Seasonal Dynamics of the Silica-Scaled Chrysophytes as Potential Markers of Climate Change in Natural Model: Deep Cold Lake–Shallow Warmer Reservoir
by
, , ,
Anna Bessudova
*
,
Yuri Galachyants
,
Alena Firsova
,
Diana Hilkhanova
,
Artyom Marchenkov
,
Maria Nalimova
,
Maria Sakirko
and
Yelena Likhoshway
Limnological Institute, Siberian Branch of the Russian Academy of Sciences, 3 Ulan-Batorskaya, 664033 Irkutsk, Russia
*
Author to whom correspondence should be addressed.
Sustainability 2024, 16(17), 7299; https://doi.org/10.3390/su16177299 (registering DOI)
Submission received: 5 July 2024
/
Revised: 13 August 2024
/
Accepted: 23 August 2024
/
Published: 25 August 2024
(This article belongs to the Special Issue Aquatic Biodiversity under the Impact of Climate Change)
Abstract
:In the context of global climate changes, it is important to assess the sustainability perspective of aquatic ecosystems based on marker organisms. In this work, we analyzed seasonal dynamics of silica-scaled chrysophytes in freshwater communicating environments which have considerable differences in water temperature between two ecosystems: the deep and cold oligotrophic Lake Baikal versus the shallower and warmer downstream Irkutsk Reservoir having mesotrophic features. During three seasons of the open water period of 2023, 38 species of silica-scaled chrysophytes were observed at 17 stations using scanning and transmission microscopy. The distribution of silica-scaled chrysophytes was shown to correlate with the water temperature. The greatest species richness was observed in the spring season in a large bay of the Irkutsk Reservoir (23 species), the smallest in the cold spring waters of Southern Baikal (up to 7 species). Widespread species living in Southern Baikal continued to grow in warmer waters of the reservoir. Using the example of silica-scaled chrysophytes, the stability of the high-latitudinal freshwater ecosystems affected by climate change is discussed. Continuous increment of the water temperature can lead to an increased abundance of widespread species and the displacement of psychrophilic species, affecting the overall biodiversity in such ecosystems.
1. Introduction
Increasing climate warming and an increase in anthropogenic pressure in high-latitude regions will inevitably lead to a cascade of changes that will affect both the physical and chemical characteristics of freshwater ecosystems [1,2,3]. Phytoplankton communities used in ecosystem monitoring will react most quickly to such dynamic changes in the aquatic environment [4]. As a rule, the method of light microscopy is used to assess the functioning of phytoplankton as the main producer of the aquatic environment. However, this method does not take into account the entire set of phytoplankton groups, thereby underestimating the current biodiversity of the ecosystem, and as is known, biodiversity is the leading factor of sustainability. A group common in reservoirs but underestimated by algologists includes silica-scaled chrysophytes. These heterokont protists are part of the class Chrysophyceae, and the orders Paraphysomonadales, Synurales, and Chromulinales. Their cells are covered with a shell of overlapping silica scales with bristles extending from them. The species concept of this group is based on the fine species-specific morphology of silicon elements and is generally consistent with molecular phylogenetic data [5,6]. The complexity of their detection and identification is associated with the use of electron microscopy methods: scanning (SEM) and transmission (TEM).
The prevalence of this group of microeukaryotes is associated with a diverse type of nutrition (from autotrophy to phagotrophy) and the ability to form stomatocysts at the end of the growth season or under unfavorable conditions. This ecological adaptation allows silica-scaled chrysophytes to disperse with the watercourse due to the flow of the river and, once in suitable conditions, give new growth. Thus, despite the widespread distribution of silica-scaled chrysophytes, different requirements for environmental conditions within the group allow us to consider some species as ecological markers. The basis for the identification of such marker species was laid by P. Siver [7,8]. Based on an extensive analysis of the literature and his own data, P. Siver classified some species of silica-scaled chrysophytes into categories according to the gradient of environmental variables (pH, T, trophic, and salinity) [8]. This knowledge is especially useful in reconstructing environmental conditions. After the destruction of cells, siliceous scales and bristles of chrysophytes can be preserved in sediments, and by knowing the values of the variables in which the species is able to grow, it is possible to recreate the living conditions in the past. For example, evidence of the prosperity of silica-scaled chrysophytes in the Arctic freshwater ecosystem in the Eocene [9,10,11,12] and Paleocene [13] epochs under greenhouse conditions are clusters of scales, bristles, and stomatocysts found in the northwest of Canada in sediment and in the kimberlite Giraffe Pipe. According to the reconstruction data, the climate in the early and late Eocene seasons was similar to the modern, tropical one [14]. Currently, under similar conditions, a high percentage of endemic species has been found in the territories of Northeast Asia, as well as species whose scale sizes and ultrastructural features are characteristic of fossil Eocene taxa [15,16].
Lake Baikal is the deepest oligotrophic lake in the world, and it is characterized by low water temperatures. The Angara River flows from the Southern part of the lake, passing into the Irkutsk Reservoir, which is well warmed up in the summer season. Such a lake–river–reservoir transition is a unique natural model object with a temperature gradient of water to identify the features of the growth of the population of silica-scaled chrysophytes as ecological markers. It was previously established that the temperature difference during the spring season in the waters of the Southern Baikal–Irkutsk Reservoir, which differs in formation conditions, affects the species structure and richness of silica-scaled chrysophytes [17] and phytoplankton in general. However, questions remain open, and this study is devoted to clarifying the following: how stable is the diversity, and what is the distribution of silica-scaled chrysophytes during the following seasons: summer and autumn?
2. Materials and Methods
Sampling and Microscopy
The analysis of the seasonal dynamics of silica-scaled chrysophytes communities was carried out using published data from June 2023 [17], as well as on the basis of samples collected in the summer and autumn seasons. Sampling was carried out in 2023 from aboard the scientific research vessels «Papanin» and «Titov» at 9 stations in Southern Baikal and 8 stations in the Irkutsk Reservoir, including bays (Table 1), as follows: in the spring season, immediately after the opening of reservoirs from ice, 22–26 June [17]; in the summer the season, 7–20 August; in the autumn season, 15–18 October. During sampling, T and pH were measured, as well as the transparency of the water, using a Secchi disk (S, m). Hydrochemical analyses were carried out in the laboratory for the content of Si, PO43−, NO2−, NO3−, and NH4+. Information about these areas of research, methods of sampling, sample preparation, and methods of statistical analysis can be found in our previous article [17].
The relative abundance of each scaled chrysophyte species was ranked by the number of scales observed in the microscope as follows: rare (1) 1–200 observed on the entire filter, common (2) 2–100, and abundant (3) if the number of scales was >100 observed at ×1000 magnification using SEM.
3. Results
3.1. Water Variables
The water temperature was the only parameter that varied widely in the study area from June to October. In the spring season (June) in Southern Baikal, the water temperature varied between 3.6 and 4.5 °C. At station 10 (Burduguz, Angara River section), the temperature increased to 5.3 °C, and in the reservoir, it already reached 7.6–11.5 °C [17]. In the summer season (August), summer warming of the waters was observed, and the temperature reached maximum values both in Southern Baikal (6.3–16.2 °C) and in the reservoir (16.6–18.3 °C). In the autumn season (October), the water temperature dropped, and the temperature difference was less pronounced. In Southern Baikal, it varied in the range of 5.1–9.8 °C, and in the reservoir, it varied in the range of 9.3–10.5 °C. The water temperature in the river section was 8.5 °C (Table S1). The pH values in the study area corresponded to slightly alkaline waters. The lowest pH values were observed in spring in Southern Baikal, 7.0–8.0, and the highest in the reservoir, up to 8.7 [17]. In summer, the pH values in both Southern Baikal and the reservoir were similar, 7.9–8.4. In autumn, the pH was opposite to spring; the highest values were noted in Southern Baikal, which was up to 8.7, while in the reservoir, the values varied between 7.5 and 8.2 (Table S1). The lowest Si concentrations were observed in spring, while in Southern Baikal, they varied over a wider range, 0.17–0.53 mg/L, unlike in the reservoir, 0.40–0.56 mg/L [17]. In the summer, Si concentrations increased to 0.40–0.68 mg/L in Southern Baikal and to 0.80–0.91 mg/L in the reservoir. In autumn, Si concentrations were comparable to the spring values. The concentration of phosphates (PO43−) in Southern Baikal and the reservoir in the spring and summer varied between 0.005 and 0.023 mg/L; in autumn, it decreased to 0.001–0.016 mg/L. The concentration of nitrites (NO2−) in the spring and summer did not exceed 0.001 mg/L. In autumn, the concentration of nitrites reached the maximum value of 0.006 mg/L in Southern Baikal. The concentration of nitrates (NO3−) reached its maximum value in the spring in Southern Baikal, 0.41 mg/L. In summer and autumn, the values ranged from 0.04 to 0.35 mg/L. The water transparency by the Secchi disk in Southern Baikal significantly decreased in summer (4.5–9.0 m) compared to the spring (10–22 m) [17]; the same was noted in the reservoir (3.0–5.0 m in spring and 2.5–4.5 m in summer). In autumn, the water transparency in Southern Baikal was as low as in summer (5.5–9 m), and in the reservoir, it decreased to 1.5–2 m (Table S1).
3.2. Analysis of Factors Affecting the Structure of Silica-Scaled Chrysophytes Communities
Among environmental variables (Table S1), phosphate and nitrate anion concentrations had a strong positive correlation. At the same time, they negatively correlated with the water temperature (Figure 1A). The concentration of Si had a strong positive correlation with water temperature. The constrained ordination of the relative abundance of scaled chrysophytes via CCA using both forward selection and reverse exclusion of variables allowed us to generate a model with a single explanatory variable, water temperature. In this model, temperature alone explained 15% out of 23% of the adjusted total limited variation in the species relative abundance matrix. CCA showed that silica-scaled community profiles were separated into groups according to the sampling site location type and the sampling month (Figure 1B). Profiles of silica-scaled chrysophytes sampled across Lake Baikal and Irkutsk Reservoir in June were less similar, whereas in August and October, the differences between lake and reservoir sites decreased. This effect is associated with low water temperature accompanied by high nitrate/phosphate anion concentrations in the June Lake Baikal water samples.
3.3. Seasonal Dynamics of Silica-Scaled Chrysophytes
In total, 38 species of silica-scaled chrysophytes were found in Southern Baikal and the Irkutsk Reservoir during three hydrological seasons, of which the genus Chrysosphaerella had 3 species, Paraphysomonas had 6, Lepidochromonas had 2, Spiniferomonas had 9, Mallomonas had 12 and Synura had 6 (Table 2). The greatest species richness was observed in the large Kurma Bay, with 23 species. Over the course of three seasons, the species richness changed, forming a characteristic change of communities.
The structure of the silica-scaled chrysophyte communities in Southern Baikal and the Irkutsk Reservoir changed with the warming of the waters (Figure 2).
In the spring season, 31 species were found in Southern Baikal and the reservoir [17]. In the spring season in Southern Baikal, the species richness varied from 3 to 7 species, and at the end of early spring, a growth period was observed. This is evidenced by the cells and single scales of Chrysosphaerella baikalensis, Mallomonas alpina, single cells of Spiniferomonas trioralis f. cuspidata, and scales and bristles of M. vannigera. The stomatocysts C. baikalensis and S. trioralis f. cuspidata were often found. All species found in the waters of Southern Baikal were also found in the reservoir (Figure 3).
However, only the M. alpina species, whose growth was over in Southern Baikal, was found again in the form of whole cells when entering the warmer waters of the reservoir; other species from Southern Baikal were found in the waters of the reservoir in the form of single scales. In general, the enrichment of the species composition of silica-scaled chrysophytes and the change of the “Baikal” early spring core of species were observed in the reservoir. M. alpina cells, as well as Synura glabra cells and colonies, prevailed in relative abundance. Cells of the typically summer species M. acaroides and M. crassisquama were found in the bays, as well as the summer–autumn Spiniferomonas abrupta, S. bourrellyi, S. cornuta, and S. silverensis [17].
In the summer season in Southern Baikal and the reservoir, the total species richness of silica-scaled chrysophytes was lower than in the spring season; only 23 species were found. In Southern Baikal, the species richness was replenished with eight species, five of which were found in the bays of the reservoir in the spring season; these are M. tonsurata, Paraphysomonas sp. 1, Chrysosphaerella coronacircumspina, S. abrupta, and S. cornuta. Three species, Paraphysomonas gladiata, Spiniferomonas septispina, and S. takahashii, were added to the general list of species in the summer season. Four species found in spring, M. alpina, S. bourrellyi, S. trioralis, and S. trioralis f. cuspidate, continued to grow in the summer, the last two prevailing in relative numbers. The species C. baikalensis and M. vannigera, which are characteristic of the early spring season, did not occur in summer, even in the form of single scales.
All species found in the waters of Southern Baikal during the summer season were also found in the reservoir (Figure 2). At the same time, the species richness of silica-scaled chrysophytes in the reservoir decreased by 13 species compared to the spring season. These species that have fallen out of the reservoir’s species composition can be characterized as spring species: C. baikalensis, Paraphysomonas sp. 2, P. bandaiensis, S. triangularis, M. getseniae, M. grachevii, M. punctifera, M. trummensis, M. vannigera, Mallomonas sp., Synura echinulata, S. punctulosa, and S. spinosa f. longispina. Three species, P. uniformis hemiradia, Lepidochromonas cf. stephanolepis, and L. cf. canistrum, were added to the general list of species in the summer season (Figure 4). The relative abundance of most species of silica-scaled chrysophytes was low in this season. Only the species M. alpina, S. trioralis, and S. trioralis f. cuspidata, which predominate in Southern Baikal and at some stations of the reservoir, were often found in the form of single scales.
The autumn season was characterized by the lowest total species richness (13 species in total) and a relative abundance of silica-scaled chrysophytes.
In Southern Baikal, the species richness was comparable to the spring season, in which seven species were found: C. coronacircumspina, M. alpina, S. abrupta, S. septispina, S. cornuta, S. trioralis, S. trioralis, and f. cuspidata. All the registered species, except S. abrupta, were found in the form of whole cells, rarely. Also, during this period, the appearance of a larger number of stomatocysts belonging to the species listed above was noted. Ten species were found in the waters of the reservoir, four of which were also found in the waters of Southern Baikal. Three species of S. abrupta, S. septispina, and S. cornuta from Southern Baikal were not found in the waters of the reservoir. A previously unidentified species of Paraphysomonas sp. was found in the reservoir. At some stations of the reservoir, M. alpina, M. elongata, and M. crassisquama species were found in the form of whole cells.
Thus, during the open-water period, the growth of silica-scaled chrysophytes in Southern Baikal was already on the decline, as evidenced by the occurrence of single scales and stomatocysts. At the same time, it is the spring season that was characterized by the greatest species richness of silica-scaled chrysophytes in the bays of the reservoir. Species typical of the spring, summer, and autumn seasons grew in them at the same time. In the summer season, with the warming of the waters in Southern Baikal, the species composition changed, and the species richness of silica-scaled chrysophytes increased due to the appearance of the summer–autumn complex, which was found in the spring season in the bays of the reservoir. During the same period, with an increase in temperature in the reservoir to maximum values, species richness decreased due to the loss of spring species from the structure. In the autumn season, with the equalization of water temperature in Southern Baikal and the Irkutsk Reservoir, the difference in species richness decreased, but the difference in species structure between the studied reservoirs increased. Some species that were previously characteristic of the summer complex in the Irkutsk Reservoir no longer supported their growth but grew in the waters of Southern Baikal.
3.4. Spatio-Temporal Distribution of Silica-Scaled Chrysophytes in the Context of Differences Trophic Modes
In the context of differences in the trophic modes of silica-scaled chrysophytes (photo-, mixo-, or heterotrophic), their distribution had some patterns. As shown above, phosphate and nitrate anion concentrations were negatively correlated with water temperature, while the concentration of Si had a strong positive correlation with water temperature (Figure 1A). At the same time, the greatest species richness of silica-scaled chrysophytes was noted in warmer waters. Thus, most species, with the exception of those prevailing in Southern Baikal in spring, are adapted to development at low concentrations of phosphate and nitrate anion. A strong positive correlation between water temperature and Si was associated with the predominance of non-silicon-dependent microalgae in the study area in summer and autumn. An additional important factor affecting the distribution of silica-scaled chrysophytes with different trophic modes may be the transparency of the waters. This factor is also associated with warming up the water. An increase in water temperature contributes to the growth of phytoplankton, depletion of phosphate and nitrate anion concentrations, and a decrease in transparency. Thus, photoautotrophic species of the genera Mallomonas and Synura prevailed in the spring, when the transparency of waters both in Southern Baikal (on average 10–22 m) and in the reservoir (3–5 m) had the highest values (Table S1). However, in the bays of the reservoir during this period, lower transparency was observed than in the rest of the reservoir area by 0.5–1 m, which was associated with a more active growth of phytoplankton. At the same time, mixotrophic species of the genus Spiniferomonas began to grow in the bays. With the summer warming of the waters, the transparency decreased to 4.5–9 m in Southern Baikal and to 2.5–3 m in the reservoir. At the same time, heterotrophic species of the genus Paraphysomonas and mixotrophic species of the genus Spiniferomonas, as well as Chrysosphaerella coronacircumspina, appeared in the structure of communities. In the autumn, transparency increased slightly in Southern Baikal, up to 6.5–9.5 m, but mixotrophic silica-scaled chrysophytes still dominated. In the reservoir, despite the continued decrease in transparency to 1.5–2 m, in addition to mixotrophic species of the genus Spiniferomonas, whole cells of photoautotrophic species of the genus Mallomonas were found.
4. Discussion
4.1. Species Diversity of Silica-Scaled Chrysophytes in the Study Area
This study used electron microscopy to reveal the diversity of silica-scaled chrysophytes in the oligotrophic Irkutsk Reservoir with mesotrophic features, from the previously known 5 [18] and 31 [17] to 38 species. In Lake Baikal, an earlier revision of the silica-scaled chrysophytes revealed 25 species [19]. Recent studies of under-ice communities in the pelagic zone of the lake added three species new to science to this list, M. sibirica Bessudova, M. baicalensis Bessudova, and M. grachevii, as well as rare species M. pechlaneri Němcová & Rott, M. voloshkoae Gusev, Němcová & Kulikovskiy, and M. striata var. balonovii Voloshko [20].
Thus, a total of 31 species of silica-scaled chrysophytes live in Lake Baikal. The greatest species richness was noted in the middle and northern basins of the lake due to the influence of rivers flowing into them. However, in the southern basin of the lake, due to the lack of large tributaries, the species richness of silica-scaled chrysophytes is less diverse, with only 18 species. A feature of the distribution of silica-scaled chrysophytes in the waters of the reservoir is the continuity of species from Southern Baikal. However, in the warmer waters of the reservoir, not all species adapted to the low temperatures of the lake survive there. One species native to Southern Baikal, M. baicalensis, was not found in the reservoir at all. For example, the species M. grachevii and M. getseniae, characteristic of under-ice communities in the lake, were found only in the form of single scales. At the same time, M. alpina, after the end of growth in Southern Baikal, continued in the reservoir (Table 2).
4.2. Features of Seasonal Dynamics of Silica-Scaled Chrysophytes
The change of seasons and communities in the studied reservoirs is closely related to the warming of the water. Due to the differences in the thermal regime of the lake and reservoir, the phenology of the species also differs. In the warmer waters of the reservoir, a shift in the phenology of the silica-scaled chrysophytes communities was observed; the hydrological summer and autumn began earlier. The greatest differences in the species richness of silica-scaled chrysophytes between Southern Baikal and the Irkutsk Reservoir were noticeable in spring (Table 3). Three species, S. trioralis, S. trioralis f. cuspidata, and M. alpina, were found as whole cells during three seasons both in Southern Baikal and in the reservoir when the water temperature varied from 3.6 to 18.3 °C, which indicates their wide ecological valence (Table 3).
The presence of both species richness and relative abundance in summer and autumn of mixotrophic species of the genus Spiniferomonas, as well as C. coronacircumspina, indicates the competitive advantage of this trophic mode. Apparently, these mixotrophic species prefer to grow at low concentrations of phosphates and nitrates, do not depend on the concentration of Si, and tolerate low water transparency well. The temperature range of their growth ranged from 9.9 to 11.5 °C in spring, from 6.3 to 18.3 °C in summer, and from 5.1 to 10.5 °C in autumn. However, the distribution of various trophic modes of silica-scaled chrysophytes, despite the expected patterns, had interesting features. One of them was the growth of photoautotrophic species M. crassisquama, M. elongata, and M. alpina in the reservoir during the autumn period, characterized by the lowest water transparency. At the same time, these same species were found in the form of whole cells in spring, where M. alpina and M. crassisquama formed the largest relative abundance. According to our data, the low-light conditions in the subarctic lakes of Yakutia observed a similar growth of photoautotrophic species of silica-scaled chrysophytes. In under-ice communities of phytoplankton with an ice thickness of 86–111 cm and snow thickness of 0.5–35 cm, we observed the growth of M. crassisquama, Mallomonas crassisquama var. papillosa, and Mallomonas sp. Also, when studying the dynamics of phytoplanktons in a lake permanently covered with ice located in the south of Victoria Land, Antarctica, the growth of Mallomonas sp. was shown as part of phytoplankton [21].
4.3. Silica-Scaled Chrysophytes as Markers of Climate Change
The main patterns of distribution of silica-scaled chrysophytes from the cold-water Lake Baikal to the warmer waters of the reservoir and their bays can be applied in conditions of arctic or polar amplification. These conditions, expected at high latitudes for the formation of significantly higher temperatures compared to the global average, can be comparable to the Eocene greenhouse conditions. Significantly higher concentrations of CO2 in the atmosphere in the Early and Late Eocene stimulated the growth of autotrophic Synurales [3,22]. This is explained by the lack of mechanisms of CO2 concentration and external carbonic anhydrase in these organisms, making them metabolically dependent on the direct diffusion of CO2 for Rubisco during photosynthesis [22,23]. In the Eocene period, silicon-dependent representatives of the Chrysophyceae class (including the Synurales) prevailed in most samples throughout the core in Giraffe sediments, accounting for up to 72% of the total number of microfossils [3]. The prerequisites for accelerating warming are already being observed in some boreal, subarctic, and Arctic reservoirs. For example, a high species diversity of silica-scaled chrysophytes was noted in the Arctic rivers of Yakutia, where, along with arctic-boreal species, species of the boreal latitude were found [24]. In modern microfossils of boreal, subarctic, and Arctic reservoirs in North America, an increase in populations of silica-scaled chrysophytes was observed [22,25,26,27]. These changes, as the authors suggest, are also associated with climate warming, which causes an increase in the concentration of CO2 in lakes, stimulating their growth [22]. Our results show that in oligotrophic reservoirs, an increase in temperature can increase the species richness of silica-scaled chrysophytes (Figure 2). Since silica-scaled chrysophytes have low requirements for the concentration of biogenic elements [28,29], this factor may be of paramount importance.
Thus, the continued increase in temperature at high latitudes may indirectly, through atmospheric and limnological changes, stimulate the growth of some widespread species. For example, in the reservoir, we found the growth of M. crassisquama species and, to a lesser extent, M. elongata (since cells of this species were rare), which were observed as whole cells twice during the growing season, in June and October. An increase in the concentration of M. crassisquama scales was previously described in the core of modern sediments of boreal lakes in North America [26]. Two of the three species present during the studied seasons, S. trioralis and M. alpina, are widespread species. The S. trioralis f. cuspidata, which forms a high relative abundance in the waters of Southern Baikal, as a rule, lives only in northern reservoirs [30]. The forecast for the growth of cold-water species with an increase in water temperature remains disappointing. Shifts in the timing of ice melting and the beginning and duration of temperature stratification can lead to their displacement. Analysis of the Eocene sediments showed that many thermophilic species that lived in the conditions of the greenhouse conditions became extinct, probably without surviving the onset of the cold snap. If we consider silica-scaled chrysophytes on a wide time scale, then these organisms, despite their widespread distribution and different types of trophic and spore formation abilities, are sensitive indicators of climate change, both warming and cooling.
5. Conclusions
Biodiversity is known to be an important condition for the sustainability of ecosystems. The present study indicates a higher species richness of silica-scaled chrysophytes in the Irkutsk Reservoir than was previously known. This indicates a broader opportunity for the community to adapt to changes in environmental conditions and the sustainability of the ecosystem of the Southern Baikal–Irkutsk Reservoir. In spring, when the thermal gradient is most pronounced, the communities of silica-scaled chrysophytes in the lake and reservoir differ mostly by structure and species richness. During this season, species previously characterized as spring were found in Southern Baikal, and a summer complex of species was already found in the bays of the reservoir. As the water warms up in the summer season, differences in the structure and species richness of the silica-scaled chrysophytes community were smoothed out, and in the autumn season, on the contrary, they increased. Thus, the peculiarities of the hydrological regime, including temperature-derived factors, regulate the silica-scaled chrysophytes community composition. This once again proves the sensitivity of this group of microeukaryotes in natural reservoirs to environmental changes related, among other things, to climate.
Supplementary Materials
The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/su16177299/s1, Table S1: Hydrochemical parameters of samples in Southern Baikal and Irkutsk Reservoir in June, August, and October 2023.
Author Contributions
A.B. electron microscopy, identification of silica-scaled chrysophytes, a search of the literature, interpreting the results, and writing the first version of the manuscript; Y.G., statistical analysis; Y.L., A.M., M.N. and D.H., sampling; A.F. and D.H. electron microscopy; M.S., hydrochemical analysis; Y.L., writing, review, and editing. All authors have read and agreed to the published version of the manuscript.
Funding
This work was performed with financial support from the Russian Science Foundation No 23-14-00028 of the project, “Communities of microeukaryotes in Angara Cascade Reservoirs” https://rscf.ru/en/project/23-14-00028/, accessed on 4 July 2024.
Institutional Review Board Statement
Not applicable.
Informed Consent Statement
Not applicable.
Data Availability Statement
The original contributions presented in the study are included in the article, further inquiries can be directed to the corresponding author.
Acknowledgments
The study was performed using microscopes of the Instrumental Center “Electron Microscopy” (http://www.lin.irk.ru/copp/, accessed on 4 July 2024) of the Shared Research Facilities for Research “Ultramicroanalysis”.
Conflicts of Interest
The authors declare no conflicts of interest.
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Figure 1.
Exploratory analysis of environmental variables and relative abundance of silica-scaled chrysophytes. (A) Correlation of environmental variables. Numerical values are Pearson correlation coefficients with the color legend on the right. Strikeouts are non-significant correlations (p > 0.05). (B) Constrained ordination of species relative abundance data using correspondence analysis. The shape of the point designates the month of sampling, and the color denotes the sampling site type: Lake Baikal or Irkutsk Reservoir. The letters correspond to the station IDs (Table 1). Red isolines show the gradient of water temperature.
Figure 1.
Exploratory analysis of environmental variables and relative abundance of silica-scaled chrysophytes. (A) Correlation of environmental variables. Numerical values are Pearson correlation coefficients with the color legend on the right. Strikeouts are non-significant correlations (p > 0.05). (B) Constrained ordination of species relative abundance data using correspondence analysis. The shape of the point designates the month of sampling, and the color denotes the sampling site type: Lake Baikal or Irkutsk Reservoir. The letters correspond to the station IDs (Table 1). Red isolines show the gradient of water temperature.
Figure 2.
Distribution of silica-scaled chrysophytes by genera in different sampling seasons with a change in water temperature. For station numbers, see Table 1 (1–9 Southern Baikal, 10–17 Irkutsk Reservoir).
Figure 2.
Distribution of silica-scaled chrysophytes by genera in different sampling seasons with a change in water temperature. For station numbers, see Table 1 (1–9 Southern Baikal, 10–17 Irkutsk Reservoir).
Figure 3.
The relationship of the communities of silica-scaled chrysophytes from Southern Baikal (SB) and Irkutsk Reservoir (IR) in June, August, and October 2023.
Figure 3.
The relationship of the communities of silica-scaled chrysophytes from Southern Baikal (SB) and Irkutsk Reservoir (IR) in June, August, and October 2023.
Figure 4.
Species that have been added to the general list of species of silica-scaled chrysophytes in the summer season of 2023. TEM (d,i), SEM (a–c,e–h): (a) Paraphysomonas uniformis hemiradia, (b) P. gladiata, (c,d) Paraphysomonas sp. 3, (e) Spiniferomonas takahashii, (f,g) S. septispina, (h) Lepidochromonas cf. canistrum, and (i) L. cf. stephanolepis. Scale bars: (h,i) 1 µm; (a–e) 2 µm; (f,g) 5 µm.
Figure 4.
Species that have been added to the general list of species of silica-scaled chrysophytes in the summer season of 2023. TEM (d,i), SEM (a–c,e–h): (a) Paraphysomonas uniformis hemiradia, (b) P. gladiata, (c,d) Paraphysomonas sp. 3, (e) Spiniferomonas takahashii, (f,g) S. septispina, (h) Lepidochromonas cf. canistrum, and (i) L. cf. stephanolepis. Scale bars: (h,i) 1 µm; (a–e) 2 µm; (f,g) 5 µm.
Table 1.
Sampling sites in Southern Baikal and the Irkutsk Reservoir.
| Station Number | ID/Name Station | Coordinates N/E |
|---|---|---|
| Southern Baikal | ||
| 1. | 12K_12 km from Kultuk | 51° 40.578/103° 52.309 |
| 2. | 3M_3 km from Marituy | 51° 45.546/104° 13.222 |
| 3. | MS_Marituy-Solzan | 51° 38.710/104° 13.715 |
| 4. | 3S_3 km from Solzan | 51° 31.428/104° 14.417 |
| 5. | TS_cape Tolsty-Snezhnaya River | 51° 36.402/104° 44.147 |
| 6. | 3T_3 km from Tankhoi | 51° 35.440/105° 06.968 |
| 7. | KM_cape Kadilny-Mishikha | 51° 46.731/105° 22.528 |
| 8. | LT_Listvyanka-Tankhoi | 51° 42.262/105° 00.720 |
| 9. | 3L_3 km from Listvyanka | 51° 49.033/104° 54.616 |
| Angara River | ||
| 10. | B_Burduguz | 52° 04.105/104° 59.451 |
| Irkutsk Reservoir | ||
| 11. | KB_Kurma Bay | 52° 06.845/104° 45.926 |
| 12. | cKB_center against Kurma Bay | 52° 10.874/104° 47.935 |
| 13. | ElB_Elovy Bay | 52° 09.906/104° 25.172 |
| 14. | cElB_center against Elovy Bay | 52° 14.548/104° 45.243 |
| 15. | cErB_center against Ershovsky Bay | 52° 21.511/104° 37.550 |
| 16. | IErB_Ershovsky Bay | 52° 20.851/104° 34.439 |
| 17. | Ups_head water | 52° 23.478/104° 33.722 |
Table 2.
List of silica-scaled chrysophytes and relative abundance (see the rank in the Section 2 «Materials and Methods») in samples from Southern Baikal and the Irkutsk Reservoir during three seasons in 2023 (The station numbers correspond to Table 1). The absence of data on the abundance of the species in any month means that the species was not detected in the sample that month. The species characteristic of a particular season are highlighted in color (the highlight colors, blue, orange, and green, correspond to the color of the season (Figure 2 and Figure 3), and purple highlights the species that live throughout all seasons in Southern Baikal and the Irkutsk Reservoir. (*)—species that have added the spring species richness in the study area during the summer season.
Table 2.
List of silica-scaled chrysophytes and relative abundance (see the rank in the Section 2 «Materials and Methods») in samples from Southern Baikal and the Irkutsk Reservoir during three seasons in 2023 (The station numbers correspond to Table 1). The absence of data on the abundance of the species in any month means that the species was not detected in the sample that month. The species characteristic of a particular season are highlighted in color (the highlight colors, blue, orange, and green, correspond to the color of the season (Figure 2 and Figure 3), and purple highlights the species that live throughout all seasons in Southern Baikal and the Irkutsk Reservoir. (*)—species that have added the spring species richness in the study area during the summer season.
| No. | Species | Station Number (See Table 1) | Month of Sampling | ||||||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Southern Baikal | Irkutsk Reservoir | ||||||||||||||||||
| 1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | 9 | 10 | 11 | 12 | 13 | 14 | 15 | 16 | 17 | |||
| 1. | Chrysosphaerella baikalensis Popovskaya | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | June | |
| 1 | October | ||||||||||||||||||
| 2. | C. brevispina Korshikov | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | June | |||||||
| 1 | August | ||||||||||||||||||
| 3. | C. coronacircumspina Wujek & Kristiansen | 1 | 1 | June | |||||||||||||||
| 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | August | ||||
| 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | October | |||||
| 4. | Paraphysomonas bandaiensis Takahashi | 1 | June | ||||||||||||||||
| 5. | P. gladiata * Preisig & Hibberd | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | August | |||
| 6. | P. uniformis hemiradia * Scoble & Cavalier-Smith | 1 | 1 | 1 | 1 | August | |||||||||||||
| 1 | October | ||||||||||||||||||
| 7. | Paraphysomonas sp. 1 | 1 | June | ||||||||||||||||
| 1 | 1 | 1 | 1 | 1 | August | ||||||||||||||
| 8. | Paraphysomonas sp. 2 | 1 | June | ||||||||||||||||
| 9. | Paraphysomonas sp. 3 * | 1 | October | ||||||||||||||||
| 10. | Lepidochromonas cf. stephanolepis (Preisig & Hibberd) Kapustin & Guiry * | 1 | August | ||||||||||||||||
| 11. | L. cf. canistrum (Preisig & Hibberd) Kapustin & Guiry * | 1 | August | ||||||||||||||||
| 12. | Spiniferomonas abrupta Nielsen | 1 | 1 | 1 | 1 | June | |||||||||||||
| 1 | 1 | 1 | 1 | August | |||||||||||||||
| 1 | October | ||||||||||||||||||
| 13. | S. bourrellyi Takahashi | 1 | 1 | 1 | 1 | 1 | June | ||||||||||||
| 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | August | ||||||
| 14. | S. cornuta Balonov | 1 | June | ||||||||||||||||
| 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | August | ||||
| 1 | October | ||||||||||||||||||
| 15. | S. septispina * Nicholls | 1 | 1 | 1 | August | ||||||||||||||
| 1 | 1 | October | |||||||||||||||||
| 16. | S. silverensis Nicholls | 1 | 1 | 1 | 1 | June | |||||||||||||
| 1 | 1 | 1 | August | ||||||||||||||||
| 17. | S. takahashii * Nicholls | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | August | ||||||
| 18. | S. triangularis Siver | 1 | 1 | June | |||||||||||||||
| 19. | S. trioralis Takahashi | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | June | |||||||
| 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 1 | 1 | 2 | 1 | 1 | 1 | 1 | 1 | August | ||
| 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | October | |||||
| 20. | S. trioralis f. cuspidata Balonov | 1 | 1 | 1 | 2 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | June | |
| 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 2 | 1 | 1 | 1 | 1 | 1 | August | ||
| 2 | 2 | 2 | 2 | 2 | 1 | 2 | 2 | 2 | 1 | 1 | 1 | 1 | October | ||||||
| 21. | Mallomonas acaroides Perty | 2 | 1 | 2 | 1 | June | |||||||||||||
| 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | August | ||||||||||
| 22. | M. alpina Pascher & Ruttner | 2 | 1 | 2 | 2 | 2 | 1 | 1 | 1 | 1 | 1 | 3 | 3 | 3 | 3 | 3 | 3 | 3 | June |
| 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 2 | 1 | 1 | 1 | 1 | 1 | 1 | August | ||
| 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 2 | 1 | 1 | 1 | 1 | 2 | 2 | October | ||||
| 23. | M. crassisquama (Asmund) Fott | 2 | 1 | 1 | 1 | 1 | 1 | 1 | June | ||||||||||
| 1 | 1 | 1 | August | ||||||||||||||||
| 2 | 1 | 1 | 1 | 2 | 1 | October | |||||||||||||
| 24. | M. elongata Reverdin | 1 | June | ||||||||||||||||
| 1 | October | ||||||||||||||||||
| 25. | M. getseniae (Voloshko) Bessudova Voloshko | 1 | June | ||||||||||||||||
| 26. | M. grachevii Bessudova | 1 | 1 | 1 | June | ||||||||||||||
| 27. | M. punctifera Korshikov | 1 | 1 | 1 | June | ||||||||||||||
| 28. | M. striata Asmund | 1 | 1 | June | |||||||||||||||
| 1 | 1 | August | |||||||||||||||||
| 29. | M. tonsurata Teiling | 1 | June | ||||||||||||||||
| 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | August | ||||||||
| 30. | M. trummensis Cronberg | 1 | June | ||||||||||||||||
| 31. | M. vannigera Asmund | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | June | ||||||||
| 32. | Mallomonas sp. | 1 | 1 | June | |||||||||||||||
| 33. | Synura echinulata Korshikov | 1 | June | ||||||||||||||||
| 34. | S. glabra (Korshikov) Škaloud & Kynclová | 1 | 3 | 3 | 3 | 3 | 3 | 3 | 3 | June | |||||||||
| 1 | 1 | 1 | 1 | 1 | 1 | August | |||||||||||||
| 1 | October | ||||||||||||||||||
| 35. | S. punctulosa Balonov | 1 | 1 | 1 | June | ||||||||||||||
| 36. | S. spinosa f. longispina Petersen & Hansen | 1 | June | ||||||||||||||||
| 37. | Synura sp. 1 | 1 | 1 | June | |||||||||||||||
| 1 | 1 | 1 | 1 | 1 | August | ||||||||||||||
| 38. | Synura sp. 2 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | June | |||||||||
| 1 | 1 | August | |||||||||||||||||
Table 3.
Seasonal and temperature attribution of some species of silica-scaled chrysophytes from Southern Baikal (SB) and the Irkutsk Reservoir (IR). The species characteristic of a particular season is highlighted in color (the highlight colors, blue, orange, and green correspond to the color of the season (Figure 3)). To analyze the temperature limits of growth, only those species that were found in the form of whole cells were taken into account, even if their relative abundance was small.
Table 3.
Seasonal and temperature attribution of some species of silica-scaled chrysophytes from Southern Baikal (SB) and the Irkutsk Reservoir (IR). The species characteristic of a particular season is highlighted in color (the highlight colors, blue, orange, and green correspond to the color of the season (Figure 3)). To analyze the temperature limits of growth, only those species that were found in the form of whole cells were taken into account, even if their relative abundance was small.
| SB Spring T, °C 3.6–4.5 | IR Spring T, °C 7.6–11.5 | SB Summer T, °C 6.3–15.6 | IR Summer T, °C 16.6–18.3 | SB Autumn T, °C 5.1–9.8 | IR Autumn T, °C 9.3–10.5 |
|---|---|---|---|---|---|
| C. baikalensis | S. abrupta | S. abrupta | M. tonsurata | S. cornuta | Paraphysomonas sp. 3 |
| M. vannigera | S. triangularis | M. tonsurata | Paraphysomonas sp. 1 | C. coronacircumspina | M. elongata |
| S. trioralis | S. bourrellyi | Paraphysomonas sp. 1 | S. cornuta | S. septispina | M. crassisquama |
| S. trioralis f. cuspidata | Synura sp. 1 | S. cornuta | P. gladiata | S. trioralis | S. trioralis |
| M. alpina | Synura sp. 2 | P. gladiata | S. takahashii | S. trioralis f. cuspidata | S. trioralis f. cuspidata |
| S. glabra | S. takahashii | C. coronacircumspina | M. alpina | M. alpina | |
| S. silverensis | C. coronacircumspina | S. septispina | |||
| M. acaroides | S. septispina | S. trioralis | |||
| M. crassisquama | S. trioralis | S. trioralis f. cuspidata | |||
| C. coronacircumspina | S. trioralis f. cuspidata | M. alpina | |||
| S. trioralis | M. alpina | ||||
| S. trioralis f. cuspidata | |||||
| M. alpina |
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Bessudova, A.; Galachyants, Y.; Firsova, A.; Hilkhanova, D.; Marchenkov, A.; Nalimova, M.; Sakirko, M.; Likhoshway, Y. Seasonal Dynamics of the Silica-Scaled Chrysophytes as Potential Markers of Climate Change in Natural Model: Deep Cold Lake–Shallow Warmer Reservoir. Sustainability 2024, 16, 7299. https://doi.org/10.3390/su16177299
AMA Style
Bessudova A, Galachyants Y, Firsova A, Hilkhanova D, Marchenkov A, Nalimova M, Sakirko M, Likhoshway Y. Seasonal Dynamics of the Silica-Scaled Chrysophytes as Potential Markers of Climate Change in Natural Model: Deep Cold Lake–Shallow Warmer Reservoir. Sustainability. 2024; 16(17):7299. https://doi.org/10.3390/su16177299
Chicago/Turabian StyleBessudova, Anna, Yuri Galachyants, Alena Firsova, Diana Hilkhanova, Artyom Marchenkov, Maria Nalimova, Maria Sakirko, and Yelena Likhoshway. 2024. "Seasonal Dynamics of the Silica-Scaled Chrysophytes as Potential Markers of Climate Change in Natural Model: Deep Cold Lake–Shallow Warmer Reservoir" Sustainability 16, no. 17: 7299. https://doi.org/10.3390/su16177299
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