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Article

Spatial Distribution of the Taxonomic Diversity of Phytoplankton and Bioindication of the Shallow Protected Lake Borovoe in the Burabay National Natural Park, Northern Kazakhstan

by
Sophia Barinova
1,*,
Elena Krupa
2,3 and
Elena Khitrova
3
1
Institute of Evolution, University of Haifa, Mount Carmel, 199 Abba Khoushi Ave., Haifa 3498838, Israel
2
Institute of Zoology, Ministry of Science and Higher Education of the Republic of Kazakhstan, 93 Al Farabi Str., Almaty 050060, Kazakhstan
3
Kazakh Agency of Applied Ecology, 42 Amangeldy Str., Almaty 050038, Kazakhstan
*
Author to whom correspondence should be addressed.
Diversity 2022, 14(12), 1071; https://doi.org/10.3390/d14121071
Submission received: 31 October 2022 / Revised: 28 November 2022 / Accepted: 2 December 2022 / Published: 5 December 2022
(This article belongs to the Special Issue Diversity of Inland Wetlands: Important Roles in Mitigation of Human Impacts)
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Abstract

:
The Burabay National Natural Park unites six lakes located among the steppe landscape, with Lake Borovoe being the most visited among them. The phytoplankton of the protected Lake Borovoe was examined in the summer season of 2019, at eight stations, which were defined for the first time as the monitoring sites on the lake surface. Altogether, 72 algae and cyanobacteria species from seven taxonomic phyla were found in the Lake Borovoe phytoplankton during the study period. The most species-rich were three phyla: diatoms, green algae, and cyanobacteria. The average phytoplankton abundance was 3012.6 cells L−1, and biomass was 2383.41 mg L−1. The ecological status of the lake in 2019 was assessed based on the species richness, abundance, biomass, and calculated indices of organic pollution and toxic impact. The statistical mapping, calculated community similarity, correlation, and Redundancy Analysis (RDA) revealed zones affected by human impact. These were located in the lake shores and low-alkaline water with the saprobity index of 1.63–2.00. This is typical for naturally clean lakes, indicating the oligotrophic-to-mesotrophic status of the lake during the study period. The increase in cyanobacteria species in coastal communities can be associated with an increase in the biogenic load on the lake ecosystem in recent times. Therefore, our multivariate analysis allowed us to assess the ecological state of Lake Borovoe, which can be the result of the interaction of many external environmental factors, such as climatic conditions, long-term accumulation of organic substances, the intensity and duration of anthropogenic press, and internal lake processes such as the development of algae communities. The results suggest a tendency for the eutrophication of Lake Borovoe to increase because of pollution coming from the human impact zones on the lake shores.

1. Introduction

The shallow Lake Borovoe is located on the Schuchinsk-Borovsk resort area in Northern Kazakhstan as a part of the territory of the National Natural Park “Burabay” [1]. International Union for Conservation of Nature and Natural Resources, IUCN [2], classified the Burabay wetlands as Category II—a national park that can be managed in a way that may contribute to local economies through promoting to educational and recreational tourism on a scale that will not reduce the effectiveness of conservation efforts. Lake Borovoe is not only the site most visited by tourists; it is also occupied by a few balneological resorts. The enrichment of the lake water with nutrients has been going on since the foundation of the first resort 100 years ago [3]. Increased anthropogenic pressure on the lake is causing serious problems in regard to the water quality. High abundances of phytoplankton and zooplankton in the lake in the last decades have been documented, along with the blooming of Cyanobacteria [4,5,6].
Phytoplankton and zooplankton communities in Lake Borovoe demonstrate high heterogeneity, but the species richness has not been regularly studied. Nevertheless, research into the algae in Lake Borovoe was started in 1947 by N. Voronikhin [7,8,9], and it continued sporadically up until 2013; only a few species were mentioned in the previous reports [6,10,11,12,13,14,15]. The monitoring of the protected waterbodies has started revealing the species richness of its communities. All monitoring programs usually included the research of biodiversity and quantitative variables of the biological part of ecosystem, as well as the definition of major environmental variables [16,17]. Assessing the water quality of the protected waterbody is also an important task to identify the main sources of its pollution [18,19]. Floristic studies in aquatic systems are very important because the flora are environmental indicators that can be used to infer the environmental impacts on the natural, climatic, and economic conditions of the Burabay National Natural Park, as was revealed during the hydrochemical and hydrobiological study of five other lakes in the park territory [20]. Studies of algae are of special interest since the formation of their floras occurs under conditions of water flowing from the catchment basin and thus represents an accumulative result of natural and anthropogenic conditions throughout the entire catchment area over many years. So, the first step for the monitoring program is the screening of major chemical and biological variables on the net of sampling stations on the lake surface. Despite the occasional hydrochemical and hydrobiological studies of Lake Borovoe, a comprehensive assessment of its ecological status has not been performed yet.
Statistical data mapping is an effective tool for solving this application problem [21,22]. The effectiveness of this method in monitoring studies of water bodies in Kazakhstan has been shown previously [23,24]. The mapping of environmental and biological variables helps to reveal human impact zones in aquatic objects, as well as the ecosystem damage by them.
The purpose of this work was to study the species composition, abundance, and biomass of phytoplankton in Lake Borovoe in the protected area of the Burabay National Natural Park. We hypothesized that the distribution of algae indicators over the surface of the lake and the comparison of it to environmental variables, using statistical methods can, for the first time for Northern Kazakhstan, show the zones and main factors of human impact on the shallow lake.

2. Materials and Methods

2.1. Description of Study Site

Lake Borovoe is located at an altitude of 315.0 m above sea level. Borovoe is separated from the nearby lakes by ridges 400–900 m high (Figure 1a). It has an almost circular shape. The maximum length of the lake is about 4 km, with a width of 3.27 km. It is a shallow lake with a maximum depth of about 5 m. Two bays are placed in the western part (Figure 1b). The catchment area is 164.0 km2. The east coast is sandy, sloping. The banks are overgrown with pine and birch. The Sary-Bulak River is inputted into the lake. The lake is fed by this small river, temporary streams, and precipitation. Only one small river, Kyrkyruek, flows from the lake. Sediments are represented by black silts. The coastal zone and northwestern bays are overgrown with Potamogeton lucens L. Macrophyte overgrowth is no more than 35–40% of the lake’s surface and shoreline. The bottom is overgrown with Charophyta algae, except for the central part of the lake [25]. The position of Northern Kazakhstan in the depths of the mainland causes a sharp continental climate. Its characteristic features are a long cold winter with strong winds and snowstorms, and a short but hot summer [20,26]. Average long-term temperatures of the coldest month of January are about −17.6 °C to −18.5 °C, with a minimum of −45.0 °C. In July, the air temperature reaches an average of +19.0 °C to +19.5 °C, with an absolute maximum of +41.0 °C. The average annual precipitation varies from 290–295 to 425–435 mm. The snow cover lasts for about 5 months, from November to March. The Lake Borovoe area has been a resort of national importance since 1920. The lake received conservation status in 2000 when the Burabay National Natural Park was created. The Borovoye village is located on the eastern shore of the lake, with numerous rest houses and balneological resorts. The two largest resorts are located on the southeast and northwest shores of the lake.

2.2. Sampling and Laboratory Analysis

The Lake Borovoe was examined in the summer season (29 July of 2019). It was the first trip with sampling and measurements that covered the entire lake’s surface as a screening stage for preliminary assessment for the purpose of monitoring. A total of eight sampling stations have been identified for the first time as monitoring sites on the surface of the lake. Coordinate referencing of the stations was performed by Garmin eTrex GPS-navigator. The temperature, Total Dissolved Solids (TDS), and pH values of the surface layers of water were measured in parallel with sampling with HANNA HI 9813-0, and N-NO3 with HANNA HI 93728 (HANNA Instruments, Vensokit, RI, USA), with three repetitions. The transparency of the water was measured by using a Secchi disk.
Phytoplankton samples were taken from the surface water layers about 0–0.5 m into 1 L plastic containers [27], fixed in 3% neutral formaldehyde, and transported to the lab in an icebox. The sedimentary method was used to process phytoplankton samples, with the final volume of the concentrated sample being 5–10 mL [28,29]. Fixed phytoplankton samples were also studied in the lab in three repetitions, from wet and permanent slides [30], under light microscopes A Nikon ECLIPSE E200 (Nikon Instruments Inc., Melville, NY, USA) was used, with a magnification of ×100–×2000. Cells’ abundance was calculated in the Nageotte counting chamber (Hausser Scientific, Horsham, PA, USA). Wet biomass was calculated from the volume of the cell in mg L−1. Species identification was performed by using standard methods with relevant guides to the species identifications [31,32,33,34,35,36]. Modern taxonomy was adopted with [37].
The Shannon Diversity Index [38] was calculated with the Primer 6 program, using the following Formula (1):
H = − ∑ i = 1 n p i × l o g 2   p i      
where H is the Shannon Index (bits/ind.), pi is the share of the i-th species in the total abundance, log2 is the logarithm to base 2, n is the number of species in the sample, and ∑ is the sum of values for the sample.
Index saprobity S was calculated for each algal community, according to V. Sládeček [39], as a function of the number of saprobic species and their relative abundances (2):
S = ∑ i = 1 n ( s i h i ) / ∑ i = 1 n ( h i )
where S is the index of saprobity for algal community (unitless), s is species-specific saprobity index [40,41], and h is the cell density of each species, n is the number of species in the sample, and ∑ is the sum of values for the sample.
Bioindicator analysis was performed with species-specific ecological preferences of planktonic algae found at each sampling station [40,41,42] for revealing influencing external factors such as temperature, salinity, pH, oxygen conditions, organic pollution level, and trophic status of a water body.
Statistical maps [22] that reflect the probability of mapped variable distribution over the lake surface were built in the Statistica 12.0 Software based on the GPS coordinates of sampling points for each measured biological and chemical variable. Cluster analysis of the Bray–Curtis similarity of phytoplankton communities was carried out by using the Biodiversity-Pro program. A correlation analysis of the revealed data was carried out by using the JASP 0.16.4.0 program [43]. A heat map was constructed in the ExStatR program [44]. The linear ordination method Redundancy Detrended Analysis (RDA) was processed in the CANOCO 4.5 program in order to recognize the species–environment relationships [45].

3. Results

3.1. Environmental Characteristics of the Lake Borovoe

The lake was shallow, as can be seen in Appendix Table A1 and Figure 2c. During the study period, the temperature of the surface water reached 22.0–22.86 °C (Appendix Table A1) and was lowest in the central part of the lake (Figure 2b). The water was fresh, with a TDS of about 200 mg L−1, and highest ionic content was found in the central part of the lake (Figure 2a). The water was slightly alkaline, with a pH of about 8.3 and transparency of about 0.5–0.8 m (Figure 2d). So, major environmental variables can demonstrate the uniform condition in two parts of the Lake Borovoe surface—northwestern and southeastern parts—as represented in the maps in Figure 2a,b. The distribution of TDS and water temperature was controversial (R = –0.93, p = 0.001), especially in the central part with no correlations with the depth (p = 0.53) (Figure 2c). The water transparency was not correlated with temperature (p = 0.39), but visually, we can see a similar distribution near the wetlands of Station 3 and Borovoe village (Figure 2b,d).

3.2. Phytoplankton in the Lake Borovoe

Altogether, 72 algae and cyanobacteria taxa from seven taxonomic phyla were found in Lake Borovoe during the sampling period (Appendix Table A2). The diatom species was the richest, with 29 taxa, followed green algae, with 18, and cyanobacteria, with 15 taxa (Table 1). Species richness at sampling stations varies within a small range, from 21 to 29 taxa (Table 1). The lowermost species number was in Station 4, where water transparency was maximal (Figure 2d).
The Bray–Curtis similarity analysis divided the species richness into two clusters, the first of which included the three most species-rich phyla–diatoms, green algae, and cyanobacteria (Figure 3); the second cluster included four other phyla, which contained a small number of species (Table 1).
Phytoplankton species occupy the first level of the food pyramid and depend on the concentration of essential nutrients such as nitrate and phosphate. Thus, phytoplankton species are rich where nutrients can be available. We tried to reveal the relationship between phytoplankton species richness in sampling stations by using statistical methods to reveal some homogeneity of the lake environment. Figure 4 shows a graph of JASP analysis of the correlation of phytoplankton species number at sampling stations. At a similarity level of more than 50%, the graph divides the phytoplankton species richness into three groups. The most similar communities are at Stations 1, 2, and 6 (Group 1); 3 and 7 (Group 2); and 4, 5, and 8 (Group 3).
The averages of the parameter values (Table 2) were calculated to indicate the differences in the stations grouped in Figure 4. Group 1 includes Stations 1, 3, and 6, where, compared to other groups, there is less depth, transparency, TDS, and biomass, but higher water warming, which indicates not only the high ecosystem activity work of the lake, but also greater stress for phytoplankton, when the WESI index decreases. The second group of stations (Stations 3 and 7) is characterized by a higher abundance of phytoplankton, mainly at Station 7. Both stations are located near actively visited or populated lake shores. Group 3 consists of three stations (Stations 4, 5, and 8) that are deeper, transparent, cool, mineralized, and alkaline, where there are fewer nitrates, and the WESI index was higher. The stations of Group 3 are located closer to the middle of the lake and are the most remote from anthropogenic influence.
Therefore, to understand the importance of species dynamics at the phylum level, we constructed statistical maps for each taxa distribution in the sampling stations. Figure 5a shows that the total number of species was minimal at Station 4, which had the highest water transparency and temperature, as well as lower TDS values (Appendix Table A1). Figure 5b shows that the total number of phytoplankton species was determined by the number of green algae species that take a part of its composition. The distribution of diatoms is inversely relative to the distribution of green algae (Figure 5c). Cyanobacteria are most represented offshore, where the water temperature and anthropogenic load were higher, and the TDS was lower (Figure 5d). Euglenoids were mainly in the central part (Figure 5e), but charophyte planktonic species were concentrated in the northwestern bay of the lake (Figure 5f).
Spatial maps of phytoplankton abundance and biomass show an opposite distribution (Figure 6a,b). The abundance of phytoplankton was greatest where an influx of nitrates was found (Figure 6c). At the same time, the distribution of the WESI index (Figure 6d), which shows stress zones for algae, outlines the entire coast, including the points of nitrate inflow, as vulnerable, and the middle of the lake as the most preferable.

3.3. Phytoplankton Indicators of Water Quality

The bioindication results on the basis of phytoplankton species’ ecological preferences (Appendix Table A2) are represented in Appendix Table A3 and visualized in Figure 7. Even though the indicator values for stations represent a mosaic, it is possible to single out the main characteristic groups: Bacillariophyta and Chlorophyta species, planktonic and plankto-benthic inhabitants, and middle oxygenated water indicators of Class 3 of water quality.
An RDA triplot was constructed on the base of environmental data (Appendix Table A1) and species richness in phyla (Table 1). Figure 8 shows that nitrate-nitrogen-stimulated Charophyta and Cyanobacteria grow in the waters of Stations 1 and 8 with less transparency (Figure 2d) and depth (Figure 2c). Diatom, green algae, and euglenoids were diverse in Stations 5, 6, and 7, where there was the highest TDS (Figure 2a) and total species richness (Figure 5a,b). Miozoa species (Ceratium hirundinella) were richest in Stations 2 and 3, which had highest temperature (Figure 2b) and lowest TDS (Figure 2a).

4. Discussion

Northern Kazakhstan abounds in shallow lakes, most of which are objects of WWF protection, as they are located on the migratory routes of birds [46]. Therefore, it is especially important not only to identify the diversity of organisms at protected sites, but also to determine the main influencing anthropogenic or natural factors. Algae, as the first level of the trophic pyramid, are the first to respond to changes in the lake’s ecosystem, with the most noticeable impact on the example of phytoplankton [47]. Phytoplankton in the lakes of Northern Kazakhstan, including Lake Borovoe, has been studied sporadically [6,7,8,9,10,11,12,13,14,15]. In connection with the projects of the WWF on the status of protection, we undertook a large-scale study of phytoplankton during 1999–2000 in 34 North Kazakhstan lakes that have a conservation status or are under preparation [48]; with the help of bioindication and statistical analysis, it was possible to identify the main factor affecting the diversity of communities in the lakes of this region, i.e., salinity [49]. A subsequent comparison with lakes of similar size in the semi-arid climate zone in the Eastern Mediterranean not only confirmed the conclusion made, but also expanded the understanding of the importance of using bioindication to identify the main factors affecting phytoplankton [48]. The mentioned studies on protected lakes have shown that salinity is a regional natural factor related to climate. Our studies at Lake Borovoe also revealed a close inverse relationship between temperature and TDS (p = 0.001). A study of phytoplankton in the nearby Lake Zerenda showed that, for lakes whose shores are visited by tourists, the anthropogenic factor is the influx of nitrates [50]. At the same time, nitrates in all the studied lakes of Northern Kazakhstan turned out to be a factor stimulating the diversity of algae, and in Lake Borovoe, also its abundance and biomass. Thus, saprobity indices were higher where nitrate concentrations were higher [48]. Lake Borovoe, where the saprobity indices were in the range of 1.52–2.00, is comparable with freshwater lakes in terms of this indicator and the number of species in the community.
Our calculations of the index toxicity WESI were comparable with its values in the lakes of Northern Kazakhstan for those lakes where salinity (TDS) was higher, which indicates a long history of evaporation and a small inflow of surface water, that is, the natural state of the lakes [48]. For Lake Borovoe, the WESI index was higher (better condition) in the center of the lake, away from coastal pollution, where TDS is higher and water temperature is lower. This distribution shows that the phytoplankton of the lake was affected by organic pollution coming from the shore zone, which does not reach the center of the lake. Therefore, the lake retains sufficient self-purification capacity.
The spatial distribution of phytoplankton suggests that the lake water is influenced by pollution of the communal services of the Borovoye village and two resorts (Figure 1). The main contribution of the village is associated not only with wastewater discharges but also with surface runoff from the beach area along all east coasts. As can be seen from Figure 2d and Figure 5, in the eastern and southeastern parts of the water surface, the signs of eutrophication of the lake can be recognized. Here, the high species richness of phytoplankton due to Chlorophyta taxa was recorded, as well as minimum values of water transparency and maximal value of TDS show that phytoplankton communities are formed under the conditions of a constant influx of fresh nutrients. As is known, the number of phytoplankton species decreases with an increase in their abundance and biomass [16], which we observe on spatial statistical maps for Lake Borovoe.
The spatial distribution of phytoplankton and environmental parameters in the lakes of Northern Kazakhstan were studied for the first time on Lake Borovoe. However, for more southerly lakes, this method has been applied with effective results. For a fairly large regional lake Balkhash, the zones of influence of both climatic (salinity) and anthropogenic (organic pollution) factors were clearly shown, using statistical mapping [51]. The phytoplankton of smaller lakes in Kazakhstan revealed the anthropogenic factor of organic pollution coming with the tourist flow to the lakes of the Kolsay cascade [52] or with runoff from fields and inflow to the Shardara reservoir [53]. Thus, statistical mapping, statistical methods, and bioindication can serve together as effective tools for identifying factors and zones of natural and anthropogenic impact in this region.
According to the results of the analysis of the main environmental variables in the summer of 2019 (Table 1), the water of Lake Borovoe can be assessed as fresh and low alkaline, corresponding to the level of clean, slightly polluted waters of Classes 2 and 3 of water quality [39]. This may be due to historically low nutrient content [4,6], even during the period of fish mortality in 1974 [3]. It is known that the best period for studying phytoplankton is the middle of summer, as in our case, when all processes in the lake give the maximum diversity and biomass of plankton communities [52,53,54]. The total species richness of phytoplankton in Lake Borovoe is currently determined mainly by the number of Chlorophyta species. This and phytoplankton abundance and biomass are typical for naturally clean lakes and may indicate the oligotrophic status of the lake during the study period. At the same time, the increase in cyanobacteria species in coastal communities may be associated with an increase in the biogenic load on the lake ecosystem in recent times [1]. The analysis shows that pollutants entering the lake water are associated with villages and resort areas located on the coast. However, they are utilized by algae almost completely, which can be seen in the distribution of pollution indices, showing cleaner water in the middle of the lake.
The phytoplankton is a part of total autotrophic organisms that, together with macrophytes, settled the lake and therefore can use only part of the total value of nutrient inflow to the lake. Since the IUCN protected Charophyte species [55] grow in the coastal area, it is important to monitor water quality and the state of their populations during monitoring, since the disappearance of charophytes will indicate the loss of a protected object in the IUCN system. The Lake Borovoe shores are inhabited by five species of Chara, Nitellopsis obtusa, and Nitella flexilis [25]. There is a unique diversity of charophytes in this one lake. Therefore, the role of macrophytes and charophytes in the trophic condition of the lake is very important. The anthropogenic load may be one of the reasons for the eutrophication of Lake Borovoe, leading to degradation of the macrophyte communities. The Lake Fund monitoring showed that macrophytes occupied 65–80% of the bottom surface in 1964–2002 [3], while their density had decreased to approximately 30–35% by 2019. Therefore, a decrease in the role of macrophytes consuming nutrients [56] has created favorable conditions for planktonic algae [19] and caused changes in the trophic conditions of the lake.
The differences in environmental and biological variables distribution were revealed with the help of statistical mapping, even in the case of low amplitude of variables [21], as in Lake Borovoe. The preliminary hydrochemical and hydrobiological assessment of the lakes of the Shchuchinsko-Borovsk resort zone [20] confirm that this approach can be recommended in the monitoring of different protected lakes’ sustainability.

5. Conclusions

Our study showed that the ecological state of Lake Borovoe can be the result of the interaction of many environmental factors, such as climatic conditions, long-term accumulation of organic matter, the intensity and duration of anthropogenic pressure, as well as intralake processes, such as the development of a community of macrophytes, algae, and invertebrates. An assessment of the phytoplankton communities showed a trend towards an increase in eutrophication of the lake, as revealed during statistical mapping, because of organic pollution from populated and resort areas. The assessment of water quality by the bioindication of plankton species revealed weakly alkaline and slightly organically polluted water of Classes 2 and 3. With the help of indications and statistics, the salinity was determined as a climatic factor and organic pollution as an anthropogenic factor affecting the ecosystem of Lake Borovoe. Thus, the indication of phytoplankton and environmental parameters in Lake Borovoe reflect the state of the lake as oligotrophic with a transition to the mesotrophic stage, subject to organic pollution in the coastal part, but coping with anthropogenic impact.

Author Contributions

Conceptualization, S.B. (Sophia Barinova) and E.K. (Elena Krupa); methodology, S.B.; software, S.B.; validation, S.B., E.K. (Elena Krupa), and E.K. (Elena Khitrova); formal analysis, E.K. (Elena Khitrova) and S.B.; investigation, E.K. (Elena Krupa); resources, E.K. (Elena Krupa); data curation, S.B. and E.K. (Elena Khitrova); writing—original draft preparation, S.B. and E.K. (Elena Krupa); writing—review and editing, S.B.; visualization, S.B.; supervision, E.K. (Elena Krupa); project administration, E.K. (Elena Krupa). All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

The work was carried out under project No. BR05236529 for the Committee of Science, Ministry of Education and Science, Republic of Kazakhstan, “A comprehensive assessment of the ecosystems of the Shchuchinsko-Borovsk resort area with the determination of the environmental load for the sustainable use of the recreational potential”, as well as partly supported by the Israeli Ministry of Aliyah and Integration.

Conflicts of Interest

The authors declare no conflict of interest.

Appendix A

Table
Table A1. Averaged environmental variables with standard deviation and coordinates of sampling stations on the Lake Borovoe, 2019.
Table A1. Averaged environmental variables with standard deviation and coordinates of sampling stations on the Lake Borovoe, 2019.
Station12345678Average
North53.0815253.0832153.0818653.0755753.0746753.0751253.0674853.06682
East70.2561370.2699570.2852970.2641670.2759670.2901470.2686470.28679
Depth, m3.92 ± 0.065.06 ± 0.054.55 ± 0.064.25 ± 0.064.85 ± 0.043.4 ± 0.023.89 ± 0.043.53 ± 0.024.18
Secchi, m0.5 ± 0.090.6 ± 0.090.7 ± 0.080.8 ± 0.060.6 ± 0.050.6 ± 0.050.6 ± 0.050.6 ± 0.060.63
T °C22.61 ± 0.622.92 ± 0.522.86 ± 0.622.8 ± 0.621.3 ± 0.521.8 ± 0.522 ± 0.321.9 ± 0.522.27
pH8.17 ± 0.018.16 ± 0.018.18 ± 0.028.16 ± 0.028.43 ± 0.018.19 ± 0.018.16 ± 0.018.12 ± 0.018.20
TDS, mg L−1180 ± 11.51180.8 ± 11.2182.2 ± 10.8183.8 ± 9.58207.8 ± 11.0204.6 ± 10.0201.4 ± 9.56191.7 ± 9.12191.5
N-NO3, mg L−10.816 ± 0.320.599 ± 0.120.700 ± 0.240.090 ± 0.010.000 ± 0.00.272 ± 0.020.466 ± 0.100.039 ± 0.010.373
Index S1.82 ± 0.181.98 ± 0.151.77 ± 0.171.94 ± 0.181.99 ± 0.161.63 ± 0.132.00 ± 0.201.52 ± 0.111.83
Index WESI1.001.001.002.004.001.331.334.001.96
Abundance, cells L−12982.9 ± 193.33026.5 ± 220.73238.9 ± 245.92642.7 ± 222.82226.9 ± 137.91540.2 ± 80.15968.4 ± 575.02474.3 ± 141.53012.6
Biomass mg L−11403.2 ± 78.44086.6 ± 270.04087.5 ± 215.02044.2 ± 95.61732.5 ± 101.6772.5 ± 38.82386.8 ± 129.92554 ± 149.02383.4
Shannon Index0.753 ± 0.170.614 ± 0.150.659 ± 0.140.552 ± 0.110.797 ± 0.170.885 ± 0.180.401 ± 0.100.864 ± 0.160.691
Table
Table A2. Diversity of algae and cyanobacteria on the sampling stations (1–8) of the Lake Borovoe, 2019. Abbreviations: Hab, substrate preferences: B, benthic; P-B, plankto-benthic; and P, planktonic. T, temperature indicators: temp, inhabitants of temperate-temperature waters; and eterm, eurythermic. Oxy, Dissolved oxygen and water mobility indicators: str, inhabitants of streaming well-oxygenated waters; st-str, inhabitants of standing to streaming middle-oxygenated waters; st, inhabitants of standing low-oxygenated waters; H2S, sulfides anoxia indicators. pH, water acidity indicators: acf, acidophilic; ind, pH indifferent; alf, alkaliphilic; alb, alkalibiontes. Sal, salinity indicators: i, chlorides indifferent; hl, halophiles; mh, mesohalobes; oh, broad spectrum oligohalobes. D, Watanabe diatom indicators for organic pollution: sx, saproxenes; es, eurysaprobes; sp, saprophiles. Sap, saprobity indicator categories with species-specific index S: b-a, 2.4–beta-alpha-mesosaprobiont; b-o, 1.6–beta-oligosaprobiont; o, 1.0–oligosaprobiont; o-a, 1.8–oligo-alpha-mesosaprobiont; o-b, 1.4–oligo-beta-mesosaprobiont; o-x, 0.6–oligo-xenosaprobiont; x, 0.0–xenosaprobiont; x-b, 0.8–xeno-beta-mesosaprobiont; x-o, 0.4–xeno-oligosaprobiont. Index S, species-specific index saprobity S. Tro, trophic-state indicators: o, oligotraphentes; o-m, oligo-mesotraphentes; m, mesotraphentes; me, meso-eutraphentes; e, eutraphentes; o-e, oligotraphentes to eutraphentes. Aut-Het, indicators of autotrophy-heterotrophy nutrition type: ats, autotrophes-inhabited low-nitric-nitrogen waters; ate, autotrophes-inhabited high-nitric-nitrogen waters; hne, facultative-heterotrophes-inhabited low organically enriched waters; “-”, no data.
Table A2. Diversity of algae and cyanobacteria on the sampling stations (1–8) of the Lake Borovoe, 2019. Abbreviations: Hab, substrate preferences: B, benthic; P-B, plankto-benthic; and P, planktonic. T, temperature indicators: temp, inhabitants of temperate-temperature waters; and eterm, eurythermic. Oxy, Dissolved oxygen and water mobility indicators: str, inhabitants of streaming well-oxygenated waters; st-str, inhabitants of standing to streaming middle-oxygenated waters; st, inhabitants of standing low-oxygenated waters; H2S, sulfides anoxia indicators. pH, water acidity indicators: acf, acidophilic; ind, pH indifferent; alf, alkaliphilic; alb, alkalibiontes. Sal, salinity indicators: i, chlorides indifferent; hl, halophiles; mh, mesohalobes; oh, broad spectrum oligohalobes. D, Watanabe diatom indicators for organic pollution: sx, saproxenes; es, eurysaprobes; sp, saprophiles. Sap, saprobity indicator categories with species-specific index S: b-a, 2.4–beta-alpha-mesosaprobiont; b-o, 1.6–beta-oligosaprobiont; o, 1.0–oligosaprobiont; o-a, 1.8–oligo-alpha-mesosaprobiont; o-b, 1.4–oligo-beta-mesosaprobiont; o-x, 0.6–oligo-xenosaprobiont; x, 0.0–xenosaprobiont; x-b, 0.8–xeno-beta-mesosaprobiont; x-o, 0.4–xeno-oligosaprobiont. Index S, species-specific index saprobity S. Tro, trophic-state indicators: o, oligotraphentes; o-m, oligo-mesotraphentes; m, mesotraphentes; me, meso-eutraphentes; e, eutraphentes; o-e, oligotraphentes to eutraphentes. Aut-Het, indicators of autotrophy-heterotrophy nutrition type: ats, autotrophes-inhabited low-nitric-nitrogen waters; ate, autotrophes-inhabited high-nitric-nitrogen waters; hne, facultative-heterotrophes-inhabited low organically enriched waters; “-”, no data.
Taxa12345678HabTOxypHSalDSapIndex STroAut-Het
Cyanobacteria
Anabaena contorta Bachmann00000100P-st-str-------
Anagnostidinema amphibium (C. Agardh ex Gomont) Strunecký, Bohunická, J.R. Johansen and J. Komárek10000000P-B, S-st-str, H2S-hl-a-o2.6m-
Anathece clathrata (West and G.S. West) Komárek, Kastovsky and Jezberová11111111P---hl-o-a1.8me-
Aphanocapsa holsatica (Lemmermann) G. Cronberg and Komárek00100000P---i-o-b1.4me-
Aphanocapsa incerta (Lemmermann) G. Cronberg and Komárek00000110P-B---i-b2.2me-
Aphanocapsa planctonica (G.M. Smith) Komárek and Anagnostidis11100100P---i---o-
Chroococcus minimus (Keissler) Lemmermann10000000P-B---hl---o-m-
Chroococcus minutus (Kützing) Nägeli00011000P-B--indi-o-a1.8o-m-
Merismopedia tenuissima Lemmermann10000000P-B---hl-b-a2.4e-
Microcystis aeruginosa (Kützing) Kützing11111111P---hl-b2.1e-
Planktolyngbya contorta (Lemmermann) Anagnostidis and Komárek00100000P-----o-a1.8me-
Planktolyngbya limnetica (Lemmermann) Komárková-Legnerová and Cronberg11010000P-B, S-st-str-hl-o-b1.5e-
Radiocystis geminata Skuja10101011P-------me-
Rhabdoderma lineare Schmidle and Lauterborn00000111P-----b2.2--
Snowella atomus Komárek and Hindák00111111P-------me-
Bacillariophyta
Achnanthidium minutissimum (Kützing) Czarnecki00000100P-Betermst-strindiesx-b0.95o-eate
Amphora ovalis (Kützing) Kützing00010000Btempst-stralfisxo-b1.5meate
Aulacoseira granulata (Ehrenberg) Simonsen11010000P-Btempst-strindiesb2meate
Caloneis bacillum (Grunow) Cleve00011000Btempst-strindieso1.3meats
Cyclotella meneghiniana Kützing01101010P-Btempstalfhlspa-o2.8ehne
Cymbella cistula (Ehrenberg) O. Kirchner00001000B-st-stralfisxo1.2eats
Cymbella helvetica Kützing00000100B-strindi-o-x0.6o-m-
Diatoma vulgaris Bory00100000P-B-st-strindisxb2.2meate
Discostella stelligera (Cleve and Grunow) Houk and Klee11111111P--indi-o-b1.4o-m-
Epithemia adnata (Kützing) Brébisson00000001Btempstalbisxo1.2meats
Eunotia arcus Ehrenberg00010000B-st-stracfi-x-o0.5otats
Fragilaria capucina Desmazières01000000P-B--indiesb-o1.6m-
Fragilaria radians (Kützing) D.M.Williams and Round11111111P-B-st-stralfisxb-o1.7o-m-
Gomphonella olivacea (Hornemann) Rabenhorst01111111B-st-stralfieso-b1.45eate
Gomphonema acuminatum Ehrenberg10000000B-stindieso-b1.4o-mats
Eunotia arcus Ehrenberg00010000B-st-stracfi-x-o0.5otats
Fragilaria capucina Desmazières01000000P-B--indiesb-o1.6m-
Fragilaria radians (Kützing) D.M. Williams and Round11111111P-B-st-stralfisxb-o1.7o-m-
Gomphonella olivacea (Hornemann) Rabenhorst01111111B-st-stralfieso-b1.45eate
Gomphonema acuminatum Ehrenberg10000000B-stindieso-b1.4o-mats
Gomphonema gracile Ehrenberg01000000Btempstalfiesx-b0.8mats
Gyrosigma strigilis (W. Smith) J.W. Griffin and Henfrey00100000B---mh-----
Halamphora veneta (Kützing) Levkov00010100B-st-stralfiesa-o2.6eate
Lindavia comta (Kützing) Nakov, Gullory, Julius, Theriot, and Alverson01000100P-stalfisxo1.2o-m-
Melosira varians C.Agardh11111111P-Btempst-strindhlesb2.1mehne
Pauliella taeniata (Grunow) Round and Basson00001010B--alfmh-b2.0--
Pinnularia viridis (Nitzsch) Ehrenberg00000010P-Btempst-strindiesx0.3o-eate
Sellaphora pupula (Kützing) Mereschkovsky00000001Betermstindhlsxo-a1.9meate
Staurosira leptostauron (Ehrenberg) Kulikovskiy and Genkal00000100 ------1.1--
Stephanodiscus hantzschii Grunow10111111Ptempstalfiesa-o2.7o-mhne
Surirella elegans Ehrenberg01000000P-B-stralfi-o1me-
Ulnaria acus (Kützing) Aboal10000100P-B-st-stralfieso-a1.85o-m-
Ulnaria amphirhynchus (Ehrenberg) Compère and Bukhtiyarova01000000P-B--alfiesb2o-m-
Ulnaria capitata (Ehrenberg) Compère00000010P-B-st-stralfieso-b1.5eats
Euglenozoa
Lepocinclis ovum (Ehrenberg) Lemmermann00011011Petermstindi-b-a2.4--
Trachelomonas hispida (Perty) F.Stein00101000P-Betermst-str-i-b2.2--
Miozoa
Ceratium hirundinella (O.F. Müller) Dujardin11101111P-st-str-i-o1.3--
Gymnodinium variabile E.C. Herdman00000010P-----o-b1.5--
Naiadinium polonicum (Woloszynska) Carty01110001P-st---o1.3--
Peridinium bipes F. Stein00000001P-st-str-oh-o1.3--
Peridinium cinctum (O.F. Müller) Ehrenberg00100000P-B-st-str-i-b-o1.6--
Ochrophyta
Dinobryon divergens O.E. Imhof11111111P-st-strindi-o-b1.45--
Chlorophyta
Binuclearia lauterbornii (Schmidle) Proschkina-Lavrenko10000000------o-a1.8-
Chlorella vulgaris Beyerinck [Beijerinck]11101111P-B, pb,S---hl-a3.1-
Desmodesmus brasiliensis (Bohlin) E.Hegewald00001111P-B-st-str---b2-
Monoraphidium contortum (Thuret) Komárková-Legnerová10100000P-B-st-str-i-b2.2-
Monoraphidium convolutum (Corda) Komárková-Legnerová00000101P-B-st-str---b2.3-
Monoraphidium minutum (Nägeli) Komárková-Legnerová00000001P-B-st-str-i-b-a2.5-
Mucidosphaerium pulchellum (H.C. Wood) C.Bock, Proschold and Krienitz00001000P-B-st-strindi-b2.3-
Myrmecia irregularis (J.B. Petersen) Ettl and Gärtner10101111P---oh----
Neglectella solitaria (Wittrock) Stenclová and Kastovsky00101000P-stindi-b-o1.7-
Oocystis borgei J.W. Snow01000000P-B-st-strindi-o-a1.9-
Oocystis pusilla Hansgirg00000011P---oh-o-b1.4-
Pseudodidymocystis planctonica (Korshikov) E.Hegewald and Deason01000110------o-a1.8-
Scenedesmus quadricauda (Turpin) Brébisson11011111P--indi-b2.1-
Schroederia setigera (Schröder) Lemmermann10000000P-st-str-i-b-o1.7-
Tetradesmus obliquus (Turpin) M.J.Wynne01101011P-B, S-st-i-b-a2.4-
Tetraëdron minimum (A. Braun) Hansgirg11110111P-B-st-str-i-b2.1-
Tetraëdron minutissimum Korshikov00101001P-B-st-str-i-b2.1-
Tetrastrum staurogeniiforme (Schröder) Lemmermann00000100P-B-st-str-i-b2.2-
Charophyta
Cosmarium baileyi Wolle11111111B-----o1.2--
Cosmarium undulatum Corda ex Ralfs10000000P-B--acfi---m-
Table
Table A3. Distribution of species richness in phyla, total species number in community, and ecological properties of bioindicators for sampling stations on Lake Borovoe, 2019. Abbreviations: B, benthic; P-B, plankto-benthic; P, planktonic; temp, inhabitants of temperate-temperature waters; eterm, eurythermic; str, inhabitants of streaming well-oxygenated waters; st-str, inhabitants of standing to streaming middle-oxygenated waters; st, inhabitants of standing low oxygenated waters; H2S, sulfides anoxia indicators; acf, acidophilic; ind, pH-indifferent; alf, alkaliphilic; alb, alkalibiontes; i, chlorides indifferents; hl, halophiles; mh, mesohalobes; sx, saproxenes; es, eurysaprobes; sp, saprophiles; Classes 1–4 of water-quality indicators according to Index S; o, oligotraphentes; o-m, oligo-mesotraphentes; m, mesotraphentes; me, meso-eutraphentes; e, eutraphentes; o-e, oligotraphentes to eutraphentes; ats, autotrophes-inhabited low-nitric-nitrogen waters; ate, autotrophes-inhabited high-nitric-nitrogen waters; hne, facultative-heterotrophes-inhabited low organically enriched waters.
Table A3. Distribution of species richness in phyla, total species number in community, and ecological properties of bioindicators for sampling stations on Lake Borovoe, 2019. Abbreviations: B, benthic; P-B, plankto-benthic; P, planktonic; temp, inhabitants of temperate-temperature waters; eterm, eurythermic; str, inhabitants of streaming well-oxygenated waters; st-str, inhabitants of standing to streaming middle-oxygenated waters; st, inhabitants of standing low oxygenated waters; H2S, sulfides anoxia indicators; acf, acidophilic; ind, pH-indifferent; alf, alkaliphilic; alb, alkalibiontes; i, chlorides indifferents; hl, halophiles; mh, mesohalobes; sx, saproxenes; es, eurysaprobes; sp, saprophiles; Classes 1–4 of water-quality indicators according to Index S; o, oligotraphentes; o-m, oligo-mesotraphentes; m, mesotraphentes; me, meso-eutraphentes; e, eutraphentes; o-e, oligotraphentes to eutraphentes; ats, autotrophes-inhabited low-nitric-nitrogen waters; ate, autotrophes-inhabited high-nitric-nitrogen waters; hne, facultative-heterotrophes-inhabited low organically enriched waters.
Station12345678
Species richness in phyla
Bacillariophyta71181091197
Chlorophyta767288810
Charophyta21111111
Cyanobacteria84755765
Euglenozoa00112011
Miozoa12311123
Ochrophyta11111111
Total Species number2625282127292828
Substrate
B23365434
P-B121296109109
P11914912131415
Temperature
temp34354243
eterm00112112
Water moving and oxygenation
str01000100
st-str10911111113911
st25535246
H2S10000000
pH
acf10010000
ind67589666
alf37456663
alb00000001
Salinity
i1516171417171516
hl86545455
mh00101010
Watanabe
sx12222213
es56364653
sp01101010
Class of water quality based on species-specific index saprobity S
Class 100010010
Class 2610787989
Class 3121213914131314
Class 432233332
Trophic state
o11110100
o-m64344633
m22000000
me44765456
e34344342
o-e00000110
Autotrophy–heterotrophy
ats11022011
ate12241322
hne22323232

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Figure 1. Map of study site on Lake Borovoe, Northern Kazakhstan, in July of 2019. Position of Lake Borovoe in Kazakhstan (a). Position of the phytoplankton sampling stations 1–8 on the lake surface (b). Map creating in ESRI ArcGIS 10.8. USA program on the base of our measurements of GIS coordinates and the lake depth on each sampling station.
Figure 1. Map of study site on Lake Borovoe, Northern Kazakhstan, in July of 2019. Position of Lake Borovoe in Kazakhstan (a). Position of the phytoplankton sampling stations 1–8 on the lake surface (b). Map creating in ESRI ArcGIS 10.8. USA program on the base of our measurements of GIS coordinates and the lake depth on each sampling station.
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Figure 2. Distribution of major environmental variables in the sampling stations of Lake Borovoe’s surface, 2019. TDS (a), water temperature (b), lake depth (c), and transparency by Secchi disk (d).
Figure 2. Distribution of major environmental variables in the sampling stations of Lake Borovoe’s surface, 2019. TDS (a), water temperature (b), lake depth (c), and transparency by Secchi disk (d).
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Figure 3. Cluster dendrogram of phytoplankton community species richness in the Lake Borovoe, 2019.
Figure 3. Cluster dendrogram of phytoplankton community species richness in the Lake Borovoe, 2019.
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Figure 4. JASP correlation plot of the phytoplankton species richness in Lake Borovoe, 2019. Bold line shows largest similarity on type of analysis, “Huge” correlation > 0.5.
Figure 4. JASP correlation plot of the phytoplankton species richness in Lake Borovoe, 2019. Bold line shows largest similarity on type of analysis, “Huge” correlation > 0.5.
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Figure 5. Statistical maps of distribution of phyla species richness in phytoplankton communities on the sampling stations of the Lake Borovoe surface, 2019. Total species richness (a), Chlorophyta (b), Bacillariophyta (c), Cyanobacteria (d), Euglenozoa (e), and Charophyta (f).
Figure 5. Statistical maps of distribution of phyla species richness in phytoplankton communities on the sampling stations of the Lake Borovoe surface, 2019. Total species richness (a), Chlorophyta (b), Bacillariophyta (c), Cyanobacteria (d), Euglenozoa (e), and Charophyta (f).
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Figure 6. Maps of the surface phytoplankton abundance (a), biomass (b), nitrates (c), and WESI index (d) in Lake Borovoe, summer 2019.
Figure 6. Maps of the surface phytoplankton abundance (a), biomass (b), nitrates (c), and WESI index (d) in Lake Borovoe, summer 2019.
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Figure 7. Heat map for distribution of indicators in phytoplankton communities over the sampling stations at Lake Borovoe, 2019. Abbreviations: Bacil, Bacillariophyta; Chlor, Chlorophyta; Cyano, Cyanobacteria; Eugle, Euglenozoa; Mioz, Miozoa; Ochro, Ochrophyta; B, benthic; P-B, plankto-benthic; P, planktonic; temp, inhabitants of temperate-temperature waters; eterm, eurythermic; str, streaming well-oxygenated waters inhabitants; st-str, inhabitants of standing to streaming middle-oxygenated waters; st, inhabitants of standing low-oxygenated waters; H2S, sulfides anoxia indicators; acf, acidophilic; ind, pH indifferent; alf, alkaliphilic; alb, alkalibiontes; i, chlorides indifferent; hl, halophiles; mh, mesohalobes; sx, saproxenes; es, eurysaprobes; sp, saprophiles; Classes 1–4 of water-quality indicators according to Index S; o, oligotraphentes; o-m, oligo-mesotraphentes; m, mesotraphentes; me, meso-eutraphentes; e, eutraphentes; o-e, oligotraphentes to eutraphentes; ats, autotrophes-inhabited low-nitric-nitrogen waters; ate, autotrophes-inhabited high-nitric-nitrogen waters; hne, facultative-heterotrophes-inhabited low organically enriched waters. In the x-axis are station numbers, and in the y-axis are the same abbreviations as in Appendix Table A3. The color of the cells varies from white to blue and then to red, according to the proportion of the number in the entire distribution.
Figure 7. Heat map for distribution of indicators in phytoplankton communities over the sampling stations at Lake Borovoe, 2019. Abbreviations: Bacil, Bacillariophyta; Chlor, Chlorophyta; Cyano, Cyanobacteria; Eugle, Euglenozoa; Mioz, Miozoa; Ochro, Ochrophyta; B, benthic; P-B, plankto-benthic; P, planktonic; temp, inhabitants of temperate-temperature waters; eterm, eurythermic; str, streaming well-oxygenated waters inhabitants; st-str, inhabitants of standing to streaming middle-oxygenated waters; st, inhabitants of standing low-oxygenated waters; H2S, sulfides anoxia indicators; acf, acidophilic; ind, pH indifferent; alf, alkaliphilic; alb, alkalibiontes; i, chlorides indifferent; hl, halophiles; mh, mesohalobes; sx, saproxenes; es, eurysaprobes; sp, saprophiles; Classes 1–4 of water-quality indicators according to Index S; o, oligotraphentes; o-m, oligo-mesotraphentes; m, mesotraphentes; me, meso-eutraphentes; e, eutraphentes; o-e, oligotraphentes to eutraphentes; ats, autotrophes-inhabited low-nitric-nitrogen waters; ate, autotrophes-inhabited high-nitric-nitrogen waters; hne, facultative-heterotrophes-inhabited low organically enriched waters. In the x-axis are station numbers, and in the y-axis are the same abbreviations as in Appendix Table A3. The color of the cells varies from white to blue and then to red, according to the proportion of the number in the entire distribution.
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Figure 8. RDA plot of the relationships between environmental variables: temperature, nitrates-nitrogen concentration, TDS, depth, and species richness in phyla of phytoplankton in the Lake Borovoe, 2019. Monte Carlo test summary for 945 permutations: eigenvalue = 0.421; p-value = 0.136.
Figure 8. RDA plot of the relationships between environmental variables: temperature, nitrates-nitrogen concentration, TDS, depth, and species richness in phyla of phytoplankton in the Lake Borovoe, 2019. Monte Carlo test summary for 945 permutations: eigenvalue = 0.421; p-value = 0.136.
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Table
Table 1. Species richness of phytoplanktonic algae and cyanobacteria in Lake Borovoe, summer 2019.
Table 1. Species richness of phytoplanktonic algae and cyanobacteria in Lake Borovoe, summer 2019.
Phylum12345678Percent
Bacillariophyta7118109119740
Chlorophyta76728881025
Cyanobacteria8475576521
Euglenozoa001120113
Miozoa123111237
Ochrophyta111111111
Charophyta211111113
Total2625282127292828100
Table
Table 2. Distribution of averaged environmental and biological variables of phytoplankton over groups of stations in Figure 4.
Table 2. Distribution of averaged environmental and biological variables of phytoplankton over groups of stations in Figure 4.
Station Group123
Depth, m4.134.224.21
Secchi, m0.570.650.67
T, °C22.4422.4322.00
pH8.178.178.24
TDS, mg L−1188.47191.80194.43
N-NO3, mg L−10.560.580.04
Index S1.811.891.81
Index WESI1.111.173.33
Abundance, cells L−12516.54603.72448.0
Biomass mg L−12087.43237.22110.2
Shannon Index0.7510.5300.738
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Barinova, S.; Krupa, E.; Khitrova, E. Spatial Distribution of the Taxonomic Diversity of Phytoplankton and Bioindication of the Shallow Protected Lake Borovoe in the Burabay National Natural Park, Northern Kazakhstan. Diversity 2022, 14, 1071. https://doi.org/10.3390/d14121071

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Barinova S, Krupa E, Khitrova E. Spatial Distribution of the Taxonomic Diversity of Phytoplankton and Bioindication of the Shallow Protected Lake Borovoe in the Burabay National Natural Park, Northern Kazakhstan. Diversity. 2022; 14(12):1071. https://doi.org/10.3390/d14121071

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Barinova, Sophia, Elena Krupa, and Elena Khitrova. 2022. "Spatial Distribution of the Taxonomic Diversity of Phytoplankton and Bioindication of the Shallow Protected Lake Borovoe in the Burabay National Natural Park, Northern Kazakhstan" Diversity 14, no. 12: 1071. https://doi.org/10.3390/d14121071

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