1. Introduction
Free-living microeukaryotes are ubiquitous organisms [1,2,3]. They provide the primary productions of different waterbodies and of the planet in as a whole [4,5,6]. Scaled chrysophytes, Chrysophyceae Pascher, as well as diatoms, participate in the global Si cycle and play an important role in fresh waters. They transform water-dissolved siliceous acid to species-specific silica elements of their shells—scales and spines. At the end of their vegetation, they become dormant, forming siliceous stomatocysts which favor the dispersal of species [7,8]. Scaled chrysophytes are one of the most ancient groups of organisms. The age of stomatocysts preserved in sediments reaches back as far as ca. 100 million years BP [9], with molecular clock analysis predicting that their age maybe close to 330 Ma BP [10]. Some Eocene and Palaeocene chrysophyte species are morphologically similar to existing species [11,12,13,14]. It is evident that knowledge of the autecology of existing species allows for the reconstruction of past environments.
Scaled chrysophytes are thought to be euplanktic organisms mostly inhabiting freshwater ponds and lakes [15]. A significant species diversity of these organisms occurs in large, slow-flowing rivers and small streams [16,17,18]. In general, these organisms are considered to beindicators of pure cold waters, though they have various ecological and trophic preferences [15]. The order Synurales includes strict autotrophs, while representatives of the order Paraphysomonadales, from the genera Chrysosphaerella Lauterborn and Spiniferomonas Takahashi are mixotrophs, and those of the genus Paraphysomonas De Saedeleer are heterotrophs [19,20,21]. Several species of scaled chrysophytes have a limited distribution and show different tolerances to environments [8,15,22,23], allowing some of these species to serve as bioindicators [15]. The majority of scaled chrysophytes refer to widespread and cosmopolitan species [24,25], e.g., representatives of the order Synurales from the most investigated and species-rich genera Synura and Mallomonas occur worldwide [8,26].
There are two hypotheses regarding the dispersal of siliceous scales protists [8]: abiotic (water and wind transfer) [24] and biotic, i.e., dispersal on the hair of animals and the feathers of water fowl [8,24,27,28]. The circumpolar dispersal of scaled chrysophytes in the northern hemisphere could occurat the border of the High Pleistocene–Holocene through a network of ice-dammed lakes and streams [29]. Nowadays, rivers may also play an important role in the dispersal of scaled chrysophytes [8]. Water courses of the northern hemisphere, running into the Arctic ocean, are able to transfer boreal species a thigh arctic latitudes, while global warming creates suitable conditions for their acclimatization there [29]. Large lowland rivers are subject to seasonal water level changes. Spring floods deluge adjacent areas and form new ecotopes, such as shallow still bays, that dry out at the end of summer when the water level falls. In order to reinforce the hypothesis that there are different species compositions of scaled chrysophytes in primary channels and in such short-lived bays, we studied samples collected downstream of the Ob river during high water. We revealed high species richness and showed a sensibility of organisms that have different trophic preferences to various abiotic factors such as turbidity and river flow rate. We consider high water to be one of the mechanisms favoring the enrichment of species diversity and dispersal through river flow in the context of the hypothesis of omnipresence [3].
2. Materials and Methods
2.1. Study Site
The Ob river is one of the largest rivers of Russia; its catchment area is one of the largest in the world [30,31]. It flows through West Siberia rising in the Altai mountains at the confluence of the Biya and Katun rivers [30]. The river feeds mainly from precipitation, more than 50% of which being snow and 20–25% being rain and ground water [31,32]. It provides more than 30% runoff into the Kara sea, impacting water circulation there and, according to some estimates, in the whole Arctic ocean [33,34].
We studied three transects in the low Ob within the Yamalo-Nenets Autonomous Okrug (Figure 1, Table 1).
The Azovy transect (St. A) goes over the Little Ob river. The bottom of the left bank is covered with sand and organic silt; that of the right bank consists of solid sandy deposits. The Kazym-Mys transect (St. K) is located against Kazym-Mys village. The bottom of the right bank is formed by boulders and coarse pebbles intermitting with sand and organic silt in bays; that of the left bank is covered with solid coarse sandy deposits. The Salemal transect (St. C) is situated at the Ob river 8 km upstream from the Salemal village at the narrowing of the riverbed. The bottom of the right bank is covered with medium-sized and coarse pebbles and boulders; that of the left bank is formed by solid silt–clayey deposits with detritus.
2.2. Field and Laboratory Methods
For our study we collected 14 samples over the period 7–13 June 2022 (Figure 1). We applied hydrochemical and hydrometric methods that had been described earlier [35]. Sampling coordinates, data and time as well as hydrochemical parameters of each station are given in Table 1. The maximum depth (Hmax) at each station was undertaken using a Garmin GPS map 420s (Garmin, Lenexa, KS, USA) chartplotter. The chartplotter showed that near-shore sections are 5–8 m deep on average, 50 m from the right bank and 150 m from the left bank there are steep slopes to the main channel, the central flat part of the channel is 24–26 m deep (Table 1). pH and dissolved oxygen (O2) were determined in situ using a WTW 3420 multimeter (Xylem Analytics, Weilheim, Germany). Water flow rate and temperature were measured with a GRS-3 device (NPO Typhoon, Obninsk, Russia). Water transparency (S) was measured with a white Secchi disc 30 cm in diameter.
All phytoplankton samples were processed by standard hydrobiological methods [36]. Samples were collected from water surface at all stations using a 5 L Ruttnertube sampler. For scanning electron microscopy (SEM), 10–12 mL samples were filtered through 13 mm filter with 0.8 µm pores (Whatman Part of GE HealthCare, Chicago, IL, USA). The filter with precipitate was dried at room temperature and then attached to the SEM stub with double tape, coated with gold in an SDC 004 vacuum evaporator (Balzers, Liechtenstein) and examined using a QUANTA 200 SEM (FEI Company; Hillsboro, OR, USA). Before the calculation of diatom cells and the detection of scaled chrysophytes by means of transmission electron microscopy (TEM), samples taken with a water bottle were filtered through 35 mm acetate cellulose membrane filters with 0.85–1.0 µm pores (Vladipor, Vladimir, Russia) using a filtering plant. Precipitate was washed from the filters with 500 µL of water, and 4% formaldehyde solution was added in a 1:10 ratio for fixation. The further processing of sample for TEM analysis was undertaken according to an established protocol [21].
Precipitate meant for the enumeration of diatom cells was washed from the filters with 500 µL of filtered water into 10 mL bottles; the volumes of filtered samples and those of the samples in each bottle were measured for the calculation of the quantity and biomass of phytoplankton. Diatom cells were identified and counted with a light microscope Laboval 4 (Carl Zeiss, Jena, Germany) in a 0.1 mL Nageotte counting chamber. For the estimation of biomass, the volume of cells was calculated using approximations to geometrical shapes. Species with the maximum contribution to abundance and biomass were taken as phytoplankton dominants.
3. Results
3.1. Water Parameters
According to Table 1, water temperature, pH and dissolved oxygen concentrations, both in the flooded areas (stations K4 and A4) and in the main current, varied insignificantly. Only at stations S1–S6 did the cross-section water temperature change within 12.9–14.4 °C, regardless of sampling depth. Samples collected near the surface, e.g., at St. S1 (0.1 m), had lower temperatures than those taken deeper, e.g., at St. S4 (5.4 m) (see Table 1).
Water flow rate at the studied cross-sections varied significantly, e.g., 0.12 (St. K1) to 0.38 m·s−1 (St. S4) in the main channel. In the shallow bay St. K4 and riparian St. A1, the water flow rate was within 0–0.03 m·s−1; however, in one case (riparian St. A4) there was a weak reverse flow (0.1 m·s−1) against the main current.
Visual examinations of SEM filters with collected material show water samples that, regardless of similar Secchi disc transparency (S = 0.35–0.60 m), differed in turbidity, i.e., they had different contents of mineral particles (see Table 1, Figure 2).
Samples collected in the main current contained many clayey particles. Particles at St. K1–K3, A1–A4, S1–S6 consisted of mineral particles approximately 0.5 to 32 µm in size (Figure 2B,C). One station at the Kazym-Mys transect (St. K4) was located at a shallow bay (0.5 m) at the right flooded swampy bank of the river. There was no current, and the sampled water had almost no mineral particles. Only microalgae precipitated on the filters, and mineral particles were rare (Table 1, Figure 2D). At the Azovy transect, the high right bank was flooded insignificantly. One of the right bank stations (A4) was shallow. A sample was taken from sunken willow branches and contained few mineral particles (see Table 1). Silt–sandy beaches at the left bank and around the islands of the Salemal cross-section as well as the rocky shoals of the right bank were under water. Station S1 is located near the Yamburina channel and is influenced with its water. Water transparency at that station is minimal (0.35 m), while the number of mineral particles is high.
3.2. Diversity and Distribution of Chrysophytes
The study area has high species richness of scaled chrysophytes, with a total of 67 species from 5 genera Chrysosphaerella (n = 2), Paraphysomonas (n = 5), Spiniferomonas (n = 10), Mallomonas (n = 32), and Synura (n = 18) identified (Table 2, Figure 3, Figure 4, Figure 5, Figure 6, Figure 7 and Figure 8).
Distributions of scaled chrysophytes at the stations of the Ob mouth had some patterns.
First, the riparian stations showed higher species diversity than those at the main channel. The highest species diversity was observed at the right bank stations K3 (19 species), K4 (54 species), and A4 (31 species) and the left bank station A1 (22 species). Stations K4 and A4 are situated far from the main channel, with samples at those stations collected near the bank at a depth of 0.5 m, without current and with a small number of mineral particles at St. A4 (see Table 1). It is noteworthy that the bottom of St. K4—which had the highest number of species, including intact cells—was covered with silt and that mineral particles in the water were scarce. Among the stations with various species of scaled chrysophytes, we note that St. K3 had an increasing sampling depth (1.4 m) and showed a burst of flow rate of up to 0.19 m·s−1. The species composition at that station was very similar to that of the adjacent St. K4 (Table 2). This may be explained by the transfer of scales downstream, as scaled chrysophytes here occurred as individual scales. Twenty-two species of scaled chrysophytes were found at the left bank station (St. A1) where a current was fine to nonexistent. Species diversity at stations K1, K2, A2, A3, and S2–S6, situated in the main channel, was low varying within 5–13 species. The depth of the river at the Salemal cross-section reaches 16–27 m and the narrowing of the bed increases the flow rate at the surface by up to 0.38 m·s−1 (see Table 1). Stations with a low species diversity or without scaled chrysophytes (St. S1) were found in the center of the river or near deep stony banks with high flow rate and high content of mineral particles (see Table 1). No scaled chrysophytes were identified at St. S1, regardless of its small maximum depth (1.9 m). Nevertheless, a diatom bloom was observed at that station (see Table 1). The station is located near a river branch and is under the influence of its water.
Second, according to the frequency of scales in the samples, species in the main channel are ubiquitous and cosmopolitan Spiniferomonas trioralis, S. bourrellyi, Mallomonas acaroides, M. akrokomos, M. alpina, M. caudata, M. crassisquama, M. crassisquama var. papillosa, M. punctifera, M. tonsurata, Synura americana, S. glabra, S. borealis, S. petersenii, S. spinosa and S. uvella.
Third, the highest diversity of scaled chrysophytes was observed when there was almost no ability to derive silicon from diatoms. Thus, the minimum number and biomass of diatoms was observed at St. K4 (21.6 × 103 cells·L−1 and 0.03 g·m−3, respectively) (see Table 1), while at the same time the number of species at that station was the highest, with 54 species (see Table 2).
The dominant complex of diatoms at the cross-sections included a planktic species Asterionella formosa Hassall and planktic–benthic species Aulacoseira granulata (Ehrenberg) Simonsen and A. distans (Ehrenberg) Simonsen. At the same time, A. granulata occurred at all stations, but in different quantities.
3.3. Rare Species and Species with Specific Morphology
Two rare species—Synura biseriata and S. punctulosa—previously found in boreal waters were identified in the study area. Our investigation provides additional data on their autecology.
S. biseriata (Figure 8K–N). This species was described for the first time in ponds and marshes of the Napaskiak area (Alaska), mainly from submergent Carex and Sphagnum [37], as an undesignated species in June (Figure 15 in [38]). Later, the species was identified in the Rybinsk reservoir in May at a pH = 7.15–7.3, T = 11.2–13 °C [39]. The species may thus be typical for boreal waters. In our study, scales of S. biseriata occurred at T = 14–14.4 °C. The main diagnostic features of the scales coincide with those previously described: scales are oval to oval–triangular, 3.3–3.7 × 2.6–3.1 µm, the spine is cylindrical up to 2.1 µm, and the basal folded edge is 0.63–0.69 µm wide.
S. punctulosa (Figure 7D). This species was described from samples taken in Rybinsk (April, May) and Kama (October) reservoirs at pH = 7.0–7.4, T = 5.0–12.1 °C [39]. Further, the species was found in September in a small lake of the Low Yenissei catchment area at pH = 7.3, T = 4.5 °C, EC25 = 41.5 µS·cm−1 [40], in a pond of Finland [41], as well as in the mouth of the Barguzin river and the delta of the Selenga river in May, June and September at pH = 7.31–8.15, T = 3.2–13.4 °C, EC25 = 144–200 µS·cm−1 [17]. Thus, the species may be typical of northern waters irrespective of the season. In this study, the scales of S. punctulosa occurred at T = 13.1–14.33 °C. The parameters of the diagnostic features of the scales coincide with those described previously: scales are oval, 3.0–3.7 × 1.9–2.2 µm, the spine is cylindrical up to 1.2 µm, and the basal folded edge is 0.23–0.35 µm wide.
The cells of Spiniferomonas bourrellyi (Figure 3A), S. silverensis (Figure 3B) and S. triangularis (Figure 3H) found at station K4 had very long spines atypical for their diagnoses, measuring 16.6, 16.6 and 15.3 µm, respectively.
Some spines of the S. bourrellyi found in the study area had pores (Figure 3L). We had observed such morphological features in spines in Lake Labynkyr (Figure 2I in [21]). Pores on spines are not typical of species of the genus Spiniferomonas [42,43], most often they characterize representatives of Chrysosphaerella [44]. Nonetheless, the found specimens cannot be referred to as the genus Chrysosphaerella as they have lamellar scales of simple structure, with one lacuna. Furthermore, a septum is typical of Chrysosphaerella spines [44] but was absent from the specimens found. The cells may belong to a new species, though only molecular studies can resolve the issue.
3.4. Undetermined Species
We also found scales with a morphology that differed from all species previously described. These might be new species; a description of their scales and spines is given below.
Chrysosphaerella sp. (Figure 3A,B,D). Two types of plate scales were found, including subcircular (2.5–2.9 × 2.2–2.4 µm in diameter) and oval scales (2.9–3.5 × 1.9–2.4 µm). Both types of scales were ornamented with a series of elongated, round ridges, forming a scalloped pattern. Considerably large round ridges differentiate these scales from structures in other known species. Spines have a shaft joining two plates of a bobbin-like structure. Spines are 8–14 µm long. We had previously found lamellar scales with similar morphology at the mouth of the Olenyok river, Yakutia (Figure S1c,d in [18]). Scales were observed at stations A4, S2, and S6, at pH = 7.52–7.87 and T = 12.9–14.3 °C.
Spiniferomonas sp. (Figure 4F,G). Cells are covered with plate and spine scales. Plate scales are elliptical (0.9–1.3 × 0.5–0.7 µm) with a wide thickened margin creating a single central elliptical lacuna. There are up to 16 spine scales per cell. Spines are 2.4–3.2 µm long, slightly curved in the distal part at one-third of their length, triangular in cross section, and comprise three membranes united along a common edge. A median rib tapers to an obtuse apex 0.52–0.74 µm long. In the area of the bend of the spine, margins of two membranes end in an obtuse apex 0.16–0.20 µm long. Spine shafts are anchored on large conical bases 0.7–1.1 µm in diameter and 0.28–0.41 µm high. The combination of lamellar scales with one lacuna and triangular spines with shafts and a conical base distinguishes these cells from known species of the genus Spiniferomonas. Scales were found at St. K4, at T = 14.3 °C.
Paraphysomonas sp. 1 (Figure 3F). The baseplate is round-to-oval, 1.5–1.9 µm in diameter, with a dense rim. Spine is straight, 1.3–2.2 µm long, with an acute tip. Scales were found at St. K4, at T = 14.0 °C.
Paraphysomonas sp. 2 (Figure 3H). The baseplate is round, 1.3–1.7 µm in diameter, without a dense margin. The central part of the baseplate has a looser area. The spine is straight, 4.3–5.2 µm long, with an acute tip. Scales were found at St. A4, at T = 14.3 °C.
Mallomonas sp. (Figure 6E,F). Has a small apical oval scale, 1.0 × 2.5 µm, with a long spine rounded at the end, and is 6.6 µm long. The shield area of the scale is unstructured with pores in some places. The V-rib is acute and without a hood. The distal ends of the V-rib arms curve and become continuous with the anterior submarginal ribs. Anterior flanges are smooth and narrow. The anterior ends of the scales have a structure similar to carina. The posterior flange is smooth. Scales were found at St. K4, at T = 14.0 °C.
Several morphotypes of the Synura petersenii sensu lato species complex were observed. We provide descriptions of morphotypes observed in our samples.
Synura sp. 1 (Figure 8F–H). The body scales are 3.7–4.8 × 1.7–2.5 µm. The Keel is cylindrical, sometimes slightly widened anteriorly, ornamented by pores of different sizes—medium (diameter, 47–70 nm) to very large (diameter, 120–180 nm)— and ends in a prominent acute tip. The baseplate is ornamented by small pores. The foramen pore on the baseplate is circular, 0.38–0.47 µm in diameter. Numerous struts (28–32) extend regularly from the keel to the scale perimeter, sometimes these are interconnected by transverse folds. The rim of the baseplate is broad (up to 0.60 µm wide) and encircles more than half of the perimeter of the scale. Scales were found at stations K4, A3, and S2, at pH = 7.48–7.87 and T = 12.9–14.3 °C.
Synura sp. 2 (Figure 8C,D). The body scales are 3.5–3.9 × 1.7–2.1 µm. A wide cylindrical keel ornamented with medium-sized pores ends in a prominent acute tip. The baseplate is ornamented by small pores. The foramen pore on the baseplate is circular and is0.28–0.34 µm in diameter. Numerous struts (23–26) extend from the base of the keel towards the margin and are sometimes somewhat reduced, without transverse folds. The rim of the baseplate is broad (up to 0.44 µm wide) and encircles more than half of the perimeter of the scale. Scales were found at stations K4, A3, and S2, at pH = 7.77 and T = 14.0–14.15 °C.
3.5. Stomatocysts
Thirty-one various morphotypes of chrysophycean stomatocysts were identified in the study area (Figure 9 and Figure 10). The most various morphotypes of stomatocysts were found in samples collected at riparian stations K4 and St. A4, with 20 and 7 morphotypes respectively. Five morphotypes were found at St. K3. At stations K1, K2, A1–A3, and S1–S6 of the main channel, stomatocysts were rare, and only one-to-three morphotypes were observed.
As a rule, widespread morphotypes of stomatocysts prevailed [45,46,47,48,49,50,51,52,53,54,55]. Four of the found morphotypes conformed to stomatocysts of the species Chrysosphaerella longispina Lauterborn—Stomatocyst 49, Duff and Smol, 1991 (identified at St. A1), Ochromonas globosa Skuja—Stomatocyst 112 Zeeb et al., 1990 (identified at St. A4), Urostipulosphaera Pusztai and Skaloud (U. notabilis (B. Mack) Pusztai and Škaloud U. lindiae (Bourrelly) Pusztai and Škaloud, U. soniaca (Conrad) Pusztai and Škaloud)—135 Duff and Smol, 1992 (identified at St. K4) as well as some species of Paraphysomonas, forming Stomatocyst 1 Duff and Smol, 1988 (identified at St. S2).
Stomatocyst 462 Firsova and Bessudova, 2018 was the most common among the morphotypes. This morphotype had been already described in tributaries of North Baikal [52] and Boguchany reservoir [53], thoughits species is unknown.
We would like to note that the list of scaled chrysophytes given in Table 2 does not contain the species Chrysosphaerella longispina, whose stomatocysts we found. This may indicate that the species has either already completed its vegetation and moved toa dormant stage or was brought by the river during the observation period. Beyond this species, among the discovered morphotypes of stomatocysts, there may be additional species of scaled chrysophytes of an identification unknown in the literature. Thus, the diversity of scaled chrysophytes in the study area maybe even higher than that in Table 2.
A new morphotype was discovered among stomatocysts at stations A1 and S1. Here is its description:
Stomatocyst 507 Firsova and Bessudova (Figure 10K,L)
Negative number: 18114_002, 18119_004, 18119_003
Biological affinity: unknown
Locality: Stations A1, S1
SEM description: Spherical stomatocyst (diameter 11.5–12.5 µm) with a cylindrical collar (diameter 4.1 µm; height 1.3 µm), and an acute apex. The surface is ornamented with numerous (about 100) echinate spines that are sometimes a little twisted at the ends (spine height 1.0–2.6 µm).
References: We were not able to link this stomatocyst with any previously published morphotype.
4. Discussion
We suggest that the hydrologic regime is the most important factor governing the biodiversity and distribution of scaled chrysophytes downstream of the Ob river during high water. The present study was undertaken during high water when the riverbed became wider and the banks were flooded forming still backwaters in which, as opposed to the main channel with a high flow rate, there were less turbidity. At that time, according to Table 1, at the studied stations, the flow rate, turbidity and water transparency varied significantly from 0 to 0.38 m·s−1 and 0.35 to 0.60 m, respectively, while other water parameters were comparable. Our data bear evidence that these differences were enough to create different ecotopes, and consequently to manifest peculiarities in the distribution of species diversity of scaled chrysophytes. The high diversity of scaled chrysophytes (75 species) we previously observed at the mouth of the arctic lowland Olenyok river (Yakutia) was closely related to the slower flow, temperature, transparency and impact of small tundra tributaries [18]. Only five species [18] were identified in the same area in the mountain Indigirka river, which lacks large lowlands and has a minimal amount of meanders.
The various environmental conditions in the study area during the observation period favored the formation of a high species richness of scaled chrysophytes (67 species). Such a high biodiversity is comparable tot hat of the mouths of arctic rivers in Yakutia (82 species) [18], Baikal region (79 species) [56], Bolshezemelskaya tundra (75 species) [57], and the small arctic ponds near Tiksi (65 species) [58] that we have described previously. Therefore, the northern waters of East Siberia have a high species diversity of scaled chrysophytes. The highest diversity of scaled chrysophytes during this study occurred in shallow sites without flow, isolated from the main channel (such as stations K4, A4 and A1).
The differences in habitat parameters distributed the species in accordance with their ecological preferences, once again indicating the sensitivity of scaled chrysophytes to different parameters of the habitat [15]. Our data show (see Table 1 and Table 2) that increasing flow rate and turbidity remove most the of species that occur in hydrologically stable environments of backwaters and riparian stations, such as Mallomonas actinoloma, M. alata, M. eoa, M. calceolus, M. insignis, M. mangofera var. mangofera, M. multiunca, M. papillosa, M. kuzminii, M. scalaris, M. scrobiculata, M. torquata var. torquata, Synura cf. asmundiae, S. conopea, S. praefracta, S. multidentata, S. spinosa f. longispina, and S. splendida from the species composition of the main channel.
Vegetation of scaled chrysophytes in the study area was also limited by an active bloom of diatoms at some stations, e.g., at St. S1. The lowest number and biomass of diatoms was observed at St. K4, which had the highest variety of species composition of scaled chrysophytes, where they occurred as whole cells (see Table 1). Vegetative peaks of scaled chrysophytes are known to coincide, as a rule, with the end of vegetation of large diatom species [59,60]; this seems to be related to an ability toproduce Si.
If we analyze the list of species in termsof biogeography (see Table 2), we will see the cosmopolitan and widespread species Mallomonas acaroides, M. akrokomos, M. alpina, M. caudata, M. crassisquama, M. crassisquama var. papillosa, M. punctifera, M. tonsurata, Synura americana, S. glabra, S. borealis, S. petersenii, S. spinosa and S. uvella occurred in the main channel, sometimes as whole cells, and manifestedtheir vegetation during sampling. The same species had been shown to predominate by frequency of cells and scales at the mouths of the mountain Yenissei [61], Upper Angara, Kichera [62] rivers as well as at the mouths of the arctic Indigirka and Kolyma rivers [18], i.e., these species may be described as current-tolerant. The distribution of representatives of the order Paraphysomonadales is less investigated. In this study, species of the genus Spiniferomonas with limited distribution, such as S. abrupta, S. cornuta, S. minuta, S. serrata, S. silverensis, S. takahashii and S. triangularis, occurred in ditchwater at stations K4, A4 and A1, indicating their sensibility to current. A high species richness of species of the genus Spiniferomonas, including the species mentioned above, has already been described in the Baikal [59], Labynkyr and Vorota [21,60] lakes, in warm bays of the northern part of Baikal lake [62], in lakes near the Bothnian bay [63], in waters of the Bolshezemelskaya tundra [56], and in lakes of Connecticut [64]. Single cells of the cosmopolitan species Spiniferomonas bourrellyi and S. trioralis have been found in the main channel of the Ob river. These species havebeen previously described at the mouths of the Yenissei, Upper Angara, Kichera, Indigirka and Kolyma rivers [18,61,62] and may be considered current-tolerant. Species of the genus Paraphysomonas are also typical of lakes [20,57], though their high species diversity may be more frequent in backwaters with slow current [18]. In this study, species P. cf. v. vulgaris, Paraphysomonas sp. 1 and Paraphysomonas sp. 2 occurred only in riparian ditchwater. Two species, P. u. uniformis and P. gladiata, occurred in the main channel.
Formation of chrysophycean stomatocysts is known to have two peaks during a year—spring and summer-autumn [52,65,66]. In this study, the most variety of stomatocyst morphotypes were observed at the riparian stations K4 and A4 at T = 14–14.3 °C, manifesting around different periods of the seasonal cycles at the studied stations with different water parameters. The relatively low common diversity of stomatocyst morphotypes, with less than half of the total number of scaled chrysophytes found, may testify to the idea that the species were at a stage of intensive vegetation.
Dispersal of scaled chrysophytes at the end of the vegetative period by current in the form of thick-walled stomatocysts is highly likely [8,24,28], while their germination can be delayed for several years [8,67,68,69,70].
5. Conclusions
Lowland rivers have suitable conditions for the formation of a high diversity of scaled chrysophytes. Morphometric peculiarities of the riverbed such as meanders, large flood plain and lowlands favor the species richness of scaled chrysophytes, most of which vegetate during high water. The low diversity of scaled chrysophytes in the main channel and their high diversity near banks in bays and backwaters where the flow is almost absent or very slow bear the evidence of different sensibility to hydrological and hydrochemical conditions. Distribution of scaled chrysophytes with different trophic preferences follows some patterns. Cosmopolitan and ubiquitous representatives of the autrophic genera, such as Synura and Mallomonas, are able to inhabit the surface layer of the main channel. The turbidity and high flow rate seen during high water do not suppress their vegetation but may limit them. The main part of mixotrophic (genus Spiniferomonas) and heterotrophic (genus Paraphysomonas) representatives of scaled chrysophytes do not tolerate current and turbidity. During low water and dewatering of shallow bays in summer, chrysophytes, including their stomatocysts, may be transferred to the main channel and vegetate downstream when they meet favorable conditions.
This combination of factors, such as change of hydrologic stages, different trophic preferences, tolerance to current and capacity to form stomatocysts, may play the primary role in the formation of a high biodiversity and a dispersal of scaled chrysophytes by the current in the context of the hypothesis of omnipresence, or “everything is everywhere” [1,2,3].
A.B., electron microscopy, identification of scaled chrysophytes, literature search, interpretation of the results, and writing of the first version of the manuscript; E.M., light microscopy, counting of the Ob river phytoplankton, determination of diatoms proportion in the abundance and biomass of phytoplankton; M.K., A.S., V.K. (Vladimir Kirillov) and V.K. (Vitaly Khoroshavin), sampling, hydrochemical analysis; A.F., electron microscopy, identification of stomatocysts; Y.L., writing, review and editing. All authors have read and agreed to the published version of the manuscript.
The data that support the findings of this study are available from the corresponding authors upon reasonable request.
The microscopy studies were performed at the Electron Microscopy Center of the Shared Research Facilities “Ultramicroanalysis” of Limnological Institute,
The authors declare no conflict of interest.
Footnotes
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Enlarge this image.Figure 2. Micrographs of water samples from stations with high and low turbidity. SEM: (A) view of a part of the filter from St. S6 with numerous particles of clay and a cell of Mallomonas punctifera (red arrow); (B) a large particle of clay at high magnification (St. K2); (C) small particle of clay at high magnification (St. K2); (D) view of a part of the filter from St. K4 with low turbidity. Individual cells of Mallomonas akrokomos and M. crassisquama (red arrows) are seen on the filter. Scale bars: (C) 2 µm; (A,B,D) 50 µm.
Enlarge this image.Figure 3. Chrysosphaerella, Paraphysomonas and Spiniferomonas taxa from the Ob river, TEM (A–C,E–I,L,M), SEM (D,J,K): (A,B,D) Chrysosphaerella sp., oval (A), circular plate scales (B), and spines and plate scales (D); (C) Paraphysomonas sp., aberrant scale; (E) C. coronacircumspina, spine; (F) Paraphysomonas sp. 1; (G) P. cf. v. vulgaris; (H) Paraphysomonas sp. 2; (I) P. u. uniformis; (J) S. triangularis, a cell with overlapping scales; (K) S. cornuta, spines and plate scales; (L) Spiniferomonas bourrellyi, spine scale. The arrow points to a small circular hole; (M) S. minuta, spine scale. Scale bars: (A–C,F–M) 2 µm; (E) 5 µm; (D) 10 µm.
Enlarge this image.Figure 4. Spiniferomonas taxa from the Ob river, SEM: (A) Spiniferomonas bourrellyi, long spine; (B,C) S. silverensis, long spine (B), spines and plate scales (C); (D) S. takahashii, spines and plate scales; (E) S. trioralis, spines and plate scales; (F,G) Spiniferomonas sp., spines and plate scales; (H) S. triangularis, a cell covered with long spine and plate scales; (I) S. serrata, spines and plate scales; (J) S. abrupta, spines and plate scales. Scale bars: (C–G) 2 µm; (I,J) 5µm; (A,B,H) 10 µm.
Enlarge this image.Figure 5. Mallomonas taxa from the Ob river, TEM: (A) Mallomonas kuzminii; (B) M. alpina; (C) M. elongata; (D) M. tonsurata; (E) M. costata; (F) M. trummensis; (G) M. acaroides, caudal scale; (H) M. insignis; (I) M. kalinae; (J) M. calceolus; (K) M. punctifera; (L) M. papillosa; (M) M. caudata; (N) M. actinoloma; (O) M. actinoloma var. maramuresensis; (P) M. heterospina. Scale bars: 2 µm.
Enlarge this image.Figure 6. Mallomonas taxa from Ob River, TEM: (A) Mallomonas torquata var. torquata; (B) M. alata f. hualvensis; (C) M. alata; (D) M. lychenensis; (E,F) Mallomonas sp., bristle (E) and scale (F); (G,H) M. munda, body (G) and apical scales (H); (I) M. scalaris, apical scale; (J) M. akrokomos; (K–M) M. mangofera var. mangofera; (N,O) M. striata var. serrata; (P) M. annulata; (Q) M. eoa. Scale bars: (A–D,F–Q) 2 µm; (E) 5 µm.
Enlarge this image.Figure 7. Mallomonas and Synura taxa from Ob River, TEM: (A) Mallomonas scrobiculata; (B) M. multiunca; (C) Synura splendida; (D) S. punctulosa; (E–G) M. crassisquama, various variants of the coarse reticulum on shield; (H) M. crassisquama var. papillosa; (I,J) S. multidentata; (K)S. spinosa f. longispina; (L) S. spinosa; (M) S. petersenii; (N) S. uvella; (O) S. echinulata; (P,Q) S. cf. asmundiae; (R) S. borealis. Scale bars: (D,I–R) 1 µm; (A–C,E–H) 2 µm.
Enlarge this image.Figure 8. Synura taxa from the Ob river, TEM: (A,B) Synura americana; (C,D) Synura sp. 2, a wide, cylindrical keel, ornamented with medium-sized pores. Numerous struts somewhat reduced, without transverse folds; (E) S. conopea; (F–H) Synura sp. 1, the keel is ornamented by pores of different sizes—from medium to very large; (I) S. praefracta, apical scales with rounded spine terminated by several short teeth; (J) S. glabra; (K–N) S. biseriata, body scales, the arrow shows an additional row of meshes (E); (O–S) S. cf. hibernica, apical scales with prominently protruding keel tip (O–Q), body scale (R), rear scale (S). Scale bars: 1 µm.
Enlarge this image.Figure 9. Stomatocysts from the Ob river, SEM: (A) Stomatocyst 001 Duff and Smol, 1988; (B) Stomatocyst 29 Duff and Smol, 1989; (C) Stomatocyst 41 Piątek, 2007; (D) Stomatocyst 49 Duff and Smol, 1991; (E) Stomatocyst 188 Brown and Smol, 1994; (F) Stomatocyst 58 Duff and Smol, 1994; (G) Stomatocyst 183 Brown and Smol, 1994; (H) Stomatocyst 234 Duff et al., 1995; (I) Stomatocyst 152 Zeeb and Smol, 1993; (J) Stomatocyst 181 Brown and Smol, 1994; (K) Stomatocyst 112 Zeeb et al., 1990; (L) Stomatocyst 198 Duff and Smol, 1994; (M) Stomatocyst 203 Duff and Smol, 1994; (N) Stomatocyst 462 Firsova and Bessudova, 2018; (O) Stomatocyst 10 Duff and Smol, 1988; (P) Stomatocyst 279 Gilbert and Smol, 1997; (Q) Stomatocyst 380 Wilkinson and Smol; (R) Stomatocyst 135 Duff and Smol, 1992; (S) Stomatocyst 262 Zeeb and Smol, 1996; (T) Stomatocyst 263 Zeeb and Smol, 1996. Scale bars: 2 µm.
Enlarge this image.Figure 10. Stomatocysts from the Ob river, SEM: (A) Stomatocyst 467 Firsova and Bessudova, 2018; (B) Stomatocyst 207 Duff and Smol, 1994; (C) Stomatocyst 319 Brown and Smol, 1997; (D) Stomatocyst 239 Duff et al., 1995; (E) Stomatocyst 131 Pang and Wang, 2017; (F) Stomatocyst 178 Zeeb andSmol, 1993; (G,H) Stomatocyst 464 Firsova and Bessudova, 2018; (I) Stomatocyst 307 Duff, 1996; (J) Stomatocyst 410/13 Safronova, 2018; (K,L) a new Stomatocyst 507 Firsova and Bessudova, this study. Scale bars: 2 µm.
A list of sampling sites and physicochemical parameters of the mouth of the Ob river included in this study (site numbers in
| River Transect | St. No. | Station Position in the Riverbed | Coordinates N/E | Date of Sampling |
Time of Sampling |
Hmax,m | h, m | T, °C | pH | S, m | V, m·s−1 | O2 |
General View of the Sample in the SEM, Magnification |
Diatoms |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Kazym- |
K1 | Left bank | 64.6555° |
8 June 2022 | 08:35 | 18.8 | 3.8 | 13.1 | 7.31 | 0.54 | 0.12 | 9.5 | [Image omitted. Please see PDF.] | 90.4/1.27 |
| K2 | The center of the riverbed | 64.6532° |
8 June 2022 | 10:00 | 15.8 | 3.0 | 13.1 | 7.30 | 0.45 | 0.22 | 9.58 | [Image omitted. Please see PDF.] | 57.1/1.08 | |
| K3 | Right bank | 64.6655° |
8 June 2022 | 11:00 | 7.0 | 1.4 | 13.1 | 7.20 | 0.55 | 0.19 | 9.35 | [Image omitted. Please see PDF.] | 91.2/0.86 | |
| K4 | Shallow bay | 64.6666° |
7 June 2022 | 11:30 | 0.5 | 0.1 | 14.0 | - | to the bottom | 0.0 | - | [Image omitted. Please see PDF.] | 21.6/0.03 | |
| Azovy | A1 | Left bank | 64.8666° |
9 June 2022 | 10:30 | 10.1 | 2.0 | 14.33 | 7.52 | 0.50 | 0.03 | 9.23 | [Image omitted. Please see PDF.] | 48.5/0.78 |
| A2 | The center of the riverbed | 64.8769° |
9 June 2022 | 15:00 | 22.7 | 4.5 | 14.27 | 7.53 | 0.50 | 0.15 | 9.50 | [Image omitted. Please see PDF.] | 45.6/0.81 | |
| A3 | Right bank | 64.8666° |
9 June 2022 | 16:30 | 22.0 | 4.4 | 14.33 | 7.48 | 0.45 | 0.35 | 9.18 | [Image omitted. Please see PDF.] | 92.0/0.62 | |
| A4 | Right bank | 64.8789° |
9 June 2022 | 09:30 | 0.5 | 0.0 | 14.33 | - | to the bottom | −0.1 reverse flow | 8.81 | [Image omitted. Please see PDF.] | 50.4/0.58 | |
| Salemal | S1 | Left bank, tributaries | 66.7932° |
12 June 2022 | 16:30 | 1.9 | 0.1 | 13.0 | - | 0.35 | 0–0.15 | 9.85 | [Image omitted. Please see PDF.] | 208.5/2.48 |
| S2 | Left bank | 66.7831° |
12 June 2022 | 24:00 | 16.0 | 3.2 | 12.9 | 7.87 | 0.50 | 0.20 | 10.18 | [Image omitted. Please see PDF.] | 92.4/1.17 | |
| S3 | To the left of the riverbed center | 66.7804° |
12 June 2022 | 22:30 | 25.0 | 5.0 | 14.4 | 7.82 | 0.54 | 0.26 | 9.37 | [Image omitted. Please see PDF.] | 61.0/0.90 | |
| S4 | The center of the riverbed | 66.7769° |
12 June 2022 | 19:10 | 27.0 | 5.4 | 14.4 | 7.78 | 0.57 | 0.38 | 9.71 | [Image omitted. Please see PDF.] | 62.7/0.80 | |
| S5 | The right of the center of the riverbed | 66.7741° |
12 June 2022 | 16:30 | 25.0 | 5.0 | 14.33 | 7.77 | 0.60 | 0.27 | 9.83 | [Image omitted. Please see PDF.] | 70.4/0.80 | |
| S6 | Right bank | 66.7715° |
12 June 2022 | 13:00 | 18.0 | 3.8 | 14.15 | 7.77 | 0.60 | 0.30 | - | [Image omitted. Please see PDF.] | 38.5/0.52 |
List of scaled chrysophytes and their distribution in the Ob river. Station numbers correspond to those in
| Site Species | K1 | K2 | K3 | K4 | A1 | A2 | A3 | A4 | S2 | S3 | S4 | S5 | S6 | |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| 1. | Chrysosphaerella coronacircumspina Wujek and Kristiansen in Wujek, Gretz and Wujek | + | ||||||||||||
| 2. | Chrysosphaerella sp. | + | + | + | ||||||||||
| 3. | Paraphysomonas gladiata Preisig and Hibberd | + | + | + | ||||||||||
| 4. | P. cf. vulgaris vulgaris Scoble andCavalier-Smith | + | + | |||||||||||
| 5. | P. uniformis uniformis Scoble and Cavalier-Smith | + | + | + | + | |||||||||
| 6. | Paraphysomonas sp. 1 | + | ||||||||||||
| 7. | Paraphysomonas sp. 2 | + | ||||||||||||
| 8. | Spiniferomonas abrupta Nielsen | + | ||||||||||||
| 9. | S. bourrellyi Takahashi | + | + | + | + | + | + | |||||||
| 10. | S. cornuta Balonov | + | ||||||||||||
| 11. | S. minuta Nicholls | + | + | |||||||||||
| 12. | S. serrata Nicholls | + | + | |||||||||||
| 13. | S. silverensis Nicholls | + | ||||||||||||
| 14. | S. takahashii Nicholls | + | ||||||||||||
| 15. | S. triangularis Siver | + | ||||||||||||
| 16. | S. trioralis Takahashi | + | + | + | + | + | + | + | ||||||
| 17. | Spiniferomonas sp. | + | ||||||||||||
| 18. | Mallomonas acaroides Perty | + | + | + | + | + | + | + | + | + | ||||
| 19. | M. actinoloma Asmund and Takahashi | + | + | |||||||||||
| 20. | M. actinoloma var. maramuresensis Asmund and Takahashi | + | + | + | ||||||||||
| 21. | M. annulata Harris | + | + | + | ||||||||||
| 22. | M. akrokomos Ruttner | + | + | + | + | |||||||||
| 23. | M. alpina Pascher and Ruttner | + | + | + | + | |||||||||
| 24. | M. alata Asmund | + | + | + | ||||||||||
| 25. | M. alata f. hualvensis Asmund, Cronberg and Dürrschmidt | + | + | + | ||||||||||
| 26. | M. elongata Reverdin | + | + | |||||||||||
| 27. | M. eoa Takahashi in Asmund and Takahashi | + | + | |||||||||||
| 28. | M. caudata Iwanoff | + | + | + | + | |||||||||
| 29. | M. calceolus Bradley | + | ||||||||||||
| 30. | M. crassisquama (Asmund) Fott | + | + | + | + | + | + | + | + | + | + | + | + | + |
| 31. | M. crassisquama var. papillosa Siver and Skogstad | + | + | + | + | |||||||||
| 32. | M. costata Dürrschmidt | + | + | |||||||||||
| 33. | M. heterospina Lund | + | + | + | ||||||||||
| 34. | M. insignis Pénard | + | ||||||||||||
| 35. | M. lychenensis Conrad | + | + | + | ||||||||||
| 36. | M. mangofera var. mangofera Harris and Bradley | + | + | |||||||||||
| 37. | M. multiunca Asmund | + | + | |||||||||||
| 38. | M. munda (Asmund, Cronberg and Dürrschmidt) Nemcova | + | ||||||||||||
| 39. | M. papillosa Harris and Bradley | + | + | + | ||||||||||
| 40. | M. punctifera Korshikov | + | + | + | + | + | + | + | + | + | + | |||
| 41. | M. kalinae Řezáčová | + | + | |||||||||||
| 42. | M. kuzminii Gusev and Kulikovskiy | + | ||||||||||||
| 43. | M. scalaris Dürrschmidt | + | ||||||||||||
| 44. | M. scrobiculata Nicholls | + | ||||||||||||
| 45. | M. striata var. serrata Harris and Bradley | + | + | + | ||||||||||
| 46. | M. tonsurata Teiling | + | + | + | + | + | + | + | + | |||||
| 47. | M. torquata var. torquata Asmund and Cronberg | + | ||||||||||||
| 48. | M. trummensis Cronberg | + | + | + | ||||||||||
| 49. | Mallomonas sp. | + | ||||||||||||
| 50. | Synura americana Škaloud, Kynčlová, Benada, Kofroňová, Škaloudová | + | + | + | + | + | + | + | + | + | + | + | ||
| 51. | S. cf. asmundiae (Cronberg and Kristiansen) Škaloud, Kristiansen and Škaloudová | + | ||||||||||||
| 52. | S. conopea Škaloudand Kynclová | + | ||||||||||||
| 53. | S. glabra (Korshikov) Škaloud and Kynclová | + | + | + | + | + | + | + | ||||||
| 54. | S. echinulata Korshikov | + | + | + | ||||||||||
| 55. | S. biseriata Balonov | + | + | + | ||||||||||
| 56. | S. borealis Škaloud and Škaloudová | + | + | + | + | + | ||||||||
| 57. | S. cf. hibernica Škaloud and Škaloudová | + | + | |||||||||||
| 58. | S. petersenii (Korshikov) Škaloud and Kynclová | + | + | + | + | + | + | + | + | + | ||||
| 59. | S. praefracta (Asmund) Škaloud and Škaloudová | + | ||||||||||||
| 60. | S. punctulosa Balonov | + | + | + | + | + | ||||||||
| 61. | S. multidentata Péterfi and Momeu | + | + | + | ||||||||||
| 62. | S. spinosa Korshikov | + | + | + | + | |||||||||
| 63. | S. spinosa f. longispina Petersen and Hansen | + | ||||||||||||
| 64. | S. splendida Korshikov | + | ||||||||||||
| 65. | S. uvella Ehrenberg | + | + | + | + | |||||||||
| 66. | Synura sp. 1 | + | + | + | ||||||||||
| 67. | Synura sp. 2 | + | + | |||||||||||
| TOTAL | 8 | 7 | 19 | 54 | 22 | 9 | 13 | 31 | 11 | 5 | 11 | 6 | 13 |
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; Likhoshway, Yelena 1
; Firsova, Alena 1 ; Mitrofanova, Elena 2 ; Koveshnikov, Mikhail 2 ; Soromotin, Andrey 3
; Khoroshavin, Vitaly 4 ; Kirillov, Vladimir 2 1 Limnological Institute, Siberian Branch of the Russian Academy of Sciences, 3 Ulan-Batorskaya, 664033 Irkutsk, Russia;
2 Institute for Water and Environmental Problems, Siberian Branch of the Russian Academy of Sciences, 1 Molodezhnaya, 656038 Barnaul, Russia
3 Research Institute of Ecology and Natural Resource Management, Tyumen State University, 6 Volodarsky, 625003 Tyumen, Russia
4 Institute of Earth Sciences, Tyumen State University, 2 Osipenko, 625048 Tyumen, Russia