Phylogeographic Affinities, Distribution and Population Status of the Non-Native Asian Pond Mussels Sinanodonta Lauta and S. Woodiana in Kazakhstan

Ecologica Montenegrina 27: 22-34 (2020) This journal is available online at: www.biotaxa.org/em

Phylogeographic affinities, distribution and population status of the non-native Asian pond mussels Sinanodonta lauta and S. woodiana in Kazakhstan

ALEXANDER V. KONDAKOV1,2, EKATERINA S. KONOPLEVA1,2,*, ILYA V. VIKHREV1,2, YULIA V. BESPALAYA1,2, MIKHAIL YU. GOFAROV1,2, MIKHAIL B. KABAKOV1, ALENA A. TOMILOVA1, MAXIM V. VINARSKI3,4 & IVAN N. BOLOTOV1,2

1Federal Center for Integrated Arctic Research, Russian Academy of Sciences, Northern Dvina Emb. 23, 163000 Arkhangelsk, Russia 2Northern Arctic Federal University, Northern Dvina Emb. 17, 163002 Arkhangelsk, Russia 3Saint-Petersburg State University, Universitetskaya Emb. 7/9, 199034 Saint-Petersburg, Russia 4Omsk State Pedagogical University, Tukhachevskogo Emb. 14, 644099 Omsk, Russia *Corresponding author. E-mail: [email protected]

Received 26 November 2019 │ Accepted by V. Pešić: 29 December 2019 │ Published online 10 January 2020.

Abstract Here, we present an integrative review of the non-native Sinanodonta spp. from Kazakhstan based on molecular and morphological data. Sinanodonta woodiana (Lea, 1834) inhabits the Syr Darya River, while two species, S. woodiana and S. lauta (Martens, 1877), have established viable populations in the Ili River basin, a tributary of the Balkhash Lake. The latter species was probably introduced in 1961-1971 from the Sungari River, a Chinese tributary of the Amur River. A distribution map of the two Sinanodonta species spreading in Middle Asia is provided. In Kazakhstan and Uzbekistan, these species were recorded from endorheic drainages limiting their native expansion throughout the region, although further human-mediated dispersal events are expected. There are no reliable records of these alien freshwater mussels from Kyrgyzstan, Tajikistan, and Turkmenistan. Our study highlight that Sinanodonta lauta represents one more invasive lineage of the Asian pond mussels and that this East Asian species can successfully colonize plain water bodies of inland desert areas such as Middle Asia.

Key words: Asian pond mussels, aquatic invasion, Ili River, Balkhash Lake, Syr Darya River, mitochondrial DNA.

Introduction

The Asian pond mussel Sinanodonta woodiana (Lea, 1834) represents a complex of several cryptic species, whose native range spreads throughout East Asia from the Russian Far East, China and Japan to Vietnam (Bolotov et al. 2016; Kondakov et al. 2018; Konečný et al. 2018). Two species-level mitochondrial DNA (mtDNA) lineages in this complex were considered successful invaders sharing completely allopatric non- native ranges (temperate vs tropical latitudes) (Bolotov et al. 2016). The temperate lineage of Sinanodonta woodiana has established invasive populations in Europe, Siberia, and Uzbekistan (Bespalaya et al. 2018;

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Kondakov et al. 2018; Urbańska et al. 2019), while a single tropical non-native population of this cryptic species has been discovered in northern Myanmar (Vikhrev et al. 2017). The tropical invasive lineage of Sinanodonta woodiana colonized Malaysia, Indonesia, Singapore, and the Philippines (Bolotov et al. 2016; Zieritz et al. 2016, 2018; Vikhrev et al. 2017; Stelbrink et al. 2018). It was shown that the temperate invasive lineage of Sinanodonta woodiana reveals a broader host range and faster glochidial development than those of native freshwater mussels in Europe (Huber and Geist 2019) and that this alien species may compete with native species for hosts and resources (Urbańska et al. 2019). A preliminary taxonomic review of the Sinanodonta woodiana species complex by means of a molecular approach indicates that there are at least eight separate species-level lineages, some of which were linked to available nominal taxa (Kondakov et al. 2018). The taxonomic identity of the two invasive lineages is still under discussion. Kondakov et al. (2018) suggested that the temperate invasive lineage could be linked to Sinanodonta gibba, while the tropical invasive lineage can be considered S. cf. woodiana. However, Arthur E. Bogan (pers. comm., 2018) recommended using the name Sinanodonta woodiana for both invasive lineages until the final revision of this species complex is done. Here, we follow this taxonomic opinion. Additionally, we previously noted Sinanodonta lauta (Martens, 1877) under the name Sinanodonta ovata Bogatov & Starobogatov, 1996 (e.g. Bespalaya et al. 2018; Kondakov et al. 2018), which is considered a junior synonym of the first species (Manuel Lopes-Lima, pers. comm., 2019). Two nominal Sinanodonta species, i.e. S. gibba (Benson in Cantor, 1842) and S. puerorum (Heude, 1880), were recorded from Kazakhstan (Uvaliyeva 2001; Uvaliyeva and Kan 2001). These records were not listed in the analytical catalogue of fresh and brackish water molluscs of Russia and adjacent countries as being published in non-peer-reviewed papers and without data allowing one to check the correctness of species identification (Vinarski and Kantor 2016). The taxonomic affinities and modern status of the non- native Sinanodonta populations in Kazakhstan were unknown. It was unclear, which lineage(s) of the Sinanodonta woodiana species complex inhabits this country, because molecular sequence data on Kazakhstan’s populations was not available. Taking into account the concerns, outlined above, this study aims to: (1) assess the presence and modern status of non-native Sinanodonta populations in Kazakhstan, (2) clarify the current distribution of this taxon in the country using published and original data, (3) estimate the origin and phylogeographic affinities of Kazakhstan’s lineage(s) by means of a molecular approach, and (4) revise the taxonomic identity of the lineage(s) from Kazakhstan.

Material and methods

Data sampling. Samples of Sinanodonta spp. were collected by wading from two localities in the Ili River basin, a tributary of the Balkhash Lake, on 15-16.ix.2019 (Table 1; Figs. 1-2). Tissue snips taken from each specimen were preserved in 96% ethanol (Bespalaya et al. 2018). The tissue and shell samples are deposited in the Russian Museum of Biodiversity Hotspots [RMBH], Federal Center for Integrated Arctic Research, Russian Academy of Sciences, Arkhangelsk, Russia [voucher No. RMBH biv762, RMBH biv763 and RMBH biv764].

Molecular and phylogeographic analyses. The cytochrome c oxidase subunit I (COI) gene fragment was amplified and sequenced from 24 specimens as described in our previous study (Bolotov et al. 2016). Additionally, we collected 10 COI sequences of Sinanodonta lauta and 62 COI sequences of the temperate lineage of S. woodiana from NCBI GenBank (Table 2). To study the phylogeographic affinities of Kazakhstan’s sample, we used a median joining network approach with Network v. 4.6.1.3 software with default settings (Bandelt et al. 1999).

Morphological study and age estimation. Shell length, shell height, and shell width (all at maximum diameter) were measured by a digital caliper (Digimatic Coolant Proof, Mitutoyo, Japan) as described previously (Bespalaya et al. 2018). Based on the shell measurements, two morphometric indexes, i.e. the shell convexity index (SCI = width/length ratio × 100) and the shell elongation index (SEI = height/length ratio × 100) (Bolotov et al. 2018), were calculated. To estimate the age of mussels, we counted growth rings which are clearly visible on the shell surface in case of Sinanodonta spp.

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Range mapping. The distribution of the non-native Sinanodonta spp. in Middle Asia was mapped on the basis of published georeferenced records and original data (Table 1) with ESRI ArcGIS 10 software (www.esri.com/arcgis). The base of the map has been compiled from free open sources such as Natural Earth Free Vector and Raster Map Data (http://www.naturalearthdata.com), GSHHG (http://www.soest.hawaii.edu/pwessel/gshhg), HydroSHEDS (http://www.hydrosheds.org), and GADM (http://gadm.org).

Results

Non-native populations of Sinanodonta spp. from Kazakhstan. We found that two Sinanodonta species, i.e. S. lauta and S. woodiana, have established viable populations in Kazakhstan (Table 1; Figs. 1-3). Morphologically, these species are indistinguishable, and we applied a molecular approach for their identification. Our COI data indicate that Sinanodonta woodiana inhabits the middle section of the Ili River basin, where this species was identified from the Kapchagay Reservoir, while S. lauta was recorded from an irrigation channel of the Ili River near Topar settlement, in the downstream section of the basin (Table 1).

Table 1. Status and distribution of non-native populations of Sinanodonta lauta and the temperate invasive lineage of S. woodiana throughout endorheic basins of Middle Asia.

Endorheic Population Country Locality N E Species Reference basin status Kazakhstan Ili River => Bays in southern part of 45.8073 74.2723 S. lauta Old record Uvaliyeva and Kan Lake Balkhash Lake Balkhash (2001) Kazakhstan Lake Balkhash Mynanaral Bay of Lake 45.4217 73.6690 S. lauta Old record, a Abrosov (1973) Balkhash possible site of the initial invasion Kazakhstan Ili River => Ili River near Topar 45.0402 74.9288 S. lauta Recent viable This study Lake Balkhash settlement population Kazakhstan Ili River => Kapchagay Reservoir 43.7925 77.1469 S. woodiana Recent viable Uvaliyeva (2001); Lake Balkhash population this study Kazakhstan Syr Darya River Syr Darya River below 41.2877 67.9500 S. woodiana Old record Uvaliyeva (2001) => Aral Sea the Chardara Dam Uzbekistan Syr Darya River Mouth of the Chirchik 40.8994 68.7086 S. woodiana Recent viable Izzatullaev and => Aral Sea River population Boymurodov (2016) Uzbekistan Syr Darya River Chinaz Channel 40.9286 68.7900 S. woodiana Recent viable Izzatullaev and => Aral Sea population Boymurodov (2016) Uzbekistan Amu Darya Amu Darya River near 41.5358 60.8864 S. woodiana Recent viable Kondakov et al. River => Aral the town of Xonqa population (2018) Sea Uzbekistan Zarafshon River Dargom Channel 39.7953 66.7447 S. woodiana Recent viable Izzatullaev and population Boymurodov (2016) Uzbekistan Zarafshon River Zarafshon River near 39.7028 67.0094 S. woodiana Recent viable Izzatullaev and Samarkand population Boymurodov (2016) Uzbekistan Zarafshon River Kattakurgan Reservoir 39.8257 66.3049 S. woodiana Recent viable Izzatullaev and population Boymurodov (2016) Uzbekistan Zarafshon River Chelek fish farm 40.0155 67.0425 S. woodiana Recent viable Izzatullaev and population Boymurodov (2016) Uzbekistan Zarafshon River Ponds near the town of 39.5278 67.1575 S. woodiana Recent viable Izzatullaev and Taylaq population Boymurodov (2016)

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Table 2. List of COI sequences of Sinanodonta lauta and the temperate invasive lineage of S. woodiana used in this study

Species Region Country Population COI GenBank acc. no. Reference S. lauta Middle Asia Kazakhstan: Ili River near Topar Alien MN809939 This study S. lauta Middle Asia Kazakhstan: Ili River near Topar Alien MN809940 This study S. lauta Middle Asia Kazakhstan: Ili River near Topar Alien MN809941 This study S. lauta Middle Asia Kazakhstan: Ili River near Topar Alien MN809942 This study S. lauta Middle Asia Kazakhstan: Ili River near Topar Alien MN809943 This study S. lauta Middle Asia Kazakhstan: Ili River near Topar Alien MN809944 This study S. lauta Middle Asia Kazakhstan: Ili River near Topar Alien MN809945 This study S. lauta Middle Asia Kazakhstan: Ili River near Topar Alien MN809946 This study S. lauta Middle Asia Kazakhstan: Ili River near Topar Alien MN809947 This study S. lauta Middle Asia Kazakhstan: Ili River near Topar Alien MN809948 This study S. lauta Middle Asia Kazakhstan: Ili River near Topar Alien MN809949 This study S. lauta Middle Asia Kazakhstan: Ili River near Topar Alien MN809950 This study S. lauta Middle Asia Kazakhstan: Ili River near Topar Alien MN809951 This study S. lauta Middle Asia Kazakhstan: Ili River near Topar Alien MN809952 This study S. lauta East Asia Russia: Eastern Siberia (Yenisei) Alien KY561633 Bespalaya et al. (2018) S. lauta East Asia Russia: Eastern Siberia (Yenisei) Alien KY978737 Bespalaya et al. (2018) S. lauta East Asia Russia: Eastern Siberia (Yenisei) Alien KY978739 Bespalaya et al. (2018) S. lauta East Asia Russia: Eastern Siberia (Yenisei) Alien KY978740 Bespalaya et al. (2018) S. lauta East Asia Russia: Eastern Siberia (Yenisei) Alien KY978741 Bespalaya et al. (2018) S. lauta East Asia Russia: Primorsky Krai Native KY978742 Bespalaya et al. (2018) S. lauta East Asia Russia: Primorsky Krai Native KY978743 Bespalaya et al. (2018) S. lauta East Asia South Korea Native GQ451869 GenBank S. lauta East Asia South Korea Native GQ451870 GenBank S. lauta East Asia Japan Native AB055627 GenBank S. woodiana Middle Asia Kazakhstan: Kapchagay Alien MN809929 This study Reservoir S. woodiana Middle Asia Kazakhstan: Kapchagay Alien MN809930 This study Reservoir S. woodiana Middle Asia Kazakhstan: Kapchagay Alien MN809931 This study Reservoir S. woodiana Middle Asia Kazakhstan: Kapchagay Alien MN809932 This study Reservoir S. woodiana Middle Asia Kazakhstan: Kapchagay Alien MN809933 This study Reservoir S. woodiana Middle Asia Kazakhstan: Kapchagay Alien MN809934 This study Reservoir S. woodiana Middle Asia Kazakhstan: Kapchagay Alien MN809935 This study Reservoir S. woodiana Middle Asia Kazakhstan: Kapchagay Alien MN809936 This study Reservoir S. woodiana Middle Asia Kazakhstan: Kapchagay Alien MN809937 This study Reservoir S. woodiana Middle Asia Kazakhstan: Kapchagay Alien MN809938 This study Reservoir S. woodiana Middle Asia Uzbekistan Alien MG581711 Kondakov et al. (2018) S. woodiana Middle Asia Uzbekistan Alien MG581712 Kondakov et al. (2018) S. woodiana Europe Ukraine Alien JQ253893 GenBank S. woodiana Europe Ukraine Alien JQ253894 GenBank

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Species Region Country Population COI GenBank acc. no. Reference S. woodiana Europe Poland Alien AF468683 Soroka (2005) S. woodiana Europe Poland Alien EF440349 Soroka (2010) S. woodiana Europe Poland Alien HQ283344 GenBank S. woodiana Europe Poland Alien HQ283345 GenBank S. woodiana Europe Poland Alien HQ283346 GenBank S. woodiana Europe Poland Alien HQ283347 GenBank S. woodiana Europe Poland Alien HQ283348 GenBank S. woodiana Europe Poland Alien KJ125078 Soroka et al. (2014) S. woodiana Europe Hungary Alien KJ125079 Soroka et al. (2014) S. woodiana Europe Italy Alien KF731775 Froufe et al. (2017) S. woodiana Europe Italy Alien KF731776 Froufe et al. (2017) S. woodiana Europe Italy Alien KF731777 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414328 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414329 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414330 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414331 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414332 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414333 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414334 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414335 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414336 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414337 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414338 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414339 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414340 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414341 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414342 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414343 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414344 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414345 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414346 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414347 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414348 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414349 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414350 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414351 Froufe et al. (2017) S. woodiana Europe Italy Alien MF414352 Froufe et al. (2017) S. woodiana Southeast Asia Myanmar Alien MF497807 Vikhrev et al. (2017) S. woodiana Southeast Asia Myanmar Alien MF497808 Vikhrev et al. (2017) S. woodiana Southeast Asia Myanmar Alien MF497809 Vikhrev et al. (2017) S. woodiana East Asia Russia: Eastern Siberia (Yenisei) Alien KY978735 Bespalaya et al. (2018) S. woodiana East Asia Russia: Eastern Siberia (Yenisei) Alien KY978736 Bespalaya et al. (2018) S. woodiana East Asia Russia: Eastern Siberia (Yenisei) Alien KY978738 Bespalaya et al. (2018) S. woodiana East Asia China Native KJ434482 GenBank

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Species Region Country Population COI GenBank acc. no. Reference S. woodiana East Asia China Native KJ434483 GenBank S. woodiana East Asia China Native KJ434484 GenBank S. woodiana East Asia China Native KJ434485 GenBank S. woodiana East Asia China Native KJ434486 GenBank S. woodiana East Asia China Native KM272949 Zhang et al. (2016) S. woodiana East Asia China Native MG463060 Huang et al. (2018) S. woodiana East Asia China Native MG463068 Huang et al. (2018) S. woodiana East Asia China Native MG463069 Huang et al. (2018) S. woodiana East Asia China Native MG463070 Huang et al. (2018) S. woodiana East Asia China Native MG463073 Huang et al. (2018) S. woodiana East Asia China Native MG463075 Huang et al. (2018) S. woodiana East Asia China Native MG463076 Huang et al. (2018) S. woodiana East Asia China Native MG463078 Huang et al. (2018) S. woodiana East Asia China Native MG463080 Huang et al. (2018)

Figure 1. Ranges and population status of Sinanodonta lauta and the temperate invasive lineage of S. woodiana in Middle Asia. The circles indicate recent well-established populations, and the squares indicate old unconfirmed records of S. lauta (green) and S. woodiana (red). The green star indicates the site of putative initial introduction of S. lauta to Kazakhstan between 1961 and 1971. The color filling indicates freshwater basins, in which non-native populations of S. lauta and S. woodiana (light green) and S. woodiana (pink) were established. The species occurrence data are presented in Table 1.

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Figure 2. Habitat of a viable population of Sinanodonta lauta in Kazakhstan: irrigation channel of the Ili River near Topar settlement. (Photo: Ilya Vikhrev).

Morphometric data and age. Morphometric and age characteristics of our samples are presented in Table 3 and Fig. 4. These data reveal that Sinanodonta lauta and S. woodiana seem to be lacking any reliable differences by conchological features. The maximum age values for both species are 9-10 years (Table 3).

Table 3. Size and age of the non-native Sinanodonta lauta and the temperate invasive lineage of S. woodiana from Kazakhstan.

Sinanodonta woodiana, Kapchagay Sinanodonta lauta, Ili River near Topar Parameters Reservoir (N = 10) settlement (N = 20) Mean ± s.e.m. Min-max Mean ± s.e.m. Min-max Shell length (mm) 155.9±8.1 124.6–187.1 116.7±7.7 54.9–170.7 Shell height (mm) 99.6 ±4.5 79.1–122.2 76.1±4.1 41.0–103.3 Shell width (mm) 54.6±2.8 43.8–70.0 44.2±2.5 18.3–59.2 Snell convexity index (SCI) 35.25±1.27 30.11–40.36 38.43±0.86 33.37–45.11 Snell elongation index 64.16±1.14 58.46–71.31 66.43±1.20 57.31–76.22 (SEI) Age (years) 7.6±0.8 4–10 5.4±0.5 2–9

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Figure 3. Shells of Sinanodonta lauta and the temperate invasive lineage of S. woodiana from Kazakhstan. A-C) S. lauta, irrigation channel of the Ili River near Topar settlement [specimens RMBH biv764_7, RMBH biv763_1, and RMBH biv763_5, respectively]. D-F) Temperate invasive lineage of S. woodiana, Kapchagay Reservoir [specimens RMBH biv762_3, RMBH biv762_5, and RMBH biv762_2, respectively]. Scale bar = 20 mm. (Photo: Ekaterina Konopleva).

Phylogeographic data. Sinanodonta woodiana from Kazakhstan shares a single COI haplotype that is presented in non-native populations in European countries, Myanmar (Irrawaddy River), and Siberia (Yenisei River) (Fig. 5). Sinanodonta lauta also reveals a single COI haplotype that was recorded from an alien population in Eastern Siberia (Yenisei River) (Fig. 5).

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Figure 4. Shell morphometry and age of Sinanodonta lauta (N = 20) and the temperate invasive lineage of S. woodiana (N = 10) from Kazakhstan. A) Shell length vs shell height scatterplot. B) Shell length vs shell width scatterplot. C) Shell length vs age scatterplot. D) Shell elongation index vs shell convexity index scatterplot.

Discussion

Distribution of the non-native Sinanodonta spp. in Middle Asia. Unexpectedly, two non-native Sinanodonta species, i.e. S. lauta and the temperate invasive lineage of S. woodiana, were recovered from Kazakhstan under this study. Our results confirm that these taxa should be considered two cryptic species that could be distinguished by means of a molecular approach only (Kondakov et al. 2018). A well-established population of Sinanodonta lauta was found in the downstream section of Ili River basin, while S. woodiana was recorded from the Kapchagay Reservoir, a large artificial water body in the middle section of the Ili River. A sympatric occurrence of these two species was previously recorded from the Yenisei River, Eastern Siberia (Bespalaya et al. 2018). Sinanodonta woodiana also inhabits the Zarafshon and Amu Darya rivers in Uzbekistan, and the Syr Darya River in Uzbekistan and Kazakhstan, in which this species established viable populations (Izzatullaev and Boymurodov 2016; Kondakov et al. 2018). We could conclude that earlier recordings of Sinanodonta gibba and S. puerorum from Kazakhstan (Uvaliyeva 2001; Uvaliyeva and Kan 2001) refer to S. woodiana and(or) S. lauta. It is unclear how the nominal taxa Sinanodonta gibba and S. puerorum identified by earlier authors correspond to the two species due to the lack of morphological differences between them. No records of Sinanodonta spp. from other countries of Middle Asia (i.e. Kyrgyzstan, Tajikistan, and Turkmenistan) are known. In Kazakhstan and Uzbekistan, Sinanodonta species were recorded from

KONDAKOV ET AL. endorheic drainages such as rivers emptying into the Aral Sea and Balkhash Lake that prevents broader expansion of these invasive species via waterways. Extreme arid climate, mountain relief, and low density of river network throughout Middle Asia also reduce the possibility of their natural expansion throughout the region, while further human-mediated dispersal events (e.g. with farm fishes) within and beyond the country are highly expected. It was proposed that two European Anodonta species, i.e. A. anatina (Linnaeus, 1758) and A. cygnea (Linnaeus, 1758), were introduced to the Balkhash Lake drainage together with their host fish Sander lucioperca (Linnaeus, 1758) from the Ural River in 1958-1968 (Abrosov 1973; Asylbekova 2016). Later, a variety of “comparatory” nominal taxa of anodontine mussels, i.e. Colletopterum piscinale (Nilsson, 1822), C. ponderosum volgense (Shadin, 1938), C. kakandicum [sic!] Starobogatov & Izzatullaev, 1984, C. sogdianum (Kobelt,1896), was mentioned as occurring in Kazakhstan (Uvaliyeva 2001). These nominal taxa are junior synonyms of Anodonta anatina but in Kazakhstan these freshwater mussels were primarily found in sympatry with Sinanodonta spp. (Uvaliyeva 2001). According to the maximum shell length (up to 188 mm) (Uvaliyeva 2001), these samples may partly belong to Sinanodonta lauta and S. woodiana. We did not find these species in the two sites of the Ili River drainage surveyed in 2019.

Figure 5. Median joining networks of the COI sequences of Sinanodonta spp. The list of sequences is given in Table 2. The red numbers near branches indicate the numbers of nucleotide substitutions between haplotypes. Size of circles corresponds to the number of available sequences for each haplotype (smallest circle = 1 sequence). A) Temperate invasive lineage of Sinanodonta woodiana (N = 72). B) S. lauta (N = 24).

Introduction of Sinanodonta lauta to Kazakhstan. The Balkhash Lake and the Ili River in Kazakhstan were a focus of multiple introduction events of fish and invertebrate species during the period of 1950s- 1970s (Abrosov 1973). The silver and grass carp larvae were introduced in 1961-1971 from the Sungari River, a Chinese tributary of the Amur River (Abrosov 1973). Several small fishes, i.e. stone moroko Pseudorasbora parva (Temminck & Schlegel, 1846), Chinese false gudgeon Abbottina rivularis (Basilewsky, 1855), sharpbelly Hemiculter leucisculus (Basilewsky, 1855), Chinese sleeper Perccottus glenii Dybowski, 1877, and Amur goby Rhinogobius brunneus (Temminck & Schlegel, 1845), were accidentally introduced with these larvae. We assume that Sinanodonta lauta was introduced with these fishes, and this freshwater mussel species was initially appeared at the Mynanaral Bay of Lake Balkhash (Abrosov 1973). Based on a field study during the period of 1973-1974, it was found that muskrats Ondatra zibethicus (Linnaeus, 1766) in the Ili River delta consumed a number of large freshwater mussels (maximum shell

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ASIAN POND MUSSELS SINANODONTA LAUTA AND S. WOODIANA IN KAZAKHSTAN length 150 mm, maximum shell height 85 mm) that were identified as Anodonta sp. (Shiryaev 1976). This data indicates that a Sinanodonta species (probably S. lauta) has established an abundant non-native population in the Ili River delta at least since 1970. In our samples, Sinanodonta specimens of 150 mm long were 6-7 years old (see Fig. 4) supporting the hypothesis that the possible dating of initial invasion is confined to as the early 1960s. Sinanodonta lauta is distributed throughout South Korea, Japan, and the coastal rivers of the South Primorye Region in Russia (Kondakov et al. 2018). This species was not recorded from the Russian section of the Amur River, which is inhabited by another species, Sinanodonta schrenkii (Lea, 1870) (Kondakov et al. 2018). Although no data on freshwater mussels of the Sungari River are available, we can assume that Sinanodonta lauta can be found there, taking into account its broad range. A further spreading of this species into the mainstream of the Amur River can be limited by climatic parameters. A single haplotype of Sinanodonta lauta was found in Kazakhstan that is identical to the haplotype recorded from a non-native population of this species in the Yenisei River, Eastern Siberia (Bespalaya et al. 2018). This haplotype clusters with those from South Korea, but not from the Russian Far East and Japan (Bespalaya et al. 2018). In summary, we assume that the Sungari River was a possible source of Sinanodonta lauta invasion to Kazakhstan, while this preliminary hypothesis needs to be checked in the future using an expanded molecular dataset with sequences of this species from northern China.

Introduction of the temperate invasive lineage of Sinanodonta woodiana to Kazakhstan. A population of Sinanodonta woodiana from the Ili River in Kazakhstan shares the same COI haplotype as that in non-native populations from Europe, Myanmar and Eastern Siberia indicating their common origin from one source population from the Yangtze Basin, China (Huang et al. 2018; Kondakov et al. 2018). The molecular sequence data on a Sinanodonta population from the Syr Darya River in Kazakhstan and Uzbekistan is not available. However, we can assume that this population is originated from the same stock as that in the nearby Amu Darya River in Uzbekistan, in which the temperate lineage of Sinanodonta woodiana sharing a unique COI haplotype (a singleton) was found (Kondakov et al. 2018). In Uzbekistan, Sinanodonta woodiana appeared between 1960 and 1965 with two fish species, i.e. the silver carp Hypophthalmichthys molitrix (Valenciennes, 1844) and the grass carp Ctenopharyngodon idella (Valenciennes, 1844), introduced from the Yangtze Basin, China (Kondakov et al. 2018).

Acknowledgements This study was partly supported by the Ministry of Science and Higher Education of Russia, the Ministry of Europe and Foreign Affairs of France (MEAE), and the Ministry of Higher Education, Research and Innovation of France (MESRI) under project No. 05.616.21.0114 of the Hubert Curien Partnership (PHC) for the Franco-Russian Cooperation for Science and Technology (PHC Kolmogorov 2019). The work was carried out with the support and equipment of the Russian Museum of Biodiversity Hotspots, N. Laverov Federal Center for Integrated Arctic Research, Russian Academy of Sciences, a unique scientific setting (www.ckp-rf.ru/usu/352654).

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