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Article

Bithyniid Abundance in the South of Western Siberia Water-Courses and Water Reservoirs (Russia)

by
Elena A. Serbina
1,2
1
Institute of Systematics and Ecology of Animals Siberian Branch Russian Academy of Sciences, Frunze, Street 11, Novosibirsk 630091, Russia
2
Department of Radio Engineering Devices and Technosphere Safety, Institute of Telecommunications, Siberian State University of Telecommunications and Informatics, Kirov Street, 86, Novosibirsk 630091, Russia
Diversity 2022, 14(10), 791; https://doi.org/10.3390/d14100791
Submission received: 12 August 2022 / Revised: 15 September 2022 / Accepted: 18 September 2022 / Published: 24 September 2022
(This article belongs to the Special Issue Functional Diversity in Freshwater Organisms: Historical Patterns and Impact of Anthropogenic Activities)
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Abstract

:
Gastropoda are an important component of the freshwater benthic communities of Western Siberia and participate in a number of trophic relationships and as the intermediate hosts of trematodes. The purpose of this study is defining the ratio of Bithyniidae mollusks between other gastropods with regard to species diversity, and to compile all information about the abundance of bithyniid snails that we examined over 27 years in four major basins situated in the Novosibirsk region. Analyzing the data diversity and abundance of gastropod communities from freshwater ecosystems south of Western Siberia, we found that 22% of the water bodies contained bithyniid snails. In total, 201 samples that were abundant with bithyniid snails of reproductive age were collected in 34 localities in 25 water bodies. While these freshwater snails are not abundant in most of the inspected reservoirs (fewer than 10 mollusks per square meter), two of the water bodies accommodated a great number of Bithyniidae (more than 100 ind.·m−2). Bithyniid snail abundance may vary tenfold in different years in the same water body. This and the study of seasonal dynamics show that the abundance of bithyniid snails of reproductive age decreased from June to August in all years. The results of this study can be used to identify and predict the natural foci of opisthorchiasis in the south of Western Siberia.

1. Introduction

Gastropoda communities are the most diverse class of mollusks and the foremost constituent in the freshwater ecosystems [1,2]. They inhabit different kinds of water bodies and reach a relatively high abundance. Gastropods are also good water-quality indicators, and the abundance of some species may reveal the current status of any water reservoir. They are an important component of benthic communities and take part in a number of trophic relationships. Hence, scientific studies pertaining to their diversity, distribution, and abundance are essential.
While the ecology of gastropod snails is well-studied in the water bodies of the central part of European Russia [3,4,5], the authors emphasize the necessity of conducting similar studies in Siberia. Some information about the ecology of gastropod species was presented in the publications of E.A. Novikov [6], V.N Dolgin [7], and M.V. Vinarski et al. [8]. These authors showed that the highest species and generic diversity of freshwater gastropods is found in the water bodies of the forest—steppe zone; from there, these parameters significantly decrease northwards, reaching their minimum beyond the Arctic Circle. However, there is a gap in the knowledge and documentation of freshwater gastropod abundance from selected Western Siberian Plain freshwater ecosystems. The Novosibirsk Reservoir and Lake Chany are the largest reservoirs in the forest–steppe zone in the Novosibirsk region. Analysis of the long-term dynamics of species richness and the relative density of Pulmonata snails in Lake Chany shows their correlation with water temperature and water level [9]. Some data on long-term dynamics of density for separate snail species Prosobranchia were also shown for the Lake Malye Chany basin [10] and the Novosibirsk reservoir [11].
By examining gastropods for their parasites, we can obtain information on trematodes present in the studied ecosystems. Despite comprising only ~5% of the world’s gastropod fauna, freshwater gastropods play a significant role as the intermediate hosts of trematodes, whose marites are the parasites of domestic animals and commercial species, and sometimes humans. The highest incidence rate of human infection with opisthorchiasis is reported in the areas adjacent to the Ob and Irtysh Rivers, Western Siberian Plain [12]. While epidemiology and parasite incidence in humans are well-studied, ecological information on the intermediate hosts of Opisthorchiidae remains limited. The range of species that could act as second intermediates or final hosts for opisthorchiid liver flukes is quite wide, although their first intermediate hosts belong to a single family of snails (Bithyniidae Gray, 1857).
In Western Siberia, opisthorchiid trematodes were detected in Bithynia leachii (Sheppard, 1823), Bithynia troschelii (Paasch, 1842), Bithynia inflata (Hansen, 1845) and Bithynia tentaculata (Linnaeus, 1758) [13,14,15,16]. Some authors regarded B. troschelii to be a geographical race of B. leachii [17]. However, Ya.I Starobogatov [18] listed B. troschelii as a distinct species in his monograph. The authors of subsequent studies [19,20], while emphasizing the distinctness of B. leachii and B. troschelii, indicated their close relationship, similarity, and ability, though rare, to produce hybrids. It is crucial to know in which water reservoirs the intermediate-host snails live, so that local hotbeds of opisthorchiasis can be detected [21,22,23]. However, information on bithyniid snail abundance in Western Siberia (and in the Novosibirsk region) is rare. Some relevant data were originally collected in the 1960s and 1970s [24], and in 1986–1996 [25]. Previously, we presented data on the abundance of bithyniid snails in the Ob River floodplain near the city Novosibirsk [26,27], at the mouth of the Kargat River [10], and in Lake Krotovo [28].
The purpose of this study is to define the ratio of Bithyniidae mollusks between other gastropods with regard to species diversity, and to compile all information regarding the abundance of bithyniid snails in four major basins situated in the Novosibirsk region that we examined over 27 years.

2. Materials and Methods

2.1. Study Area

Three major hydrographic systems could be singled out inside the territory of the Novosibirsk region. The northeastern area covers about 28,000 km2 and belongs to the Ob River basin, the northwestern sector encompasses nearly 60,000 km2 and falls within the Irtysh River basin, and the rest of the territory corresponds to the main part of the internal endorheic lake basin (Lake Chany basin and water bodies of Northern Kulunda). Lake Chany is a large brackish end orheic water reservoir in the Ob-Irtysh interfluve situated in the central part of the Baraba lowland. It is mostly fed by the Kargat and Chulym rivers. Lake Chany is critically important for the migratory birds of Siberia, and is listed as a Ramsar Site of International Importance (Date of Ramsar designation: 13 September 1994). Water bodies of Northern Kulunda are located in the steppe zone in the Western Siberian Plain; in the southern part is the Novosibirsk region. Conventionally, the border between the Barabinskaya lowland and the Kulundinskaya steppe is at 54 degrees north latitude.
The diversity of gastropods in August 2009 from water bodies of Northern Kulunda was studied. Samples were collected from different parts of the Karasuk River, upstream (54°26′53.2″ N; 80°55′50.5′ E and 54°09′53.2″ N; 80°02′54.2′ E) (Sampling site/geographical coordinates (N, E)). and downstream (53°45′19.4″ N; 78°20′15.1′ E and 53°43′19.7″ N; 77°56′29.5′ E), and in six lakes of Northern Kulunda: Astrodym 53°36′59.4″ N; 77°48′04.7′ E, Krivoye (reaches: Blagodatnoye 53°49′59.3″ N; 78°03′17.3″ E, Sopatoye 53°48′28.7″ N; 78°02′18.5″ E and Gusinoye 53°48′13.0″ N; 78°04′00.8″ E), Krotovo 53°43′30″ N; 77°51′31″ E, Kusgan 53°44′23″ N; 77°53′25″ E, Melkoye 53°47′37.9″ N; 78°16′34.91″ E, Titovo 53°45′25.8″ N; 77°56′13.2″ E (Figure 1).
The bithyniid snails in four major basins are situated in the Novosibirsk region that we examined in 1994–2020 (Figure 2). We examined bithyniid snails from the Ob basin, including the Ob River from floodplains downstream from the Novosibirsk hydroelectric power station from the river’s secondary, left, and right tributaries (left and right banks being from the point of view an observer facing downstream), and the Ob reservoir (left and right coasts). In the Irtysh River basin, snails were taken from the river’s secondary tributaries (i.e., Rivers Icha, Kama, and Musikha, and Lake Murashevskoe). Most thoroughly examined were Bithyniidae from the Ob–Irtysh drainless interfluve: Lake Malye Chany (Cape Tchernenky, Zolotye Rossypi Bay, near the village Shirokaya Kuria) and the Kargat River (estuary and the middle reach near the village Verkh-Kargat). In the water bodies of northern Kulunda, we studied snails from the Kuria, Burla, and middle and lower Karasuk Rivers, and from Lake Krotovo. In total, 201 samples with an abundance of bithyniid snails of reproductive age in 34 localities in 25 watercourses and water reservoirs were collected (Table 1).

2.2. Mollusk Sampling and Examination

Gastropods were collected according to the standard technique [3]. The mollusks were collected by hand out of 3–6 sampling sites of 0.25 m−2 at a depth between 0.1 and 0.7 m. Bithyniid snails of breeding age (from 2 to 6 years) had shell heights 5.6–11.2 mm and weighed 61–197 mg [29]. We monitored the number of bithyniid snails from the Kargat River estuary 1–3 times every 10 days in June–September 1994, May–September 1995–2000 and 2002–2005, and June 2006–2007 and 2012–2013. Temperature, the most important single abiotic factor, was recorded every day from May until September in all years of the study. The water temperature in the estuary of the Kargat River was measured three times a day (at 9:00, 15:00, and 21:00). On the basis of this information, average daily and ten-day temperatures were calculated [30,31]. Bithyniidae from the Ob Basin were collected monthly from floodplains downstream of the Novosibirsk hydroelectric power station dam in May to August 1996–1997, and once a year in late May or June in 1995 and 1998–2020. In the Kargat River estuary and the Ob River floodplain, long-term research was conducted, and the two water bodies were investigated for 15 and 27 years, respectively. Bithyniid snails were taken from Krotovo Lake in July 1994–1995, June 2006–2007, and August 2009. Other water bodies were inspected only on one occasion during the summer in different years.
The seasonal dynamics abundance of young (0+) and mature (shell heights >5 cm) bithyniid snails from the Kargat River estuary from May to September 1995–1996 was studied. Bithyniid snails were collected by sieving.
The gastropod species were identified according to the shell and genital system using the keys [5,18,32,33]. The index of copulatory apparatus (ICA) was one of the major criteria for the species definition of Pulmonata [34]. The compression method was used to examine more 2000 pulmonates and 17,000 bithyniid snails.
Statistical analyses were performed using the MS EXCEL 2003 and STATISTICA 6.0 software packages. The data on snail and trematode occurrence were compared using the chi-squared test with a 95% confidence interval (p < 0.05). The biodiversity of snails was studied using the Shannon–Weaver index.

3. Results

3.1. Diversity of Gastropods in Water Bodies of Northern Kulunda

Gastropoda in the modern freshwater bodies of the Western Siberian Plain are pulmonates and some prosobranchs. We examined gastropods from the lake and river ecosystems of northern Kulunda, in the south of the Novosibirsk region (Figure 1). Both subclasses were recorded in the water bodies of northern Kulunda. Prosobranchia snails are the most ancient colonizers of continental water bodies and are represented by only one family, Bithyniidae: Bithynia tentaculata (Linne, 1758) and B. troschelii (Paasch, 1842) (syn. Bithynia transsilvanica (Bielz, 1853). For Pulmonata snails, 6 families were recorded. Both secondary aquatic pulmonate snails (four families) and terrestrial species (two families) were recorded. The most widespread family, Lymnaeidae, was represented by 10 species: L. (Lymnaea) stagnalis (L., 1758), L. (L.) fragilis (L., 1758), L. (L.) doriana (Bourguignat, 1862), L. (Radix) auricularia (L.,1758), L. fontinalis sensu Kruglov and Starobogatov 1993, L. (Peregriana) balthica (L., 1758) (syn. Ampullaceana balthica), L. (P.) ovata (Drap., 1805), L. (P.) ampla (Hartmann, 1821) L. (P.) tumida (Held, 1836), and Lymnaea (Stagnicola) saridalensis (Mozley, 1934). Ramshorn snails were presented by two families, Planorbidae (Planorbis planorbis (L., 1758), Anisus vortex (L., 1758), A. contortus (L.,1758), Segmentina nitida (Mull., 1774) and Bulinidae—Planorbarius corneus (L., 1758). The Physidae family was represented by two species, Physa fontinalis (L.,1758) and Aplexa nypnorum (L., 1758). Terrestrial gastropods were defined by the genera Succinea sp. (Succineidae) and Zonitoides sp. (Zonitidae). Sixteen gastropod species were collected from the different sites of the Karasuk River. Twenty gastropod species were recorded in different lake ecosystems. However, 15 species were common for both the river and the lakes. Snails L. (P.) ovata were found in only the river, and five species were found only in the lakes: L. (P.) ampla and L. (L.) doriana, only in Lake Astrodym; S. nitida only in Lake Krotovo; A. nypnorum only in Lake Melkoye). Ramshorn snails P. corneus were found in the in three lake systems of Krotovo, Titovo, and the Sopatoye reaches (Lake Krivoye). The total number of gastropod species was from 5 to 12 in the water bodies of northern Kulunda (Table 2).
The abundance of gastropods in the Karasuk River varied from 10 up to 123 ind./m−2 and from 16 up to 82 ind./m−2 in the lake ecosystems of northern Kulunda (Figure 3). We found that separate families of gastropods are an important component in terms of abundance in lakes and river systems (Table 2). Lymnaeiid snails dominate in the water bodies of northern Kulunda (except one). Bithyniid snails were subdominants in the river, and Planorbiid snails were subdominants in the lakes (Table 3). In the Blagodatnoye reach, Succineiid snails dominated, and Lymnaeidae were subdominants. The Blagodatnoye reach has more boulder rocks, and fewer soil substrates and grasses along the bank that could serve as favorable habitat to aquatic gastropods. The terrestrial snails inhabit plants that grow close to the water’s edge and reeds (Phragmites) or cattails (Typha).
The Shannon—Weaver index, as calculated under the gastropod population density, was the highest at three water bodies (Lake Titovo; Sopatoye reach, and Karasuk River, downstream) compared to the other study locations (Figure 3). In lakes, the Shannon–Weaver index varied from 0.56 to 1.9 bit/ind. Shannon–Weaver indices revealed an increase in species diversity from the upper to the lower stream of Karasuk River.
Analyzing data diversity and abundance of gastropods communities from 9 freshwater bodies of northern Kulunda showed that only Karasuk River and Lake Krotovo contained bithyniid snails.

3.2. Bithyniid Abundance in the Four Major Basins Situated in the Novosibirsk Region

More than 100 water reservoirs bodies of the four major basins in the Novosibirsk region were examined for bithyniid snails (Figure 2). We included only bithyniid snails of reproductive age (shell height of 5 mm and more) when calculating snail abundances for the present study. Regarding the abundance of bithyniid snails, they were collected in 34 localities in 25 water bodies.

3.2.1. Ob River Basin

The mean abundance of bithyniid snails of reproductive age in the water bodies situated in the Ob River basin varied from 8 to 27 ind.·m−2 in the tributaries (Inya and Baksa Rivers), and from 19 to 128 ind.·m−2 in the Ob floodplain in different years (multiyear average, 48 ± 25 ind.·m−2). Over the last 27 years of research, bithyniid densities of more than 40 ind.·m−2 were noted in 10 different years, including 5 years of over 60 ind.·m−2. The snail densities in the river were several orders of magnitude higher than those in the Ob reservoir, e.g., density dropped to 1 ind. per 10 m−2 in estuarine parts of the rivers draining into the Ob reservoir (Figure 4).
Both B. troschelii and B. tentaculata were present in the 10 out of 18 sites in the Ob basin. The abundance ratio of B. troschelii was higher than that of B. tentaculata in Berd River, in the Ob reservoir (left and right coasts), in the Orda River, in Berdsky Bay (left and right coasts), and the Talmenka, Karakan, and Tulka Rivers. However, their share was smaller in the floodplain in the Ob, Uen, and Chauz Rivers. In four rivers (Suenga, Baksa, Miltyush and Sosnovka), only B. tentaculata was found (Figure 5).

3.2.2. Irtysh River Basin

In the northwest of the Novosibirsk region, the secondary and tertiary tributaries of the Irtysh River are situated: we sampled snails from the secondary tributaries, i.e., the Icha, Kama, Musikha Rivers, and Lake Murashevskoe. Densities varied from 2 ind.·m−2 in the Kama River to 21 ind.·m−2 in the Musikha River, to 13 ind.·m−2 in Lake Murashevskoe. Both B. troschelii and B. tentaculata were present. In the Musikha River, B. troschelii constituted 75% of bithyniids, but in the lake, their fraction shrunk to a mere 12%. Only B. tentaculata was found in the Icha and Kama Rivers.

3.2.3. Lake Chany Basin

Bithyniidae were picked up for examination from both river and lake biotopes of the Lake Chany basin (Figure 2C). Monitoring studies of snail abundance were carried out in the Kargat River estuary in 1994–2013. Daily monitoring surveys were carried out recording the water temperature, level, and 10-day estimates of the numbers of bithyniid snails from June to August (inclusive). According to the average ten-year (1995–2005) data from the Kargat River mouth, the densities of bithyniid snails of reproductive age ranged from 62 ± 48 ind./m−2 in June, decreasing to 13 ± 9 ind./m−2 in July, and to single individuals (1–2 ind./m−2) in August. Analysis of the data shows that the average summer abundance of bithyniid snails was not related to the average summer temperature regime, but positively correlated with the water temperature in the second 10-day period of June (r = 0.52, p < 0.05). The maximal abundance (186 ind./m2) of B. troschelii of reproductive age was recorded in the second 10-day period of June 2004. The densities of bithyniid snails may vary tenfold in different years in the same water body (Figure 6). Bithynia tentaculata was uncommon in the biotope under discussion—the density ratio of B. troschelii to B. tentaculata was as far as 14:1 (Figure 5). In the middle reach of the Kargat River, only B. tentaculata was present, while in lake biotopes (Lake Malye Chany: Zolotye Rossypi Bay, Tchernenky Cape), only B. troschelii was encountered.

3.2.4. Water Bodies of Northern Kulunda

We examined bithyniid snails from the lake and river ecosystems of northern Kulunda. Snail abundance was explored in Lake Krotovo and the Karasuk, Kuria, and Burla Rivers. The densities of bithyniid snails decreased from 26 ind.·m−2 in central Karasuk to 2 ind.·m−2 in lower Karasuk, while in the Kuria and Burla Rivers, the snails were scanty, with no more than 5 ind.·m−2. Long-term mean density in Lake Krotovo stood at 13 ind.·m−2, although it varied from 3 to 28 ind.·m−2 during the years of study. Both B. troschelii and B. tentaculata were encountered in the lake and Karasuk River, though in the other two rivers, only B. troschelii was found.
Our 27-year study of the abundance of mollusks in the water reservoirs of the Novosibirsk region shows that bithyniid snails were found in lakes and rivers from all four major basins. Their typical habitats are running waters ranging from small creeks to streams, lakes, and estuaries. The preference of B. troschelii for organic-rich water bodies was statistically greater (χ2 = 6.27, p = 0.012), whereas B. tentaculata preferred river-type biotopes (χ2 = 4.14, p = 0.042). Both species were present in 15 of 25 water bodies of the Novosibirsk region see (Figure 5). B. troschelii inhabited organic-rich water bodies featuring silt, and overgrown with common reeds (Phragmites) and cattails (Typha). B. tentaculata preferred river-type biotopes, and was collected from rivers or areas with running water, where macrophytes are represented not only by common reeds and cattails, but also by frogbits (Hydrocharis), yellow water lilies (Nuphar lutea), arrowheads (Sagittaria), water soldiers (Stratiotes), and pondweeds (Potamogeton).

3.3. The Seasonal Dynamics of Bithyniid Snail Abundance in the South of Western Siberia

Daily observations in the estuarine areas of the Kargat River for the summer periods (1995–2005) show that peak numbers of snails were present in the middle of summer. The young of the year comprise 71–76% of the population.
Trends in abundance were the same from year to year, but actual mean abundance differed significantly between years. For instance, the mean abundance in the second 10-day period of July 1995 was almost four times lower than that in the corresponding period of 1996, i.e., 296 and 1155 ind.·m−2, respectively (Figure 7). Since the temperature in the water bodies in June 1995 was lower (17.10 ± 2.65 °C) than that in June 1996 (19.83 ± 2.45 °C; p < 0.001) it can be assumed that temperature affected the timing of the end of winter diapauses and the intensity of reproduction, and thereby the abundance of snails. Visual observations in the following years corroborated that assumption. Average daily summer water temperatures in the Kargat River from 1995 and 1996 are shown in Figure 8. Thus, there may be substantial fluctuations in numbers of B. troschelii between spring and autumn in the same water reservoir.

4. Discussion

Quantitative data on mollusk communities are scanty. Therefore, this study was performed to identify the species composition, and to determine the diversity and abundance of gastropod communities from water bodies in the south of western Siberia in Novosibirsk region freshwater ecosystems. In total, 21 species of gastropod snails belonging to 7 families, pulmonates and prosobranchs, were recorded in the present study. In the studied water bodies in the south of Western Siberia, pulmonates are widespread, inhabit different water bodies, and dominate in abundance and biomass [9,28,35]. Many pulmonates have broad environmental tolerance, tend to be more resistant to eutrophication and brief exposure to air, are capable of self-fertilization, and have high fecundity. This renders many of them more resilient to human-mediated threats and less extinction-prone than freshwater prosobranchia snails are. The L. stagnalis species is the most widespread and numerous in water bodies in the south of Western Siberia. It was recorded in all habitats of this study (Table 2). For water bodies of Eastern Europe, L. fragilis and L. doriana are synonymous with L. stagnalis because they are identical in their anatomy and their molecular genetics [36], but similar studies in Siberia are also necessary. The L. (S.) saridalensis, L. (P.) balthica, P. planorbis, and Succinea sp. species were recorded in 91% of the habitats. The prosobranch species of the Bithyniidae family were found in 22% of the water bodies. Bithyniids cannot breathe atmospheric air.
The larval trematode community of bithyniid snails shows little overlap with the trematode fauna of pulmonate snail hosts [37,38,39]. Bithyniid snails are obligatory intermediate hosts of more than 40 trematode species of 14 families [13,37,38,39]. In Western Siberia, opisthorchiid trematodes were detected in four bithyniid species [13,14,15,16]. Bithyniidae in lakes and rivers situated in the Novosibirsk region are represented by B. troschelii and B. tentaculata. Both B. troschelii and B. tentaculata act as first intermediate hosts for opisthorchiid trematodes: Opisthorchis felineus (Rivolta, 1884) parthenitae were encountered only in B. troschelii, and Metorchis xanthosomus (Heinemann, 1937) only in B. tentaculata, while Metorchis bilis (Braun, 1890) (syn. M. albidus (Braun, 1893)) arthenitae were found in both [12,15,16]. O. felineus and M. bilis are two opisthorchiid species that are perilous to human health.
Data on bithyniid snail abundance in the water bodies of the Ob-Irtysh basin are fragmentary [40]. Some data on abundance in the Novosibirsk region were initially collected in the 1960s and 1970s. K. P. Fedorov [24] published data on bithyniid snail abundance in the bodies of northern Kulunda. The abundance peaks in the coastal area of Lake Krotovo were 160 ind.·m−2 in 1967 and 250 ind.·m−2 in 1973; however, no information was presented on either the dates of the collection or the size of the counted snails. There is no doubt that one of the main factors stimulating the transition of poikilothermic organisms from physiological depression to an active lifestyle is an increase in ambient temperature; for prosobranch snails, this is water in a reservoir. The study of interannual and seasonal dynamics of snail abundance shows that, in the south of Western Siberia, the period of active life of bithyniid snails does not exceed three months, namely, May–July, for mature mollusks (age from 1+ to 5+) and from mid-June to mid-September for the young (0+). Although the first yearlings can be found at the end of June, a huge number of young bithyniid snails are present by July (Figure 7). The increase in population size in August is caused by the release of juveniles from all clutches. Another study showed [30] that, in one reproductive season, up to 5414 egg capsules of bithyniid snails develop on one square meter of the reservoir. It is possible that snails of all sizes were included in these figures, unlike in our calculations [24]. Thus, we cannot really compare these data to the numbers from our study. Moreover, the review mentioned Bithyniidae in the Astrodym, Kusgan, and Titovo Lakes. We failed to find any bithyniid snails in these lakes in our study in 2009 (Table 2). Regarding the adult population (age from 1+ to 5+) of bithyniid snails, we also noted a decrease in their number in August every year. This was noted in all ten years of observation, although in the first 10 days of August, the water temperature is still quite warm, from 18.7 °C (2004) to 23.5 °C (in 2000), and the long-term average is 21.5 ± 1.59 °C. The reasons for the transition of bithyniid snails from active life to diapause are changes in the quality of the environment (water in reservoirs). Many researchers studied a number of abiotic factors [14,21,41] that can decrease the number of bithyniid snails in August. For example, there is an assumption that the main reason may be the decrease in water level in the river, increasing its mineralization [14,41]. However, we observed a decrease in the density (and total number) of bithyniid snails in August both in years with low (in 1994–1996) and in years with high water level (in 1997–1998). Earlier studies of S.A. Beer et al. [21] of the seasonal dynamics of hydrochemical parameters in the water bodies of Western Siberia showed that the content of oxygen dissolved in water decreases from 7 mg/L (in July) to 2 mg/L (in August). The “water bloom”, which significantly reduces the amount of dissolved oxygen, also causes a decrease in the number of bithyniid snails. After 2 days, their number decreases 14 times, and after a week, more than 20 times. Without rejecting the opinions presented in the literature, we assume that the decrease in the number of bithyniid snails in August was caused by both abiotic and biotic factors. When the reproductive period is over, and the body’s reserves are running out, there are two ways, either diapause or death, and a change in water quality or the photoperiod performs only a signal function. The low number of the adult bithyniid snail population, in combination with a huge number of young individuals, may have important biological significance. Although intraspecific competition for food among bithyniid snails is unlikely, competitive relations between adults and yearlings are possible for oxygen dissolved in water, the content of which decreases in August [21].
Bithyniid abundance in the right-bank secondary Irtysh tributaries was studied in 1986–1996. Karpenko et al. [25] collected data on the number of bithyniid snails in near-riverbed oxbows of the Tartas and Tara Rivers, and at the junction of the Om and Kama Rivers, with maximal abundance reaching 20–25 ind.·m−2. Similar data on a bithyniid snail abundance of 0.5–16 ind.·m−2 in left-bank secondary Irtysh tributaries (the Rivers Tura, Tavda, Ikin Sverdlovsk and Kurgan regions) were published earlier [41,42]. These figures match the corresponding data from our study.
The abundance of bithyniid snails in the Ob River and Lake Chany basins are only known from our data [26,27]. Snail densities were low in most examined water bodies (Figure 4), but the densities of bithyniid snails may vary tenfold in different years in the same water body (Figure 6). The quantitative data of this study can be used to identify and predict the natural foci of opisthorchiasis in the south of Western Siberia.

5. Conclusions

We calculated the quantitative characteristics of gastropods (21 species, 7 families) from the modern freshwater lake and river ecosystems of northern Kulunda in the south of the Novosibirsk region. Data analysis of the diversity and abundance of gastropod communities showed that 22% of the water bodies contained bithyniid snails. Both B. troschelii and B. tentaculata are present in the Novosibirsk region and act as first intermediate hosts for opisthorchiid trematodes that are perilous to human health. More than a hundred water reservoirs were examined for freshwater snails, with a total of 34 localities in the 25 water bodies of the 4 major basins situated in the Novosibirsk region containing bithyniid snails. Snail densities were low in most examined water bodies (10 ind.·m−2 and fewer). Bithyniid snail abundance may vary tenfold in different years in the same water body.

Funding

The study was funded by the Federal Fundamental Scientific Research Program for 2021–2025, project number 122011800267-4.

Institutional Review Board Statement

Our work conforms to the legal requirements and guidelines in the Russian Federation, and to international ethical standards. The species from our study is not included in the Threatened category of the IUCN Red List of Threatened Species.

Data Availability Statement

Not applicable.

Acknowledgments

The author is grateful to A.P. Yanovskii, A.I. Chechulin, K.P. Fedorov, S.N. Vodyanitskaya, M.A. Mosina, A.V. Katokhin and K.V. Romanov for their help with snail samplings; M.V. Vinarski for their help snail Peregriana and Radix identification. We also wish to thank researchers of the Chany Field Station and of the Karasuk Scientific Station (The Institute of Systematics and Ecology of Animals, Novosibirsk) for their help with accommodation and providing conditions for the field work.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Sampling sites of examined gastropod snails in water bodies of Northern Kulunda. (A) Western Siberia. (B) Novosibirsk region. (C) Water bodies of Northern Kulunda: Karasuk River, upstream near Bystrukha village (1); Karasuk River, upstream near Tchernovka village (2); Karasuk River, downstream near Gramotino village (3); Karasuk River, downstream Sorochikha village (4); Lake Astrodym (5); Lake Krotovo (6); Lake Kusgan (7); Lake Melkoye (8); Lake Titovo (9); Lake Krivoye—reach Blagodatnoye (10); Lake Krivoye—reach Sopatoye (11); Lake Krivoye—reach Gusinoye (12).
Figure 1. Sampling sites of examined gastropod snails in water bodies of Northern Kulunda. (A) Western Siberia. (B) Novosibirsk region. (C) Water bodies of Northern Kulunda: Karasuk River, upstream near Bystrukha village (1); Karasuk River, upstream near Tchernovka village (2); Karasuk River, downstream near Gramotino village (3); Karasuk River, downstream Sorochikha village (4); Lake Astrodym (5); Lake Krotovo (6); Lake Kusgan (7); Lake Melkoye (8); Lake Titovo (9); Lake Krivoye—reach Blagodatnoye (10); Lake Krivoye—reach Sopatoye (11); Lake Krivoye—reach Gusinoye (12).
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Figure 2. Sampling sites of examined bithyniid snails in four major basins in the Novosibirsk region. (A) Ob River basin: Ob River, downstream Novosibirsk HPS dam (1); Inya River (2); Berd River (3); Suenga River (4); Baksa River (near Pikhtovka and Laptevka villages) (5,6); Uen River (7); Chauz River (8); Ob reservoir left coast near Krasny Yar village (9); Orda River (10); Ob reservoir right coast near Zav’yalovo village (11); Berdsky bay, left and right coasts (12,13); Talmenka River, estuary (14); Karakan River, estuary (15); Tulka River, estuary (16); Miltyush River, estuary (17); Sosnovka River (18). (B) Irtysh River basin: Om River tributaries: Icha River (19); Kama River (20); Musikha River (21); Lake Murashevskoe (22). (C) Lake Chany basin: Lake Malye Chany (23); Zolotye Rossypi bay (24); Kargat River, estuary Chany Field Station (25); Kargat River, estuary-2 (26); Kargat River, middle reaches (27). (D) Water bodies of Northern Kulunda: upstream near Bystrukha village (28); Karasuk River, upstream near Tchernovka village (29); Karasuk River, downstream near Gramotino village (30); Karasuk River, downstream Sorochikha village (31); Kuria River (32); Burla River (33); Lake Krotovo (34).
Figure 2. Sampling sites of examined bithyniid snails in four major basins in the Novosibirsk region. (A) Ob River basin: Ob River, downstream Novosibirsk HPS dam (1); Inya River (2); Berd River (3); Suenga River (4); Baksa River (near Pikhtovka and Laptevka villages) (5,6); Uen River (7); Chauz River (8); Ob reservoir left coast near Krasny Yar village (9); Orda River (10); Ob reservoir right coast near Zav’yalovo village (11); Berdsky bay, left and right coasts (12,13); Talmenka River, estuary (14); Karakan River, estuary (15); Tulka River, estuary (16); Miltyush River, estuary (17); Sosnovka River (18). (B) Irtysh River basin: Om River tributaries: Icha River (19); Kama River (20); Musikha River (21); Lake Murashevskoe (22). (C) Lake Chany basin: Lake Malye Chany (23); Zolotye Rossypi bay (24); Kargat River, estuary Chany Field Station (25); Kargat River, estuary-2 (26); Kargat River, middle reaches (27). (D) Water bodies of Northern Kulunda: upstream near Bystrukha village (28); Karasuk River, upstream near Tchernovka village (29); Karasuk River, downstream near Gramotino village (30); Karasuk River, downstream Sorochikha village (31); Kuria River (32); Burla River (33); Lake Krotovo (34).
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Figure 3. Diversity and abundance of gastropods in water bodies of Northern Kulunda: Karasuk River, upstream near Bystrukha village (1); Karasuk River, upstream near Tchernovka village (2); Karasuk River, downstream near Gramotino village (3); Karasuk River, downstream Sorochikha village (4); Lake Astrodym (5); Lake Krotovo (6); Lake Kusgan (7); Lake Melkoye (8); Lake Titovo (9); Lake Krivoye—Blagodatnoye reach (10); Lake Krivoye—Sopatoye reach (11); Lake Krivoye—Gusinoye reach (12).
Figure 3. Diversity and abundance of gastropods in water bodies of Northern Kulunda: Karasuk River, upstream near Bystrukha village (1); Karasuk River, upstream near Tchernovka village (2); Karasuk River, downstream near Gramotino village (3); Karasuk River, downstream Sorochikha village (4); Lake Astrodym (5); Lake Krotovo (6); Lake Kusgan (7); Lake Melkoye (8); Lake Titovo (9); Lake Krivoye—Blagodatnoye reach (10); Lake Krivoye—Sopatoye reach (11); Lake Krivoye—Gusinoye reach (12).
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Figure 4. Bithyniid snail abundance (ind.·m−2) in different water bodies of the Novosibirsk region. Abundance of bithyniid snails.
Figure 4. Bithyniid snail abundance (ind.·m−2) in different water bodies of the Novosibirsk region. Abundance of bithyniid snails.
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Figure 5. Mean density ratios of Bithynia troschelii to B. tentaculata in water bodies of the Novosibirsk region (average values for sites sampled more than once). Ob River basin: Ob River, downstream Novosibirsk HPS dam (1); Inya River (2); Berd River (3); Suenga River, (4); Baksa River (5); Uen River (6); Chauz River (7); Ob reservoir left and right coasts (8); Orda River (9); Berdsky Bay (left and right coasts) (10); Talmenka River (11); Karakan River (12); Tulka River (13); Miltyush River (14); Sosnovka River (15). Irtysh River basin: Om River tributaries: Icha River (16); Kama River (17); Musikha River (18); Lake Murashevskoe (19). Lake Chany basin: Lake Malye Chany and Zolotye Rossypi Bay (20); Kargat River (21). Water bodies of Northern Kulunda: Karasuk River (22); Kuria River (23); Burla River (24); Lake Krotovo (25). Bithyniid snails from the Icha, Kama, and Baksa Rivers were sampled by A.P. Yanovskii; those from the Musikha River by A.I. Chechulin; those from the Karakan River by K.P. Fedorov those from Lake Murashevskoe by S.N. Vodyanitskaya; those from the Kuria River by M.A. Mosina; those from the Orda and Suenga Rivers by A.V. Katokhin; and those from the Burla River by K.V. Romanov.
Figure 5. Mean density ratios of Bithynia troschelii to B. tentaculata in water bodies of the Novosibirsk region (average values for sites sampled more than once). Ob River basin: Ob River, downstream Novosibirsk HPS dam (1); Inya River (2); Berd River (3); Suenga River, (4); Baksa River (5); Uen River (6); Chauz River (7); Ob reservoir left and right coasts (8); Orda River (9); Berdsky Bay (left and right coasts) (10); Talmenka River (11); Karakan River (12); Tulka River (13); Miltyush River (14); Sosnovka River (15). Irtysh River basin: Om River tributaries: Icha River (16); Kama River (17); Musikha River (18); Lake Murashevskoe (19). Lake Chany basin: Lake Malye Chany and Zolotye Rossypi Bay (20); Kargat River (21). Water bodies of Northern Kulunda: Karasuk River (22); Kuria River (23); Burla River (24); Lake Krotovo (25). Bithyniid snails from the Icha, Kama, and Baksa Rivers were sampled by A.P. Yanovskii; those from the Musikha River by A.I. Chechulin; those from the Karakan River by K.P. Fedorov those from Lake Murashevskoe by S.N. Vodyanitskaya; those from the Kuria River by M.A. Mosina; those from the Orda and Suenga Rivers by A.V. Katokhin; and those from the Burla River by K.V. Romanov.
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Figure 6. Long-term dynamics of Bithynia troschelii abundance and water temperature in the Kargat River estuary in 1995–2013 (only in the second 10-day period of June).
Figure 6. Long-term dynamics of Bithynia troschelii abundance and water temperature in the Kargat River estuary in 1995–2013 (only in the second 10-day period of June).
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Figure 7. Seasonal dynamics of Bithynia troschelii abundance in the Kargat River estuary in 1995–1996.
Figure 7. Seasonal dynamics of Bithynia troschelii abundance in the Kargat River estuary in 1995–1996.
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Figure 8. Water temperature from May until September (every day) in Kargat River estuary in 1995–1996.
Figure 8. Water temperature from May until September (every day) in Kargat River estuary in 1995–1996.
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Table
Table 1. Sampling-site bithyniid snails in water bodies of the Novosibirsk region in 1994–2020.
Table 1. Sampling-site bithyniid snails in water bodies of the Novosibirsk region in 1994–2020.
Sampling SiteGeographical
Coordinates (N, E)		YearsSamples *
Ob River basinOb River downstream
Novosibirsk HPS dam		54°53′23″, 83°05′18″1995–202033
Ob River
tributaries
(right)		Inya River54°09′17″, 83°07′31″19981
Berd River54°69′55″, 83°22′50″20131
Suenga River, Berd River tributaries54°25′39″, 84°32′33″20181
Ob River
tributaries
(left)		Baksa River (near Pikhtovka and Laptevka villages)55°99′21″, 82°70′81″19971
55°79′10″, 82°30′80″19971
Uen River55°31′0, 83°16′01996, 1998, 1999, 20034
Chauz River55°31′0, 83°16′020141
Ob reservoirOb reservoir left coast Near Krasny Yar village55°13′11″, 82°54′29″20171
Orda River54°22′76″, 81°55′26″20181
Ob reservoir right coast
Near Zav’yalovo village		54°54’45″, 82″47°57′81″20071
Berdsky Bay (right coast)54°78′, 83°09″20021
Berdsky Bay (left coast)54°77′, 83°09″20071
Talmenka River, in estuary54°42′25″, 83°16′50″20071
Karakan River, in estuary54°50′22″, 82°44′94″20071
Tulka River, in estuary54°56′20″, 82°65′46″20091
Miltyush River, in estuary54°65′57″, 82°86′12″20091
Sosnovka River, in estuary54°68′43′, 82°96′71″20091
Irtysh River basinOm River tributaries: Icha and Kama Rivers55°99′, 82°70′19961
55°79′, 82°30′19961
Musikha River55°52′16″, 80°05′18″20081
Lake Murashevskoe55°43′16″, 75°34′39″2007, 20082
Lake Chany basinLake Malye Chany54°37′21″, 78°09′21″2003, 20122
Zolotye Rossypi Bay54°34′12″, 78°08′39″1996, 19972
Kargat River, estuary (1)
Chany field station		54°37′76″, 78°13′07″1994–2000, 2002–2007, 2012, 2013126
Kargat River, estuary (2)54°61′, 78°22′20131
Kargat River, middle reaches54°47′37″, 79°06′19951
Water bodies of Northern KulundaKarasuk River 54°26′53″, 80°55′50″20091
54°09′53″, 80°02′54″20091
53°45′19″, 78°20′15″20091
53°43′19″, 77°56′29″20091
Kuria River53°50′56″, 78°22′34″20071
Burla River53°20′, 78°20′20101
Lake Krotovo, Karasuk scientific station53°43′30″, 77°51′31″1994, 1995, 2006, 2007, 20095
In total201
* Sample abundance of bithyniid snails. Bithyniidsnails from the Icha, Kama, and Baksa Rivers were sampled by A.P. Yanovskii; those from the Karakan River by K.P. Fedorov; those from the Musikha River by A.I. Chechulin; those from Lake Murashevskoe by S.N. Vodyanitskaya; those from the Kuria River by M.A. Mosina; those from the Orda and Suenga Rivers by A.V. Katokhin; and those from the Burla River by K.V. Romanov.
Table
Table 2. Number of gastropod species in water bodies of northern Kulunda in 2009.
Table 2. Number of gastropod species in water bodies of northern Kulunda in 2009.
Water BodiesFamiliesKarasuk RiverLake
Families 1 *23456789101112
Lymnaeidae435554336364
Planorbidae221213111131
Physidae000101010000
Bulinidae000001001010
Succineidae101111111111
Zonitidae110000010000
Bithyniidae211102000000
All species1077107125795116
* Water bodies of northern Kulunda: Karasuk River, upstream near Bystrukha village (1); Karasuk River, upstream near Tchernovka village (2); Karasuk River, downstream near Gramotino village (3); Karasuk River, downstream Sorochikha village (4); Lake Astrodym (5); Lake Krotovo (6); Lake Kusgan (7); Lake Melkoye (8); Lake Titovo (9); Lake Krivoye—reach Blagodatnoye(10); Lake Krivoye—reach Sopatoye (11); Lake Krivoye—reach Gusinoye (12).
Table
Table 3. Abundance (ind./m2) of gastropods in August 2009 from water bodies of northern Kulunda (Novosibirsk region).
Table 3. Abundance (ind./m2) of gastropods in August 2009 from water bodies of northern Kulunda (Novosibirsk region).
Water
Bodies *		LymnaeidaePlanorbidaePhysidaeBulinidaeSuccineidae ZonitidaeBithyniidae
10.1–176/81.4 **0–32/12000–4/1.30–4/1.30–68/26.7
20.2–10/6.10–1/0.50000–0.1/0.050–8/4
316–20/21.50–2/1000–4/200–4/2
412–31/25.50–6/40–5/200–3/201–6/4
50.02–37/22.30–18/6000–3/100
66–28/173–80/410.2–4/20–0.2/0.10.8–12/6.400–6/3
70.03–88/330.01–4/1.7000–1/0.300
824–99/55.31–64–/25.30–2/0.700–1/0.30–1/0.70
922–45/330–27/11.700–6/20–8/300
100–45/22.50–0.12/0.06000–49/24.500
110.25–81/400–6/300.1–2.0/10–7/3.500
122–28/150–1/0.3000–2/100
* Water bodies of northern Kulunda: Karasuk River, upstream near Bystrukha village (1); Karasuk River, upstream near Tchernovka village (2); Karasuk River, downstream near Gramotino village (3); Karasuk River, downstream Sorochikha village (4); Lake Astrodym (5); Lake Krotovo (6); Lake Kusgan (7); Lake Melkoye (8); Lake Titovo (9); Lake Krivoye –Blagodatnoye reach (10); Lake Krivoye –Sopatoye reach (11); Lake Krivoye –Gusinoye reach (12). ** Minimum—maximum/average.
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Serbina, E.A. Bithyniid Abundance in the South of Western Siberia Water-Courses and Water Reservoirs (Russia). Diversity 2022, 14, 791. https://doi.org/10.3390/d14100791

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Serbina EA. Bithyniid Abundance in the South of Western Siberia Water-Courses and Water Reservoirs (Russia). Diversity. 2022; 14(10):791. https://doi.org/10.3390/d14100791

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Serbina, Elena A. 2022. "Bithyniid Abundance in the South of Western Siberia Water-Courses and Water Reservoirs (Russia)" Diversity 14, no. 10: 791. https://doi.org/10.3390/d14100791

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