% (Table 1).

Taxonomic account

Family Unionidae Rafinesque, 1820

Subfamily Gonideinae Ortmann, 1916

Tribe Pseudodontini Frierson, 1927

Pseudodontina Frierson, 1927

Remarks

Currently the Pseudodontina is composed of 45 species in ten genera, including the new taxa described herein (Bolotov et al. 2023). These genera are Bineurus Simpson, 1900 (5 species), Isannaia gen. nov. (2 species), Lannanaia gen. nov. (1 species) Namkongnaia Jeratthitikul et al., 2021 (2 species), Nyeinchanconcha Bolotov et al., 2020 (1 species), Pilsbryoconcha Simpson, 1900 (9 species), Pseudodon Gould, 1844 (9 species), Songkhlanaia Konopleva et al., 2023 (1 species), Sundadontina Bolotov et al., 2020 (12 species), and Thaiconcha Bolotov et al., 2020 (3 species). Pseudodon mekongi (Bolotov et al., 2020) was nested within a clade of Pseudodon vondembuschianus (Lea, 1840) in the phylogenetic analysis in this study. Therefore, we recognize it as a subspecies of P. vondembuschianus.

Lannanaia gen. nov.

https://zoobank.org/6999F44B-DA95-451C-BDAC-E088A0EF84CE

Type species

Lannanaia kokensis gen. et sp. nov., by present designation.

Species included

The new genus currently contains only one species, L. kokensis sp. nov.

Diagnosis

This new genus is distinguished from other Pseudodontini genera by its compressed, rather short and high shell, with sub-trigonal outline, and distinct posterior wing. The hinge plate is without dentition, or with very rudimentary broad pseudocardinal tooth in each valve, and posterior end of the hinge structure with rather wide V-shaped fossette (Fig. 2). It is also represented as a distinct clade in multi-locus phylogenetic analyses (Fig. 1).

Figure 2. 

Shells of Lannanaia kokensis sp. nov., showing the inner side of the right valve, the outer side of the left valve, and the dorsal view of both valves. A. Holotype MUMNH-UNI0825; B. Paratype MUMNH-UNI0824. Scale bars: 10 mm.

Description

Shell medium-sized, thin, rather short and high, winged, sub-trigonal outline, inequilateral, rather compressed. Anterior margin rounded; posterior margin angulate, somewhat pointed. Umbo tiny, not prominent, eroded. Ligament long, very narrow. Hinge without dentition, or with very rudimentary broad pseudocardinal tooth in each valve; posterior end of the hinge structure with rather wide V-shaped fossette. Anterior adductor muscle scar very shallow, ovate, contiguous with anterior pedal retractor muscle scar, but separated from anterior protractor scar; posterior adductor muscle scar round, very shallow, almost invisible. Pallial line very faint, continuous. Umbo cavity shallow.

Etymology

The generic name “Lannanaia” is from the word “Lanna”, a name of the kingdom located in present-day northern Thailand during the 13th to 18th centuries, and the Greek word “naiad” meaning freshwater mussel. The name of this genus thus means “freshwater mussels from Lanna” or “freshwater mussels from northern Thailand”. The gender is feminine.

Distribution

Endemic to Kok River, a tributary of the Mekong River in northern Thailand (Fig. 3).

Figure 3. 

Map showing type localities of the new species: circle Lannanaia kokensis sp. nov., triangle Isannaia fortunata sp. nov., and square Isannaia occultata sp. nov. Map was generated using QGIS v3.24.3 with the outline of Mekong basin from the Freshwater Ecoregions of the World (Abell et al. 2008), river and lake topology from the HydroSHEDS database (https://www.hydrosheds.org), and the map raster data from the NASA EARTHDATA (https://www.earthdata.nasa.gov/).

Remarks

The phylogenetic tree generated in this study places Lannanaia gen. nov. as a sister group to Songkhlanaia, with strong support from both analyses (BS = 100%, bpp = 0.99; Fig. 1), and with a 11.42% p-distance based on the COI gene (Table 1). Both genera share general characteristics of a short shell outline and rather compressed shell. However, Lannanaia gen. nov. can be distinguished from Songkhlanaia by having a sub-trigonal shell outline and a curved ventral margin (vs a rectangular shell outline and an almost straight ventral margin in Songkhlanaia), distinct posterior wing (vs absent posterior wing), and not prominent umbo (vs slightly elevated and easily visible umbo) (Konopleva et al. 2023). In addition, the biogeography of the two genera is also distinct. The monotypic genus Songkhlanaia was described from the Songkhla Lake Basin in southern Thailand (Konopleva et al. 2023), while Lannanaia gen. nov. is restricted to the Kok River, a tributary of the Mekong River in northern Thailand.

Lannanaia kokensis sp. nov.

https://zoobank.org/873CE4DB-F862-43DF-BFF7-8863B7CBA3C7
Figs 1, 2, 3

Type material

Holotype. Thailand • Chiang Rai Province, Mueang Chiang Rai District, Rop Wiang Subdistrict, Kok River; 19.9131°N, 99.8697°E; E. Jeratthitikul and K. Wisittikoson leg.; MUMNH-UNI0825; shell length 57.2 mm, shell height 40.8 mm, and shell width 14.4 mm. Paratype. Thailand • 1 shell; same collection data as for holotype; MUMNH-UNI0824.

Description

Shell medium-sized (shell length 57.1–57.2 mm, shell height 40.8–43.8 mm, shell width 14.4–14.8 mm; Table 2), thin, rather short and high (H/L ratio = 0.71–0.77), winged, sub-trigonal outline, inequilateral, rather compressed. Anterior margin rounded; posterior margin angulate, somewhat pointed; ventral margin curved. Dorsal margin straight; anterior low and short, gradually elevated to posterior end; posterior end high and winged. Umbo tiny, not prominent, eroded. Posterior ridge wide and obtuse, not prominent; posterior slope with two fine lines running as curved line from umbo to posterior margin. Periostracum thin, greenish to dark brown, the eroded part white to coppery-brown. Shell surface with very fine growth lines. Ligament long, very narrow, dark brown. Hinge without dentition, or with very rudimentary broad pseudocardinal tooth in each valve; posterior end of hinge structure with rather broad V-shaped fossette. Anterior adductor muscle scar very shallow, ovate, contiguous with anterior pedal retractor muscle scar, but separated from anterior protractor scar; posterior adductor muscle scar round, very shallow, almost invisible. Pallial line very faint, continuous. Umbo cavity shallow. Nacre blue-whitish.

Table 2.
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Shell measurements and GenBank accession numbers for the type series of the new species described in this study. Measurements in millimetres (mm).

Taxa Status of specimen Specimen voucher Shell length Shell height Shell width Genbank accession
COI 16S rRNA 28S rRNA
Lannanaia kokensis sp. nov. Holotype MUMNH-UNI0825 57.2 40.8 14.4 OR987589 OR987515 OR987524
Paratype MUMNH-UNI0824 57.1 43.8 14.8 OR987588 OR987514 OR987523
Isannaia fortunata sp. nov. Holotype MUMNH-UNI1950 54.1 29.9 18.4 OR987590 OR987516 OR987525
Paratype MUMNH-UNI1951 45.5 25.6 14.4 OR987591 OR987517 OR987526
Paratype MUMNH-UNI1952 61.4 35.1 21.6 OR987592 OR987518 OR987527
Paratype MUMNH-UNI1953 43.3 24.5 13.4 OR987593 OR987519 OR987528
Isannaia occultata sp. nov. Holotype MUMNH-UNI2895 53.8 31.7 20.4 OR987594 OR987520 OR987529
Paratype MUMNH-UNI2896 43.8 26.7 13.8 OR987595 OR987521 OR987530
Paratype MUMNH-UNI2897 47.9 27.9 14.8 OR987596 OR987522 OR987531

Exhalant aperture smooth, shorter than inhalant. Inhalant aperture with a row of conical papillae, varying in length. Small epithelial fold divides exhalant and inhalant apertures. Gills elongated and slightly ribbed; outer gills much narrower (about half) than inner gills; anterior margin of inner gills slightly longer than that of outer gills. Labial palps elongate, round at tip. Glochidia unknown.

Etymology

The species name “kokensis” refers to the type locality, the Kok River in Chiang Rai Province, northern Thailand.

Distribution

This new species is known only from the type locality.

Remarks

Two living specimens were collected from a small stream that is a tributary to the Kok River, with a muddy bottom. We searched multiple times and locations for this species but failed to find additional specimens. In contrast, Lens contradens (Lea, 1838) and Pilsbryoconcha exilis (Lea, 1838) were found nearby in high abundance, both living and as empty shells. We assume this new species has a low population density and is possibly endemic to the Kok River Basin.

Isannaia gen. nov.

https://zoobank.org/ADD0E6C8-E5BD-4E05-828B-FC89CA662F02

Type species

Isannaia fortunata gen. et sp. nov., by present designation.

Species included

The new genus is currently composed of two species, the type species and I. occultata sp. nov.

Diagnosis

The new genus is distinguished from other genera in the Pseudodontini by its thin and moderately inflated shell, and with rhomboidal to ovate outline (Fig. 4). The overall shape is somewhat elongated but relatively shorter when compared to those of Bineurus, Pilsbryoconcha or Namkongnaia. The anterior margin is rounded, shouldered, and the posterior margin is truncated to rounded. Its pseudocardinal teeth are rather small, one on each valve, hill-like or triangulate shape, and less developed on the left valve. Its umbo is slightly elevated and the umbo cavity moderately deep. It is also represented as a distinct clade in multi-locus phylogenetic analyses (Fig. 1).

Figure 4. 

Shells of Isannaia gen. nov., showing the inner side of the right valve, the outer side of the left valve, and the dorsal view of both valves. A. Holotype (MUMNH-UNI1950) and B. Paratype (MUMNH-UNI1952) of Isannaia fortunata sp. nov.; C. Holotype (MUMNH-UNI2895) and D. Paratype (MUMNH-UNI2897) of Isannaia occultata sp. nov. Scale bars: 10 mm.

Description

Shell medium-sized, rather thin, rhomboidal to ovate outline, elongate, very inequilateral, moderately inflated; anterior margin rounded, shouldered; posterior margin truncated to rounded. Umbo slightly elevated and usually eroded. Ligament very narrow. One shallow hill-like or triangulate pseudocardinal tooth on right valve; left valve with one less developed hill-like to tubercule-like pseudocardinal tooth. End of hinge structure with V-shaped fossette. Anterior adductor muscle scar shallow to well-developed, ovate, contiguous with pedal retractor and anterior protractor muscle scars; posterior adductor muscle scar round, very shallow. Pallial line faint to well-marked, continuous. Umbo cavity moderately deep.

Etymology

The generic name “Isannaia” is from the word “Isan”, the name of the region of northeastern Thailand, and Greek word “naiad” meaning freshwater mussel. The name of this genus thus means “freshwater mussels from northeastern Thailand”. The gender is feminine.

Distribution

Endemic to tributaries of the Mekong River in northeastern Thailand (Fig. 3).

Remarks

Phylogenetic analyses have failed to recover a robustly supported position of Isannaia gen. nov. among other Pseudodontina genera. However, in terms of genetic distance, it is nearest to Namkongnaia, with a separation of 11.77% p-distance of the COI gene (Table 1). Isannaia gen. nov. can be easily distinguished from Namkongnaia by having a much shorter shell (Jeratthitikul et al. 2021b).

In general, Isannaia gen. nov. bears conchological resemblance to certain species within the Sundadontina, such as S. brandti Bolotov et al., 2020 or S. plugpomenica Konopleva et al., 2023 (Bolotov et al. 2020; Konopleva et al. 2023). Nevertheless, its thin shell with less developed pseudocardinal teeth set it apart from the latter genus, which typically features a thicker and sturdier shell with stout and tubercular-like pseudocardinal teeth (Bolotov et al. 2020).

Isannaia fortunata sp. nov.

https://zoobank.org/B84B9959-FEBF-4AFF-9E9B-B1B965BE8605
Figs 1, 3, 4A, B

Type material

Holotype. Thailand • Nakhon Phanom Province, Tha Uthen District, Tha Uthen Subdistrict, Thuai River; 17.5621°N, 104.6090°E; E. Jeratthitikul, P. Prasankok, and K. Wisittikoson leg.; MUMNH-UNI1950; shell length 54.13 mm, shell height 29.96 mm, and shell width 14.39 mm. Paratypes. Thailand • 3 shells; same collection data as for holotype; MUMNH-UNI1951 to UNI1953.

Description

Shell medium-sized (shell length 43.3–61.4 mm, shell height 24.5–35.1 mm, shell width 13.4–18.4 mm; Table 2), rhomboidal, elongate (H/L ratio = 0.55–0.57), rather thin, very inequilateral, moderately inflated. Anterior margin rounded, rather constricted, shouldered; posterior margin truncated, slightly elongate ventrally; ventral margin slightly curved. Dorsal margin slightly curved; anterior low, posterior end slightly higher. Umbo slightly elevated, heavily eroded even in young specimens. Posterior ridge wide and obtuse, not prominent; posterior slope with two faint lines running from umbo to posterior margin. Periostracum thin, brownish-black, eroded part white to coppery-brown. Shell surface with visible growth lines. Ligament long, very narrow, dark brown. One very shallow hill-like or triangulate pseudocardinal tooth on right valve; pseudocardinal tooth on left valve less developed, tubercule-like, or almost absent. Posterior end of hinge structure with small V-shaped fossette. Anterior adductor muscle scar shallow, ovate, contiguous with pedal retractor and anterior protractor muscle scars; posterior adductor muscle scar round, very shallow, almost invisible. Pallial line faint, continuous. Umbo cavity moderately deep, with 1 to 2 tiny muscle scars in the cavity. Nacre blue-whitish with yellowish tint around the umbo cavity.

Exhalant aperture almost smooth, with a row of tiny tubercle-like papillae on edge of aperture, shorter than inhalant. Inhalant aperture with a row of conical papillae, varying in length. Small epithelial fold divides exhalant and inhalant apertures. Gills elongated and slightly ribbed; inner gills slightly wider, and anterior margin of inner gills slightly longer than that of outer gills. Labial palps elongate, slightly curved, pointed at tip. Glochidia unknown.

Etymology

The species name “fortunata” is derived from the Latin adjective “fortunatus” meaning lucky. This name refers to the fortuitous discovery of this rare freshwater species.

Distribution

This new species is known only from the type locality.

Remarks

This new species is rare and restricted to the Thuai River. Specimens were collected from hard clay along the river bank. It was found sympatrically with several unionid species endemic to Songkhram Basin and nearby tributaries of the Mekong Basin, including Lens maenamensis Pfeiffer et al., 2021, Physunio pellucidus Pfeiffer et al., 2021, Ensidens jaculus (Rochebrune, 1882), Scabiellus songkramensis (Kongim et.al., 2015), Pseudodon cambodjensis (Petit de la Saussaye, 1865) and Scabies scobinatus (Lea, 1856).

Isannaia occultata sp. nov.

https://zoobank.org/F83569B6-8E5D-43BE-9DD4-4D44C9AD937B
Figs 1, 3, 4C, D

Type material

Holotype. Thailand • Udon Thani Province, Wang Sam Mo District, Nong Ya Sai Subdistrict, Yang Stream (a tributary of Lam Pao River); 16.9886°N, 103.3638°E; K. Wisittikoson leg.; MUMNH-UNI2895; shell length 53.84 mm, shell height 31.68 mm, and shell width 20.41 mm. Paratypes. Thailand • 2 shells; same collection data as for holotype; MUMNH-UNI2896, UNI2897.

Diagnosis

This species resembles I. fortunata sp. nov., but it can be distinguished by the overall shell shape being more rounded (vs rhomboidal), slightly higher shell (H/L ratio 0.58–0.60 vs 0.55–0.57), wider anterior margin (vs rather constricted), more truncated and rounded posterior margin (vs slightly ventrally elongate), less curved ventral margin (vs curved ventral margin). It also differs in characteristics inside the shell by having higher and more triangulate pseudocardinal tooth on the right valve (vs very shallow and hill-like pseudocardinal tooth), well-developed muscle scars (vs very shallow and sometimes almost invisible), 3 to 5 well-developed muscle scars in the umbo cavity (vs 1 to 2 tiny muscle scars in the umbo cavity), and well-marked pallial line (vs faint pallial line). It can also be distinguished from its congeners by fixed nucleotide substitution positions in the COI gene fragment of base A on the 54th, 114th, 363rd, and 414th; base T on the 90th, 141st, 591st, and 609th; base C on the 57th, and 216th; and base G on 150th, 117th, 192nd, 558th, 480th, 552nd, 627th, 639th, 645th, and 657th.

Description

Shell medium-sized (shell length 43.8–53.8 mm, shell height 26.7–31.7 mm, shell width 13.8–20.4 mm; Table 2), ovate to rectangular, elongate (H/L ratio = 0.58–0.60), rather thin, very inequilateral, moderately inflated. Anterior margin rounded, shouldered; posterior margin truncated to rounded; ventral margin straight to slightly curved. Dorsal margin slightly curved; anterior low, posterior end slightly higher. Umbo slightly elevated, heavily eroded even in young specimens. Posterior ridge wide and obtuse, not prominent; posterior slope with two faint lines running from umbo to posterior margin, invisible in old specimens. Periostracum thin, brown to brownish-black, eroded part white to coppery-brown. Shell surface with visible growth lines. Ligament long, very narrow, dark brown. One hill-like or triangulate pseudocardinal tooth on right valve; pseudocardinal tooth on left valve less developed, hill-like. Posterior end of hinge structure with small V-shaped fossette. Anterior adductor muscle scar well-developed, ovate, contiguous with anterior pedal retractor and anterior protractor muscle scars; posterior adductor muscle scar round, shallow, contiguous with posterior retractor muscle scars; posterior retractor muscle scars triangular. Pallial line well-marked, continuous. Umbo cavity moderately deep, with 3 to 5 muscle scars in cavity. Nacre blue-whitish to yellowish, more yellowish toward the umbo cavity.

Exhalant aperture almost smooth, with a row of tiny tubercle-like papillae on the edge of aperture, similar length with inhalant. Inhalant aperture with a row of very short conical papillae. Small epithelial fold divides exhalant and inhalant apertures. Gills elongated and slightly ribbed; inner gills slightly wider, and anterior margin of inner gills slightly longer than that of outer gills. Labial palps elongate, slightly curved, pointed at tip. Glochidia unknown.

Etymology

The species name “occultata” is derived from the Latin adjective “occultatus” meaning concealed or hidden, a reference to this new freshwater mussel being hidden in a small stream far from the main river.

Distribution

This new species is known only from the type locality, Yang Stream in Udon Thani Province. Yang Stream is a headwater tributary of the Lam Pao River in the Chi River Basin. The type locality is above the Lam Pao Dam.

Remarks

This new species is rare and difficult to find despite repeated surveys. They were collected from a network of dense tree roots on a clay wall of a small stream. Nearby, there was a community of unionid mussels living in muddy or sandy substrate of the stream bottom, including Scabies phaselus (Lea, 1856), Physunio modelli Brandt, 1974, Namkongnaia inkhavilayi Jeratthitikul et al., 2021, P. exilis, S. brandti, and Thaiconcha callifera (Martens, 1860).

Discussion

Our findings have revealed previously unknown freshwater mussels within the Mekong basin, comprising two distinct genera and three new species. The discovery of new taxa in this study increases the known diversity of the Pseudodontini to eleven genera with 50 extant species. This makes this tribe the most species-rich clade endemic to Southeast Asia, more than in Contradentini (35 species) or Gonideini (27 species), for example (Graf and Cummings 2021; Bolotov et al. 2023). In the past decade, the diversity within this tribe has significantly increased, with several lineages (species and genera) being recently described from Indochina (Bolotov et al. 2020, 2023; Jeratthitikul et al. 2021b, 2022; Konopleva et al. 2021, 2023; Jeratthitikul and Sutcharit 2023). This highlights the unique evolutionary history of the region and underscores the tribe’s remarkable diversity.

Both two new genera share shell characteristics with other genera in Pseudodontini by having a V-shaped fossette at the posterior end of the hinge structure, and absence of lateral teeth (Lopes-Lima et al. 2017). However, we cannot confirm another distinctive feature of the tribe which is the presence of a double-looped or W-shaped pattern on the umbonal area (Lopes-Lima et al. 2017), because the umbonal area of all of the examined specimens was extensively eroded, even in young specimens. Similarly, we were unable to examine the glochidia of the new genera since no brooding individuals were collected during this study. However, it is likely that their glochidia exist as an unhooked and semi-elliptical structure, which is the typical shape of glochidia among the Gonideinae (Pfeiffer and Graf 2015; Lopes-Lima et al. 2017).

Molecular phylogenetic analyses further strongly support the inclusion of these two new genera within the subtribe Pseudodontina, with high support values (BS = 99%, bpp = 1). The two new genera possess shell characteristics that fit well with other members of the subtribe, such as fairly thin shells with much reduced or even lacking pseudocardinal teeth (Bolotov et al. 2020, 2023; Konopleva et al. 2021; Jeratthitikul et al. 2022). These shell characteristics make them different from members in the subtribe Indopseudodontina, which generally have thicker shells and possess well-developed knob-like pseudocardinal teeth (Bolotov et al. 2023). However, the phylogenetic relationships among genera within the Pseudodontina in this study, as well as in some previous studies that used similar genetic markers (i.e., a concatenated dataset of COI + 16S rRNA + 28S rRNA), remain largely unclear and still controversial (e.g., Jeratthitikul et al. 2021b; Bolotov et al. 2023; Konopleva et al. 2023). To clarify these relationships, future investigations should incorporate longer nucleotide sequences and additional gene fragments, or utilize more informative molecular markers such as mitogenomic or nuclear genomic data which have been previously successfully employed in the phylogenetic studies of freshwater mussels (Pfeiffer et al. 2019, 2021; Froufe et al. 2020; Zieritz et al. 2021a; Wu et al. 2024).

The three new species described in this study are rare, restricted to small geographic areas, and likely confined to a single drainage. Species with limited ranges are more vulnerable to threats from human activities and climate change compared to widely distributed species (Randklev et al. 2015; da Silva et al. 2023), with some already extinct on a local scale, such as several endemic species in North America (Bogan 1993; Haag and Williams 2014). Urgent conservation efforts are needed. However, essential biological data, such as their geographical distribution, habitat preferences, and fish hosts for their glochidia, remain unknown. Addressing these knowledge gaps is crucial for developing effective conservation strategies and for further understanding freshwater mussel biodiversity in Southeast Asia.

Ethical statement

The animal uses in this study have been approved by the Faculty of Science, Mahidol University Animal Care and Use Committee, SCMU-ACUC (MUSC65-013-606).

Author contributions

EJ and PP developed the concept of the study. All authors collected specimens. EJ performed phylogenetic analyses and prepared taxonomic accounts with input from CS. CS prepared shell images. EJ prepared the manuscript and all illustrations. All authors discussed, gave input and acknowledged the final version of the manuscript.

Acknowledgements

We thank K. Wisittikoson and S. Klomthong for their assistance in collecting samples, and extend our thanks to D.J. Anderson for grammar checking and comments.

This study was financially supported by SUT Research and Development Fund (IRD1-104-66-12-22).

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Supplementary material

Supplementary material 1 

List of voucher specimens with GenBank accession numbers used in phylogenetic analysis

Ekgachai Jeratthitikul, Chirasak Sutcharit, Pongpun Prasankok

Data type: docx

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.
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