1. Introduction
Lake Issyk-Kul (an alternative spelling—Issyk Kool) is one of the largest lakes in Central Asia (Figure 1), and the second largest (after the Aral Sea) waterbody situated in so-called “Middle Asia” (a part of Central Asia that lay within the ex-USSR’s territory). Nowadays, this lake belongs to the Republic of Kyrgyzstan. It is located at an altitude of 1606 m and forms an oval-shaped basin with a surface area of 6236 km2 [1]. The lake depression is located between two ridges of the Tien Shan Mts—Kungay-Alo-Too and Terskey-Ala-Too. The maximum depth of Issyk-Kul is 668 m (the average depth is 278 m), which makes it one of the deepest lakes in the world [2]. This is an oligotrophic basin. The water of the lake is slightly brackish; its salinity reaches 5.8–5.9‰ [2]. The lake is now drainless and has about 80 small tributaries. Issyk-Kul is of tectonic origin; initially, an isolated intermountain depression was formed by intensive tectonic movements and then it was filled with water [1,3]. The history of Issyk-Kul can be traced back to the early Miocene period, and its absolute age is about 20 myr [1]. That history was very complicated: according to some authors [3], over time, the lake has experienced strong fluctuations in its water level as well as salinity variations. In some epochs, it became a completely freshwater basin [3].
The Issyk-Kul Lake malacofauna, according to available publications, is rather poor. The first European explorer of the lake, Russian traveller Pyotr Semyonov, visited the lake twice, in 1856 and 1857, and published a pioneering account of the physical and geographical properties and natural history of Issyk-Kul [4]. He collected some shells of molluscs deposited on the lake’s shores and in other places in the Tien Shan Ridge; later, these materials were sent to Eduard von Martens, a prominent German malacologist of the 19th century. Von Martens established that there were three new species of snails, two belonging to the terrestrial genus Helix, and the third classified by him as a lymnaeid—Limnaeus obliquatus Martens, 1864 [5,6]. Another German malacologist of that epoch, S. Clessin, published two articles with descriptions of continental molluscs of Issyk-Kul Lake and its surroundings [7,8]. This author compiled the first list of the Issyk-Kul snails and bivalves, containing 16 species [8]. One of the most characteristic snail species of the lake is Caspia issykkulensis Clessin, 1894, whose empty shells are very abundant on the northern shore of Issyk-Kul. In 1972, this snail was reclassified as a member of the genus Pseudocaspia, Starobogatov, 1972 [9].
Zhadin [10], in his monograph on freshwater Mollusca of the former USSR, listed only three species of molluscs living in the lake: Caspia issykkulensis, Radix auricularia var. obliquata (Martens), and Radix ovata (Draparnaud, 1805) var. (undefined by the author). Since Zhadin’s work, no comprehensive survey of the Issyk-Kul malacofauna has been published. A drastic difference between species lists published by Clessin [8] and Zhadin [9] (16 species vs. 3) indicates that a revised study of the malacofauna of this waterbody is an urgent task. The taxonomic identity of several nominal species of molluscs, described by Clessin (Ancylastrum ovatum Clessin, 1907; A. turkestanicum Clessin, 1907; Gyraulus acutus Clessin, 1907; Pisidium schmidti Clessin, 1907; etc.), remains unresolved. All these species listings were established based on empty shells only and, unfortunately, living specimens of them are inaccessible. For example, nobody since Clessin has ever found a single species of freshwater limpet of the genus Ancylastrum Bourguignat, 1853, established by him. Hubendick [11] synonymized the four species of Ancylastrum of Issyk-Kul with the widespread Northern Eurasian species Ancylus fluviatilis O.F. Müller, 1774 (Gastropoda: Planorbidae), however, the existence of this species in Central Asia is highly problematic, and the taxonomic position of Clessin’s limpets remains extremely obscure [12].
Despite the low species richness of the Issyk-Kul malacofauna, Izzatullaev and Starobogatov [13] separated this lake and its drainage basin into a special malacofaunistic province. The last species of molluscs described from Lake Issyk-Kul is Odhneripisidium issykkulense, Izzatullaev and Starobogatov, 1986, from the family Sphaeriidae (Bivalvia) [14].
The use of molecular approaches to phylogeny and systematics is today a standard for the taxonomy of freshwater Mollusca, and the absence of fresh material on most of the nominal species mentioned by Clessin, Starobogatov, and other researchers makes it impossible to present now a full checklist of the Issyk-Kul malacofauna. In this research, we took a first step towards the full understanding of the Issyk-Kul molluscs. We report the results of a molecular revision of lymnaeid snails of the genus Radix Montfort, 1810, inhabiting this basin. Zhadin [10] mentioned two species of Radix in the lake (see above). More recently, Kruglov and Starobogatov [15] and Kruglov [16], in their comprehensive studies of the Lymnaeidae of Eurasia, also recognized two species of Radix [=Lymnaea (Radix) sensu Kruglov and Starobogatov, 1993]—R. obliquata and R. subdisjuncta (Nevill, 1878).
Another goal of our publication is to review all species of Radix reported from the ancient deep lakes of the world, with remarks on their taxonomy and ecology. We believe this provides helpful comparative material to all interested in molluscan radiations in ancient lakes.
2. Material and Methods
2.1. Primary Material and Morphological Studies
The type series of the two species of Radix recently reported in Issyk-Kul Lake (i.e., Radix obliquata and R. subdisjuncta), were examined by us (Figure 2). The type series of Limnaeus obliquatus contains two syntypes and is kept in the Natural Historical Museum of Berlin, Germany (ZMB) [6,17]. The taxonomic identity and shell variability of this species have been discussed many times in the literature [16,17,18,19,20,21,22]. The whereabouts of the holotype of Limnaea lagotis var. subdisjuncta is unknown to us. Probably, it is kept in the Indian Zoological Museum in Kolkata. We studied seven paratypes of this taxon deposited in the Natural History Museum of the United Kingdom, London, UK (NHMUK, see Figure 2). The type locality of R. subdisjuncta lies in Kashmir (“neighbourhood of Leh”; see [23]). Though Kruglov and Starobogatov [15,16,21] accepted it as a “good” species, subsequent researchers consider it a species of unclear identity [24]. Though this species was reported in Inner Mongolia (China) [15], it is absent from Yen’s comprehensive account on the Chinese freshwater snails [25,26]. In a more recent work, Liu [27] also did not discuss this snail. Subba Rao [28], in his survey of Indian molluscs listed this taxon as a variety of Lymnaea peregra (O.F. Müller, 1774). However, this species (Peregriana peregra of the current system) does not inhabit India [29].
In addition, numerous samples of Radix collected from the Issyk-Kul Lake and its basin as well as from other regions of Central Asia were examined. These lots are kept in the abovementioned museums in Berlin and London as well as in other depositories in Europe: Zoological Institute of the Russian Academy of Sciences, Saint-Petersburg, Russia (ZIN); the Naturmuseum Senckenberg, Frankfurt am Main, Germany (SMF); Zoological Museum of Copenhagen University, Denmark (ZMUC); Zoological Museum of Moscow State University, Russia (ZMMU); and Museum of the Institute of Plant and Animal Ecology, the Ural Branch of the Russian Academy of Sciences (UB RAS), Yekaterinburg, Russia (IPAE).
We sampled molluscs in Issyk-Kul Lake thrice, in 2013, 2018, and 2023, in several habitats located along the northern shore of this waterbody. Most samples were collected in vicinities of Cholpon-Ata (approximate coordinates: 42.639 N, 77.072 E) and Ananievo (approximate coordinates: 42.706 N, 77.696 E) settlements. The collected specimens were represented by empty shells and live individuals (mostly subadult) sampled from sand beaches (see Figure 1E) and from bottom sediment and /or vegetation in shallow areas of bays protected from the strong wave action typical of open parts of the lake. These samples are kept in the Laboratory of Macroecology and Biogeography of Invertebrates at the St.-Petersburg State University, Russia (LMBI) and the Russian Museum of Biodiversity Hotspots, N. Laverov Federal Center for Integrated Arctic Research, UB RAS, Arkhangelsk, Russia (RMBH).
In August 2023, a series of invertebrate samples was taken from the shallow part of the lake (northern shore) by two scuba divers. Live specimens of Radix sp. were found in two samples: (1) Issyk-Kul Lake off Kosh-Kol settlement [coordinates: 42.4846 N 76.486 E]; depth 2.5 m; substrate—underwater vegetation (thickets of Sparganium, with admixture of other macrophytes) and (2) Issyk-Kul Lake off Cholpon-Ata settlement [coordinates: 42.5906 N 77.082 E]; depth 17.5 m; substrate—stones and vegetation. In addition to living Radix snails, the samples contained numerous empty shells of Pseudocaspia issykkulensis.
The initial taxonomic identification of collected individuals was carried out using Kruglov’s monograph [16]. Our specimens were also compared with the type specimens of R. obliquata and R. subdisjuncta. Shell measurements were taken by means of ocular-micrometer of a binocular microscope with accuracy to 0.1 mm. The measurement scheme of Vinarski [30] was followed. Six measurements were taken: shell height and width, spire height, body whorl height, and height and width of aperture. Whorl number was counted with accuracy to 1/8. These primary variables were then subjected to statistical analysis, including descriptive statistics and PCA (principal component analysis).
We did not have fixed adult specimens of the Issyk-Kul Radix at our disposal. All individuals that could be found in the shallow bays of the lake were juvenile or subadult. The macrostructure of genital organs was, therefore, studied on these immature specimens. The absence of mature snails made it impossible for us to reveal if there are diagnostically significant structures in their genital system. The reproductive anatomy of the Lymnaeidae was thought to serve as a major source of taxonomic and phylogenetic signal in this family [16,31]. However, the recent studies on taxonomy and variation in Radix have shown that anatomy does not provide an effective tool for species delineation in this group; the reproductive anatomy of these snails appears to be almost identical among species whose taxonomic independence was supported molecularly [29,32,33]. Therefore, in this study, we report and illustrate some features of the soft body of studied snails, but do not use them in our phylogenetic and taxonomic conclusions.
For comparative purposes, samples of Radix collected by us in various regions of Eurasia and Africa were used. In particular, we examined, both molecularly and morphologically, samples of Radix natalensis (Krauss, 1848) s. lato (near Entebbe, Uganda: sampling date 07.2018) and R. skutaris Glöer and Pešić, 2008, from Skadar Lake, Montenegro and adjacent waterbodies (sampling date: 08.2021). In August 2018, a sample of Radix was also collected from Albert Lake near Butiaba (Uganda). The materials sampled from Albert and Victoria Lakes are kept in LMBI and RMBH; those from Skadar Lake—in RMBH only.
2.2. DNA Analysis, Sequence Alignment, Phylogenetic Study, and Species Delimitation
In the course of this research, 28 new sequences were generated (Table 1). Total genomic DNA was extracted from 96% ethanol-preserved tissues of collected specimens using the NucleoSpin Tissue Kit (Macherey-Nagel GmbH & Co. KG, Düren, Germany), following the manufacturer’s protocol. In the present study, we used data from the mitochondrial cytochrome c subunit I (COI) gene, 16S ribosomal RNA (16S rRNA) gene, and the nuclear 28S ribosomal RNA (28S rRNA) gene fragment. COI primers were LCO1490 and HCO2198 [34]. For 16S, the primers 16Sar and 16Sbr [35] were used. 28S primers were D23F [36] and D2 [37]. The PCR mix contained approximately 200 ng of total cellular DNA, 10 pmol of each primer, 200 μmol of each dNTP, 2.5 μL of PCR buffer (with 10 × 2 mmol MgCl2), 0.8 units of Taq DNA polymerase (SibEnzyme Ltd., Novosibirsk, Russia), and H2O, which was added up to a final volume of 25 μL. Thermocycling was implemented with markers-specific PCR programs as follows: (I) COI and 16S: 95 °C (4 min), followed by 28–30 cycles of 95 °C (50 s), 50 °C (50 s), 72 °C (50 s), and a final extension at 72 °C (5 min) and (II) 28S: 95 °C (4 min), followed by 30–31 cycles of 95 °C (50 s), 58 °C (50 s), 72 °C (50 s), and a final extension at 72 °C (5 min). Forward and reverse sequencing was performed on an automatic sequencer (ABI PRISM3730, Applied Biosystems, Foster City, CA, USA) using the ABI PRISM BigDye Terminator v.3.1 reagent kit. The resulting sequences were checked using a sequence alignment editor, BioEdit version 7.2.5 [38]. The phylogenetic affinities of the nucleotide sequences of certain specimens were identified using the Basic Local Alignment Search Tool, BLAST [39].
The sequences were aligned using the MUSCLE algorithm of MEGAX [40]. The phylogeographic analyses of Radix auricularia were performed based on a median-joining network approach using Network ver. 4.6.1.3 software with default settings [41]. Two hundred and thirty COI sequences of R. auricularia were obtained from NCBI GenBank in addition to those freshly generated (Table S1 of Supplementary Materials).
For species delimitation procedures, we added five COI haplotype sequences of Radix species from Lake Issyk-Kul and three haplotypes of R. skutaris from Skadar Lake basin to a comprehensive dataset of Aksenova et al. [42], containing 763 COI haplotypes of various Lymnaeidae. A sequence of Aplexa hypnorum (Linnaeus, 1758) (Physidae) was used as an outgroup. The COI haplotype phylogeny was reconstructed using a maximum likelihood approach through an online Web server for IQ-TREE v.1.6.12 (
The maximum likelihood multi-locus phylogeny (three codons of COI + 16S rRNA + 28S rRNA) was also based on the dataset of Aksenova et al. ([42], Table S1 of Supplementary Materials), which contains 123 ingroup haplotypes of 113 lymnaeid species. To this dataset, we added newly generated haplotype-level data for Radix obliquata and R. auricularia from Lake Issyk-Kul, as well as for Radix skutaris, from Lake Skadar basin in Montenegro. Haplotypes of Physella acuta (Draparnaud, 1805) and Sibirenauta elongata (Say, 1821) were used as outgroups. The maximum likelihood multi-locus phylogeny was reconstructed with an online Web server for IQ-TREE v.1.6.12 (
3. Revision of Radix Species in Lake Issyk-Kul
A multi-locus phylogeny obtained during our research has revealed that Lake Issyk-Kul is inhabited by two species of Radix (Figure 3). One of them is identical to the widespread Palearctic species R. auricularia (Linnaeus, 1758). The other one belongs to an apparently endemic clade, which can properly be named Radix obliquata sensu lato (using the only available taxonomic name established for a Radix species with the type locality situated in Issyk-Kul). The results of a COI-based species delimitation procedure (Figure S1 in Supplementary Materials) are in good agreement with the multi-locus phylogentic analysis.
The presence of R. auricularia in Issyk-Kul is not surprising. This snail is ecologically plastic and able to colonize very diverse waterbodies, varying from deep ancient lakes (e.g., Lake Baikal) to the smallest thermal pools and ponds [49,50,51]. R. auricularia is very common in Central Asia and could have penetrated the lake from adjacent waterbodies. It is not known how long this snail has lived in Issyk-Kul Lake, and it is not improbable that it has only recently colonized the waterbody (as is the case with R. auricularia in Lake Baikal [50]). However, the presence of two, rather distant, haplotypes of R. auricularia in the lake suggests that there could be at least two events of invasion of Issyk-Kul by this snail, and that the sources of invasion were geographically distinct. One of the haplotypes (AUR1) is identical to those found in Northern Siberia (widely distributed from the Novosibirsk Region in the west to Transbaikalia in the east) and in Northeastern Europe (Figure 4). Haplotype AUR2 forms a sister lineage to a haplotype found in Tibet (GenBank No. MH189863). In turn, there is a sample from Xinjiang (Western China) that is a sister lineage to the clade (AUR2 + MH189863). Thus, the second haplotype of R. auricularia from Issyk-Kul has a clear Central Asian ancestry.
The species R. obliquata in the studied sample was represented by three haplotypes, which, given the limited size of the sample, indicates a notable genetic diversity. One of these haplotypes (OBL2) is markedly different from the other two (distance 1.2–1.4%, according to COI). There are two explanations for this fact. First is that the haplotype divergence is a product of a more or less prominent intralacustrine radiation (comparable with that of Radix in the ancient Lake Lugu, Yunnan, China [52]). Alternatively, R. obliquata may present as not truly endemic to Issyk-Kul but, instead, as a certain Central Asian species of Radix, still underrepresented in GenBank. If true, this would explain the high genetic diversity by the hypothesis of its double (at least) introduction into Lake Issyk-Kul. However, the deficiency of Radix sequences from China, Tajikistan, Afghanistan, and other Central Asian countries located close to Issyk-Kul makes this assumption unverifiable.
The question of the taxonomic identity of the two Radix species reported in Issyk-Kul Lake by Kruglov and Starobogatov [15,16] needs special consideration. Specimens of Radix found in the samples of the Issyk-Kul molluscs examined by us belonged to three morphospecies (Figure 5A–C,H–J), corresponding to the species Radix obliquata and R. subdisjuncta sensu Kruglov and Starobogatov and Radix auricularia [15,16]. Unfortunately, the living specimens of Radix used in the molecular analysis were not full-grown (Figure 6), and, potentially, may belong to either of the two species.
Conchologically, Radix obliquata and R. subdisjuncta sensu Kruglov and Starobogatov [15] can be distinguished from each other by different shell size and shape (see Figure 5; Table S2 in Supplementary Materials for this article). A PCA analysis has revealed that these entities form two very closely situated but nonetheless distinct “clouds” in the space of the first two PCs (Figure 7). However, one can note that the separation between these clouds is chiefly along the first PC, which is the “size component”, explaining 98.18% of the total variance (see Table S3 in Supplementary Materials). Most linear measurements, except for spire height, correlate with it. In simple terms, this means that the two groups are separated by their absolute size and, thus, may represent two age cohorts of a single species. Indeed, the trend lines approximating linear shell growth in these two groups are similar, albeit not identical (Figure 8), indicating a slight dissimilarity in the parameters determining linear shell growth in ontogeny. There is, nonetheless, an alternative explanation, which considers these morphospecies as ecotypes (or ecological “races”) of the same species: R. obliquata, with its broadly auriculate shell and enlarged aperture, may inhabit deeper part of the lake (according to Pavlova [53], this mollusc occurs at depths up to 60 m), whereas R. subdisjuncta is a morph adapted to relatively shallow habitats. It is characterized by a slender and relatively small shell with a high spire and a moderately or weakly inflated body whorl. However, this assumption should be checked by direct observation of snails inhabiting different depth zones of the lake. Unfortunately, during diving into Issyk-Kul Lake, to depths of 2.5–17.5 m, only small-sized specimens of Radix were found (see Figure 6).
Typical specimens of Radix obliquata, with greatly enlarged aperture and short spire, have never been found alive and, thus, neither anatomical nor molecular data on them are available. Though there still remains a possibility that R. subdisjuncta sensu Kruglov and Starobogatov is a species distinct from R. obliquata, the available data are not enough to support such a decision. Although the mean values of all studied shell parameters differ markedly between R. obliquata and R. subdisjuncta, we were unable to find a hiatus in the distribution of any of these quantitative variables (see Table S2 in Supplementary Materials).
Specimens of Radix from Issyk-Kul Lake that were analysed by us have small shells (up to 10 mm in height) with a high spire and a moderately enlarged body whorl (Figure 6A–E), are relatively thick-walled, and are light brown coloured. The shell surface sculpture has thin axial growth lines. The whorl number is 3.5–4.0. The whorls are very weakly convex and are separated by a shallow suture. The aperture is drop-shaped or ovoid, with an evenly rounded basal margin.
The mantle is light grey with black spots (see Figure 6A–D) or black with grey spots (Figure 6E) and “freckles” on the back of the head. There is a slight difference between R. auricularia and R. obliquata in the colour pattern of their soft body. Specimens of the former species from Issyk-Kul Lake have dark pigmentation with numerous small spots of white colour (see Figure 6F,G). R. obliquata snails demonstrate an opposite pattern—light background with black spots (see Figure 6A–D). However, we have only a limited number of specimens at our disposal and, thus, it remains unknown whether this difference is stable and can serve as a diagnostic feature.
The morphology of the copulatory apparatus of R. obliquata is typical of the genus Radix (see Figure 6A–E). The apparatus consists of tubular praeputium and a very thin and narrow penis sheath (see Figure 6E). The praeputium is oblong, light grey with black dots, and its width is almost the same along the entire length. The penis sheath is much narrower, and its distal end is somewhat swollen. The praeputium length is slightly shorter or equal to the length of the penis sheath, which is characteristic of many other species of this genus [29]. The spermathecal duct is long.
Conchologically, shells of R. subdisjuncta sensu Kruglov and Starobogatov [15] found in Issyk-Kul Lake are different from the paratypes of Limnaea lagotis var. subdisjuncta (compare Figure 2, lower row, and Figure 5H–J). The type locality of the latter lies far from Kyrgyzstan, and its identity is still unresolved due to the lack of molecular data on snails collected in Northern India. Most probably, it represents a junior synonym of Ampullaceana lagotis (Schrank, 1803), a lymnaeid species common to Central Asia [29,32]. The application of the taxonomic name Lymnaea lagotis var. subdisjuncta to a conchologically dissimilar morphospecies found in Lake Issyk-Kul is, in our opinion, untenable, especially since Kruglov and Starobogatov [15,16,22] did not have the opportunity to study the type series of this taxon. The identification of shells from former Soviet Central Asia with the species described from Kashmir was made by them on the basis of superficial similarities in the shape and proportions of the shells.
Radix obliquata, in terms of its true range and biogeographic affinities, poses a more complicated problem. Shells of lymnaeids with similar shape and proportions are known from various parts of Central Asia, which has led to a conclusion that the range of R. obliquata is not restricted to Lake Issyk-Kul. For example, Yen [26] reported this snail in Tibet. In different museums, we found shells of snails identified as R. obliquata that originated from such diverse regions as the Republic of Tuva (Eastern Siberia, Russia), Western Mongolia, Tibet, Uzbekistan (the environs of Tashkent), and the former Lob-Nor Lake in Western China. Their conchological traits overlap, and the measured shells formed a continuous “cloud” of points on the PC1–PC2 axes (Figure S3 in Supplementary Materials). However, it would be premature to follow Kruglov and Starobogatov ([15], p. 88) and to outline the range of R. obliquata as stretched throughout “desert and semidesert regions of Central Asia, to Inner Mongolia in the east”. Previously, we molecularly studied many dozens of Radix spp. from different regions of Northern and Central Asia, including Tibet, Tajikistan, and Xinjiang [32,33,42,49,51,54]. No sequences identical to those found in Lake Issyk-Kul were discovered. Thus, the most cautious assumption we can make now is that R. obliquata is endemic to Issyk-Kul Lake. Shells of Radix from Tuva and other regions of Central Asia, which have external similarity to R. obliquata (see Figure 5D–G), are, most probably, not conspecific with the latter. This similarity could have arisen as a product of convergent processes, which are observed among lymnaeids [51] and other groups of freshwater and terrestrial pulmonates [55,56,57]. To claim the conspecificity between snails of Lake Issyk-Kul and Tuva (or Western Mongolia) would suggest numerous instances of their long-distance dispersal, with no living populations located between lakes separated by hundreds and thousands of kilometres. As long as we do not have genetic data on snails inhabiting Western Mongolia, Tuva, or the Lob-Nor Lake region, it would be imprudent to claim that R. obliquata inhabits anywhere outside Issyk-Kul. For example, the molecular data currently available [33,58,59] indicate that literary records of this species from the Tibetan Plateau should be rejected as being based on misidentifications.
Although, unlike lakes Baikal or Tanganyika, Issyk-Kul is not home to dozens or hundreds of endemic species, some groups of invertebrates have species endemic to this basin. Endemic species are known among monogeneans, nematodes, and rotifers of Lake Issyk-Kul [3,60,61,62,63] as well as among some other invertebrates. A few species of endemic fish are also known [64]. However, the degree of endemism varies greatly among groups. For example, the fauna of Rotifera, as of 1996, contained 94 species, but only one of them, Lecane brodskii Muraveiskiy, 1937, was considered endemic to this lake [62]. The bulk of the fauna is formed by cosmopolitan species, which can be explained by the ease of long-distance passive dispersal of these animals [65,66,67]. Out of 70 species of free-living Nematoda, registered in Issyk-Kul Lake by 1989, 11 (or 15.7%) were considered endemics [61]. No unique species is known among Issyk-Kul aquatic beetles (A. Prokin, pers. comm.), crustaceans [68,69], and water mites [70].
Compared to other groups of invertebrates, molluscs of Issyk-Kul Lake do not demonstrate a high level of endemism. However, as it was noted above, an integrative revision of the nominal species of snails and clams described is needed to know the true magnitude of their diversity. This is applicable to many other taxa of Issyk-Kul animals, since most presumed endemic species were described based on morphology only. DNA taxonomy has revealed that in groups, such as Rotifera [67], cryptic speciation and hidden diversity are quite common phenomena, and all biogeographical conclusions and estimates of species richness made using a morphological approach can be questioned.
It would be interesting to compare the results of our revision of the Issyk-Kul Radix with the data on Radix diversity in other ancient lakes of tectonic origin across the world.
4. Radix Species in Deep Ancient Lakes
There is a group of large permanent waterbodies, scattered throughout the world, which are called “ancient lakes” or “deep ancient lakes” [71]. Another, similar category, is dubbed simply “large lakes” [72,73], and several lakes included in this are also considered to be “ancient lakes”. There is no commonly accepted definition for both groupings; for example, “ancient” lakes may be defined as either basins older than 1 myr [74] or, alternatively, as “those that contain sedimentary records that span timescales since at least the last interglacial (c. 128 ka before present (BP))” ([75], p. 209). Other important characteristics of the ancient lakes is that most of them are “oligotrophic and situated in active tectonic graben settings or impact craters with low sediment supply from the catchment” [74]. The low sediment supply prevents them for being filled with external matter and consequently vanish [76].
We do not aim to discuss here the question of lake classification but rather to analyse a group of lakes that were conditionally selected as having a set of features: (1) ancient age (pre-mid-Pleistocene); (2) Tectonic origin; and (3) considerable depth. The last feature was not followed very strictly, and a few relatively shallow lakes were included for consideration. This decision was based on the previous literature, where these basins were discussed from a malacologist’s point of view. For instance, Lake Inle of Myanmar is rather shallow, but Boss [71] included it in his review of freshwater molluscs of ancient lakes. Also, Skadar Lake is shallow, with an average depth of 5 m and a maximum depth of 8.3 m [77]; the lake itself cannot be termed as an ancient lake, but its basin and hydrological network with a large system of karst springs are definitely ancient, originated from more than 2.5 Ma [78]. On the other hand, the Caspian Sea, which is sometimes included in the group of large lakes [74], has been omitted from our review since this is a brackish-water basin, being a remnant of the Paratethys sea-lake of the Neogene epoch. The history of the Caspian Sea malacofauna (reviewed in [79]) is very peculiar and differs from the history of malacofaunas of other ancient lakes. In total, we collected information on 26 lakes (Table 2). Our list of basins is by no means exhaustive and could be extended, for example, to include Lake El’gygytgyn in Chukotka, Russia, or Lake Tovuti in Indonesia, which are included by some authors (e.g., [74]) in their reviews of ancient lakes.
According to Boss, “distinguished by unique faunas and floras, usually with high degrees of endemism, these lakes differ from other fresh waters in their age” ([71], p. 385). The uniqueness of the biota of these lakes has attracted researchers since the mid-19th century. In the second half of the last century, some review works, especially devoted to large lakes and their malacofauna, were published [71,77,78,90]. The considerable geological age of such basins, which have numerous ecological niches and biotopes of various sorts, makes them “natural laboratories”, where large-scale evolutionary processes can be observed [91,92]. Classical examples of intralacustrine radiations are the amphipods of Lake Baikal, cichlid fishes, and the so-called “thalassoid” snails of Tanganyika and some other lakes in Central Africa [85,93,94,95].
It is known that the lymnaeid snails, unlike some other families of freshwater gastropods (Acroloxidae, Baicaliidae, Planorbidae, Thiaridae, etc.), provide almost no examples of extensive diversification in ancient lakes [70,96,97,98,99]. However, the genus Radix seems to represent an exception to this pattern since its representatives are more or less common in lacustrine basins of relatively old age and tectonic origin [97].
We divided the lakes included in our analysis into four groups.
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Those situated outside the native range of the genus Radix. This genus is of old-world origin [32] and is distributed almost exclusively in Africa and Eurasia (known also in Alaska [99]). Among these lakes, three lie in the Americas (Tahoe, Titicaca, and Thule), and a single one, Eyre, in Australia. Potentially, non-native species of Radix can penetrate them, as is the case with Palearctic R. auricularia in the Great Lakes of North America [100].
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Old-world lakes with no data on their malacofauna. We were unable to find recent information about Radix in two large lakes in Africa, Mweru and Turkana. However, it is quite possible that the species Radix natalensis inhabits them (see below).
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Lakes having no endemic species of Radix. This group of lakes is the largest. It includes such basin as Baikal, Tanganyika, Victoria, Lanao, and some others (see below).
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Lakes with endemic representatives of the genus Radix in their fauna. In addition to Lake Issyk-Kul, such lakes as Lugu, Skadar, Yangzong, and Zaisan fall to this category.
Below, some lakes will be discussed separately (in alphabetic order).
African deep lakes (Albert, Edward, Kivu, Malawi, Tanganyika, and Victoria), which form a group of basins associated with the Central African Rift sub-system. In all the abovementioned lakes, only one species of Radix, R. natalensis sensu lato, is represented (see Table 2). According to our observations, recorded in 2018 at lakes Albert and Victoria, these snails are restricted to the shallow zone of the lakes, being found on submerged stones, vegetation, and also in small waterbodies situated on the lakes’ shores and periodically connected with them. Our results show, however, that R. natalensis represents a species complex, with at least three distinct subgroups, which are conditionally ranked here as subspecies. Lake Victoria is inhabited by the subspecies R. natalensis debaizei (Bourguignat, 1887), whereas another subspecies, R. natalensis exsertus (von Martens, 1866), has been identified in a sample from Albert Lake (see Figure 6J).
The taxonomic identity of R. natalensis from other lakes in Central Africa remains unclear. Most probably, R. natalensis sensu lato lives in the shallow zone of lakes Mweru and Turkana, but we lack evidence for this in the accessible literature.
Baikal Lake. Formerly, it was thought that this lake is inhabited by three species of Radix: R. auricularia, R. intercisa (Lindholm, 1909), and R. psilia, Bourguinat, 1862 [101]. A recent ”integrative” revision [48] has revealed, however, that all Radix populations in Lake Baikal belong to R. auricularia, which probably penetrated the waterbody several times from different sources. R. auricularia still lives in Baikal, but only at shallow depths (up to 30 m), but its expansion into deeper parts of the lake is not excluded, which may have serious consequences for the aboriginal malacofauna, with there being dozens of endemic species of Gastropoda [48].
Biwa Lake. This basin has its own endemic species of Radix—R. onychia (Westerlund, 1883). According to our results, this is the most phylogenetically isolated species of Radix in ancient lakes (see Figure 3). Perhaps, the absolute age of this species is comparable with that of some endemic fish of Lake Biwa. According to Tabata et al. ([102], p. 2601), some of the endemic fish species “diverged from their closest relatives earlier (1.3–13.0 Ma) than the period in which the present environmental characteristics of the lake started to develop (ca. 0.4 Ma)”.
Hövsgöl Lake. Sitnikova et al. [83] reported two species of Radix in this lake: R. auricularia and R. mongolica (Yen, 1939). The latter one is rather problematic and has never been subjected to molecular analysis. Its range covers Mongolia, northern China (Inner Mongolia), and the Russian Far East [15,16]. Though some malacologists accept it as a distinct species [15,16,103,104], it is absent from the most recent surveys of Central Asian and Far Eastern lymnaeids, based on the “integrative” approach [32,42].
Inle Lake. The data on the malacofauna of this lake are chiefly from the last century [28,105,106]. A single species of Radix, R. mimetica (Annandale, 1918), has been reported in Lake Inle. This is a synonym of Radix (Exsertiana) rufescens (J. E. Gray, 1822), which is common in South Asia, including Myanmar [24].
Lanao Lake. Stelbrink et al. [107] published a detailed survey of the malacofauna of this Indonesian lake. In their list, a species of Radix, whose species identity was not determined, has been included. Having compared sequences of these snails with those of our sequence library, we found that Lake Lanao is inhabited by R. rubiginosa (Michelin, 1831), a species widely distributed in Indonesia and some other countries of South-East Asia.
Lugu Lake, situated in Yunnan Province, China, represents the most intriguing case, since a small species flock of endemic Radix was found to have evolved in it [52]. Regrettably, the four Radix species identified in Lugu by means of the molecular taxonomic approach have not been formally described, and, thus, form part of the “grey names” group (sensu Minelli [108]), i.e., names non-compliant with ICZN rules. To date, this is the most intensive evolutionary radiation in a lake to be reported for Radix snails (the paleontological literature may provide other cases of such kind (e.g., [109]), but we are not sure that all fossil species classified in the genus Radix actually belong to this taxon).
Ohrid and Prespa Lakes, are two “sister lakes” in the Balkans. Albrecht et al. [86] listed two species of Radix: R. relicta (Poliński, 1929), endemic to Ohrid, and R. pinteri, Schütt, 1974, which is unique to Lake Prespa. R. auricularia was mentioned in this paper as living in Prespa. According to current taxonomy of the Lymnaeidae, both R. relicta and R. pinteri are not members of the genus Radix. Aksenova et al. [32] classified them as belonging to the genus Ampullaceana, Servain, 1882.
Skadar Lake. In 2008, an endemic species, Radix skutaris, was described for this lake [110]. The original description was exclusively based on morphological data, and lately Glöer ([111], p. 246) acknowledged that R. skutaris is “genetically conspecific with R. auricularia but there are morphological arguments enough for the distinction of this species”. Our results demonstrate that Radix skutaris is not only not genetically identical to R. auricularia but forms a phylogenetically distant clade close to the group of Central Asian members of the genus—R. alticola (Izzatullaev and Kruglov and Starobogatov, 1983) and R. euphratica (Mousson, 1874).
Trichonis Lake. Having analysed a large library of sequences of various species of Radix, Aksenova et al. [32] found that this lake maintains a separate, but still undescribed, species of the genus Radix. We do not have material on this snail at our disposal and, thus, are unable to describe it as a new species.
Yangzong Lake. This lake, situated in Yunnan Province, China, is inhabited by two undescribed species of Radix revealed by our phylogenetic and species delimitation analyses. Together with four undescribed species from Lugu Lake, they form what can be called “Yunnan lakes’ species flock” (see Figure 3). Its structure, species composition, and the relationships between its constituent species need special study.
Zaisan Lake. Vinarski [89] discussed the status of Radix gebleri (Middendorff, 1850), a species thought to be endemic to Zaisan Lake (East Kazakhstan). Unfortunately, in the 1960s, a dam was built on the Upper Irtysh River, which drastically transformed the ecosystem of Zaisan Lake and its hydrological regime [3]. Since 1965, no new findings of R. gebleri have been made. In July 2018, one of the authors (MVV) undertook a special trip to Zaisan Lake in the hope of collecting living specimens of R. gebleri. That attempt failed, and neither living individuals nor empty shells of the snails were found. However, the presence of R. auricularia in the shallow zone of Zaisan Lake was observed (M. Vinarski, unpublished data). Perhaps, R. gebleri has disappeared in the waterbody following the transformation of its ecosystem. Conchologically, this species is rather similar to another lymnaeid species, Ampullaceana ampla (Hartmann, 1821), and, probably, does not belong to the genus Radix.
5. Conclusions
-
Issyk-Kul Lake is inhabited by two genetically distinct species of the genus Radix: R. auricularia, which is broadly distributed throughout Palearctic, and the presumably endemic R. obliquata.
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Within the Lymnaeidae, Radix is the only genus whose members are widely represented in malacofaunas of ancient tectonic lakes, and several endemic species have evolved within Radix in these lakes (in Europe, Central, and East Asia).
-
A list of endemic Radix of ancient tectonic lakes includes Radix obliquata, R. onychia, and R. skutaris, as well as four undescribed species from Lake Lugu and two species from Lake Yangzong (both lakes are in Yunnan Province, China). Both the taxonomic identity and current status of R. gebleri of Zaisan Lake remain obscure.
Conceptualization, M.V.V., I.N.B. and O.V.A.; methodology, I.N.B., A.V.K., O.V.A. and M.V.V.; software, I.N.B. and M.V.V.; literary survey, M.V.V.; molecular analysis, I.S.K. and A.V.K.; statistical analysis, I.N.B., A.V.K. and M.V.V.; morphological study, M.V.V. and O.V.A.; fieldwork, M.V.V., V.M.S., V.R.A., A.V.K. and V.P.; species identification and shell measurements, O.V.A. and M.V.V.; writing—original draft preparation, M.V.V.; writing—review and editing, all authors; visualization, A.V.K., I.N.B., O.V.A., and M.V.V.; supervision, I.N.B. and M.V.V.; and project administration, M.V.V. All authors have read and agreed to the published version of the manuscript.
Not applicable.
The primary materials (gastropod samples) for this study are placed in some public repositories (ZIN, IPAE, RMBH, and LMBI). The new sequences, obtained during this research, have been made available through GenBank. Original data, used and collected during this research, are available (with reservations) upon request from the authors.
Our gratitude is due to colleagues, who helped us to find references to papers on invertebrates of Issyk-Kul other than molluscs: Vladimir Gussakov and Alexander Prokin (Borok settlement), Alexander Makhrov (Moscow), and Andrey Przhiboro (St.-Petersburg). We have to thank our Russian colleagues, who accompanied us during fieldwork in Kyrgyzstan, Kazakhstan, Uganda, and Montenegro: Maxim Grebennikov (Yekaterinburg), Artyom Lyubas, Ilya Vikhrev and Mikhail Gofarov (Arkhangelsk), Boris Filippov and Dmitry Palatov (Moscow), and Anna Evseeva (Khanty-Mansiysk). We thank curators of malacological collections examined during our research—Johnatan Ablett (NHMUK, London), Ronald Jannsen (SMF), Maxim Grebennikov (IPAE), Alexander Sysoyev (ZMMU), Pavel Kijashko (ZIN), Tom Schiøtte (ZMUC), and Christine Zorn (ZMB). Special thanks to scuba swimmers Rostislav Alekseev (St. Petersburg) and Peter Ilchishin (Cholpon-Ata, Kyrgyzstan) for sample collection in Issyk-Kul Lake. Comments and recommendations from two anonymous reviewers helped us improve the original version of this paper.
The authors declare no conflicts of interests.
Footnotes
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Enlarge this image.Figure 1. (A–D). Views of the northern shore of Lake Issyk-Kul and (E) lake deposits on a beach in Cholpon-Ata settlement. Empty shells of Pseudocaspia issykkulensis and juvenile Radix sp. are seen; (F) shallow zone of a bay of the Issyk-Kul Lake in Cholpon-Ata—a habitat of Radix sp. Photos by M. Vinarski.
Enlarge this image.Figure 2. Upper row—syntypes of R. obliquata and their labels, ZMB (accession No. 7164). Lower row—three paratypes of R. subdisjuncta with their labels, NHMUK (accession number 1824). Scale bars—2 mm (R. subdisjuncta) and 5 mm (R. obliquata). Photos by Maxim Vinarski.
Enlarge this image.Figure 3. Maximum likelihood consensus multi-locus phylogeny of the genus Radix (three codons of COI + 16S rRNA + 28S rRNA) reconstructed through IQ-TREE v.1.6.12. Black numbers near nodes are ultrafast bootstrap support values. Labels of haplotypes from Lake Issyk-Kul are red. Labels of haplotypes from other ancient lakes are blue. This tree is a fragment of a global phylogeny of the family Lymnaeidae (non-target clades and outgroup are omitted). The scale bar indicates the branch lengths (substitutions per site).
Enlarge this image.Figure 4. Median joining network of the COI sequences of Radix auricularia. Circle symbols represent different haplotypes, with the size reflecting their frequency (smallest = 1). Numbers near branches are numbers of nucleotide substitutions per site. The dataset contains 234 COI sequences (length = 572 bp).
Enlarge this image.Figure 5. Shells of Radix obliquata (A–G) and R. subdisjuncta sensu Kruglov and Starobogatov (H–J) from various localities of Central Asia. (A–C) Issyk-Kul Lake, Cholpon-Ata, 07.2013 (LMBI, accession No. 15-2535); (D,E) Russia, Republic of Tuva, Terekhol Lake, 07.1980 (IPAE, accession No. 130); (F) Mongolia, east of Ubsunur Lake, 06.1978 (ZIN, accession No. 23); (G) China, Inner Mongolia, Alashan Desert, Djaratay-dabasun (ZMUC, accession No. unknown); (H) Issyk-Kul Lake, Kutarga settlement, 07.1979 (ZIN, uncatalogued); and (I,J) Issyk-Kul Lake, Cholpon-Ata, 07.2013 (LMBI, accession No. 15-2536). Scale bars 5 mm. Photos by Maxim Vinarski.
Enlarge this image.Figure 6. Shells, mantle pigmentation, and anatomy of the Radix species discussed in this study. (A) Radix obliquata, Issyk-Kul Lake (RMBH, accession No. MLym-984); (B) R. obliquata, Issyk-Kul Lake (RMBH, accession No. MLym-984/2); (C) R. obliquata, Issyk-Kul Lake (RMBH, accession No. MLym-984/3; (D) R. obliquata, Issyk-Kul Lake (RMBH, accession No. MLym-1336/2); (E) R. obliquata, Issyk-Kul Lake (RMBH, accession No. MLym-1348/4); (F) R. auricularia, Issyk-Kul Lake, (RMBH, accession No. MLym-985/1); (G) R. auricularia, Issyk-Kul Lake, (RMBH, accession No. MLym-985); (H) R. skutaris from Sitnica River, Skadar Lake basin, Montenegro (RMBH, accession No. MLym-1220/1); (I) R. skutaris from Crnojevića River, Skadar Lake basin, Montenegro (RMBH, accession No. MLym-1226/2); (J) R. natalensis exsertus from Albert Lake, Uganda (RMBH, accession No. MLym-743/3); and (K) R. natalensis debaizei, Lake Victoria, Uganda (RMBH, accession No. MLym-739/1). Scale bars 1 mm. Photos by Olga Aksenova.
Enlarge this image.Figure 7. Principal component analysis of whorl number and shell measurements of two nominal species of Radix of Lake Issyk-Kul. The first three principal components (PC) combined account for 99.72% of variance (PC1 98.18%, PC2 1.06%, and PC3 0.48%).
Enlarge this image.Figure 8. A scatterplot of shell width vs. shell height in two nominal species of Radix of Lake Issyk-Kul.
New DNA sequences generated from Radix specimens from Kyrgyzstan and Montenegro, with their GenBank numbers. N/A—not available.
| Species | Voucher No. | Locality, Coordinates | COI Haplotype | COI acc. No. | 16S rRNA acc. No. | 28S rRNA acc. No. |
|---|---|---|---|---|---|---|
| R. auricularia | RMBH MLym985/1/1 | Issyk-Kul Lake, 42.706389, 77.686389 | AUR1 | PQ771848 | N/A | N/A |
| R. auricularia | RMBH MLym985/1/2 | Issyk-Kul Lake, 42.706389, 77.686389 | AUR1 | PQ771849 | N/A | N/A |
| R. auricularia | RMBH MLym985/2 | Issyk-Kul Lake, 42.706389, 77.686389 | AUR2 | PQ771850 | N/A | N/A |
| R. obliquata | RMBH MLym985/3 | Issyk-Kul Lake, 42.706389, 77.686389 | AUR2 | PQ771851 | N/A | N/A |
| R. obliquata | RMBH MLym984/1/1 | Issyk-Kul Lake, 42.646944, 77.098056 | OBL1 | PQ771843 | PQ772053 | PQ772069 |
| R. obliquata | RMBH MLym984/1/2 | Issyk-Kul Lake, 42.646944, 77.098056 | OBL1 | PQ771844 | PQ772054 | PQ772070 |
| R. obliquata | RMBH MLym984/2 | Issyk-Kul Lake, 42.646944, 77.098056 | OBL2 | PQ771845 | PQ772055 | PQ772071 |
| R. obliquata | RMBH MLym984/3 | Issyk-Kul Lake 42.646944, 77.098056 | OBL3 | PQ771846 | PQ772056 | PQ772072 |
| R. obliquata | RMBH MLym984/4 | Issyk-Kul Lake 42.646944, 77.098056 | OBL3 | PQ771847 | PQ772057 | PQ772073 |
| R. skutaris | RMBH MLym1220/1 | Montenegro: Sitnica River, 42.46081, 19.176929 | SKU1 | PQ771852 | PQ772058 | PQ772074 |
| R. skutaris | RMBH MLym1226/1 | Montenegro: Crnojevića River, 42.355589, 19.022553 | SKU2 | PQ771853 | PQ772059 | PQ772075 |
| R. skutaris | RMBH MLym1226/2 | Montenegro: Crnojevića River, 42.355589, 19.022553 | SKU3 | PQ771854 | PQ772060 | PQ772076 |
A summary of diversity of the genus Radix in ancient tectonic lakes (with basic morphometric data on the lakes *).
| Lake Name | Country | Surface Area, km2 | Volume, km3 | Elevation, m a.s.l. | Depth, m | Species of Radix | Source | |
|---|---|---|---|---|---|---|---|---|
| Mean | Maximum | |||||||
| Albert | Congo (DRC)/Uganda | 5300 | 280 | 619 | 25 | 58 | R. natalensis exsertus | ([ |
| Baikal | Russia | 31,500 | 23,000 | 456 | 680 | 1741 | R. auricularia | [ |
| Balkhash | Kazakhstan | 18,200 | 106 | 340 | 5.8 | 26.5 | R. auricularia | [ |
| Biwa | Japan | 674 | 27.5 | 87 | 41 | 103 | R. onychia | [ |
| Edward | Congo (DRC)/Uganda | 2150 | 78 | 912 | 34 | 117 | R. natalensis | [ |
| Eyre | Australia | 7690 | 30.1 | −12 | ? | 3.1 | No | This study |
| Hövsgöl (Khubsugul) | Mongolia | 2620 | 480 | 1624 | 246 | 480 | R. auricularia | [ |
| Inlé | Myanmar | 116 | Fluctuating | 880 | 2.1 | 3.7 | R. rufescens | This study |
| Issyk-Kul | Kyrgyzstan | 6236 | 1738 | 1606 | 278 | 668 | R. auricularia | This study |
| Kivu | Congo (DRC)/Rwanda | 2220 | 333 | 1460 | 240 | 480 | R. natalensis | [ |
| Lanao | Philippines | 375 | 21.28 | 700 | 60.3 | 112 | R. rubiginosa | This study |
| Lugu | China | 48.5 | 1.953 | 2685 | 40.3 | 105.3 | Four, still undescribed species | [ |
| Malawi | Malawi/Mozambique/Tanzania | 29,600 | 8400 | 475 | 292 | 706 | R. natalensis | [ |
| Mweru | Congo (DRC)/Zambia | 5120 | 32 | 922 | 7.5 | 27 | Unknown (no data) | |
| Ohrid | Albania/Macedonia | 358 | 53.63 | 693 | 155 | 288 | No | This study |
| Prespa | Albania/Greece/Macedonia | 259 | 55.5 | 849 | 14 | 48 | R. auricularia | [ |
| Skadar (Shkodra) | Albania/Montenegro | 372 | 1.93 | 5 | 5 | 8.3 | R. skutaris | This study |
| Tahoe | USA | 499 | 156 | 1899 | 249 | 501 | No | This study |
| Tanganyika | Burundi/Congo (DRC)/Tanzania/Zambia | 32,000 | 17,827 | 774 | 572 | 1471 | R. natalensis | [ |
| Titicaca | Bolivia/Peru | 8030 | 903 | 3809 | 107 | 304 | No | [ |
| Trichonida (Trichonis) | Greece | 98.6 | 2868 | 15 | ~10 | 58 | Radix sp. (still undescribed) | This study |
| Tule | USA | 53 | 40 | 1230 | 1.22 | ? | No | This study |
| Turkana | Ethiopia/Kenya | 6750 | 203.6 | 427 | 30.2 | 73 | Unknown (no data) | This study |
| Victoria | Kenya/Tanzania/Uganda | 62,940 | 2518 | 1134 | 40 | 85 | R. natalensis debaizei | This study |
| Yangzong | China | 32 | 0.617 | 1777 | 19.5 | 30 | Two undescribed species | This study |
| Zaisan | Kazakhstan | 5510 | 53 | 386 | 5 | 10 | R. auricularia | ([ |
* The morphometric data are taken mostly from Herdenford [
Supplementary Materials
The following supporting information can be downloaded at:
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Details
; Aksenova, Olga V 2
; Khrebtova, Irina S 2 ; Kondakov, Alexander V 2
; Spitsyn, Vitaly M 2 ; Alekseev, Victor R 3
; Pešić, Vladimir 4
; Bolotov, Ivan N 2
1 Laboratory of Macroecology & Biogeography of Invertebrates, St.-Petersburg State University, 7/9 Universitetskaya Emb., 199034 St. Petersburg, Russia; Laboratory of Systematics and Ecology of Invertebrates, Omsk State Pedagogical University, 14 Tukhachevskogo Emb., 644099 Omsk, Russia
2 N. Laverov Federal Center for Integrated Arctic Research of the Ural Branch, Russian Academy of Sciences, 20 Nikolsky Ave., 163020 Arkhangelsk, Russia;
3 Zoological Institute of the Russian Academy of Sciences, 1 Universitetskaya Emb., 199034 St. Petersburg, Russia;
4 Department of Biology, University of Montenegro, Cetinjski put bb., 81000 Podgorica, Montenegro;