Freshwater mussels are ecosystem engineers and keystone species in aquatic environments. Unfortunately, due to dramatic declines this fauna is among the most threatened globally. Here, we clarify the taxonomy and biogeography of Russian Unionidae species based on the most comprehensive multi-locus dataset sampled to date. We revise the distribution and assess the conservation status for each species. This fauna comprises 16 native species from 11 genera and 4 tribes: Anodonta, Pseudanodonta (Anodontini); Amuranodonta, Beringiana, Buldowskia, Cristaria, Sinanodonta (Cristariini); Middendorffinaia, Nodularia, Unio (Unionini); and Lanceolaria (Lanceolariini). No country-level endemic species are known in Russia, except for Buldowskia suifunica that may also occur in China. Sinanodonta woodiana, a non-native species, was introduced from China. Russia comprises the northern parts of Western and Eastern Palearctic subregions. The first subregion with six species encompasses a huge area from the western boundary of Russia to the Lena Basin in Siberia. The second subregion with 10 species covers the Amur Basin, rivers east of the Lena Basin, coastal basins of the Japan Sea, and the North Pacific Islands. The fauna of Russia primarily includes widespread generalist species that are here considered Least Concern (LC). However, Buldowskia suifunica and Sinanodonta lauta have restricted distributions and are assessed here as Vulnerable (VU) and Endangered (EN), respectively.
Freshwater mussels (order Unionida) are ecologically and economically important aquatic animals1 that are sensitive to water pollution, habitat loss, climate changes, and other negative anthropogenic and natural impacts2,3,4. These animals are widely distributed throughout Russia, representing keystone taxa in various water bodies of European Russia, Siberia, and the Russian Far East (mainland, Sakhalin, and Kurile Archipelago)5. However, freshwater mussels are not known to occur in the Polar Urals, Yamal and Taymyr peninsulas, Arctic Ocean Islands, and several mountain rivers (e.g. headwaters and middle reaches of the Amgun River, a tributary of the Amur River)6,7. Furthermore, several large, hard-to-reach river basins in Eastern Siberia and the Far East are still to be explored. In general, the freshwater mussel fauna in Russia largely reflects natural biogeographic and environmental patterns8, but a human footprint can also be traced in a few non-native populations of Unio and Sinanodonta species discovered in Siberia9,10.
The study of freshwater mussel systematics in Russia has a long history. The earliest taxonomic works on the unionid fauna of the Russian Empire and its regions appeared in the middle of the 19th century11,12,13,14,15,16. A few decades later, Alexander Buldowski developed a research project on economically important freshwater mussels of the Russian Far East17. Prof. Vladimir Zhadin published two large monographs with comprehensive reviews of the taxonomy, distribution, biology and ecology of freshwater mussels throughout the USSR5,6. In the early 1970s, Dr. Iya Moskvicheva presented three papers revising the taxonomy of the Unionidae from the Russian Far East, with supplementary data on freshwater mussels from Mongolia, Korea, Japan, and China7,18,19. During the next 40 years, Prof. Yaroslav Starobogatov and his disciples published a plethora of taxonomic works and identification guides on freshwater mussels from Russia, with a special focus on the Russian Far East and Siberia20,21,22,23,24. A thorough review of the body of historical literature is presented in the recent catalogue of molluscs from fresh and brackish water bodies of ex-USSR25.
However, all of these historical works were based solely on a morphological approach that has biased the taxonomic solutions due to the high variability of the shell shape, convexity and anatomical features in freshwater mussels26,27,28,29,30,31. While the taxonomy and distributional patterns of the Russian Margaritiferidae species have been clarified in detail using an integrative approach combining molecular, morphological and biogeographic evidences27,28,29,32,33, those of the family Unionidae, remain largely unclear25.
Graf26 provided the first critical taxonomic revision of freshwater mussels from the Northern Palearctic Region based on morphological features. Several local integrative revisions on Russian Unionidae taxa have been published, i.e. works on the taxonomy of the genera Cristaria34,35, Sinanodonta36,37, Anodonta38, Unio9, Nodularia39, and Middendorffinaia40. Lopes-Lima et al.41 revisited the tribal and generic clades within Unionidae using a global multi-locus phylogeny. A broad-scale review of freshwater mussels in Europe includes important information from European Russia42. Zieritz et al.43 compiled a useful summary of the recent knowledge on freshwater mussels of Asia. Recently, Lopes-Lima et al.44 prepared a comprehensive overview of freshwater mussels of East Asia with a description of several new taxa. However, a revision of the Unionidae in Russia is far from being complete, with multiple taxa having a doubtful taxonomic status, especially those from Siberia and the Far East.
Considering the issues outlined above, this study aims to provide an integrative revision of the Russian Unionidae based on the most comprehensive molecular data set sampled to date. We clarify the actual taxonomic richness of this family in Russia and describe the distribution patterns for each genus and species. Using the distribution data and our multi-locus phylogeny, we propose an updated biogeographic division for Unionidae of Russia and briefly discuss their species richness in each biogeographic region and province. Finally, we assess the conservation status of every valid species-level lineage and propose the national-level priorities for further freshwater mussel research in Russia.
Multi-locus phylogeny and species richness of the Russian Unionidae
Based on our novel multi-locus phylogeny (Fig. 1) and morphological data, we found that the Russian Unionidae fauna includes 16 native species from 11 genera and 4 tribes: Anodonta, Pseudanodonta (Anodontini), Amuranodonta, Beringiana, Buldowskia, Cristaria, Sinanodonta (Cristariini), Middendorffinaia, Nodularia, Unio (Unionini), and Lanceolaria (Lanceolariini) (Table 1 and Figs. 2–5). Additionally, the non-native species Sinanodonta woodiana was introduced from China. General information on each genus is given in Taxonomic Account. A modern taxonomic concept for every valid biological species in Russia is established in the Supplementary Note. The genus Anemina in its current understanding includes three highly divergent subclades (Fig. 1) that are here considered separate genera: Anemina s. str. (occurs in China, South Korea, and Japan but not in Russia), Amuranodonta (Amur Basin in Russia and China), and Buldowskia (Russian Far East, Korea, and Japan). Typical habitats of the Russian Unionidae are illustrated in Supplementary Figs. 1 and 2.
Two completely different unionid faunas are recorded in Russia (Figs. 6 and 7, Dataset 1, and Supplementary Fig. 3). The first faunal group includes six species from three European genera (Anodonta, Pseudanodonta, and Unio) occurring throughout European Russia east to Siberia up to the Lena River basin. The second group covers the Siberian rivers east of the Lena Basin, coastal basins of the Far East, and the huge Amur Basin. This faunal group contains 10 species from eight East Asian genera (Amuranodonta, Beringiana, Buldowskia, Cristaria, Lanceolaria, Middendorffinaia, Nodularia, and Sinanodonta).
Most species in the Russian fauna represent common taxa with broad distributions, and they are considered as Least Concern (LC): Amuranodonta kijaensis, Anodonta anatina, A. cygnea, Beringiana beringiana, Buldowskia shadini, Cristaria plicata, Lanceolaria grayii, Middendorffinaia mongolica, Nodularia douglasiae, Pseudanodonta complanata, Sinanodonta schrenkii, Unio pictorum, U. tumidus, and U. crassus (Dataset 2). However, Buldowskia suifunica and Sinanodonta lauta have restricted ranges and are assessed as Vulnerable (VU) and Endangered (EN), respectively (Dataset 2).
Family Unionidae Rafinesque, 1820
Subfamily Unioninae Rafinesque, 1820
Tribe Anodontini Rafinesque, 1820
Genus Anodonta Lamarck, 1799
=Colletopterum Bourguignat, 1880 (type species: Anodonta letourneuxi Bourguignat, 1870 = Anodonta anatina; subsequent designation by Simpson, 1900)25.
=Piscinaliana Bourguignat, 1881 (type species: Anodonta piscinalis Nilsson, 1823 = Anodonta anatina; subsequent designation by Locard (1890); unavailable name, primary junior homonym of Piscinaliana Paladilhe, 1866, Gastropoda, Valvatidae)25.
Type species: Mytilus cygneus Linnaeus, 1758 (monotypy).
Diagnosis. Anodonta is very similar to Pseudanodonta but can be distinguished by a broadly rounded anterior margin, a shorter hinge length from the umbo to the ligament’s posterior limit45, and shorter and less closely spaced papillae of the inhalant siphon46.
Distribution. Two species of this genus are recorded from Russia (Fig. 2A–D and Table 1). Anodonta anatina inhabits European Russia, Urals, and Siberia eastwards to the Lena River basin (Fig. 6D), while the range of A. cygnea is restricted to water bodies of the Baltic, Black, Azov, and Caspian Sea drainage basins (Fig. 6E).
Comments. Phylogenetically, this genus-level clade appears to be paraphyletic because it contains Pseudanodonta complanata lineage (Fig. 1). The taxonomy of these two genera has not been discussed due to insufficient molecular data on Anodonta species from North America.
Genus Pseudanodonta Bourguignat, 1876
Type species: Anodonta complanata Rossmässler, 1835 (subsequent designation by Westerlund, 1902)25.
Diagnosis. See above.
Comments. This genus may represent a junior synonym of Anodonta.
Tribe Cristariini Lopes-Lima et al . , 2017
Genus Amuranodonta Moskvicheva, 1973
Type species: Amuranodonta kijaensis Moskvicheva, 1973 (original designation).
Diagnosis. This genus is most similar to Buldowskia, Anemina s. str., and Beringiana but can easily be distinguished from these taxa by an elongated shell with a characteristic elongated, triangular posterior margin (vs ovate or rounded shell with rather rounded posterior margin).
Comments. This monotypic genus represents a lineage that is phylogenetically distant from the Buldowskia and Anemina s. str. clades (mean COI p-distance = 15.0% and 14.6%, respectively) (Fig. 1). Our first reviser action on the precedence of simultaneous synonyms: Amuranodonta kijaensis over A. parva (see Supplementary Note for explanation).
Genus Beringiana Starobogatov in Zatravkin, 1983
Type species: Anodonta cellensis var. beringiana Middendorff, 1851 (original designation).
Diagnosis. This genus can be distinguished from Amuranodonta by a less elongated, inequilateral shell with a rounded posterior margin and from Buldowskia by a comparatively weakly pronounced umbo. Both Cristaria and Sinanodonta have much higher, elliptical shells, although several morphological varieties of B. beringiana from small lakes have short, rounded shells with broad posterior margin (Fig. 4H).
Distribution. Beringiana beringiana occurs in Russia, being widespread in rivers and lakes east of the Lena Basin, coastal rivers of the Japan and Okhotsk Sea drainage basins northeast of Vladivostok (from the Kievka River), and on the North Pacific Islands (Kuriles and Sakhalin) (Fig. 6B and Table 1). This is a conchologically variable species, with the largest number of synonyms introduced for its morphotypes from different water bodies of the Russian Far East (Fig. 4F–H and Supplementary Note). Outside Russia, this species is known from Alaska, Western Pacific Region, and Canada in North America, and from Japan44,49.
Comments. Williams et al.49 assumed that Beringiana is a junior synonym of Sinanodonta, but this genus represents a distant genus-level phylogenetic lineage and the two are here treated as distinct taxa (Fig. 1). Kunashiria is a synonym of Beringiana, because its type species, B. japonica, belongs to the latter genus44.
Genus Buldowskia Moskvicheva, 1973
Type species: Anodonta arcaeformis var. suifunica Lindholm, 1925 (original designation).
Diagnosis. This genus can be distinguished from Amuranodonta by an ovate shell with a rounded posterior margin, and from Beringiana by a comparatively pronounced umbo, while in some lacustrine populations of Buldowskia shadini the umbo is not pronounced (Fig. 3E). Buldowskia and Anemina s. str. are almost indistinguishable morphologically.
Distribution. Two Buldowskia species are recorded in Russia (Fig. 3A–F and Table 1). This genus is distributed in the Amur and Razdolnaya River basins, and in the coastal rivers southwest of Vladivostok (Fig. 6A,C).
Comments. This genus is phylogenetically distant from the Amuranodonta and Anemina s. str. clades (mean COI p-distance = 15.0% and 16.7%, respectively) (Fig. 1). In addition to Buldowskia suifunica and B. shadini, it contains two lineages endemic to South Korea, i.e. B. flavotincta (Martens, 1905) and B. iwakawai (Suzuki, 1939), and a species new to science from Japan44,50. Our first reviser action on the precedence of simultaneous synonyms: Buldowskia shadini over B. fuscoviridis and B. buldowskii (see Supplementary Note for explanation).
Genus Cristaria Schumacher, 1817
Type species: Cristaria tuberculata Schumacher, 1817 (monotypy).
Diagnosis. Cristaria species can be distinguished from those of Sinanodonta by the presence of reduced lateral teeth, which Sinanodonta species lack, the absence of pseudocardinal teeth, and a comparatively thick shell. Additionally, Cristaria species have a well-developed dorso-posterior keel and a more angulate, higher shell with clear angle between dorsal and posterior margin, although Sinanodonta schrenkii often has an angulate shell with clear angle between dorsal and posterior margin.
Distribution. Cristaria plicata was recorded throughout the Amur Basin, and in the Tym’ River, central Sakhalin51 (Figs. 4E, 6C and Table 1). There are several records of subfossil shells of this species from the Pleistocene deposits in the Tym’ Valley6,52.
Genus Sinanodonta Modell, 1945
Type species: Symphynota magnifica Lea, 1834 (by typification of a replaced name)25.
Diagnosis. This genus can be distinguished from Cristaria by the lack of lateral teeth and a comparatively thin, rather fragile shell. Usually, Sinanodonta taxa have more ovate shells with a rather rounded angle between dorsal and posterior margin and a weakly developed or lacking dorso-posterior keel. However, Sinanodonta schrenkii often has an angulate shell with clear angle between dorsal and posterior margin.
Distribution. Two native Sinanodonta species are recorded in Russia (Fig. 2F–H and Table 1). This genus is distributed in the Amur and Razdolnaya basins, and in the coastal rivers southwest of Vladivostok (Fig. 6A,B). The non-native species Sinanodonta woodiana was recorded from the Yenisei River, in which it was found in a thermally polluted river channel in sympatry with an introduced population of S. lauta10 (Fig. 6A).
Tribe Lanceolariini Froufe et al . , 2017
Genus Lanceolaria Conrad, 1853
=Cylindrica Simpson, 1900 (type species: Nodularia cylindrica Simpson, 1900; original designation; unavailable name, primary homonym of Cylindrica Clessin, 1882, Gastropoda, Hydrobiidae)25.
=Pericylindrica Tomlin, 1930 (replacement name for Cylindrica Simpson, 1900)25.
Type species: Unio grayanus Lea, 1834 (monotypy).
Diagnosis. This genus can easily be distinguished from the other Russian Unionidae by its unique lanceolate shell shape.
Distribution. Lanceolaria grayii inhabits Lake Khanka, Ussuri Basin, and Lower Amur (Figs. 4D, 6A and Table 1), representing the most northern enclave for this remarkable lineage of the Yangtze Basin fauna44,53.
Tribe Unionini Rafinesque, 1820
Genus Middendorffinaia Moskvicheva & Starobogatov, 1973
Type species: Unio mongolicus Middendorff, 1851 (original designation).
Diagnosis. This monotypic genus is externally similar to Nodularia, from which it can be distinguished by a higher, shorter shell, a strongly convex or even angulate hinge plate, more convex dorsal margin, and fine umbonal sculpture with small regular tubercles and narrow ridges in young shells. However, umbonal sculpture is often weakly developed or absent.
Distribution. Middendorffinaia mongolica is distributed in the Amur and Razdolnaya river basins, and in coastal rivers west of Nakhodka54 and southwest of Vladivostok (Figs. 5A–D, 6G and Table 1). The record from a coastal river of the Okhotsk Sea drainage basin40,55 is Nodularia douglasiae (Fig. 5F).
Comments. Middendorff (p. 277)12 described his Unio mongolicus based on a single specimen, which must be considered the holotype (by monotypy). The type locality was stated as follows: “Aus einem Gebirgsbache ohnfern Gorbitza in Daurien” [Russia, Transbaikalia, a mountain spring near Gorbitsa village (53.1027°N, 119.2169°E)]. The holotype was lost a long time ago, at least before 197318,20,24,25. The two figures of Middendorff12 show outside of the left valve and dorsal side of the shell. A relatively high shell with convex dorsal margin and umbo situated near the anterior margin indicates that Unio mongolicus sensu Middendorff is a distinct species, not a synonym of Nodularia douglasiae.
Zhadin5 assumed that Unio mongolicus sensu Middendorff is a rare member of the Margaritiferidae, and placed it in the genus Margaritana Schumacher, 1817. However, in his later work this species was called Unio douglasiae var. mongolicus with a question mark6. Moskvicheva and Starobogatov18 identified several specimens from the Ussuri Basin as prospective representatives of Unio mongolicus, but their specimens belong to Nodularia douglasiae (Fig. 5G). A new genus, Middendorffinaia, was established, with Unio mongolicus Middendorff as its type species18. This genus included three subgenera: Middendorffinaia s. str., Pseudopotomida, and Suifununio. Taxa placed within Middendorffinaia s. str., with exception of Unio mongolicus sensu Middendorff, belong to Nodularia douglasiae. In contrast, the Pseudopotomida and Suifununio species represent conchological varieties of Unio mongolicus sensu Middendorff (Supplementary Note). Two more such varieties are described as separate nominal species7,24.
Graf26 placed Middendorffinaia s. str. taxa as synonyms of Unio crassus mongolicus Middendorff, and Pseudopotomida and Suifununio taxa as synonyms of Inversidens pantoensis (Neumayr, 1899). This point of view highlighted differences between Unio mongolicus sensu Middendorff (with Pseudopotomida and Suifununio taxa) and U. mongolicus sensu Moskvicheva and Starobogatov (with their additional Middendorffinaia s. str. taxa belonging to Nodularia douglasiae). However, Unio mongolicus Middendorff with its varieties (Pseudopotomida and Suifununio spp.) is phylogenetically and morphologically distant from both the European Unio and East Asian Inversidens56,57.
Klishko et al.40 followed the concept of Unio mongolicus sensu Moskvicheva and Starobogatov18 and pictured a Nodularia douglasiae shell collected near Gorbitsa village as the prospective topotype of this taxon. It was stated that the holotype dimensions in Middendorff’s protologue does not correspond to the proportions of the shell pictured in his book (Pl. 27, Figs. 7–8 12), and that this original holotype picture was “digitally corrected according to the measurements of Middendorff”40. However, this statement is not entirely true, because the shell height vs shell length ratio is 0.47 and 0.46 by the original image and by Middendorff’s measurements12, respectively. This difference is too small and seems to reflect rather slightly inaccurate original measurements than the incorrect holotype picture of Unio mongolicus sensu Middendorff.
To retain the original concept of Unio mongolicus sensu Middendorff as a taxon distinct from Nodularia douglasiae, and to secure the stability of nomenclature, we designate the sequenced specimen RMBH biv229_5 labelled “Russia, Primorye Region, downstream of Gladkaya River (42.7065°N, 130.9084°E), 26.x.2016, Bolotov and Vikhrev leg.” as the neotype of this species (Fig. 5A). The reference sequences accession numbers for the neotype are as follows: MH974549 for COI, MK574414 for 16S rRNA, and MK574555 for 28S rRNA. The shell measurements are as follows: shell length 71.7 mm, height 37.6 mm, width 27.3 mm. The neotype is designated in accordance with the conditions specified in Art. 75 of ICZN, because the name-bearing type specimen was lost, and the authors consider that a name-bearing type is necessary to define the nominal taxon objectively and to avoid further speculations on this issue. We designated a specimen from the Gladkaya River as the neotype, because in this sequenced sample (three genes), we found a specimen that is nearly identical externally to the lost Middendorff’s holotype. The COI sequence of the neotype is very similar to that obtained from a specimen collected from the Shilka River, relatively close to the Middendorff’s type locality (uncorrected p-distance = 0.70%). A sequenced sample from the original type locality is not available.
Genus Nodularia Conrad, 1853
Type species: Unio douglasiae Griffith & Pidgeon, 1833 (monotypy).
Diagnosis. This genus is externally similar to Middendorffinaia, but can be distinguished from it by a narrower, elongated shell, an almost straight hinge plate, comparatively straight or slightly convex dorsal margin, and umbonal sculpture with W-shaped, broad ridges in young shells. However, umbonal sculpture is often weakly developed or absent.
Distribution. Nodularia douglasiae is widespread in the Amur and Razdolnaya basins, in several coastal rivers of the Okhotsk Sea drainage basin up to the Ola River just north of the city of Magadan, and in northwestern Sakhalin (Figs. 5E–H, 6H and Table 1). This species has a plethora of taxonomic names introduced for its conchological varieties from different parts of the Russian Far East (Supplementary Note).
Genus Unio Retzius, 1788
=Tumidiana Servain, 1882 (type species: Unio tumidus Retzius, 1788; subsequent designation by Kantor & Sysoev, 2005)25.
=Crassiana Servain, 1882 (type species: Unio crassus Retzius, 1788; subsequent designation by Graf, 2010)25.
Type species: Mya pictorum Linnaeus, 1758 (subsequent designation by Turton, 183125).
Diagnosis. There are no conchologically similar genera in European Russia and the Urals but introduced populations in the Upper Amur Basin9 can be mistaken with Nodularia and Middendorffinaia. Nodularia has a more elongated, comparatively cylindrical shell. Middendorffinaia differs from Unio by a strongly convex hinge plate and more developed pseudocardinal teeth.
Distribution. Three Unio species were recorded from Russia (Figs. 4A–C, 6E,F, and Table 1). This genus is widely distributed in European Russia and Western Urals, with an isolated native population of Unio tumidus in the Irtysh Basin in Western Siberia59 and Kazakhstan (Table 1). There were a few occasional records of Unio from the Ob’-Irtysh Basin since the middle of the 19th century5,60,61,62. Non-native populations of Unio pictorum and U. tumidus are known to occur in the Upper Amur Basin (Lake Kenon) in Transbaikalia9 (Fig. 6F).
Taxonomic richness of the Unionidae fauna in Russia
Our results support the conclusion that the Russian Unionidae fauna is rather species-poor5,6,26, with only 16 native species belonging to 11 genera of a single subfamily, the Unioninae. Most freshwater mussels in Russia belong to the tribe Cristariini41, which includes five genera (Amuranodonta, Beringiana, Buldowskia, Cristaria, and Sinanodonta) and seven native species inhabiting the Far East. The tribe Unionini63 contains five species in three genera (Middendorffinaia, Nodularia, and Unio), the Anodontini41 includes three species in two genera (Anodonta and Pseudanodonta), and the Lanceolariini41 holds one Lanceolaria species.
The species richness of unionid mussels in Russia represented by previous morphology-based taxonomic schemes23,25,64 has been dramatically overestimated. Nearly 100 taxa of freshwater mussels, including 70 species-group names and 14 genus-group names were described in Russia as new to science since the introduction of the so-called comparatory method in the early 1970s25,26,65 (Table 1 and Supplementary Note). This method is based on an assumption that the contour of the shell valve frontal section is taxon-specific and, as such, can be used as a single diagnostic feature to distinguish species, genera, and even family-group bivalve taxa23,25. Furthermore, a variety of old synonyms for several species and genera were resurrected as valid names using minute differences in the curvature of the shell frontal section25,64,66. However, the shell convexity is strongly influenced by habitat parameters and climatic factors and cannot be used as a diagnostic character3,5,9,26,27,28,31,35,38. A growing body of research critically reassessing the comparatory method in and outside of Russia has discredited its usage for taxonomy, and the last “comparatory” species, Middendorffinaia alimovi (=M. mongolica), was described in 201224.
According to our results, only six unionid taxa described in Russia during the “comparatory” period are valid, i.e. four genera (Amuranodonta, Beringiana, Buldowskia, and Middendorffinaia) and two species (Amuranodonta kijaensis and Buldowskia shadini). A plethora of other names reflecting ecophenotypic shell variability within unionid species was synonymized by recent reviewers9,26,34,35,38,39,40 and in this study. In summary, each biological species in Russia has 4.4 ± 1.1 (mean ± s.e.m.; N = 16) “comparatory” synonyms introduced by Starobogatov’s school (Table 1). This mean rate of synonymy for the national fauna of Unionidae is close to that for the freshwater pond snails, the Lymnaeidae, in which four morphological taxa appear to represent a single valid biological species67. However, this value is higher for the fauna of the Russian Far East, with 6.2 ± 1.5 “comparatory” names per biological species (N = 10). The highest synonymy load is characteristic for conchologically variable species with broad ranges, i.e. Beringiana beringiana (16 species-group and 2 genus-group names), Nodularia douglasiae (9 species-group and 2 genus-group names), and Middendorffinaia mongolica (8 species-group and 3 genus-group names). In contrast, Anodonta cygnea, Cristaria plicata, Unio tumidus, and U. crassus have no new “comparatory” names (Table 1), while each of these biological species was also divided into several morpho-taxa named using available historical synonyms23,25,64.
Biogeography of the Unionidae in Russia
Based on the results of our PCA analysis of Unionidae species ranges (Supplementary Fig. 3 and Dataset 1), the country area can be delineated into the northern parts of two subregions of the Palearctic Region, i.e. Western Palearctic and Eastern Palearctic (East Asian) subregions (Fig. 7), which are briefly described below.
(1) Western Palearctic Subregion covers most of the country from its western boundary to the Lena River Basin in Eastern Siberia. Outside Russia, this subregion encompasses countries of Europe and Central Asia westward to the Middle East and North Africa. In Russia, this area is inhabited by six native species: Anodonta anatina, A. cygnea, Pseudanodonta complanata, Unio tumidus, U. pictorum, and U. crassus.
(1.1) North European Province covers water bodies of the Arctic Ocean drainage (e.g. large basins of the Pechora, Northern Dvina, and Onega rivers), with three species: Anodonta anatina, Unio tumidus and U. pictorum. Several small and medium-sized rivers in the northern part of this province are inhabited only by Anodonta anatina (e.g. Kem, Keret, Mudyuga, and Indiga rivers), but this pattern is likely caused by environmental conditions rather than historical biogeographic events. A non-native population of Anodonta anatina was established in a warm water channel of the Kola Nuclear Power Plant68.
(1.2) East European Province covers water bodies of the Azov, Black, Caspian, and Baltic Sea drainage basins (e.g. huge basins of the Volga and Don rivers) and is inhabited by all six species known from the subregion.
(1.3) Siberian Province covers Siberia eastwards to the Lena River (e.g. Ob’, Irtysh, Taz, Yenisei, and Lena rivers). Anodonta anatina primarily inhabits water bodies in this area, while local populations of Unio tumidus were discovered in the Irtysh Basin in Western Siberia59 and Kazakhstan. The latter population can be considered native, because a few historical records of Unio are known from the southern part of the Ob’-Irtysh Basin5,60,61,62. Sinanodonta lauta and S. woodiana were introduced to the Yenisei River10. Unio tumidus and U. pictorum were introduced to the Upper Amur Basin in Transbaikalia9. Based on the COI gene sequences, the non-native Unio populations in the Upper Amur Basin may have been originated from rivers of the Black Sea drainage, e.g. Dnieper or Danube (Supplementary Table 1 and Supplementary Note).
(2) Eastern Palearctic (East Asian) Subregion covers the Amur Basin, rivers east of the Lena Basin, coastal rivers of the Okhotsk and Japan Sea drainage basins, and the North Pacific Islands (Sakhalin and Kuriles). Beyond Russia, this subregion extends throughout Mongolia, Korea, continental China, Japan, Taiwan, Hainan Island south to central Vietnam44,69,70. In Russia, this subregion is inhabited by 10 native species: Amuranodonta kijaensis, Beringiana beringiana, Buldowskia suifunica, B. shadini, Cristaria plicata, Lanceolaria grayii, Middendorffinaia mongolica, Nodularia douglasiae, Sinanodonta lauta, and S. schrenkii.
(2.1) North Asian Province covers rivers of the Kolyma Highlands (Kolyma and Indigirka rivers), Koryak Region, Chukotka, Kamchatka, North Pacific Islands (Sakhalin and Kurile Archipelago), coastal rivers of the Okhotsk and Japan Sea drainage basins northeast of Nakhodka (from the Kievka River). This severe area with mountainous landscapes and cold climate is primarily inhabited by Beringiana beringiana, but there are a few records of Nodularia douglasiae in several coastal rivers of the Okhotsk Sea39,55, and N. douglasiae and Cristaria plicata from Sakhalin51,71. Based on the phylogeographic patterns of freshwater fishes72,73, the Yana River basin could also be placed within this province, although its Unionidae fauna is unknown74 and needs a special research effort.
(2.2) Amur Province covering the Amur Basin and small rivers surrounding its mouth is the most species-rich freshwater system in Russia, with seven native species. Most species have vast distribution ranges throughout East Asia to South Korea (Buldowskia shadini and Sinanodonta schrenkii), Yangtze Basin in eastern China (Lanceolaria grayii) or even northern Vietnam (Cristaria plicata and Nodularia douglasiae)44, while Amuranodonta kijaensis and Middendorffinaia mongolica seem to be endemic lineages to this province44, partly spreading to the adjoining transition zone (see below).
(2.3) Amur–Korean–Japanese Biogeographic Transition Zone (BTZ) with five native species covers the Razdolnaya River basin, and smaller coastal rivers of the Japan Sea drainage basin west of Nakhodka (Partizanskaya and Artemovka rivers54) and southwest of Vladivostok to the boundary with North Korea and China. Its fauna represents a mix of Amur, Korean, Japanese, and Chinese elements, i.e. Middendorffinaia mongolica (Amur), Nodularia douglasiae (eastern China, Korea, Japan, and northern Vietnam), Sinanodonta schrenkii (Amur and Korea), and S. lauta (Korea and Japan)44. Buldowskia suifunica seems to have a narrow range restricted to the BTZ, but it can also inhabit North Korea and northeastern China (e.g. the nearest Tumen Basin). The Amur freshwater pearl mussel Margaritifera dahurica (Margaritiferidae) and Japanese mussel leech Batracobdella kasmiana (Glossiphoniidae) are known from this area29,75 representing two more examples of such a faunal intermixing in other groups of aquatic invertebrates supporting the delineation of the BTZ76.
In summary, no unionid species endemic to Russia has been identified, except for Buldowskia suifunica. However, this species inhabits the Razdolnaya Basin, a section of which is located in China, and may occur there. Amuranodonta kijaensis can be considered a putative single-basin endemic to the Amur Basin in Russia and China, while Middendorffinaia mongolica appears to be a lineage endemic to the Amur and Razdolnaya basins and few more coastal rivers. Besides these three species, generalist taxa with a broad distribution crossing a variety of drainage divides predominate in the country’s fauna. Furthermore, the fauna of the Eastern Palearctic Subregion in Russia is strongly influenced by Japanese (Beringiana beringiana and Sinanodonta lauta)43,44, Korean (Buldowskia shadini and Sinanodonta schrenkii)44,50, and Yangtze (Cristaria plicata, Lanceolaria grayii, and Nodularia douglasiae)43,44,53 lineages. This biogeographic pattern strongly differs from that in the Yangtze, Mekong and Irrawaddy basins, in which the proportion of single-basin and even intra-basin endemic lineages is much higher, with only a few widespread species53,69,77,78,79,80,81. In its turn, the Unionidae fauna of the Western Palearctic Subregion in Russia, including its Siberian Province, seems to be completely allochthonous and was likely originated from glacial refugia in southern basins of the Baltic Sea, and drainages of the Caspian, Black and Azov seas82,83. Our results are consistent with biogeographic patterns discovered in several freshwater fishes, i.e. rapid post-glacial dispersal events from refugia in the Ponto-Caspian Region to the Volga Basin84,85 and Siberia up to the Lena Basin85.
Anodonta anatina and Beringiana beringiana seem to be the most cold-tolerant species among the Unionidae, the ranges of which cross the Arctic Circle (66.56°N) and reach the Arctic Ocean coast via several freshwater basins (Fig. 6B,D). In contrast, Sinanodonta lauta and Buldowskia suifunica appear to be rather thermophilic species restricted to the extreme south of the Russian Far East up to 44°N, while Lanceolaria grayii inhabits the Ussuri Basin and an adjoining section of the Amur River up to 50°N, but does not spread throughout the Amur Basin (Fig. 6A).
Our updated biogeographic division of the Northern Palearctic based on unionid mussel fauna is largely congruent with that of Graf and Cummings86. However, these authors separated four subregions: Europe, Central Asia, Amur-Beringia with northern China and Korea, and Japan-Sakhalin including Kurile Archipelago86, corresponding to our Western Palearctic (Europe + Central Asia) and Eastern Palearctic (Amur-Beringia + Japan-Sakhalin) subregions. Our novel results support the hypothesis of Moskvicheva7 on significant faunal differences between the Amur Basin and coastal rivers in the southern edge of the Primorye Region (our Amur–Korean–Japanese BTZ). The close relationship between the Unionidae faunas of the latter area and Korea predicted by this author7 was also supported by our research. Moskvicheva7 delineated several biogeographic provinces within the Amur Basin (e.g. Ussuri, Khabarovsk, Argun-Zeya, and Sunggari [Songhua] provinces) based on their intra-basin endemic species, but all these taxa were found to be morphological varieties of broadly distributed lineages. Based on newly obtained results, Moskvicheva’s provinces within the Amur Basin should be joined into one province. There are some faunal differences between various parts of the Amur River system (e.g. freshwater mussels appear to be lacking in the headwaters and middle reaches of the Amgun River7), but this seems to be caused by recent environmental conditions rather than historical biogeographic events. Our biogeographic division also agrees with that of Zhadin5. In contrast, the direct comparison of our scheme with that of Starobogatov8 is impossible, because this author combined all groups of Mollusca in his global biogeographic zoning.
Based on the IUCN criteria, only Buldowskia suifunica and Sinanodonta lauta are assessed here as Vulnerable (VU) and Endangered (EN), respectively, while the other species having much broader ranges are considered Least Concern (LC). However, we recommend including five taxa to a new edition of the Red Data Book of Russia as rare species (Status 3) inhabiting a limited area (Buldowskia suifunica and Sinanodonta lauta) or sporadically distributed over an extensive area (Amuranodonta kijaensis, Lanceolaria grayii, and Middendorffinaia mongolica).
Directions for future studies
This study clarifies the taxonomy of the Russian Unionidae and opens ways for further biological and ecological investigations of valid species that were hampered for more than 40 years by the comparatory systematics with multiple conchological morphs erroneously erected to the species rank. While host fishes and life cycles of the six European species are rather well described outside Russia42, those of taxa from East Asia, especially endemic species to the Russian Far East and Korea such as Amuranodonta kijaensis, Buldowskia shadini, B. suifunica, Middendorffinaia mongolica, and Sinanodonta schrenkii need special research efforts. The population structure and dynamics, growth patterns, and maximum age of these East Asian taxa are virtually unknown.
Several species with broad ranges such as Anodonta anatina, A. cygnea, Beringiana beringiana, Cristaria plicata, Middendorffinaia mongolica, Nodularia douglasiae, Pseudanodonta complanata, Sinanodonta schrenkii, Unio pictorum, U. tumidus, and U. crassus, appear to be appropriate models for phylogeographic studies with a supplement of molecular data from adjacent countries such as Kazakhstan, China, Mongolia, Korea, Japan, and others. A few available works on this issue have revealed putative colonization and refugial patterns for several European and Chinese species87,88,89,90,91 that are of great importance to reconstruct the evolutionary history of freshwater fauna in the Palearctic Region. Widespread species can also be used as models for broad-scale studies of intraspecific shell variability92,93. It is likely that environment-induced shifts in the shell shape can be traced in species with extremely high levels of conchological variability such as Anodonta anatina, Beringiana beringiana, Buldowskia suifunica, B. shadini, Middendorffinaia mongolica, and Nodularia douglasiae. Furthermore, the shell convexity that was used to delineate comparatory taxa actually reflects shifts in summer temperatures and can be applied as a sensitive and low-cost indicator of climate changes3,94.
Reliable fossil records are essential to reconstruct robust fossil-calibrated phylogenies using multi-locus and mitogenomic approaches77,78,81,95. Paleontologists described numerous fossil species of freshwater mussels from Russia and adjacent countries96,97,98,99,100. However, a critical taxonomic revision of all these taxa is urgently needed to clarify their status, prospective phylogenetic placement, and validity. Multiple fossil species recovered from the Pleistocene deposits98 should be compared with recent representatives of the corresponding genera, as many of these nominal taxa may be synonyms of terminal species or their stem lineages33,101,102.
Finally, the Unionidae faunas of several large freshwater basins in the Russian Far East and Siberia, e.g. the Anabara River (Yakutia), Yana River (Kolyma Highlands), Penzhina River (Koryak Region), Uda River (Khabarovsk Region), and Amguema River (Chukotka Peninsula), remain unknown. However, these water bodies are surrounded by relatively well-studied freshwater systems and will hardly deliver any species new to science. In contrast, the neighboring Chinese provinces (Heilongjiang, Jilin, Liaoning, and Inner Mongolia) and North Korea seem to be crucial areas to further understanding the taxonomy and distributional patterns of freshwater mussels in Northeast Asia. The freshwater basins in these areas may harbor additional populations of near threatened species (e.g. Buldowskia suifunica and Middendorffinaia mongolica) and probably a few still undescribed endemic lineages. Now we know almost nothing about the freshwater mussel fauna in these regions43, and such an extensive knowledge gap in freshwater malacology must be a focus of international collaborative research efforts.
In this study, we studied freshwater mussel specimens collected throughout Russia, i.e. from European Russia, Western Siberia, Eastern Siberia, Russian Far East, Sakhalin Island, and Kurile Archipelago. Available lots were studied in the following collections:
RMBH – Russian Museum of Biodiversity Hotspots, Federal Center for Integrated Arctic Research of the Russian Academy of Sciences, Arkhangelsk, Russia;
ZISP – Zoological Institute of the Russian Academy of Sciences, Saint Petersburg, Russia;
INREC – Institute of Natural Resources, Ecology and Cryology, Siberian Branch of the Russian Academy of Sciences, Chita, Russia;
NCSM – North Carolina Museum of Natural Sciences, Raleigh, North Carolina, United States of America.
COI, 16S rRNA (female mitochondrial DNA) and 28S rRNA partial gene sequences were generated from 232 freshwater mussel specimens using a standard approach following our previous works69,77,78. Additional sequences were obtained from NCBI GenBank. Margaritifera species and representatives of Gonideinae and Ambleminae subfamilies were used as outgroup. The data set is presented in Supplementary Table 1.
For comparative studies, we analyzed the shell shape, structure of pseudo-cardinal and lateral teeth, muscle attachment scars, and the sculpture and position of umbo78,80. The type series of nominal taxa under discussion and other lots of freshwater mussels from museum collections, original descriptions and figures from appropriate scientific literature, and available images from the MUSSELp database103 were used for morphological investigations.
The sequence alignments of the COI, 16S rRNA and 28S rRNA gene fragments were processed and joined as described in our previous works69,77,78. The combined data set (total length of 1878 bp) was collapsed from 363 available haplotypes into a set of 199 unique haplotypes using an online FASTA sequence toolbox (FaBox v1.41)104. Five partitions (3 codons of COI + 28S rRNA + 16S rRNA) were used for phylogenetic analysis. Maximum likelihood phylogenetic searches were performed through web-server for IQ-TREE (W-IQ-TREE) with an automatic identification of the best-fit substitution model for each partition105,106 (Supplementary Table 2). An ultrafast bootstrap (UFBoot) algorithm with 7,000 replicates was implemented for estimation of the internal branches probability107. Bayesian analyses were performed in MrBayes v. 3.2.6108. The HKY evolutionary model was applied for each partition. We used four runs, each with three heated (temperature = 0.1) and one cold Markov chain, using 50,000,000 generations with sampling every 1000th generation. All calculations were carried out at the San Diego Supercomputer Center through the CIPRES Science Gateway109. The first 25% of trees were discarded as burn-in. A convergence of the MCMC chains to a stationary distribution was checked through Tracer v. 1.7.1110.
Biogeographic analysis and range mapping
We compiled a comprehensive presence-absence dataset on freshwater mussels (Unionidae) from freshwater basins of Russia (Dataset 1). To delineate the primary biogeographic units, we applied a PCA analysis algorithm implemented in PAST v. 3.04111 using this dataset. Component 1 and component 2 accounted for 43.5% and 20.2% of the total variance, respectively (Supplementary Fig. 3). The distribution maps for each species were created using ESRI ArcGIS 10 software (www.esri.com/arcgis).
Conservation status assessment
Conservation status assessment for each species was based on the Guidelines for application of IUCN Red List criteria at regional and national levels v. 4112. The extent of occurrence (EOO) values were obtained from our distribution maps with ESRI ArcGIS 10 (rounded to the nearest thousand).
The electronic edition of this article conforms to the requirements of the amended International Code of Zoological Nomenclature (ICZN), and hence the new combinations contained herein are available under that Code from the electronic edition of this article. This published work and the nomenclatural acts it contains have been registered in ZooBank (http://zoobank.org), the online registration system for the ICZN. The LSID for this publication is: urn:lsid:zoobank.org:pub:8BE71D2E-A2EE-4E30-AB17-70EA31F4D168. The electronic edition of this paper was published in a journal with an ISSN and has been archived and is available from PubMed Central.
The sequences used in this study are available from GenBank. Accession numbers for each specimen are presented in Supplementary Table 1. The shell vouchers, whole specimens, and tissue snips are available in the corresponding museum collections, i.e. RMBH, ZISP, INREC, and NCSM.
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We are grateful to the associate editor and three referees for their valuable comments that helped us to improve the earlier version of the manuscript. The Ministry of Science and Higher Education of the Russian Federation supported general research work of M.Y.G. (project No. АААА-А18-118012390161-9), Y.V.B. (project No. АААА-А17-117033010132-2), G.A.D. (project No. АААА-А19-119011500368-9), and I.N.B. (project No. 6.2343.2017/4.6) on this paper. The Russian Foundation for Basic Research partly supported phylogenetic analyses by I.N.B. (project No. 17-45-290066), O.V.A. (project No. 17-44-290016), A.V.K. (project No. 18-44-292001_r_mk), and I.V.V. and E.S.K (project No. 18-34-20033_mol_a_ved). The President of Russia Grant Council supported morphological analyses of freshwater mussel samples by I.V.V. under project No. МК-4723.2018.4. The Russian Science Foundation partly supported molecular analyses of freshwater mussels by M.V.V., Y.V.B., I.V.V., and A.V.K. under project No. 19-14-00066. The Russian Science Foundation supported fieldworks of A.A.L. under project No. 18-77-00058. Identification of freshwater mussel species by I.N.B., Y.V.B., and E.S.K. was 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 Presidium of the Russian Academy of Sciences supported fieldwork of I.N.B. (freshwater mussel collecting throughout Eastern Siberia) under the scientific program entitled “Promising Physical and Chemical Technologies of Special Purposes” (project No. АААА-А18-118012390198-5). Fieldwork of A.A.M. (freshwater mussel collecting throughout European Russia) was supported by the Presidium of the Russian Academy of Sciences under scientific program No. 41 entitled “Biodiversity of Natural Systems and Biological Resources of Russia”. The Presidium of the Ural Branch of the Russian Academy of Sciences supported morphological studies of freshwater mussels by Y.V.B., O.V.A. and S.E.S. under project No. АААА-А17-117122890059-1. M.L.-L. was supported by the Portuguese Foundation for Science and Technology (FCT) under grant SFRH/BD/115728/2016. Special thanks go to Valentina S. Artamonova, Oleg N. Bespaliy, the late Evgeny P. Dekin, Natalya V. Neverova, Roman G. Pan’kov, and Alisa A. Vlasova for their help during this study. We thank Matt Bowser (Kenai National Wildlife Refuge, Soldotna, Alaska) who kindly helped us to collect samples of Beringiana beringiana from North America.
The authors declare no competing interests.
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