Dominant species and functional complexes of phytoplankton in some unique karst lakes of the Middle Volga basin

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1. Introduction

Karst lakes are widespread and often unique water bodies in landscapes of different natural zones, characterized by peculiarities of morphometric parameters and the specificity of the hydrological and hydrochemical regime of the waters, which determine the originality of the faunistic and floristic composition of the hydrobionts inhabiting them (Ryanzhin, 2002; Ciorca et al., 2017).

Lakes of this type are often characterized by small sizes, relatively high depths, and the absence of pronounced hydrodynamics of water with frequent stratification (Maksimovich, 1963; Krevs and Kucinskiene, 2011). When comparing karst lakes of the same natural zone, which are located in similar hydroclimatic conditions, the heterogeneity of their chemical composition and a significant range of variability in the mineralization of waters are revealed, which causes a certain interest in studying the biota of these water bodies and the factors determining their formation (Ciorca et al., 2017; Chalkia et al., 2012; Alimov and Mingazova, 2001; Palagushkina, 2004; Gusev, 2008).

The majority of lakes of karst origin are found on the territory of the East European Plain, in the Urals and in Eastern Siberia (Snitko and Sergeeva, 2003). The Middle Volga region in Russia is a zone of classical manifestations of karst, represented in various forms here, including the rarest gypsum karst (Alimov and Mingazova, 2001). In the Nizhny Novgorod region, there are more than three hundred natural lakes of glacial and karst origin, most of which are located on the Right Bank of the Volga (the basins of the Oka, Tesha, Piana rivers, etc.), and a few on the Left Bank (Stankovskaya, 2014). The studied lakes, Svetloyar, Klyuchik, and Svyatoye Dedovskoye, are located in the Middle Volga basin and are natural monuments of regional and federal importance (Alimov and Mingazova, 2001).

Phytoplankton, as an integral part of aquatic ecosystems, plays important role, as well as in food chain dynamics, energy flow, and nutrient cycling (Meng et al., 2020). It has been shown that the taxonomic composition of phytoplankton in karst lakes located in temperate zones is characterized by the combined presence of chrysophytes, dinoflagellates, and diatoms (Udovič et al., 2017; Kasperovičiene, 2001), and in some lakes, there was a high diversity of green algae (Chlorophyta) (Palagushkina, 2004) and cyanobacteria (Tarasova, 2010). In lakes of the “warm zone”, Chlorophyta and Cyanobacteria take a dominant role (Danielidis et al., 1996; Valadez et al., 2013). In spring, high turbulence promotes the development and persistence of diatoms; summer stratification promotes the development of dinoflagellates and cryptomonads, mainly in the metalimnion (Danielidis et al., 1996; Miracle et al., 1992). Endemic and rare species have been found in Plitvice lakes (Udovič et al., 2017; Udovič et al., 2022; Petar et al., 2014), in karst lakes of Greece (Danielidis et al., 1996), Romania (Momeu et al., 2015), etc.

The composition of the dominant phytoplankton species in water bodies of different biolimnological types largely determines the specific structure of aquatic plankton communities and reflects the trophic status and water quality. The functional characteristics and succession (seasonal and general) of common species are of undoubted interest when studying the state of the water body ecosystem because it is the dynamics of these populations that determine the direction of changes in the quantitative development of phytoplankton as a whole (Reynolds, 1984; Trifonova, 1990; 1994).

This paper is aimed at analyzing the composition, ecological structure, and coenotic role of the dominant species and functional complexes of phytoplankton in three different types of karst lakes in the Middle Volga region (Klyuchik, Svetloyar, and Svyatoye Dedovskoye).

2. Materials and methods

The studied karst lakes are located in various types of geographical landscapes in the Nizhny Novgorod region. Lakes Klyuchik and Svyatoye Dedovskoye are situated in the zone of coniferous-deciduous forests (Right Bank of the Volga), Prioksko-Volzhsky natural region, where karst processes are actively developing. Lake Svetloyar is located in the southern taiga zone (Left Bank of the Volga), it belongs to the Privetluzhsky uplands natural region (Kharitonychev, 1978; Bakanina et al., 2003).

Lake Klyuchik is located in the basin of the Surin River (a right-bank tributary of the Oka of the second order) (Bakanina et al., 2001; Bakhireva and Astashin, 2015). This is a “voklina” (the name for the exit of an underground river to the surface) lake and is classified as a “blue” lake due to the color of its water. The lake has underground feeding, the source of which is located in its western part and is discharged in the “voklina” at a depth of 15 m (Kozlov et al., 2017). Due to this fact, the lake is not completely covered with ice in winter the water temperature here is constant throughout the year and ranges from +4 to +8 ºС. The eastern part of this lake is an ordinary karst reservoir with heated water. Lake Svyatoye Dedovskoye belongs to the basin of another right-bank tributary of the Oka, the Tesha River. It was formed as a result of the merging and filling of several karst sinkholes with water. It is the largest karst (karst-terrace) lake in the Nizhny Novgorod region (Bakka and Kiseleva, 2009). The reservoir is fed by groundwater, meltwater, and rainwater (Bakanina et al., 2001; Bakka and Kiseleva, 2009; Moiseev et al., 2019). The catchment area of Lake Svetloyar relates to the Lyunda River basin. The lake is fed by cold spring waters and has a constant level.

According to the main morphometric indicators, the lakes are typical small reservoirs in the forest zone. However, the indicators of maximum and average depths of lakes allow us to classify them as water bodies with increased and greater depths, which is explained by their genesis (Table 1).

 

Table 1. Main morphometric characteristics of the studied lakes

Parameters / typology of the water body (according to Kitaev, 2007)	Lake Klyuchik*	Lake Svetloyar**	Lake Svyatoye Dedovskoye***
Geographical coordinates	55°58′30″N; 43°19′48″E	55°49′07″N; 45°05′35″E	55°38′45″N; 42°19′01″E
Lake length (Lmax, m)	743.0	472.0	2100.0
Lake width (В, m)*: maximum, Bmax average, Bavg	293.0 167.5	338.0 254.2	1150.0 647.6
Water surface area (A, m2)	124485.0 / little	120000.0 / little	1360000.0 / small
Volume of water mass (V, thousand m3)	475925 / little	1150000 / little	–
Lake depth (D, m) maximum, Dmax, average, Davg,	13.5 / increased 3.8 / small	32.7 / large 9.5 / large	20.0 / large 8.0 / large
Coastline length (lo, m) / Coastline angularity (development) (К=0.28*(lo/√А))	2377 / 1.9 moderately rugged	1328 / 1.04 slightly rugged	13100 / 3.1 strongly rugged

Note:

* According to Petrov and Astashin, 2017

** According to Naumenko et al., 2014

*** According to Moiseev et al., 2019

 

Sampling of phytoplankton from the lakes was carried out with a Ruttner bathometer during the growing season of the following years: in Lake Svetloyar (2000-2002; 2010-2011; 2020); in Lake Klyuchik (2017, 2020); in Lake Svyatoye Dedovskoye (2020, 2021). The grid of stations contained 3-5 stations, depending on the limnological features of the lakes (Fig. 1). In parallel with the collection of algological material, measurements of some abiotic parameters were carried out. Such parameters as temperature, electrical conductivity, and pH of water were measured using a portable multiparameter YSI Pro1030 pH & Conductivity Meter (YSI Incorporated, USA). Transparency measurements were carried out using a white Secchi disk. The content of oxygen dissolved in water was measured using a VZOR Mark-303M device (VZOR LLC, Russia). The lake depth at sampling points was measured using a Lowrance HOOK2-4x GPS Bullet echo sounder (Lowrance Electronics, USA). At individual stations, water samples were also taken for hydrochemical analysis. The determination of hydrochemical indicators was carried out on the basis of the Shared Use Center “New materials and resource-saving technologies” of the Research Institute of Chemistry, Lobachevsky University, Nizhny Novgorod, Russia.

 

Fig.1. Bathiometric maps of the studied lakes with phytoplankton sampling stations (A – location of the studied water bodies on the map of the Nizhny Novgorod region, B – lake Klyuchik (photo by Dmitry Khramtsov), С – lake Sverloyar, D – lake Svyatoye Dedovskoye)

 

Both integral and vertical samples were taken (from the surface to the bottom at every meter). A detailed description of the procedure for sampling, preparing them for microscopy, counting the abundance and biomass of phytoplankton is given in our earlier works (Okhapkin et al., 2022a; Okhapkin et al., 2022b, Vodeneeva et al., 2020). Identification of species was carried out using manuals, atlases, and keys indicated in the work of Vodeneeva and Kulizin (2019), the nomenclature of species was checked in the international database Algaebase (Guiry and Guiry, 2022). Information on the geographical distribution of the majority species, their biotopic location, and their relationship to salinity, pH, and organic pollution was taken from the work of L.G. Korneva (2015). The belonging of phytoplankton species to one or another functional group was assessed using the classification of Reynolds (1984; 2002), with modifications by Padisàk (Padisàk et al., 2009).

Species whose contribution to total abundance and biomass was at least 10% of the total value were classified as dominant (Vodeneeva, 2006). For each dominant species, such indicators as frequency of occurrence (pF), frequency of dominance (DF), and order of dominance (Dt) were taken into account (Gorbulin, 2012).

These indicators were calculated using the formulas given below.

With the help of the “dominance frequency” (DF) indicator, we identified how many samples out of the total number of samples showed dominance of specific species:

$DF=\frac{D}{F}\cdot 100$

where F is the total number of processed samples of the studied reservoir, D is the number of samples, in which this species acted as the dominant one (biomass was more than 10%).

Dominance order (Dt) was the ratio of the dominance frequency to the frequency of occurrence:

$Dt=\frac{DF}{pF}\cdot 100$

where DF is the frequency of dominance, pF is the frequency of occurrence, %.

The dominance of species with indicators DF<10, Dt<10 and pF<20 is random and it is recommended to exclude them from the list of dominants (Bazhenova, 2017).

The similarity in the composition of the dominant species of the studied water bodies was assessed using the Sørensen coefficient (Ks) (Shitikov et al., 2003).

To visualize the similarity of the species composition of the dominants of the studied lakes, the method of nonparametric multivariate analysis of variance (PERMANOVA) was used. Statistical analyses were performed using the free software environment R (R Core team, 2015).

3. Results and discussion

The main hydrochemical and hydrophysical parameters of the lakes are presented in Table 2. The waters of Lake Klyuchik during the research period were characterized by relatively high mineralization (1099 to 1274 mg/l), according to literary data, these values reached 1937 mg/l (Kozlov et al., 2017), and the pH values varied within 8.2-8.4. The waters of Lake Klyuchik are slightly brackish sulfate ones of the Ca II type, which fully corresponds to the portrait of sinkhole lakes. Lakes are hydrogeological windows where the lower part of the lake basins is developed below the groundwater level, having mainly underground recharge carried out through pores at the bottom of the basin (Okhapkin et al., 2022a).

 

Table 2. Main hydrophysical and hydrochemical parameters of the studied lakes during summer low water period

Index / Water body typology (according to Kitaev, 1984; 2007)	Lake Klyuchik 19.08.2020	Lake Klyuchik 19.08.2020	Lake Svetloyar 04.08.2020	Lake Svyatoye Dedovskoye 31.08.2021
Sampling stations	1, pelagic, 10 m	5, pelagic, 8 m	1, pelagic, 15 m	4, pelagic, 14 m
Suspended substances, mg/l	< 3	< 3	< 3	10 ± 3
Transparency, m (Hex.)/ transparency class *	6.5 high	4.3 high	4.2 high	2.4 average
Water chromaticity according to Pt-Co *	40.0 mesohumous	80.0 mesohumous	10.0 oligohumous	6.7 ultra-oligohumous
рН	8.2 oligo-alkaline	8.4 oligo-alkaline	6.9 acid-neutral	6.4 acid-neutral
Mineralization, mg/l	1274.0 slightly salty	1099.0 slightly salty	127.0 medium- fresh	32.0 very fresh (oligohaline)
Ionic composition	Ca sulfate groups Type II	Ca sulfate groups Type II	hydrocarbonate groups Ca (Na), Type I	Ca hydrocarbonate groups, Type I

Note: *According to Bayanov, 2019; 2011; Kozlov et al., 2019; the report of “Russian Federal Research Institute of Fisheries and Oceanography” for 2011.

 

The waters of Lake Svetloyar belong to the hydrocarbonate class of the Ca group (in summer) or Mg (in winter), with slight mineralization and low color. The content of hydrocarbonates in water during the studied period was insignificant and did not exceed 75 mg/l. A high content of nitrite forms of nitrogen was noted in the lake, probably associated with a high recreational pressure on the reservoir in the summer months (Okhapkin et al., 2022b). Lake Svyatoye Dedovskoye is a light-watered one and has very low water mineralization because it is fed by melt and rainwater. According to the ionic composition, the lake waters belong to the hydrocarbonate class, Ca group, type 1. Mineralization during the studied period did not exceed 37.7 mg/l, and the pH varied from 6.0 to 7.0, which characterized Lake Svyatoye Dedovskoye as an acid-neutral reservoir. Obviously, the reason for the low active reaction of the environment is the swampiness of the lake`s catchment area. A small amount of nutrients is recorded in the lake.

Lakes Svetloyar and Svyatoye Dedovskoye are typical water bodies of the temperate zone with a dimictic type of water mixing. In Lake Svetloyar, the summer temperature stratification was established in early May and continued until the end of September. The metalimnium layer began in the summer period at a depth of 2.0–4.0 m, moved in the early autumn to a depth of 6.0 m, and later reached a depth of 9.0 m. In Lake Svyatoye Dedovskoye, the period of spring mixing of waters turned out to be longer. Stable temperature stratification has been observed since the end of June. At the beginning of summer, the layer of temperature jump was at a depth of 1-2 m; in July–August, it shifted to a depth of 4-6 m. Unlike other reservoirs, Lake Klyuchik has peculiarities of the thermal regime: in the western, deep enough basin of the lake, the type of water circulation should be considered cold polymictic. There is no summer temperature stratification; this fact is explained by the strong, constant influx of cold waters in the underground Surin River (Petrov and Astashin, 2017). The smoothed temperature curve in the summer months in the eastern part of the reservoir and the early onset of autumn homothermy can be explained by the existence of underwater currents carrying cold water here through a narrow isthmus from its western part.

In Lake Klyuchik, the distribution of oxygen on the surface horizon throughout the water area of the reservoir was uneven. In its western part, the oxygen content ranged from 3.7 to 12.5 mg O₂/l; in the eastern part, from 9.1 to 13.7 mg O₂/l; and in the transition zone, from 9.8 to 14.6 mg O₂/l. Taking into account these indicators, the eastern part of Lake Klyuchik belongs to water bodies with a very high oxygen content (Kitaev, 2007). The western part of the lake is characterized by the presence of hydrogen sulfide in the water and low oxygen content (30-57%) in the surface horizon, which is, probably, caused by the influence of underground flow from the “voklina.” At the deepest station 1, located in the western part of the lake, the oxygen distribution curve in July-August had a clinegrade character (Aberg and Rodhe, 1942), with a gradual decrease in oxygen content with depth due to its consumption for respiration and oxidation of organic substances. At the station 5 (the eastern part of the lake) in July in the surface horizon, the oxygen content was 10-11 mg O₂/l, at a depth of 2-3 m its amount increased to 14 mg O₂/l, which is associated with the active vegetation of small-celled green algae and representatives of dinoflagellates here. At a depth of 4 meters to the bottom, a gradual decrease in the dissolved oxygen content to almost zero indexes begins, which is characterized as a positively heterograde oxygen distribution curve. In August, at station 5, a sharp drop in the amount of dissolved oxygen at a depth of 5 m is observed due to its consumption for the mineralization of organic substances created by producers in the upper layers of the reservoir.

The oxygen regime of Lake Svetloyar in 2020, as well as in previous years of the research, was characterized by a high percentage of oxygen in the water layer from 1.0 to 5.0 m deep. The oxygen saturation varied from 108 to 127% in the surface horizon in the summer. Oxygen deficiency is often observed in the metalimnion, when the saturation of the water column with this gas does not exceed 40%. In September-October 2020, oxygen saturation in the epilimnion remained high from 83.0 to 109.0%, and the epilimnion shifted at the beginning of autumn mixing to a depth of 7-8 m.

In Lake Svyatoye Dedovskoye, the vertical distribution of oxygen was almost uniform at all levels of the water column at the end of June and was within the range of 6.36-7.78 mg O₂/l, corresponding to 40-50% saturation. With the establishment of a stable stratification during the hydrological summer, the maximum values of oxygen content (7.5 - 8.3 mg O₂/l) were recorded in the epilimnion to a depth of 4 m. In the hypolimnion, the oxygen content did not change starting from a depth of 5 m and amounted to 2.6-3.0 mg O₂/l. With the onset of autumn homothermy, the vertical distribution of oxygen becomes uniform (8.0-9.3 mg O₂/l), and the percentage of oxygen saturation in water layers reached 66.0-82.0%.

The phytoplankton composition of the studied lakes contained 347 species (432 species and infraspecific taxa), belonging to 168 genera, 42 orders, 17 classes, and 8 divisions (Lake Svyatoye Dedovskoye, 212 taxa; Lake Svetloyar, 225 taxa; Lake Klyuchik, 275 taxa). A comparative analysis of the floristic structure of phytoplankton in the studied lakes showed that in all the reservoirs, the taxonomically significant divisions were Cyanobacteria, Chlorophyta, Bacillariophyta, Ochrophyta, and Euglenophyta, which together accounted for more than 70% of the total species richness. The presence of these groups in the core of algal flora was also noted in a number of other karst lakes (Udovič et al., 2022; Kasperovičiene, 2001) due to the wide geographical distribution of their representatives. However, the proportional ratio of these groups in the phytoplankton composition of the lakes turned out to be different. In the algal flora of hydrocarbonate low-mineralized lakes (Lake Svetloyar and Lake Svyatoye Dedovskoye), the first place was occupied by green algae, and in the sulfate Lake Klyuchik, by diatoms. There was a natural increase in the number of diatom species from 18.6% to 40% (Lake Klyuchik), with a decrease of the species richness of green (from 33.5% to 24.0%) and euglenophyte (from 9.6% to 3.6%) algae, respectively. For Lake Svyatoye Dedovskoye, the participation of charophyte algae (up to 13.2% of the composition) in the composition of taxonomic diversity is more noticeable than others.

Studies of some aquatic ecosystems of the Nizhny Novgorod region (rivers and lakes of the Kerzhnesky Nature Reserve) (Vodeneeva, 2006), water bodies of the territory of Nizhny Novgorod (Okhapkin and Startseva, 2003) have shown that the dominant species in the phytoplankton of these aquatic ecosystems may constitute from 20 to 30% of the total list. In the studied lakes, the composition of the dominant species included 114 species and intraspecific taxa, or 26.38% of the total composition of algae. However, in some lakes, their contribution could be less, ranging from 13 to 20%, which may be caused by the lack of longer observation series.

In Lake Svyatoye Dedovskoye, the ratio of dominant groups generally coincided with that in the general list: green and diatom algae predominated, together determining more than 50% of the total composition of dominants, the share of ochrophytes (chrysophytes) was 14%, the representatives of other departments were listed among the dominants by less than 10%.

In other lake systems, the ratio of dominant taxa had its own characteristics. Thus, the phytoplankton of Lake Klyuchik differed significantly both in species composition and in the composition of dominants, not only in the group of lakes studied but also in comparison with other karst reservoirs of the forest and forest-steppe landscape-geographical zones of European Russia (Gusev, 2011; Palagushkina, 2004). The phytoplankton of this reservoir had a pronounced diatom character (Fig. 2) and a complete cyanobacteria absence among biomass dominant taxa. The contribution of greens, ochrophytes, cryptophytes, and dinoflagellates was 7-10%, euglenophytes and charophytes were 2-4%. The diatom character of phytoplankton is apparently typical for gypsum lakes, and was also noted in the example of Lake Goluboye (Samara region) (Tarasova, 2010).

 

Fig.2. Taxonomic diversity of dominant (by biomass) phytoplankton groups in karst lakes

 

In Lake Svetloyar, euglenoids predominated among the dominant species in terms of species richness (due to the diversity of the genus Trachelomonas), forming up to 25% of the total list. In the earlier period of the study (the beginning of the 2000s), their contribution was about 20%. Thus, in the modern period, the role of this group in the phytoplankton of the lake has noticeably increased both in taxonomic and coenotic terms, which may indicate an increase in the processes of eutrophication of this reservoir against the backdrop of increased recreational load (Okhapkin et al., 2022b). The second position in the group of dominants was taken by representatives of diatoms, greens and chrysophytes (Ochrophyta) (15-17% each), cyanobacteria and cryptomonades were in the third position (8-10%).

According to the biotopic location, among the dominant species of algocenoses in lakes Svetloyar and Svyatoye Dedovskoye, true planktonic forms predominated (58-70% of the total list) (Fig.3.). Among the dominants in Lake Klyuchik, the proportion of planktonic species was 2-2.3 times lower, and the proportion of benthic forms increased (up to 20%), which may indicate benthification processes in this reservoir. In all the lakes studied, it should be noted that there is a high proportion of species capable of inhabiting different biotopes. Their share could range from 25 to 50% of the total list of dominants.

 

Fig.3. The ecological and geographical characteristics of dominant species in the studied lakes (I - habitat, II – geographical element of flora, III - halicity, IV - pH of the environment, V – saprobity).

Notes:

I – pl. – planctonic, b. – benthic, l. – littoral, f. – foulers, e. – epibionts, hyphenated – heterotopic species;

II – cosm. – cosmopolites, n-a – north-alpine, bor. – boreal;

III – ind. – indifferents, ohb. – oligohalobes, hph. – halophiles, hpb. – halophobes;

IV – ind. – indifferents, al. – alkaliphiles, ac. – acidophiles;

V – saprobity indicators)

 

In terms of geographical distribution, the main part of the list of the dominant algae species was represented by cosmopolitan forms (95-97%), representatives of the boreal (Xanthidium antilopaeum Kützing, Spondylosium planum (Wolle) West & G.S. West from desmids) and northern alpine (Pinnularia episcopalis Cleve from diatoms) areas were sporadically found.

In relation to the content of sodium and chlorine ions, indifferent species were in the lead (76-95%), the proportion of oligohalobes varied from 5% (Lake Svyatoye Dedovskoye) to 16% (Lake Svetloyar). Halophiles capable of living in freshwater or slightly brackish water habitats, as well as halophobes that cannot withstand high NaCl contents in water, were noted only in lakes Klyuchik and Svetloyar, accounting for 4–5% of the composition of halobic indicators. More than half of the composition of dominants was characterized by an indifferent attitude to water pH. Species that prefer alkaline conditions in Lake Klyuchik made up a little less than half of the composition, in Lake Svetloyar, 19%, in Lake Svyatoye Dedovskoye, 25%. Indicators of acidic waters (Vacuolaria virescens Cienkowski, Aulacoseira distans (Ehrenberg) Simonsen) were recorded only in lakes Klyuchik and Svetloyar.

The predominance of indicators of β-mesosaprobic contamination was noted among the indicators of organic pollution in lakes Klyuchik and Svyatoye Dedovskoye. In Lake Svetloyar, in addition to a high proportion of β-mesosaprobes, a significant proportion of representatives of the α-β-mesosaprobic zone was found. According to the results of the long-term studies for this water body, there is a tendency to increase the representation in the general species composition of indicators of more polluted waters β-α, α-β mesosaprobic, α-mesosaprobic and α-meso-polysaprobic waters (from 9 to 13%), which may indicate an increase in the eutrophication of the reservoir (Okhapkin et al., 2022b).

For all dominant species, indices of occurrence (pF), dominance frequency (DF), and dominance order (Dt) were calculated. Out of 114 dominant taxa, only 13 showed high values of DF>10, Dt>10, and pF>20 (Table 3.). The observed species belonged to 5 groups of algae: cryptophytes, euglenophytes, charophytes, diatoms, and dinophytes, of which only dinoflagellates were common dominant taxa identified in all the studied lakes.

 

Table 3. The dominant phytoplankton species and Functional Groups (FG) in the studied water bodies

Lakes	Taxa	FG* Codon	D	pF	DF	Dt
Klyuchik	Bacillariophyta
	Cyclotella distinguenda	B	59	75.4	53.6	71.1
	Cyclotella sp.	A	15	39.1	13.6	34.8
	Cryptophyta
	Cryptomonas sp.	Y	17	42.7	15.4	36.1
	Dinophyta
	Ceratium hirundinella	Lo	19	22.7	17.3	76.2
	Peridinium cinctum	Lo	31	36.4	28.2	77.5
Svetloyar	Bacillariophyta
	Lindavia comta	B	11	50	14.5	29
	Asterionella formosa	C	11	50	14.5	29
	Dinophyta
	Ceratium hirundinella	Lo	20	40.8	26.3	64.5
	Peridinium cinctum	Lo	26	43.4	34.2	78.8
	Euglenophyta
	Trachelomonas Rugulosa	W2	10	21.0	13.1	62.4
	Trachelomonas Volvocina	W2	19	67.1	25	37.2
	Trachelomonas volvocina var. subglobosa	W2	12	22.4	15.8	70.5
Svyatoye Dedovskoye	Bacillariophyta
	Cyclotella sp.	A	4	45.2	12.9	28.5
	Tabellaria fenestrata	N	6	45.2	19.3	42.7
	Cryptophyta
	Komma caudate	X2	6	61.3	19.3	31.5
	Dinophyta
	Peridinium cinctum	Lo	13	45.2	41.9	92.7
	Charophyta
	Staurodesmus incus var. ralfsii	N	15	61.3	48.4	78.9

Note: * Names of codons are given with the use of functional classification of phytoplankton according to Padisàk et al., 2009

 

Freshwater dinoflagellates are an important component of the lake phytoplankton (Trifonova, 1990). The ecology of dinophyte algae is characterized by a wide distribution in water bodies of different trophic status and tolerance to low light levels, as well as the ability to migrate and have a mixotrophic type of nutrition, which allows them to compete in extreme conditions: nutrient deficiency, acidification, and increased water mineralization (Regel et al., 2004). In the studied lakes, the maximum contribution of dinophytes to the total biomass was, as a rule, noted during the period of summer stratification and could amount to up to 68-93% of the total values (lakes Svyatoye Dedovskoye and Svetloyar, respectively). In Lake Klyuchik, with water areas of different thermal regimes, the dominance of dinophytes was noticeable only in the warmed part of the reservoir, increasing here to 50-70% of the total indicators. Among the representatives of this group, large-celled armored dinophytes from the functional group L₀, Ceratium hirundinella (O.F.Müller) Dujardin (Dt = 64.5–76.2) and Peridinium cinctum (O.F.Müller) Ehrenberg (Dt = 77.5–92.74), were characterized by a high order of dominance, of which the latter was dominant in all three lakes. It is known that C. hirundinella is a common dominant of summer plankton in most lakes of temperate latitudes (Trifonova, 1990; Darki and Krakhmalnyi, 2019), one of the most heat-preferring species of dinoflagellates. It has been shown that its vegetation is determined by stratification conditions (Miracle et al., 1992; Darki and Krakhmalnyi, 2019), although this species can also occur during periods of mixing (MacDonagh et al., 2005). Maximum concentrations of C. hirundinella cells tend to occur in the thermocline zone (Hedger et al., 2004). Representatives of P. cinctum species, as well as C. hirundinella, are widespread in freshwater habitats of both temperate and tropical zones (they often develop in complexes) and are able to adapt to environmental conditions almost without restrictions (Gürkan et al., 2024). It was found (Regel et al., 2004) that for better photosynthesis, the species must migrate to an optimal depth (30% of surface illumination). In the vertical distribution of dinoflagellates in Lake Svetloyar, under conditions of pronounced summer stratification, the concentration of populations of these species was noted at the lower boundary of the metalimnion, where these representatives, due to their ability to vertically migrate, acquired advantages in the absence of nutrients in the epilimnion (Darki and Krakhmalnyi, 2019); during the period of autumn homothermy - in the surface layer. The maximum rise in biomass in C. hirundinella in summer was up to 2-3 g/m3, in P. cinctum, it was about 1 g/m3. In Lake Klyuchik, under conditions of smoothed stratification (the eastern part of the reservoir), it was not possible to note the confinement of dinophyte algae to certain horizons.

The contribution of diatoms to the development of phytoplankton in the studied lakes turned out to be maximum for the gypsum in Lake Klyuchik; their complete dominance was noted (more than 90% of the total number and 50-100% of the biomass) in the cold part of the reservoir and its transition zone. In this part of the lake, the waters of the underground river are unloaded, creating favorable conditions for diatoms sensitive to stratification; they often develop at the bottom. Under conditions of high transparency (up to 8.5 m) and no light limitation, photosynthesis was possible throughout the entire water column, including the bottom zone (Okhapkin et al., 2022a).

Among the weakly mineralized reservoirs in Lake Svyatoye Dedovskoye, the most significant share of diatoms (40-60% of the total biomass indicators) turned out to be during the spring and autumn mixing of waters. In Lake Svetloyar, mixing periods are short (about two weeks), as a result of which extended periods of low temperature (5–15°C) and water turbulence did not form in the reservoir to achieve noticeable abundance and biomass values of Bacillariophyta (Okhapkin et al., 2022b). The insignificant dominant role of diatoms (their share in the average vegetation biomass was 4.64–30.42%) in this reservoir is apparently also associated with a clear division of the water column into oxygenic and anoxygenic components, the removal of silicon, which is part of the shells of Bacillariophyta, from the trophogenic layer into the bottom, and its weak supply from the catchment area. Information about the insignificant coenosis-forming role of diatoms in plankton was also provided for some light-water lakes in the temperate zone of Russia (Gusev, 2007; Korneva, 2015).

Among centric diatoms, high values of frequency (DF) and order (Dt) of dominance were noted for representatives of the genera Cyclotella and Lindavia, belonging to functional group B, inhabitants of mesotrophic lakes, sensitive to water stratification (Padisàk et al., 2009).

The predominance of Cyclotella species is typical of karst lakes, both in the temperate zone and in the warm zone, especially during spring and autumn mixing (Danielidis et al., 1996; Petar et al., 2014; Udovič et al., 2017). Among representatives of this genus, the maximum parameters of dominance were noted for Cyclotella distinguenda Hustedt (DF=53.6, Dt=71.1, pF=75.4), which dominated only in the plankton of the gypsum Lake Klyuchik, forming monodominant algocenoses and reaching uniquely high biomass values (more than 100 g/m³). This species is considered rare for the algal flora of the Volga basin (Genkal et al., 2019, Vodeneeva et al., 2020; Okhapkin et al., 2022а), as well as for the rivers of Hungary (Kiss et al., 2012). High values of development of this species in the studied reservoir indicate optimal conditions and, apparently, a complete absence of competition with other representatives of phytoplankton in this combination and the dynamics of environmental factors (high mineralization, favorable light conditions, low temperature background, and lack of thermal stratification).

In the weakly mineralized Lake Svyatoye Dedovskoye, among the species of the genus Cyclotella, mainly small-celled forms were observed, and their maximum development occurred in the last phase of spring mixing. The share of these species more often corresponded to 15-20% of the total biomass values. In the summer season, they were inferior to dinoflagellates, and during the period of autumn homothermy, they were inferior to pennate species of diatoms or charophyte algae. In Lake Svetloyar, Lindavia comta (Kützing) T.Nakov et al. stood out among the centric diatoms (DF=14.5, Dt=29, pF=50). This species is cosmopolitan and eurythermic; in oligotrophic lakes, it is the dominant of summer plankton; in mesotrophic lakes, it acts as a subdominant in spring (Trifonova, 1990). In Lake Svetloyar, L. comta was noted as an accompanying component (10-15% of total indicators, biomass less than 1 g/m3) to the main coenotic complexes of phytoplankton, which may indicate the transitional oligotrophic-mesotrophic status of this reservoir.

Significant indicators of dominance among pennate diatoms were noted for Asterionella formosa Hassal (Dt=29, pF=50) (Lake Svetloyar) and Tabellaria fenestrata (Lyngbye) Kützing (Dt=42.7, pF=45.2) (Lake Svyatoe Dedovskoye).

It is known that species of the genus Tabellaria are included in the codon N, are acidobionts, developing in acidified water bodies (Battarbee et al., 1985; Sirenko and Parshikova, 1993; Vodeneeva, 2006). At the time of the research, the values of the slightly acidic reaction of the environment were also recorded in Lake Svyatoye Dedovskoye. Their presence as cenosis-forming species was noted in plant plankton of acidic reservoirs of Finland (Lepistö and Rosenström, 1998), South Karelia (Nikulina, 1997), Sweden (Wahlstrom and Danilov, 2003), forest lakes and watercourses of the Nizhny Novgorod Southern Trans-Volga region (Vodeneeva, 2006), etc. Among the species of this genus, T. fenestrata is one of the characteristic dominants of large oligotrophic lakes (Petrova, 1990). The constant presence of this taxon in the algocenoses of Lake Svyatoye Dedovskoye (share in the total biomass, 15-60%) confirms the oligotrophic status of this reservoir, its noticeable morphometric characteristics, as well as the swamp conditions of the catchment.

Another representative of pennate diatoms, noted as a permanent component of the phytoplankton of Lake Svetloyar, A. formosa, is also considered a typical summer dominant of algocenoses of various types of water bodies (Trifonova, 1990; Petrova, 1990), often found in aquatic ecosystems of the Volga basin (Okhapkin et al., 2022b). The massive development of this species may indicate an intensification of eutrophication processes. In the Svetloyar ecosystem, populations of this species were found in the spring and summer seasons, but their development did not reach the “blooming” stage. This species vegetated throughout the entire water column (the biomass of A. formosa varied from 0.15 (at the 7 m depth) to 0.48 g/m3 (at the surface).

In the highly mineralized Lake Klyuchik, pennate diatoms, mainly benthic species of the genera Pinnularia and Navicula, were included in the list of dominant taxa but did not have significant values of frequency and order of dominance.

In Lake Svyatoye Dedovskoye, the list of common species with high dominance indicators includes representatives of euglenophyte algae, Trachelomonas rugulosa F.Stein, Trachelomonas volvocina (Ehrenberg) Ehrenberg, and Trachelomonas volvocina var. subglobosa Lemmermann (functional group W2), preferring the bottom layers of the water column. The last representative stood out in terms of the order of dominance in this lake (DF=15.8, Dt=70.5, pF=22.4). The development of trachelomonads occurred throughout the growing season (their share varied from 10 to 15%), as well as during the under-ice period, where their contribution could be more than 90%. In the modern period, there is a tendency to a gradual increase in the role of euglena algae in algocenoses in the summer season, which may indicate an increase in the concentration of organic substances in water and an intensification of eutrophication processes.

In lakes Klyuchik and Svyatoye Dedovskoye, among the significant structure-forming phytoflagellates, representatives of cryptophyte algae (Cryptomonas spp. - DF = 15.4, Dt = 36.1, pF = 42.5; Komma caudata (L.Geitler) D.R.A.Hill - DF = 19.3, Dt = 31.5, pF = 61.3) were also noted. These species, with the ability for mixotrophy and migration, similar to dinophyte and euglena algae, are able to compete with other representatives of phytoplankton for resources. In the plankton of the studied lakes, cryptomonads more often played accompanying roles, and their share in development indicators varied from 7 to 15%.

In Lake Svyatoye Dedovskoye, among other phytoplankton groups, significant indicators of dominance were also observed for representatives of desmidian algae (division Charophyta): Staurodesmus incus var. ralfsii (West) Teiling (codon N, continuous or semi-continuous mixed layer of 2–3 m in thickness; shallow lakes where the mean depth is of this order or greater, as well as in the epilimnia of stratified lakes when the mixing criterion is satisfied) – DF=48.4, Dt=78.9, pF=61.3, which reflects the swampy nature of the catchment.

Blue-green algae as dominants and subdominants in biomass were not typical for the phytoplankton of the studied aquatic ecosystems. However, the development of small-celled colonial cyanobacteria (genera Aphanocapsa, Aphanothece), as dominants in the phytoplankton population, as well as small-celled coccoid forms of green algae (genus Dactylosphaerium, Dictyosphaerium), was noted for all of the studied lakes. In abnormally hot years (2010) with anticyclonic weather in the lake. In Svetloyar, outbreaks of flowering of diazotrophic cyanobacteria from codon H1 (species sensitive to water mixing) were observed - representatives of the genus Dolichospermum, which could form up to 32.9 g/m3 at the peak of development (Okhapkin et al., 2022b). However, in subsequent years, these species disappeared from the algocenoses of the lake.

The method of multivariate analysis of variance (PERMANOVA) of the composition of the dominant phytoplankton species involved in the composition of the abundance and biomass of the studied lakes (according to the Sørensen-Chekanovsky coefficient) showed a statistically significant low degree of their similarity (Table 4), which may indicate the originality of algae cenogenesis in each of the studied lakes due to the influence of a certain combination of factors. Visualization of the obtained data demonstrated a clear division of the studied lakes according to the composition of algocenoses (Fig. 4).

 

Table 4. Statistical parameters (F – Fisher criterion, p – level significance) when assessing the similarity of the composition of the studied lakes

Permanova
	Dominants (by abundance)		Dominants (by biomass)
	F value	P (>F)	F value	P (>F)
Lake	13.49	0,001***	11.91	0,001***
Klyuchik_vs_Svetloyar	8.66	0,001***	9.44	0,001***
Klyuchik _vs_Svyatoye Dedovskoye	17.20	0,001***	13.69	0,001***
Svetloyar _vs_ Svyatoye Dedovskoye	15.47	0,001***	12.71	0,001***

 

Fig.4. Visualization of the analysis results reflecting the similarity in cenotic (according to abundance – I, and biomass - II) structure of phytoplankton in the studied lakes.

 

When comparing the composition of functional groups of phytoplankton in the studied lakes by biomass, it also demonstrated a statistically significant low degree of similarity, however, the difference in the composition of functional groups in abundance for lakes Svetloyar and Svyatoye Dedovskoye was less pronounced (Table 5, Fig. 5). There is probably some similarity in the conditions for the formation of phytoplankton in these lakes, namely the high depth and transparency of the waters.

 

Table 5. Statistical parameters (F – Fisher criterion, p – level significance) when the similarity of the Functional Groups (FG) in the studied lakes

Permanova
	FG (by abundance)		FG (by biomass)
	F value	P (>F)	F value	P (>F)
Lakes	16.43	0,001***	19.88	0,001***
Klyuchik_vs_Svetloyar	15.53	0,001***	16.83	0,001***
Klyuchik _vs_Svyatoye Dedovskoye	21.71	0,001***	22.93	0,001***
Svetloyar _vs_ Svyatoye Dedovskoye	7.75	0,001***	19.34	0,001***

 

Fig.5. Visualization of the analysis results reflecting the similarity of the functional (according to abundance – I, and biomass - II) composition of the studied lakes

 

4. Conclusion

In the composition of the phytoplankton of lakes Klyuchik, Svetloyar and Svyatoye Dedovskoye, 432 species and intraspecific taxa of algae belonging to 8 phyla were identified. Analysis of the algal flora of the studied lakes showed the taxonomic importance of the divisions of Cyanobacteria, Chlorophyta, Bacillariophyta, Ochrophyta, and Euglenophyta, constituting more than 70% of the total species richness. The composition of the dominant species included 114 species of algae (26.38% of the total composition): in Lake Svyatoye Dedovskoye, green algae and diatoms (50%) predominated, in Lake Svetloyar, euglenids predominated (25%), in Lake Klyuchik, diatoms predominated (more than 40%).

The basis of the floristic list among the dominant species of algocenoses in lakes Svetloyar and Svyatoye Dedovskoye were planktonic forms (58-70% of the total list). In Lake Klyuchik, the proportion of planktonic species was 2-2.3 times lower, the proportion of benthic forms increased (up to 20%). Most of the identified species are characterized by a cosmopolitan distribution; representatives of the boreal and northern alpine habitats were found only sporadically.

Among 13 dominants (from 5 divisions) with high values of DF>10, Dt>10, and pF>20, dinoflagellates Ceratium hirundinella, Peridinium cinctum (functional group L₀) were noted in all lakes, with maximum development during the period of summer stratification. In the group of diatoms, species of centric diatoms from the genus Cyclotella (codon B) predominated everywhere, reaching maximum development rates under conditions of mixing of waters. The composition of the remaining dominant groups in each reservoir was determined by its limnological features.

Using the method of multivariate analysis of variance (PERMANOVA), a statistically significant (Pr(>F) = 0.001) low degree of similarity of the dominant and functional phytoplankton complexes was shown, which may indicate the uniqueness of algae cenogenesis in each of the studied lakes, due to the influence of a certain combination of factors, such as temperature, transparency, pH, and oxygen content.

The obtained data on the frequency of occurrence and indicators of dominance of the identified common species reflect their ecological characteristics as well as the potential for maximum development under certain combinations of factors, which can be used in the system of environmental monitoring of aquatic ecosystems.

Conflict of interests

Authors declare no conflict of interests.

About the authors

E. M. Sharagina

Lobachevsky State University of Nizhny Novgorod (UNN)

Author for correspondence.
Email: sharagina@ibbm.unn.ru
Russian Federation, pr. Gagarin, 23, Nizhny Novgorod, 603950

P. V. Kulizin

Lobachevsky State University of Nizhny Novgorod (UNN)

Email: sharagina@ibbm.unn.ru
Russian Federation, pr. Gagarin, 23, Nizhny Novgorod, 603950

N. A. Startseva

Lobachevsky State University of Nizhny Novgorod (UNN)

Email: sharagina@ibbm.unn.ru
Russian Federation, pr. Gagarin, 23, Nizhny Novgorod, 603950

D. A. Zhurova

Lobachevsky State University of Nizhny Novgorod (UNN); Nizhny Novgorod Branch of the Federal State Budgetary Scientific Institution “Russian Federal Research Institute of Fisheries and Oceanography”

Email: sharagina@ibbm.unn.ru
Russian Federation, pr. Gagarin, 23, Nizhny Novgorod, 603950; 31 Moskovskoe shosse St., Nizhny Novgorod, 603116

Ya. V. Seredneva

Lobachevsky State University of Nizhny Novgorod (UNN)

Email: sharagina@ibbm.unn.ru
Russian Federation, pr. Gagarin, 23, Nizhny Novgorod, 603950

T. Khedairia

Lobachevsky State University of Nizhny Novgorod (UNN)

Email: sharagina@ibbm.unn.ru
Russian Federation, pr. Gagarin, 23, Nizhny Novgorod, 603950

A. G. Okhapkin

Lobachevsky State University of Nizhny Novgorod (UNN)

Email: sharagina@ibbm.unn.ru
Russian Federation, pr. Gagarin, 23, Nizhny Novgorod, 603950

E. L. Vodeneeva

Lobachevsky State University of Nizhny Novgorod (UNN)

Email: sharagina@ibbm.unn.ru
Russian Federation, pr. Gagarin, 23, Nizhny Novgorod, 603950

References

Supplementary files