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Review

Aliens and Returnees: Review of Neobiotic Species of Freshwater Mollusks in Siberia from the Kazakhstan Steppe to the Arctic Tundra

by
Evgeny S. Babushkin
1,2,3,*,
Ivan O. Nekhaev
4,5,
Maxim V. Vinarski
2,3 and
Liubov V. Yanygina
6,7
1
Scientific and Educational Center of the Institute of Natural and Technical Sciences, Surgut State University, Lenina Ave. 1, 628403 Surgut, Russia
2
Tyumen Scientific Center, Siberian Branch of the Russian Academy of Sciences, Malygina St. 86, 625026 Tyumen, Russia
3
Laboratory of Macroecology & Biogeography of Invertebrates, St. Petersburg State University, Universitetskaya Emb. 7/9, 199034 Saint Petersburg, Russia
4
Institute of Zoology, Al-Farabi Ave. 93, Almaty 050060, Kazakhstan
5
Department of Applied Ecology, St. Petersburg State University, Universitetskaya Emb. 7/9, 199034 Saint Petersburg, Russia
6
Institute for Water and Environmental Problems, Siberian Branch of the Russian Academy of Sciences, Molodezhnaya St. 1, 656038 Barnaul, Russia
7
Department of Zoology and Physiology, Altai State University, Lenina St. 61, 656049 Barnaul, Russia
*
Author to whom correspondence should be addressed.
Diversity 2023, 15(3), 465; https://doi.org/10.3390/d15030465
Submission received: 7 February 2023 / Revised: 8 March 2023 / Accepted: 14 March 2023 / Published: 21 March 2023
(This article belongs to the Special Issue Continental Mollusca under Global Change)
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Abstract

:
This article reviews all available information on the species composition, current distribution, and origins of the neobiotic (non-indigenous and restoring the lost range) freshwater mollusks in Siberia. An extensive literary search has been carried out, and virtually all existing publications of recent decades on the findings of freshwater mollusk species new to Siberia were taken into account. We examined extensive malacological collections of some of Russia’s and Kazakhstan’s scientific organizations. The core of the examined material is our own observations and collections made in various parts of Siberia and adjacent areas. An annotated checklist of neobiotic species of mollusks reliably recorded in Siberia is presented, and probable mechanisms and “corridors” of infiltration of these species into the region are discussed. Most of the discovered snail species belong to a group popular among aquarists, and their source of introduction is obvious. Another large portion of species infiltrate into the region with the development of fish farming. A classification of species of neobiotic freshwater mollusks of Siberia was proposed and a forecast was made for changes in the Siberian freshwater malacofauna for the coming decades. In our opinion, at present it is possible to accept the newest stage in the genesis of the freshwater malacofauna of Siberia, occurring in conditions specific to the Anthropocene.

1. Introduction

Until relatively recently, 10–15 years ago, the problem of biological invasions of freshwater mollusks in Siberia was not considered a relevant research topic. Until the beginning of this century, there were practically no publications on this issue. The freshwater malacofauna of the Siberian subcontinent was considered free of alien mollusk species. Two circumstances contributed to this: (1) the almost complete isolation of Siberian water systems from the adjacent river basins, which could serve as a source of non-indigenous species; and (2) the severity of the climate of Siberia, which makes this territory unsuitable for the introduction of such species of mollusks, most of which originate from either tropical regions, or areas of temperate latitudes with a milder climate than Siberia.
Our understanding started to change in the first decade of the 21st century, when the first publications about the discovery of mollusk species new to the region in the water bodies of Siberia began to appear in the scientific literature. These species began to be found in modified water bodies: cooling reservoirs [1,2,3], long known as “foci” of aquatic invasions in northern latitudes; large artificial reservoirs (the Novosibirsk reservoir [4,5], the Bukhtarma reservoir [6]), and also natural watercourses [7]. The accumulating volume of information on this issue prompted Vinarski et al. [8] to prepare a review paper summarizing all information about alien species of mollusks in Western Siberia, in which the authors also discussed climate and other features that prevent the introductions and invasions of non-indigenous species. Eastern Siberia was left out of consideration by the authors of the review, although information about the presence of non-indigenous mollusks there also appeared in the scientific literature [9,10].
Almost eight years have passed since the publication of the review by Vinarski et al. [8]. Since then, the volume of new information about aquatic mollusk species new to Siberia has grown significantly. In addition to the registration of new species in the malacofauna of Siberia and new localities of previously known species [11,12,13,14,15,16,17], there have been works devoted to the ecology of recent migrants in Siberian reservoirs [5,18,19,20,21], as well as publications interpreting the problem from a broader point of view, in particular, raising the question of whether all newly registered species must be considered as “real” aliens, or whether one should rather speak about restoring a part of the original range once lost by some of these species, not about introductions and/or invasions in the commonly accepted sense of these terms [16,22].
In this context, the definition of the term “neobiotic mollusk” may be as follows. It is a molluscan species not registered in Siberia until the historical epoch or not found in a given area earlier, despite extensive faunal research, and registered as a new by the current generation of malacologists (i.e., within the last 15–20 years). So, it is believed to have recently settled in this area. As neobiotic mollusks, we consider both non-indigenous species (we also use the equivalent terms, “non-native species”, “alien species”, and “exotic species”) and species that lived in Siberia before the Pliocene-Pleistocene glaciations that are currently restoring their ranges.
This article aims at the synthesis of information on this issue, with consideration of the entire territory of Siberia, and not just its western part, as was done by Vinarski et al. [8]. Siberia is considered by us as a part of Northern Asia located within the basins of rivers flowing into the Arctic Ocean, the largest of which are the basins of the Ob’ (with the Irtysh), Taz, Yenisei, Lena, Yana, Indigirka, and Kolyma rivers. With regard to administrative and political borders, the predominant part of the territory of Siberia belongs to the Russian Federation, and only a relatively small area covering the upper reaches of the Irtysh basin belongs to the territory of the Republic of Kazakhstan. The Yenisei River divides this vast territory into two large parts, traditionally designated as Western Siberia and Eastern Siberia. The territory of the Russian Far East, which is also sometimes referred to as Siberia (in a broad sense), is not considered by us, nor those parts of northwestern China, where the sources of the Irtysh River (the so-called Black Irtysh) are situated. These regions have their own relief, climate, ecological, and economic features, and history of the formation of water bodies and aquatic malacofauna, so they deserve distinct consideration.
We present an annotated checklist of neobiotic species of mollusks reliably recorded in the territory of Western and Eastern Siberia, consider the likely mechanisms and “corridors” of infiltration of these species into the territory of Siberia, and discuss the possible revision of the “non-indigenous” status for some of these recent migrants.
Since the situation with molluscan migrations in the freshwater systems of Siberia is developing rapidly and dynamically, we consider this work only as a preliminary synthesis that allows us to outline the current state-of-the-art in this field of research, and do not pretend to a complete and final resolution of all the topics discussed in this article.

2. Material and Methods

The authors of this paper have studied the neobiotic component of the freshwater fauna of Siberia since early 2000s. The majority of available information on this subject is that obtained during our own research. Thus, the core of the examined material is our own observations and collections made in various parts and drainage basins of Siberia and some adjacent areas (the Urals, Eastern Kazakhstan). The mollusks, both aboriginal and non-native, were collected during our fieldwork following the standard protocols described in the literature [23,24,25,26]. In addition, we examined extensive malacological collections of some scientific and educational institutes: the Zoological Institute of the Russian Academy of Sciences, the Laboratory of Macroecology & Biogeography of Invertebrates, St. Petersburg State University (St. Petersburg), the Museum of the Institute of Plant & Animal Ecology, the Ural Branch of the Russian Academy of Sciences (Yekaterinburg), the Zoological Museum of the Institute of Biology, Tyumen State University (Tyumen), and Institute of Zoology of the Republic of Kazakhstan (Almaty).
An extensive literary search was carried out during this research, and virtually all existing publications of recent decades on the findings of freshwater mollusk species new to Siberia were taken into account. References are provided throughout the article.
The identification of collected snails and bivalves was carried out with the use of recent identification keys and manuals [24,25,26,27,28]. The nomenclature of the species and their taxonomic position are given mainly after the Vinarski & Kantor [29] catalog, with corrections, when relevant, after MolluscaBase [30].
The map (Figure 1) was developed by us using QGIS software (Available online: https://qgis.org/; accessed on 16 January 2023) with a topographic base from Natural Earth Free Vector and Raster Map Data (Available online: https://www.naturalearthdata.com; accessed on 16 January 2023).

3. Results

Species Composition and Current Distribution of Neobiotic Mollusks of Siberia

Table 1 contains an annotated list of neobiotic mollusks species registered within the borders of Siberia. In total, since 1997, 16 neobiotic species of mollusks (six bivalves and ten snails) have been registered from Siberia. The bivalves belong to two families, Unionidae and Dreisseniidae, whereas the gastropods are members of seven families (Ampullariidae, Lithoglyphidae, Physidae, Planorbidae, Thiaridae, Valvatidae, and Viviparidae).
All bivalve species represent taxa whose native ranges are situated in the temperate and (Sinanodonta) subtropical latitudes of Eurasia, whereas, among snails, five alien species of Nearctic (Ferrissia californica, Helisoma anceps, Physella acuta, Planorbella duryi) or even Neotropic (Pomacea canaliculata) origin have been recorded; their native ranges are also located in the New World. A single species, Melanoides tuberculata, may be considered a member of the Old World tropical and subtropical biota. All the snail species listed above belong to a group of mollusks popular among aquarists, and their source of introduction to Siberian waters is obvious.
Most localities of the neobiotic mollusk species known so far are situated within the Ob’ River basin (Western Siberia); see Figure 1. The water bodies of Eastern Siberia, on the other hand, remain almost free from neobiotic mollusks. Until 2021, only three localities of neobiotic freshwater mollusks were known from Eastern Siberia: Lake Kenon in Transbaikalia (Unio pictorum, U. tumidus), the Yenisei River near Krasnoyarsk City (Sinanodonta lauta, S. woodiana), and the Angara River near Ust’-Ilimsk Town (Planorbella duryi); see Table 1 and Figure 1. In July 2021, we discovered a new locality of non-indigenous freshwater snails situated in Noril’sk City, north of the Arctic Circle (GPS coordinates: N 69.3377, E 88.2052). Two species of snails, Physella acuta and Planorbella sp., were collected in large quantities from Lake Dolgoye (Figure 2B), which serves as a cooling reservoir for the Noril’sk Power Plant. The snails were also found in a warm stream inflowing the lake. The water temperature at the sampling site was +24–26 °C. Arguably, this locality is the northernmost locality of the non-indigenous snails in Siberia and, most probably, it can be considered the northernmost point of their distribution on the global scale. Before this finding, the northern limit of distribution of Ph. acuta was situated in the north of European Russia (Kola Peninsula, Lake Imandra; see [31]).
Table
Table 1. A list of neobiotic species of freshwater Mollusca registered in Siberia, with remarks on their distribution and the dates of the first registration in the studied area.
Table 1. A list of neobiotic species of freshwater Mollusca registered in Siberia, with remarks on their distribution and the dates of the first registration in the studied area.
SpeciesNative RangeInvasive RangeLocality No.First Finds in Siberia and Neighboring RegionsCoordinatesReferences
Date 1SiteLatitudeLongitude
Dreissena polymorpha (Pallas, 1771)Ponto-Caspian and Aral Sea regions; fresh waters of Balkan Peninsula [32,33,34]North America, Europe, Middle and Southern Urals, Western Siberia [17,29]12018Beloyarsk Reservoir (Pyshma River basin, Middle Urals)56.842161.2780[35]
22019Iriklinsky Reservoir (Ural River basin, Southern Urals)51.776858.7740[36]
32021Pyshma River near Tyumen (Tura River basin, Western Siberia)56.973965.3721[17]
Sinanodonta lauta (E. von Martens, 1877)Korea, Japan, and the coastal rivers of the South Primorye Region in Russia [37,38]Ob’, Volga and Yenisei basins in Russia, Lake Balkhash basin in Kazakhstan, Borneo [13,14,38,39]42016Yenisei River at the outlet of the warm water of Krasnoyarsk TPP (Arctic Ocean basin, Eastern Siberia)55.989292.8699[13]
52019Cooling reservoir and the channel of the Belovo Power Plant (Inya River basin, Western Siberia)54.4125
54.4344		86.4643
86.4500		[39]
62019Inya River just below the Belovo Reservoir (Ob’ River basin, Western Siberia)54.457186.4311[39]
Sinanodonta woodiana (I. Lea, 1834)Indochina, China, Korea, and the Amur Basin, Russia [37]Europe, North America, Central America and Caribbean, Japan, Indonesia, Philippines, Southeast Asia, Central Asia including Kazakhstan and Uzbekistan, Siberia [14,39]72016Yenisei River at the outlet of the warm water of Krasnoyarsk TPP (Arctic Ocean basin, Eastern Siberia)55.989292.8699[13]
82019Cooling reservoir and the channel of the Belovo Power Plant (Inya River basin, Western Siberia)54.4125
54.4344		86.4643
86.4500		[39]
Unio pictorum (Linnaeus, 1758)Northern, Eastern and Western Europe, European Russia, Western Urals [37]Middle and Southern Urals, southwest of Western Siberia, upper reaches of the Irtysh River basin (Eastern Kazakhstan) 2, Lake Kenon (Amur Basin, Transbaikalia) [11,16,37]91997Bukhtarma Reservoir (Irtysh River basin, Eastern Kazakhstan) 249.025983.9095[6,11]
101998Lake Isetskoye and Verkh-Isetsky Pond (Iset’ River basin, Middle Urals)57.0167
56.8652		60.4667
60.5000		[16,27]
112001Lake Kenon (Amur River basin, Transbaikalia)52.0486113.3726[9,40]
122002Uy River in Chelyabinsk region (Tobol River basin, Southern Urals)54.116761.1000[16]
132007Tobol River in Tyumen region (Irtysh River basin, Western Siberia)56.517566.3948[41]
U. tumidus Philipsson in Retzius, 1788Northern, Eastern and Western Europe, European Russia, Western Urals, Ural River in Russia and Kazakhstan, upper reaches of the Irtysh River (Eastern Kazakhstan) [16,37]Southern Urals, extreme southwest of Western Siberia, upper reaches of the Irtysh River (Eastern Kazakhstan), Lake Kenon (Amur Basin, Transbaikalia) [16,37]141829? Barnaul (probably Black Irtysh River basin, see [16])53.3728?83.7318?[16,42]
152001Lake Kenon (Amur River basin, Transbaikalia)52.0486113.3726[9,40]
162005Uvel’ka River and Uy River in Chelyabinsk region (Tobol River basin, Southern Urals)54.0884
54.1000		61.5069
61.1333		[7,16]
172018Black Irtysh River in East-Kazakhstan region (Irtysh River basin, Eastern Kazakhstan)47.900084.9000[16,37]
U. crassus Philipsson in Retzius, 1788Northern, Eastern and Western Europe, European Russia (water bodies of Baltic, Black, Azov, and Caspian Sea drainage basins), Western Urals, Ural River in Russia and Kazakhstan [37]Unknown 3182006Pond of Tagil River (Tura River basin, Middle Urals)57.800060.0167[16]
Borysthenia naticina (Menke, 1845)Eastern Central Europe, Eastern Europe and Turkey [29]Southwest of Western Siberia, upper reaches of the Irtysh River (Eastern Kazakhstan) [1,11]192004?
2009		Bukhtarma Reservoir (Irtysh River basin, Eastern Kazakhstan)49.025983.9095[6,11,18,43]
202005Cooling reservoir of the Tyumen Heat and Power Plant No. 1 (Tura River basin, Western Siberia)57.150065.6241[1,18]
Ferrissia californica (Rowell, 1863)North America: United States, southern Ontario, southern Quebec, southwest of British Columbia [29]Many European countries, Israel, Syria and south-eastern Asia, southern part of the Western Siberia, Transcaucasia and Central Asia [29]212005Cooling reservoir of the Tyumen Heat and Power Plant No. 1 (Tura River basin, Western Siberia)57.150065.6241[1,18]
222010Cooling reservoir of the Belovo Power Plant (Inya River basin, Western Siberia)54.432886.4647[3,18]
Helisoma anceps (Menke, 1830)North America from Mexico to central Canada [29]Europe, Middle Urals and Western Siberia [29]231999Riverbank drifts at Omsk (Irtysh River basin, Western Siberia)54.991273.3642[8,28]
242010Cooling reservoir of the Belovo Power Plant (Inya River basin, Western Siberia)54.432886.4647[3,18]
252013Cooling reservoirs around Nizhny Tagil (Tura River basin, Middle Urals)57.910559.9726[28]
Lithoglyphus naticoides (C. Pfeiffer, 1828)Ponto-Azov basin: rivers northwest of the Black Sea [44]Eastern and Central Europe, European Russia, upper reaches of the Irtysh River (Eastern Kazakhstan) [11,29,44]261998Bukhtarma Reservoir (Irtysh River basin, Eastern Kazakhstan)49.025983.9095[6,11,18]
Melanoides tuberculata (O. F. Müller, 1774)Africa to Southeast Asia [29]Australia and New Zealand, North America, South America, Europe and Azores, Western Siberia [29,45,46,47,48]272010Cooling reservoir of the Belovo Power Plant (Inya River basin, Western Siberia)54.432886.4647[3,18]
Physella acuta (Draparnaud, 1805)North America (Canada, the Great Lakes region and Dakota) [29]Europe, Asia, Africa, Australia, and South America (the Titicaca Lake), European Russia, Western Siberia and the Russian Far East [29]281969Floodplain waterbodies and rivers near Petropavl and Astana (Ishim River basin, Northern Kazakhstan)54.8765
51.1422		69.1195
71.4047		[49,50,51]
291979Upper reaches of the Irtysh River basin (East Kazakhstan)49.953382.5941[52]
302005Cooling reservoir of the Tyumen Heat and Power Plant No. 1 (Tura River basin, Western Siberia)57.150065.6241[1,18]
312010Cooling reservoir of the Belovo Power Plant (Inya River basin, Western Siberia)54.432886.4647[3,18]
322013Cooling reservoirs and ponds near Nizhny Tagil, Yekaterinburg and Magnitogorsk (Irtysh River and Ural River basins, Southern and Middle Urals)57.9105
56.8421
53.4075		59.9726
61.2780
58.9784		[28]
332013Water bodies of the Korgalzhyn Reserve (Ishim River basin and basin of the endorheic lake Tengiz, Northern and Central Kazakhstan)50.433369.1889[8]
342021Lake Dolgoye and warm stream inflowing the lake in Noril’sk (Pyasina River basin, Eastern Siberia)69.337788.2052This study
352022Swampy oxbow of the Ishim River (Irtysh River basin, Western Siberia)56.062069.4772This study
Planorbella duryi (Wetherby, 1879)Florida in North America [29]South America, Hawaii, Northern, Eastern and South Africa, Europe, Northern coast of the Black See, Angara River basin [29]362010Heated stream running from the Ust-Ilimsk Pulp and Paper Plant (Angara River basin, Eastern Siberia)58.0323102.7512[10]
Planorbella sp.North and South America, northeastern Asia [29]Widely distributed throughout the world (as aquarium animals, often end up in natural habitats) [29]372021Lake Dolgoye in Noril’sk (Pyasina River basin, Eastern Siberia)69.337788.2052This study
Pomacea canaliculata (Lamarck, 1822)Southern South America (lower del Plata basin) [53]South America (other parts), North America, Europe, Asia and many other regions, including Western Siberia [2,53]382002Cooling reservoir of the Belovo Power Plant (Inya River basin, Western Siberia)54.432886.4647[2,54]
Viviparus viviparus (Linnaeus, 1758)Europe except for extreme North and South, Western Transcaucasia [29]Crimean Peninsula, Western Siberia, Eastern Kazakhstan [19,29]391990sNovosibirsk Reservoir (Ob’ River basin, Western Siberia)54.734482.8416[4,5,8]
401994Bukhtarma Reservoir (Irtysh River basin, Eastern Kazakhstan)49.025983.9095[5,6,11,18]
412009Oxbow lake near Tobol’sk (Irtysh River basin, Western Siberia)58.203868.2463[8]
422015Tura River at Tyumen (Tobol River basin, Western Siberia)57.156365.5395[12]
432022Ob’ River at Barnaul (Arctic Ocean basin, Western Siberia)53.372883.7318This study
1—the dates of the first finds or the dates of the first publications about them are indicated (then they coincide with earlier one in the last column); 2—finds of U. pictorum in the upper Irtysh River basin need to be checked, we have no collections or photos of this species from this region, all our finds belong to the species U. tumidus; 3—record of U. crassus from Lake Kenon [40] was based on erroneous identification and belong to U. tumidus see [37].
So far, Physella acuta is the most widespread exotic snail species in the freshwater systems of Siberia, known from several points situated in various places of the region. Its patchy distribution is explained by the apparent inability of this species to live in water bodies with an unaltered thermal regime [28,55,56]. On the other hand, reports of findings of this mollusk in natural habitats have occasionally been published since the late 1960s [8,49,51,52,56]. All these findings were made in the warmest southwestern part of Siberia, whose climatic conditions allow the snails to survive and reproduce. The latest of such findings was made by us in July of 2022, in a swampy oxbow of the Ishim River south of Ishim Town (GPS coordinates: 56.0620 N 69.4772 E) (see Figure 2D). Only a single specimen of Ph. acuta was collected from this oxbow, along with other (aboriginal) species of snails. The rarity of these finds underlines the fact that no stable and numerous populations of this snail have been established outside artificially heated habitats on the territory of Siberia so far.
Of the neobiotic bivalve taxa, the most widespread in Siberia are representatives of the genus Unio, known from both the western and the eastern part of the region (see Table 1). The history of their appearance and dispersal in Siberia is best documented and well characterizes the complexity and multi-vector ways of distribution. It was assumed that, in the territory of Siberia, mollusks of this genus, once very widespread, disappeared in the Pleistocene [57,58]. Despite this, there were a few references in the literature to the presence of Unio in the modern period in Western Siberia [42,59]; summarized in [16]. Since the end of the last century, different species of the genus have been registered both in the upper reaches of the Irtysh basin (Bukhtarma reservoir), and at the junction of the Irtysh and Volga-Kama basins in the Transuralian region [7,27] as well as in Transbaikalia (Lake Kenon). Some of these findings can be explained by human participation in the dispersal of mollusks, and some by the eastward natural expansion of the range [7]. Finally, molecular genetic studies of recent years have shown that some Unio are not “aliens” at all, since they disperse from the refugium located in the upper reaches of the Irtysh above Lake Zaisan [16]. Probably, this explains the discovery of Unio shells in the Altai region made in 1829 by the participants of the Siberian expedition of Alexander von Humboldt [16,42,60].
Currently, according to our information, mollusks of the genus Unio, primarily U. pictorum, occur widely in the middle course of the Irtysh River. According to the results of a hydrobiological survey of the Irtysh riverbed within the boundaries of the Russian Federation, conducted in 2022, these bivalves have become quite common in this river near Omsk, as well as upstream, near the border with Kazakhstan (L. Yanygina, unpublished data). In the same year, specimens of Unio were collected in the Om’ River (a tributary of the Irtysh) above the city of Omsk (S.I. Andreeva, pers. comm.). Previously, these bivalves were found in the lower reaches of the Tobol River near Tobolsk Town [8], and, in 2021 and 2022, in the tributaries of the Irtysh River flowing from Ural Mountains (Tura, Pyshma, and Iset’ rivers; unpublished data of E. Babushkin & M. Vinarski). Thus, there is reason to believe that the genus Unio has practically restored the previously lost part of its range, once located on the territory of the Irtysh River basin.

4. Discussion

4.1. An Analysis of Neobiotic Malacofauna of Siberia

During the Tertiary and Quaternary periods, the territory of Siberia was an arena for large-scale migrations of various species of freshwater animals and even entire faunal complexes. Many groups of mollusks were actively involved in these migrations and faunogenetic processes [58,61,62,63,64]. The recent malacofauna of freshwaters of Siberia was formed as a result of climatic perturbations of the Quaternary period. It is considered to be depleted, both at the species and at the generic level, which is explained by the elimination of a large number of taxa that inhabited this territory in the Late Tertiary and Quaternary (during the warmer interglacial stages) time [58,61,65,66].
At present, one can accept the newest stage in the genesis of the freshwater malacofauna of Siberia, occurring in conditions specific to the Anthropocene. First of all, this refers to the factor of human activity, which causes the infiltration of exotic species of tropical or even extra-Eurasian origin into this territory, as well as the impact of global changes on the climate of Siberia [67,68,69], which probably contribute to the restoration of the North Asian part of the range lost in the Quaternary by some species of mollusks. From this point of view, not all the species presented in Table 1 can be considered non-indigenous in the full sense of the term. Further genetic studies could clarify this issue [70]. We propose to divide all the species of neobiotic mollusks of Siberia into two groups, of which only one can be called “true aliens”. (Figure 3, Table 2). We are talking about species and genera that have never lived on the territory of Siberia before and have penetrated here solely with the help of humans, most often as a result of unintentional introduction. Natural dispersal has to be excluded, apparently, even for the Dreissena polymorpha [17], although this species is a native inhabitant of the Volga basin, geographically adjacent to the Ob’-Irtysh basin.
The second group of neobiotic mollusk species can be considered as “the returnees” currently restoring the North Asian part of their historical range. This can occur both by natural dispersal from the East European water bodies or from some southern refugia, as in the case of the genus Unio [7,16,17].
For example, several mollusk species have been recorded in the Ob’ basin, the modern (pre-Anthropocene) range of which is limited to the river basins of Europe. These are Borysthenia naticina, Lithoglyphus naticoides, Unio crassus, and Viviparus viviparus. Paleontological data show that all these mollusks inhabited the Ob’ basin until the middle of the Pleistocene and presumably went extinct during the last (Sartan) glaciation, ca. 23.,000–10,000 BP. Modern climate warming creates favorable conditions for the restoration of their area lost during the cooling of the climate [58,61,65,67,68,69].
The natural and especially human-mediated dispersal of such returnees has the potential to create new invasive species if successful introductions grow out of control and cause ecologic or economic damage. Perhaps the greatest danger is not the returnees themselves, who previously lived in the water bodies of Siberia, but the potential invasions by the accompanying species of aquatic animals, not only mollusks. In the literature on biological invasions, it is customary to define such invasions as intracontinental, contrasting them with the intercontinental ones. The intensity of intracontinental migrations is underestimated, and the number of known instances of these migrations and invasions will likely grow significantly after the widespread introduction of genetic research into environmental monitoring practice [70]. At the same time, such intracontinental migrants can constitute a significant share of the neobiotic species richness and have a negative impact on the recipient ecosystems, becoming invaders. For example, in North America, the proportion of intracontinental invasions averages 14.7% of all registered cases, while in some taxonomic groups this proportion exceeds 50% [71].
In general, the appearance of 75% of neobiotic species in the basins of the Danube and Volga, 57% of species in the basin of the Dnieper River, and 100% of all neobiotic species in the basin of the Ob’ River is associated with intracontinental migrations (Figure 4). (Note, this statistic excludes the exotic species not able to establish sustainable populations outside the artificially heated water bodies). The majority of these neobiotic species were represented in the fossil record of the recipient basins, which indicates that the analysis of the paleoarchives can become a useful tool in predicting the modern dispersal of aquatic animals and their invasion potential.
The earliest hotspot of intracontinental molluscan migrations in the territory of the Ob’-Irtysh basin was formed already in the 1990s. It is located in the Bukhtarma reservoir, on the territory of East Kazakhstan (Upper Irtysh basin; see Figure 2A). At least four neobiotic species of snails and bivalves (Borysthenia naticina, Lithoglyphus naticoides, Unio pictorum, Viviparus viviparus) were recorded there for the first time (see Table 1). It is likely that V. viviparus entered the ecosystem of the Novosibirsk Reservoir on the Ob’ River around the same time. Until now, these reservoirs are the centers of the origin of neobiotic mollusks in this basin: they are characterized not only by a higher species richness of the neobiotic malacofauna, but also by the maximum values of the frequency of occurrence and abundance of such species [19]. In recent years, a similar role has been played by numerous reservoirs located on the eastern macroslope of the Ural Ridge, where a number of non-indigenous species and returnees have already been registered (see Table 1). The functioning of reservoirs as foci of biodiversity of neobionts is mainly associated with the development of fish farms. Due to multi-purpose use, different conditions develop in different parts of the reservoirs; for example, in July 2022, near the discharge of warm water from the Reft Power Plant in the reservoir of the same name (Pyshma River basin, Middle Urals), we found a settlement of global invaders of the genus Sinanodonta, which were not previously found in the Irtysh River basin. Among the collected mollusks were very large specimens (shell length >20 cm), which possibly indicates the long-term presence of the mussel in the waterbody. We do not provide information about the find in Figure 1 and Table 1, since species identification based on morphological characters is practically impossible [13,14,37,38,39], and DNA barcoding data have not yet been obtained. The other parts of the same reservoir are relatively cold, with no Sinanodonta individuals found there.
A key issue in the biology of invasions is the search for the causes for the success of introduced species in their conquering of new habitats and regions. An important factor helping to understand these causes is the study of paleoarchives. Paleolimnological data are still used in a very limited way in invasion biology. As a rule, they are used to clarify the time of the beginning of the infiltration to a new territory by a new species [72], and usually data covering the last tens or hundreds of years are used for these purposes. The analysis of more ancient history, spanning tens of thousands and even millions of years, can open up new perspectives in understanding the factors determining the success of invasions and other types of range expansion. For example, analysis of paleolimnological data shows that representatives of all mollusk species naturalized in recent decades in the water bodies of Siberia lived here in the Pleistocene [61,73,74].
The human-mediated dispersal of freshwater mollusk species can significantly accelerate their return to their former habitats, the restoration of the lost parts of their range. The return of species can considerably transform modern aquatic ecosystems and negatively affect the economical use of inland water bodies. For example, the introduction of Viviparus viviparus into the Novosibirsk Reservoir is accompanied by an increase in the biomass of zoobenthos to 16 kg/m2 due to the neobiotic species [75], which leads to rearrangement of the structure of macroinvertebrate communities, a decrease in their diversity and an increase in density [19]. Huge accumulations of mollusk biomass interfere with the operation of hydraulic structures, and dead mollusks and their empty shells disrupt the recreational use of water reservoirs [75].
From one of the standpoints of theoretical ecology, it can be expected that the “returnees” restore not only their former range, but also the lost niches that remain free. For instance, a preliminary analysis of stable carbon and nitrogen isotopes in the muscles of V. viviparus and dominant native gastropods [Radix auricularia (Linnaeus, 1758)] showed that the trophic niches of these mollusks in the Novosibirsk Reservoir practically do not overlap (L. Yanygina, unpublished data). If this is also true for other neobiotic mollusks, then their return to the Siberian water bodies can increase the overall diversity of aquatic ecosystems, and complicate food chains and other biotic relationships. This assumption is indirectly supported by the fact that we do not have data on the destructive influence of these species on the recipient freshwater ecosystems of Siberia. But this is a preliminary generalization, and this issue requires special studies. The case of the transforming effect of V. viviparus on the ecosystem of the Novosibirsk Reservoir described above remains the only one, and is perhaps not indicative, since artificial reservoirs are a very young type of habitats that arose only in the historical era, and there were simply no direct analogues to them in Pleistocene.
A special case of intracontinental invasions is a phenomenon that can be referred to as “intra-Siberian invasions”. A striking example of this is the recent—on a scale of the last 100–120 years—introduction of the species Radix auricularia, widely distributed in the Palearctic, into the ecosystem of Lake Baikal, which included, almost exclusively, the native mollusk species unique to this waterbody [76,77,78]. Schniebs et al. [79] undertook the reconstruction of this invasion using methods of molecular and morphological analysis and showed its continuing character. It remains unclear whether the introduction of this mollusk into the Baikal ecosystem is a serious threat to the survival of endemic gastropod species, or whether R. auricularia will be able to find and occupy free ecological space, which will not lead to the competitive elimination of the native malacofauna.

4.2. Forecast of Changes in Freshwater Malacofauna of Siberia in the Coming Decades

Currently, it can be predicted that the enrichment of Siberian malacofauna due to the arrival of species of the “returnees” complex will only continue. Paleontological literature shows that neobiotic mollusks that are now restoring their lost range lived in the Pleistocene, together with native species common to the fauna of modern water bodies of Western Siberia and Europe. This may indicate the similarity of environmental conditions in the Pleistocene to those of the present, and increases the likelihood of further, wider distribution of mollusks of the “Pleistocene complex”.
We may make assumptions about groups of mollusks that will, probably, arrive in the freshwater systems of Siberia in the foreseeable future. In our opinion, bivalves of the genus Corbicula are the most likely future invaders, primarily the species C. fluminea (O.F. Müller, 1774) and C. fluminalis (O.F. Müller, 1774), which have long proven their ability to inhabit water bodies of Central and Eastern Europe with a natural thermal regime [26,33,80,81,82]. Recent studies have shown that these mollusks are able to withstand a decrease in temperature to 0 °C for 9 weeks [83]. When the temperature rises to 16–18 °C (at least 10 degree-days), C. fluminea becomes able to reproduce, which allows it to naturalize even in subalpine lakes [84]. The conditions of the European lakes and rivers fully meet these requirements already [83,85]. In the European part of Russia, the corbiculid clams are known from localities lying quite close to the Arctic Circle [82,86], which demonstrates their high tolerance to low temperatures. The territory of Siberia was not a part of the native range of this subtropical genus; however, in the Pleistocene epoch, some species of Corbicula were able to disperse into Northern Asia during the warm interstadials, which is well documented in the fossil record [73,74,87]. This indicates the potential for the rapid infiltration, following Dreissena, of representatives of the genus Corbicula, into the Ob’-Irtysh basin and, probably, to the upper courses of the Amur River basin in the southeastern part of Eastern Siberia.
For Siberia, two species of the family Viviparidae, Cipangopaludina chinensis (Gray, 1833) and Sinotaia quadrata (Benson, 1842), whose native ranges are situated in the Far East, should also be included in the list of potentially dangerous species of freshwater molluscs, from the point of view of the probability of their introduction. Both species are currently actively conquering the freshwaters of Europe and America, and information about their new findings outside their native range appears annually in the literature [88,89,90,91,92,93]. Representatives of the genera Cipangopaludina and Sinotaia are known from the Pliocene-Quaternary deposits of Siberia, and, until the end of the Pleistocene, they lived in the water bodies of Northern Asia together with modern native and neobiotic species [61,73,74].
The neobiotic mollusk species already established in Western Siberia are also likely to broaden their distribution in the region. Considering the evolutionary history of the North Palearctic species of the genus Unio, we should expect further expansion of Unio pictorum (Linnaeus, 1758) and U. tumidus into the water bodies of Western Siberia. The situation with the third European species of the genus, U. crassus, remains less clear. This species is considered threatened in a number of European countries, where it has been assigned a certain conservation status. Perhaps this indicates a reduced adaptive and competitive potential of U. crassus compared to U. pictorum and U. tumidus, and, consequently, its limited opportunities to restore the lost part of its range, located to the east of the Ural Ridge.
The restoration of the lost range should also be expected in the case of Viviparus viviparus, already known from a number of points in the territory of the Ob’-Irtysh basin (see Table 1). Given the low number of malacologists and hydrobiologists working in Western Siberia, compared with the vastness of this region, it is not impossible to assume that the real extent of distribution of this snail here is much broader than we know.
Given the high frequency of publication of new findings of Dreissena polymorpha in water bodies belonging to the extreme western part of the Irtysh basin [17,35,36], we expect a rapid spread of this invasive bivalve downstream of rivers belonging to the Irtysh basin, and the formation, in the next 10–20 years, of stable foci of zebra mussel invasion at various points of the Irtysh basin on the territory of the West Siberian Plain. Since D. polymorpha is well known as a harmful species that has a transformative effect on both recipient ecosystems and a number of spheres of human activity, monitoring the spread of this species is a very urgent task, especially in the regions of southwestern Siberia, for example, in the Tyumen region, where we expect with the greatest probability the formation of new sustainable populations of this mollusk.

Author Contributions

Conceptualization, all authors; Methodology, E.S.B., L.V.Y. and M.V.V.; Software, E.S.B.; Literary Survey, all authors; Validation, E.S.B. and M.V.V.; Statistical Analysis, L.V.Y.; Fieldwork and Species identification, all authors; Writing—Original Draft Preparation, M.V.V. and L.V.Y.; Writing—Review & Editing, all authors; Visualization, E.S.B., L.V.Y. and M.V.V.; Supervision, E.S.B. and M.V.V.; Project Administration, E.S.B.; Funding Acquisition, all authors. All authors have read and agreed to the published version of the manuscript.

Funding

Partial financial support for this research was received from the Department of Education and Science of the Khanty–Mansi Autonomous Okrug–Yugra (project No. 2020-146-09), from the Russian Foundation for Basic Research and Tyumen Region (project No. 20-44-720008), from the State Task of the Institute for Water and Environmental Problems (project No. 121031200178-8), and from the Science Committee of the Ministry of Science and Higher Education of the Republic of Kazakhstan (Grant No. BR18574062). The field work in Eastern Siberia was funded by the Russian Science Foundation, project No. 19-14-00066/P.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The primary materials (gastropod and bivalve samples) for this study are placed in some public repositories. All data, used and collected during this research, are available (with reservations) upon request from the authors.

Acknowledgments

The authors are grateful to the curators of the malacological collections examined during our work: P.V. Kiyashko and L.L. Yarokhnovich (Zoological Institute of RAS, Saint-Petersburg), N.G. Erokhin and M.E. Grebennikov (Institute of Plant & Animal Ecology, Ural Branch of RAS, Yekaterinburg), and V.A. Stolbov (Institute of Biology of the Tyumen State University, Tyumen) for their invaluable help. We are very grateful to all colleagues who helped organize field work in various parts of the vast territory of Siberia. Our sincerest thanks are extended to the anonymous reviewers for their valuable comments, which helped us to improve the earlier version of the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Map of neobiotic freshwater species of Mollusca first occurrences in Siberia. Numbers indicate the localities, which correspond to those in Table 1.
Figure 1. Map of neobiotic freshwater species of Mollusca first occurrences in Siberia. Numbers indicate the localities, which correspond to those in Table 1.
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Figure 2. Some habitats of neobiotic freshwater species of Mollusca in Siberia. (A) The Bukhtarma Reservoir; (B) Lake Dolgoye, Noril’sk City; (C) An oxbow lake of the Irtysh River near Tobol’sk Town; (D) An oxbow lake of the Ishim River south of Ishim Town. Photos: Maxim V. Vinarski.
Figure 2. Some habitats of neobiotic freshwater species of Mollusca in Siberia. (A) The Bukhtarma Reservoir; (B) Lake Dolgoye, Noril’sk City; (C) An oxbow lake of the Irtysh River near Tobol’sk Town; (D) An oxbow lake of the Ishim River south of Ishim Town. Photos: Maxim V. Vinarski.
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Figure 3. A classification scheme for the newly registered in the fauna of Siberia species of freshwater Mollusca. ND—natural dispersal. HMD—human-mediated dispersal.
Figure 3. A classification scheme for the newly registered in the fauna of Siberia species of freshwater Mollusca. ND—natural dispersal. HMD—human-mediated dispersal.
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Figure 4. The significance of the intracontinental migrations of mollusks in the formation of the neobiotic malacofauna of some great river basins of Eurasia. 1—The total number of species of neobiotic mollusks registered in water bodies with the natural thermal regime; 2—The number of neobiotic mollusk species of Eurasian origin; 3—The number of neobiotic species of mollusks that inhabited this area in the Pleistocene according to paleolimnological data [72,73,74]. The numbers are taken from literary data surveyed during this research.
Figure 4. The significance of the intracontinental migrations of mollusks in the formation of the neobiotic malacofauna of some great river basins of Eurasia. 1—The total number of species of neobiotic mollusks registered in water bodies with the natural thermal regime; 2—The number of neobiotic mollusk species of Eurasian origin; 3—The number of neobiotic species of mollusks that inhabited this area in the Pleistocene according to paleolimnological data [72,73,74]. The numbers are taken from literary data surveyed during this research.
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Table
Table 2. Classification of species of neobiotic freshwater mollusks in Siberia according to their status in the region *.
Table 2. Classification of species of neobiotic freshwater mollusks in Siberia according to their status in the region *.
True Aliens or Non-IndigenousThe Returnees
ATFFNDHMD
Ferrissia californica, Melanoides tuberculata, Physella acuta, Helisoma anceps, Planorbella duryi, Planorbella sp., Pomacea canaliculataDreissena polymorpha (?), Sinanodonta lauta, S. woodianaUnio crassus, U. pictorum (partly), U. tumidus (partly) Borysthenia naticina, Lithoglyphus naticoides, Unio pictorum (partly), U. tumidus (partly), Viviparus viviparus
* Abbreviations: AT—dispersal through aquarium trade; FF—dispersal connected to fish farm stocking; ND—natural dispersal; HMD—human-mediated dispersal.
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Babushkin, E.S.; Nekhaev, I.O.; Vinarski, M.V.; Yanygina, L.V. Aliens and Returnees: Review of Neobiotic Species of Freshwater Mollusks in Siberia from the Kazakhstan Steppe to the Arctic Tundra. Diversity 2023, 15, 465. https://doi.org/10.3390/d15030465

AMA Style

Babushkin ES, Nekhaev IO, Vinarski MV, Yanygina LV. Aliens and Returnees: Review of Neobiotic Species of Freshwater Mollusks in Siberia from the Kazakhstan Steppe to the Arctic Tundra. Diversity. 2023; 15(3):465. https://doi.org/10.3390/d15030465

Chicago/Turabian Style

Babushkin, Evgeny S., Ivan O. Nekhaev, Maxim V. Vinarski, and Liubov V. Yanygina. 2023. "Aliens and Returnees: Review of Neobiotic Species of Freshwater Mollusks in Siberia from the Kazakhstan Steppe to the Arctic Tundra" Diversity 15, no. 3: 465. https://doi.org/10.3390/d15030465

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