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Article

Environmental Factors Controlling Zooplankton Communities in Thermokarst Lakes of the Bolshezemelskaya Tundra Permafrost Peatlands (NE Europe)

by
Elena I. Sobko
1,
Liudmila S. Shirokova
1,2,*,
Sergey I. Klimov
1,
Artem V. Chupakov
1,
Svetlana A. Zabelina
1,
Natalia V. Shorina
3,
Olga Yu. Moreva
1,
Anna A. Chupakova
1 and
Taissia Ya. Vorobieva
1
1
N. Laverov Federal Center for Integrated Arctic Research of the Ural Branch of the Russian Academy of Sciences, Nab. Northern Dvina 23, Arkhangelsk 163000, Russia
2
BIO-GEO-CLIM Laboratory, Tomsk State University, 36 Lenina Str, Tomsk 634050, Russia
3
Northern (Arctic) Federal University, Department of Drilling, Development of Oil and Gas Wells, Nab. Northern Dvina 17, Arkhangelsk 163000, Russia
*
Author to whom correspondence should be addressed.
Water 2023, 15(3), 511; https://doi.org/10.3390/w15030511
Submission received: 20 December 2022 / Revised: 18 January 2023 / Accepted: 24 January 2023 / Published: 27 January 2023
(This article belongs to the Special Issue Zooplankton in Arctic Waters: Diversity, Dynamics and Ecology)
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Abstract

:
Environmental physical and chemical factors controlling the abundance and biodiversity of zooplankton in permafrost-affected lakes are poorly known yet they determine the response of aquatic ecosystems to on-going climate change and water warming. Here, we assess the current status of zooplankton communities in lakes of the Bolshezemelskaya Tundra (permafrost peatlands of NE Europe), and provide new information about the composition and structure of zooplankton. The results demonstrate that the structure of zooplankton communities is influenced by the morphometric features of lakes and the degree of lake overgrowth by macrophytes. According to the level of quantitative development of zooplankton, most tundra lakes were of the oligotrophic type with an average wet biomass of up to 1 g/m3. The largest number of species was observed in zooplankton communities of small thaw ponds with an area of up to 0.02 km2 and overgrown with macrophytes. The analysis of factors that influence the formation of the lake zoocenosis demonstrated that the species composition and quantitative characteristics of zooplankton are chiefly controlled by pH and water mineralization. A comparison of the results obtained with the literature data on the lakes of this region collected 60 years ago suggests that the ecosystems of these lakes are in a stable state. Overall, these new insights will improve our knowledge of factors controlling the zooplankton spatial dynamics in unique but quite abundant thermokarst lakes of NE European Tundra, subjected to on-going climate warming.

1. Introduction

The influence of various local anthropogenic and global factors including climate change on the diversity of biota in aquatic ecosystems of the Arctic and subarctic is among the most important research directions [1,2,3]. These ecosystems are extremely sensitive to climate change and anthropogenic impact [4,5,6]; as a result, they are highly vulnerable to ongoing environmental changes [7]. Climate change and increased anthropogenic pressure are very likely to change the characteristics of Arctic freshwater ecosystems and modify their biotic parameters. However, inland aquatic systems of the Arctic and Subarctic are diverse in their type, chemical, physical and biotic indicators, so that they may exhibit variable response to climate changes. In this regard, the temperature is among the most important factor affecting zooplankton communities, notably the species structure and quantitative indicators of zooplankton [7,8,9]. A close correlation between zooplankton species richness and ambient temperature was noted for the tundra lakes of Central Siberia and the north-east of the Bolshezemelskaya Tundra [9,10]. It is established that the temperature is the main controller of the latitudinal structure of the species richness of crustaceans in the Norwegian lakes [11] and the Canadian Arctic [12]. In lakes of Northern Europe and Canada, temperature is identified among the most significant factors affecting the composition and structure of cladocerans [12,13,14].
On-going climate warming is likely to lead to an increase in water temperature, a reduction in the duration of the ice cover, an increase in the supply of nutrients from the catchments, which may lead to an increase in plankton production [15]. Changes in water temperature will affect zooplankton through shifts in the composition of dominant species, and changes in the phenology of some species. In addition, climate change will contribute to an increase in the frequency of biological invasions [8,16,17,18,19]. Warming is expected to lead to) a decrease in the habitat of cold-resistant and endemic species and a change in the composition of zooplankton communities in favor of more thermophilic hydrobiont species. As a result, zooplankton species with good dispersal abilities and adapted to temperature changes will become dominant in lakes of high latitudes.
The problem of preserving the biological diversity of the northern territories is currently the most urgent, since the functioning of ecosystems in their natural state is impossible without preserving their species and structural diversity [20,21,22]. Currently, ecological studies of the fauna of freshwater lakes in the northern territories, including zooplankton communities, are at the stage of intensive development. The information on the plankton fauna of the northern lakes of Russia, North America, and Fennoscandia demonstrate that the aquatic ecosystems of these territories are represented by highly specialized species of hydrobionts adapted to the harsh climatic conditions of the Arctic region [10,23,24,25,26].
Despite the low number of studies compared to the lakes and reservoirs of the temperate zone, it is in the zoocenoses of tundra lakes of the Northern Hemisphere where a large number of new and endemic species have been discovered [27,28]. Among all the Arctic territories, the fauna of the lakes of Alaska and the north-east of Siberia is of particular interest to ecologists. The zooplankton communities of these areas exhibit significant number of common species, which is probably due to the faunal exchange of these territories across the Beringian Isthmus in the Pliocene [29,30,31,32].
The species composition of the northern lakes communities is determined both by the landscape features of the catchment basins, various environmental factors, and historical background. The glaciation of the Arctic and Subarctic territories in the Pleistocene affected the biodiversity of invertebrate communities in these regions. Most of these territories escaped glaciation in the Pleistocene and, as a result, full-fledged zooplankton communities were able to form in glacial refugia. It is believed that it was from these reservoirs that the further dispersal of invertebrates took place on the territory of the Palearctic and Nearctic [33,34,35,36,37,38,39]. Therefore, study of species diversity and understanding of the patterns of species distribution are necessary to assess future changes in the structure of aquatic communities that may arise as a result of climate changes or increased anthropogenic impact on the ecosystems of the northern regions.
Currently, these two approaches to the study of the Arctic and Subarctic aquatic ecosystems are closely related and determine the scientific basis for nature conservation, reproduction of biological resources and rational use of high-latitude ecosystems. These approaches can be used to diagnose the state of lake ecosystems subject to anthropogenic and climatic deformations [16,40,41].
The limnological information of the landscapes of the north-western part of the Bolshezemelskaya Tundra (the territory of the Nenets Autonomous Okrug), which is the largest permafrost peatland in Europe, is extremely limited and is inferior to other territories of the north of the European part of Russia in terms of the degree of study. The first comprehensive studies of lake ecosystems of the Bolshezemelskaya Tundra (BZT) took place in the 1960s–1970s of the last century. During this period, lakes were studied in the western (Yushin group) and north-eastern parts of the Bolshezemelskaya Tundra (Vashutkinskie, Padimeyskie and Harbeyskie lakes), as well as lakes located in the basins of the Adzva, Korotaihi, Bolshaya Rogovaya and Seida rivers. Later, in the late 1980s, lakes were studied in the central part of the Bolshezemelskaya Tundra (Inzereysky and Khosedayussky districts). During that research program, an inventory of lakes of different categories and studies of the characteristics of the origin and features of their morphology and areal distribution, as well as the basic hydrological indicators in the largest lakes, were performed and relevant information on the flora and fauna of lakes was obtained [42,43,44,45,46,47].
The purpose of the present study was to (1) characterize the current ecological status of zooplankton communities of lake ecosystems in the north-west of the Bolshezemelskaya Tundra, the largest permafrost peatland of Europe; (2) compare these results with previous assessments of the zooplankton parameters in this region performed 40–50 years ago; and (3) identify environmental factors affecting the structural and functional characteristics of zooplankton communities of tundra lakes in this region.

2. Materials and Methods

Bolshezemelskaya Tundra is located in the North-East of the East European plain, between Pechora and the Urals, within the Nenets Autonomous district and the Komi Republic (Russian Federation). The area is a hilly plain with altitudes of 100–150 m. It is crossed by morainic ridges with peaks up to 200–250 m. The ridges are composed of sedimentary rocks: sandstones and boulder loams left by ancient glaciers [48]. Gley or structureless soils are most common in the Bolshezemelskaya Tundra. On the plains, there are peat–swamp soils (histosols). The vegetation cover of the tundra is represented by lichens, mosses, various grasses and dwarf shrubs.
The climate of the region is subarctic, with long cold winters (−16 to −20 °C) and short cool summers (8 to 12 °C). The thermal regime of the air is formed under the influence of atmospheric circulation, radiation regime, as well as local conditions. The duration of the cold period in the region (average air temperature below 0 °C) increases from west to east from 205 to 245 days, and the warm period (average air temperature above 0 °C)—in the opposite direction. The warmest month of the year is July, and the coldest is January-February. In some years, the air temperature rises to +30 °C in summer and drops to −40 °C and below in winter.
The region is located in the zone of excessive moisture (400 to 700 mm y−1). A sizable area is occupied by permafrost (to the west of the mouth of the Pechora River—isolated, to the east—continuous). Permafrost contributes to the formation of thermokarst relief and waterlogging of the area. In the European part of the tundra, the permafrost is tens of meters thick. In summer, the depth of thawing, depending on the thermophysical properties of the soil, ranges from 0.3 m (clay, peat) to 1.0 m (sandy soils).
A characteristic feature of the tundra is the abundance of thermokarst lakes. The main part of the hydrographic network of the north-east of the European tundra consists of small thaw ponds and thermokarst lakes, which are formed as a result of thawing of permafrost and subsidence of the soil. The main part of thermokarst landforms is confined to peatlands. Most tundra lakes are small and shallow bodies of water, with low, sometimes swampy, permafrost peat banks [49,50,51,52]. For convenience, all studied waterbodies (generally referred to as “lakes”) were classified according to their surface area: depressions (<0.00001 km2), thaw ponds (0.00001–0.001 km2), and thermokarst lakes (>0.001 km2) [52].
During field work, we measured the main morphometric, hydrological and hydrochemical parameters of thermokarst lakes and thaw ponds which included: the depth and area of lakes, the degree of overgrowth by macrophytes, photic layer depth by the Secchi disk, water temperature, pH, electrical conductivity, dissolved oxygen, color and content of iron and of macronutrients [53].
In the course of this study, a comparative analysis of the biocenoses of lakes at different stages of macrophyte overgrowth was carried out. The degree of overgrowth of lakes by macrophytes was calculated as the ratio of the area of thickets of higher aquatic vegetation on the lake to the area of its water area, expressed as a percentage [53]. Lakes were considered lightly and moderately overgrown if the thickets of higher aquatic vegetation occupied less than 30% of the total water area of the reservoir and strongly overgrown if the degree of overgrowth exceeded 30%. In addition, we performed a comparative analysis of the state of the biocenosis of lakes located on three different sites, taking into account the hypsometric and orographic position of the territory.
Zooplankton in the lakes was collected from the surface horizon (0–50 cm for large lakes and 0–20 cm for thaw ponds and depressions) by filtering 30–50 L of water through the Apstein network (the mesh size was 74 µm). Samples were fixed with 4% formalin and processed in the laboratory using standard hydrobiological methods [54]. In total, 50 zooplankton samples were taken from 29 lakes.
When analyzing zooplankton samples, species composition and size groups were taken into account, dominant complexes were identified, and the number (N, ind./m3) and wet biomass (B, g/m3) of organisms were calculated, and the average individual weight (W, mg) of zooplankton. Appropriate manuals were used to identify the zooplankton species [55]. Representatives with a relative number >5% were considered to be structure-forming species.
To analyze the structure of the zooplankton communities of lakes, the following indicators and indices were used: the ratio of major groups (Rotifera, Cladocera and Copepoda) by abundance (number) and biomass (Nrot:Nclad:Ncop; Brot:Bclad:Bcop), the ratio of Cyclopoida and Calanoida biomass (Bcycl:Bcal), the ratio of the biomass of predatory and peaceful zooplankton (B3:B2), the ratio of Cladocera to Copepoda abundance (Ncl:Ncop), the values of the average individual zooplankton mass in communities, the Simpson (Is) and Berger–Parker dominance indices (Ib/p), the Shannon species diversity index calculated by abundances (HN), and the index of uniformity of environmental groups Pielou (I). To identify faunal similarities, we used the Jaccard index (Ij,%) [56,57]. The combined trophic and topological classification of species was used to analyze the trophic structure [58,59,60].
Statistical data processing was performed according to generally accepted methods [61]. The average value (M) and the error of the average value (mx) were used in the analysis. The reliability of sample differences was assessed using the nonparametric Mann–Whitney U-test at a significance level of p < 0.05. The degree of correlation between the varying characteristics were evaluated using correlation analysis. We used the index of rank correlation of Spearman (r) for which values of 0.1 to 0.3 were considered a weak relationship, 0.3 to 0.5 as moderate, 0.5 to 0.7 as marked, 0.7 to 0.9 as close, and 0.90 to 0.99 as very close [62]. All numerical indicators were calculated on a personal computer using Microsoft Excel 2010 and Statistica 10.

3. Results

3.1. Morphometric and Hydrochemical Indicators of the Studied Lakes

The field work was carried out in July–August 2016. The studied water bodies were located beyond the Arctic circle on the territory of the Bolshezemelskaya Tundra (67°43′–67°86′ N, 53°89′–58°86′ E). Figure 1 shows a map of the research area. A total of 29 lakes were studied. The studied lakes were located on three sites in the zone of discontinuous permafrost distribution: the upper course of the Pechora river (Naryan-Mar district; n = 6 lakes) and the catchment basins of the Shapkina rivers (the district of the Halmermusyur ridge and the Big Salindey-musyur, Vesnimusyur, Shapkina-musyur hills; n = 7 lakes) and Kolva (the average flow of the river below and above the village of Khorey-Ver; n = 16 lakes). These sites differed in the density of the hydrographic network, hypsometric and orographic position of the lake basins. The maximum number of lakes per unit area is observed on the site of Khorey-Ver, and the minimum is on the site of Shapkino. The depth of the lakes ranged from 0.5 to 1.5 m and, normally, these lakes freeze solid in winter.
The plant communities of the studied tundra areas were dominated by Ledum palustre L., 1753, Menyanthes trifoliata L., 1753, Eriophorum angustifolium Honck, 1782, Comarum palustre L., 1753, Vetula nana L., 1753, and Rubus chamaemorus L., 1753. Aquatic vegetation in lakes is mainly represented by water sedge (Sameh aquatilis Wahlenb., 1803). Macrophytes were generally concentrated in the coastal zone. Lakes with an area of up to 0.02 km2 had a high degree of macrophyte overgrowth (from 30% to 70% of the lake area). Lakes with a total area of macrophyte overgrowth of no more than 30% were characterized by a border type of overgrowth, and for lakes with a total area of overgrowth with macrophytes of 40–65%, border–floodplain was a characteristic type of overgrowth. A particular feature of all studied aquatic ecosystems was the absence of ichthyofauna.
The studied lakes were characterized by a low degree of mineralization and high color of the water. The water temperature of the surface layers during the study period was in the range of 16–24 °C (air temperature: 14–30 °C). The water columns of the lakes were well-oxygenated. The chemical composition of thermokarst lakes was characterized by a relatively low pH, high concentration of dissolved organic carbon (DOC) and low content of nutrients [52,63]. Hydrochemical indicators of the lakes are shown in Table 1.

3.2. The Biodiversity of Zooplankton

The planktonic fauna of the lakes is represented by species common to northern lakes. In total, 60 species were observed in the zooplankton of tundra lakes (13 Rotifera species, 31 Cladocera species, and 16 Copepoda species). Species diversity was determined by cladocerans (Cladocera). The full list of planktonic invertebrate species inhabiting the studied thermokarst lakes is provided in the Supplementary Material (Table S1).
The species encountered in BZT thermokarst lakes were mainly related to the cold-water faunal complex. According to zoogeographic zoning, zoocenoses consisted of species with Holarctic (35%), Palearctic (34%) and cosmopolitan (31%) distribution. Most forms of zooplankton (23 species or 44% of the total number) were representatives of eurytopic plankton, whereas the proportion of planktonic (15 species) and littoral (14 species) forms was 29% and 27%, respectively. In the zooplankton communities of the studied lakes, oligosaprobes and oligo-β-mesosaprobes predominated (96% of the total number of planktonic organisms).
The largest number of species was observed in the lakes located in the Kola River catchment basin (Khorey-Ver district)—40 species, and in the lakes of the Shapkina and Pechora River catchment basins (Naryan-Mar district), we observed 27 and 35 species, respectively. The lakes located on the territory of the Naryan-Mar and Shapkino sites were dominated by Cladocera (representatives of the genera Bosmina, Daphnia and Polyphemus). The maximum variety of copepods is typical for the lakes of the Khorey-Ver region. Acidophilic crustacean species (Holopedium gibberum Zaddach, 1855) and forms that can tolerate acidic water were observed in thaw ponds with low pH values (representatives of the genera Bosmina, Chydorus Daphnia and Polyphemus).
The dominant core of the plankton complex of the studied lakes consisted of 3 to 6 species. The structure-forming complex was represented by the following species: Kellicottia longispina Kellicott, 1879, Conochilus unicornis Rousselet, 1892, Eudiaptomus gracilis Sars, 1863, Heterocope appendiculata Sars, 1863, Daphnia longiremis Sars, 1862, D. middendorffiana Fischer,1851, Polyphemus pediculus Linne, 1778, Bosmina longispina Leydig, 1860, and B. longirostris Müller, 1785.
For lakes heavily overgrown with macrophytes (n = 14), the largest number of zooplankton species (44 species) was noted; among them, 17 species were unique to this group of lakes. These are mainly thaw ponds with an area of up to 0.02 km2. Lakes with a high degree of overgrowth of the water area with aquatic vegetation were characterized by high diversity of rotifers and the enrichment of the fauna with phytophilic species of cladocerans (Scapholeberis mucronata Müller, Acroperus harpae Baird, 1776, Alonella nana Baird, 1857, Polyphemus pediculus Linne, 1778, Simocephalus vetulus O.F. Müller, 1776, Macrothrix hirsuticornis Norman et Brady, 1867, Oxyurella tenuicaudis G.O. Sars, 1862, g. Alona sp. and others). Among copepods in these lakes, we identified typical representatives of thicket plankton (Eucyclops serrulatus Fischer, 1851, Macrocyclops albidus Jurine, 1820, Acanthocyclops vernalis Fischer, 1853). The values of the Shannon species diversity index (HN), calculated from zooplankton abundance, for this group of lakes ranged from 1.64 to 3.14.
A total of 33 species of zooplankton were observed in lakes that were poorly overgrown with macrophytes (15 lakes), and 6 species were unique to this group of lakes. The values of the Shannon species diversity index (HN) ranged from 0.88 to 2.81. For nine lakes, low species diversity and high degree of dominance of one species in zooplankton communities were observed, mainly in the Khorey-Ver region (eight lakes). Presumably, in such ecosystems, there are free ecological niches allowing the introduction of new species.
The Shannon species diversity index (HN), calculated from the abundance of zooplankton, indicated that the studied thermokarst lakes belonged to the oligotrophic, mesotrophic and eutrophic type. The index of uniformity was 0.7 on average, which indicates a relatively stable and balanced status of zooplankton communities in the studied reservoirs [40].

3.3. Trophic Structure

The nutritional relationships of organisms in reservoirs determine the structure of aquatic ecosystems and can serve as a good indicator of their condition. For all the lakes studied, three to nine trophic groups dominated zooplankton communities.
During the analysis of the trophic structure of zooplankton, nine trophic groups were identified depending on the method of nutrition [58]. Rotifers were divided into two groups—rotifers verticators (verification) and rotifers graspers-suckers (capture and suction, suction—families Asplanchnidae, Trichocercidae). Cladocerans were represented by four groups—primary and secondary filtrators, gatherers and predators. Copepods in the trophic structure are represented by three groups—filtrators, predators and gatherers.
The most complex food web was found in lakes overgrown with macrophytes, in which the maximum number of trophic groups was noted. For lakes with a pH of less than 5.5, there was a reduction in the food web due to the absence of facultative predators. Trophic nets in these lakes were represented by a small number of species, mainly phytophagous filtrators.
Sizable proportion of the zooplankton community of thermokarst lakes consisted of primary filtrators and rotifers (except for families Asplanchnidae) that were feeding in the water column (54% of the total). These are representatives of the genera Kellicottia, Conochilus, Daphnia, Bosmina, Eudiaptomus, Arctodiaptomus. Kellicottia, Conochilus, Daphnia, Bosmina, Eudiaptomus, Arctodiaptomus. The next largest trophic group of organisms were floating–crawling secondary filtrators that extract food from the surface of the substrate (13% of the total). It includes representatives of the family Chydoridae (scrapers and facultative filter feeders). This group was widely represented in overgrown reservoirs. The third largest trophic group (swimming/active trapping) included representatives of the families Asplanchnidae, Polyphemidae, Cyclopidae (12% of the total). Predatory plankton in lakes heavily overgrown with macrophytes, as well as in lakes with an area of 0.0001 to 0.0005 km², occupied the second place in the trophic structure after organisms with a filtration type of nutrition. It is known that the dominance of large filtrators and predators in the food webs of zooplankton communities indicates the oligotrophic status of reservoirs [64].

3.4. Quantitative Characteristics of Zooplankton

The quantitative indicators of zooplankton strongly varied across the lakes. In terms of abundance and biomass, the zooplankton communities of tundra lakes were dominated by cladocerans (41% of the total population and 51% of the total biomass). The contribution of copepods to the total plankton abundance and biomass was 33% of the total abundance and 48% of the total biomass. The average abundance and biomass of zooplankton in thermokarst lakes were 21.3 thous. ind./m3 and 1.13 g/m3, respectively. The minimum number of plankton corresponded to 2.04 thous. ind./m3, the maximum—77.86 thous. ind./m3. The biomass values varied from 0.03 g/m3 to 8.25 g/m3. The quantitative indicators of zooplankton communities were strongly influenced by the degree of overgrowth of lakes with macrophytes. There was a decrease in the quantitative indicators of zooplankton with an increase in the degree of lake overgrowth. For water bodies at the initial stage of macrophyte overgrowth, the average abundance and biomass values were 23.8 thousand units/m3 and 0.73 g/m3, and in heavily overgrown lakes, these values decreased to 7.28 thousand units/m3 and 0.28 g/m3, respectively. Table 2 describes the characteristics of zooplankton communities of thermokarst lakes in three studied districts (Khorey-Ver, Naryan-Mar, and Shapkino).
High zooplankton abundance numbers are typical for lakes located in the Kolva River catchment area (Khorey-Ver district). Copepods dominated the zooplankton population in terms of abundance and biomass. The highest biomass was recorded in the lakes of the Shapkina river catchment area, which is associated with the maximum values of the average individual mass of hydrobionts (Table 2). The main contribution to the total biomass and abundance of zooplankton in this area was made by cladocerans (74% of the total biomass and 72% of the total abundance). For lakes located in the Naryan-Mar district, the leading role of cladocerae in the formation of quantitative indicators of zooplankton (71% of the total biomass and 73% of the total abundance) was noted (Figure 2 and Figure 3). Lakes in the catchments of the Kolva and Pechora rivers were characterized by an increase in the share of rotifers (20–23% of the total abundance; Figure 2, Table 2), which can indicate eutrophication. It is known that an increase in the ratio of the abundance of Cladocera and Copepoda (Nclad/Ncop) and a decrease in the average individual body weight of zooplankton indicate an increase in the trophic level of reservoirs [40].
According to the state of plankton communities, the majority of the studied lakes could be characterized as oligotrophic (22 lakes). According to the size of zooplankton biomass, 7 lakes were assigned to the mesotrophic and eutrophic type. These were mainly thermokarst lakes located in the catchment area of the Shapkina River (5 lakes).

3.5. Assessment of the Influence of Abiotic and Biotic Factors on the Qualitative and Quantitative Characteristics of Zooplankton Communities

The composition and structure of zooplankton communities are formed under the influence of a complex of abiotic and biotic environmental factors. To assess the influence of environmental factors on zooplankton diversity and its quantitative indicators, a nonparametric Spearman rank correlation coefficient was used, since the distribution in the samples did not correspond to normal (Table 3 and Table 4). Correlation analysis demonstrated that the main abiotic factors affecting the species composition and quantitative characteristics of zooplankton were mineralization, pH and lake area (Table 3, Figure 4).
The revealed correlation between total abundance and total biomass of zooplankton and pH was positive and significant (Table 3, Figure 4). A positive relationship between plankton abundance and lake water pH is well expressed for the dominant Cladocera species (D. middendorffiana, B. longispina) and negative for K. longispina (Table 4).
A positive significant relationship was noted between the abundance of zooplankton and the area of reservoirs (r = 0.42, p < 0.05). This link is most clearly traced for rotifers. For the dominant zooplankton species E. gracilis and C. unicornis, the relationship was r = 0.34 (p < 0.05) and r = 0.41 (p < 0.05), respectively (Table 4).
The mineralization of lake water affected the level of quantitative development of cladocerae and rotifers. For Cladocera, positive relationships (p < 0.05) between the quantitative zooplankton characteristics (total abundance and total biomass) and mineralization were observed (r = 0.65 and 0.70, respectively), while the number of Rotifera had a moderate negative relationship with mineralization (r = −0.34, p < 0.05). A positive significant relationship between water mineralization and the number of species in lakes was also observed (r = 0.45, p < 0.05) (Table 3, Figure 4).
Other environmental factors (dissolved oxygen, temperature, and water color) exhibited a weak or moderate negative impact on hydrobionts. There was a moderate negative relationship between the water temperature and the abundance of Cladocera and, in particular, the dominant specie of P. pediculus (r = −0.45, p < 0.05), and a moderate negative relationship between the color of the water and the abundance of copepods (r = −0.33, p < 0.05) (Table 3 and Table 4).
Analysis of interpopulation relationships between the abundance of dominant species of zooplankton revealed a marked positive relationship between the abundance of P. pediculus and the abundance of B. longispina (r = 0.55, p < 0.05), and a significant negative relationship between the abundance of P. pediculus and E. gracilis (r = −0.56, p < 0.05) (Table 4). It is known that predators, by regulating the abundance of phytophages, can stimulate the growth of some species of peaceful zooplankton and thereby weaken the competition of this ecological group for food resources [65,66] (Table 4).

4. Discussion

The planktonic fauna of studied thermokarst lakes is represented by 60 species of zooplankton belonging to 19 families. The zooplankton communities of the studied lakes consist of species widely distributed in the Palearctic and Holarctic with the addition of cosmopolitans. A characteristic feature of the plankton of the studied lakes is the poverty of the rotifer fauna. They are recorded in significant numbers only in large lakes and are almost completely absent in small thaw ponds. Other researchers also noted this feature for the lake ecosystems of the Bolshezemelskaya Tundra [25,47].
A variety of cladocera were noted for the region. Cladocera are quite widespread in the lakes of the tundra zone and they are much more successful in penetrating deep into high latitudes than copepods [8]. Due to parthenogenetic reproduction, short generation time and rapid direct development without intermediate larval stages, Cladocerans can quickly increase their numbers in a new habitat. These features give them an advantage in settling over copepods [8,39,67].
A comparison of the zooplankton species composition of the studied reservoirs with other lakes in the Arctic and subarctic zones of the Northern Hemisphere reveals a significant number of common species [22,68]. Among the rotifers, the common species are Kellicottia longispina, Conochilus unicornis, Asplanchna priodonta Gosse, 1850, Trichocerca rattus O.F. Müller, 1776, Polyarthra dolichoptera Idelson, 1925, Keratella cochlearis Gosse,1851, the cladocerans—Bosmina longirostris, Holopedium gibberum,, Daphnia cristata Sars, 1862, Daphnia pulex Leydig, 1860, Daphnia longiremis, Chydorus sphaericus, Polyphemus pediculus, Scapholeberis ucronate, Simocephalus vetulus the copepods—Eudiaptomus gracilis, Arctodiaptomus wierzejskii Richard, 1888, Heterocope appendiculata, Heterocope borealis Fischer, 1851, Paracyclops fimbriatus Fischer, 1853, Eucyclops serrulatus, Cyclops scutifer Sars, 1863, and Acanthocyclops vernalis.
It should be noted that, despite the features of the relief and the different density of the hydrographic network of the permafrost peatland territories studied in this work (Naryan-Mar, Shapkina, and Khorey-Ver), the zoocenoses of studied lakes exhibit a high degree of similarity (from 57 to 67%). Indeed, the planktofauna of the lakes of the studied region is closest to the fauna of the Vashutkinskie and Harbeyskie lakes’ systems (east of the BZT). The Jaccard similarity index was 71 and 61%, respectively. Such a pattern could be a consequence of the territorial proximity of lakes. The similarity of the zoocenoses of the studied tundra lakes with the polar lakes of Central and Eastern Siberia, the Malozemelskaya tundra is moderate and ranges from 33 to 35%, respectively. In general, the similarity between zooplankton communities of tundra lakes in Russia is especially pronounced in the common fauna of the Cladocera [25,26,69,70,71,72].
Fluctuations in the quantitative indicators of zooplankton in the lakes of the studied territory are associated with a variety of environmental conditions that determine the level of development and diversity of zooplankton communities. According to our results, the main contribution to the total abundance and biomass of the zooplankton community of the studied lakes was provided by crustaceans. The dominance in the abundance and biomass of crustaceans was also noted by researchers for tundra lakes of the Malozemelskaya tundra (~200 km to the west from the study sites), and Western and Central Siberia [9,70,72]. The average zooplankton biomass of the studied lakes (1.13 g/m3, n = 29) is comparable with the literature data for tundra lakes of the Kola Peninsula (0.91 g/m3, n = 24), Bolshezemelskaya Tundra (1.6 g/m3, n = 44) and Central Siberia (1.52 g/m3, n = 35) [9,59].
A comparison of the results obtained with the data of studies conducted in 1986–1988 on the lakes of the Bolshezemelskaya Tundra in the North-Khosedayussky and Inzereysky districts of the Nenets Autonomous District (west of the BZT) [47] shows a decrease in the average indicators of quantitative zooplankton development in the summer of 2016. In 1986–1988, the average values of zooplankton abundance and biomass varied from 70 to 404 thous. ind./m3 and from 1.8 to 5.6 g/m3. In 2016, the average values of zooplankton abundance and biomass varied from 2.0 to 78 thous. ind./m3 and from 0.03 to 8.3 g/m3. The decrease in the quantitative indicators of hydrobionts in 2016 is associated with the trophic status of lakes, most of which were characterized as oligotrophic (22 lakes). It is important to emphasize that in the period from the 1970s to the present, there have been no significant changes in the ecosystems of lakes, and thus the processes of lake ecosystem degradation are slow.
The formation of the zoocenose of tundra lakes in the region is caused by a complex of environmental factors, and the influence of certain factors for different groups of zooplankton may be unequal. As is demonstrated in this study, the species diversity and abundance of zooplankton in the thermokarst lakes were largely determined by morphometric features, hydrochemical and physical indicators, as well as the degree of lake overgrowth by macrophytes. The latter result is consistent with general knowledge that aquatic vegetation plays an important role in the functioning of freshwater ecosystems [73,74,75]. The diversity of biotopes, trophic conditions, concentration of dissolved oxygen, and temperature conditions in macrophyte thickets are favorable for the mass development of all groups of hydrobionts [60,75,76]. Here, we demonstrate that the greatest species diversity of zooplankton is characteristic of small lakes overgrown with macrophytes (up to 0.02 km2). The index of species diversity has high values for this group of reservoirs. The development of the phytophilic–littoral complex of crustaceans was noted in these lakes. Rotifers in zoocenoses were practically absent or their share was insignificant. According to the set of trophic groups, zooplankton in these lakes is more diverse.
According to previous studies in various geographical zones, the number of zooplankton species increases with an increase in the area and depth of lakes [59,77,78,79], and the present study corroborates these findings (see Table 3). However, this pattern is not always true for individual zooplankton species. The greatest species diversity of zooplankton was recorded in small lakes (up to 0.02 km2). It is possible that the highest DOC concentration in small thaw ponds due to coastal peat abrasion and ground vegetation leaching [52] provides a high amount of fresh and relatively bioavailable organic substrates [80] and this can lead to high diversification of heterotrophic bacterial population, which, in turn, can serve as diverse food substrates for various group of phytoplankton. Furthermore, we found a decrease in zooplankton biodiversity and an increase in the degree of dominance of one species with an increase in the area of lakes.
According to our data, the main abiotic factors controlling the structure and quantitative characteristics of zooplankton of tundra lakes were the pH value and water mineralization. The species diversity of zooplankton increases with increasing water mineralization. An increase in the productivity of lakes and species diversity with an increase in mineralization is noted in the literature by many authors [59,81,82,83] and was also reported for phytoplankton in thermokarst lakes of Western Siberia [84]. In the BZT, correlation analysis revealed a positive relationship between the number and biomass of cladocerans and a negative relationship between the quantitative indicators of rotifers and copepods with water mineralization.
Our study demonstrates that the biodiversity, abundance and biomass of zooplankton in lakes increase with increasing pH values. With an increase in the acidity of the lakes, a restructuring of the zooplankton communities was observed. An important role of the lake water acidity as a structure forming factor of zooplankton communities was noted by researchers for subarctic lakes of eastern Siberia [9] and Northern Finland [7].
Correlation analysis revealed a positive relationship of most crustacean species with the pH of lake water, whereas for rotifers, the relationship with this indicator was negative. With increasing pH values, the number of rotifers decreased, but their species diversity increased. In lakes with a pH < 5.5, an increase in the abundance of rotifers was observed, mainly of the species Kellicottia longispina and Conochilus unicornis. The main contribution to the total abundance and biomass of zooplankton in lakes with a pH from 5.5 to 6 was provided by copepods (representatives of the genera Eudiaptomus and Heterocope), and in lakes with a pH > 6 by cladocerans (representatives of the genera Bosmina, Daphnia, and Polyphemus). Crustaceans made the main contribution to the total number and biomass of zooplankton in lakes with a pH from 5.5 to 6. Other researchers also note the important role of crustaceans in the formation of the main part of the biomass in acidic lakes [7,9,85,86,87].

5. Conclusions

Recently, due to climate change in the north-west of the Bolshezemelskaya Tundra, the largest permafrost peatland in Europe, there has been an active degradation of permafrost, the formation of thermokarst landforms, and, as a consequence, an increase in the number of lakes. The studied freshwater ecosystems are at different stages of successional development. Analysis of the composition and structure of zooplankton allows us to assign lakes to the oligotrophic, mesotrophic, and eutrophic types. The absence of a significant anthropogenic load on the studied territories indicates the natural nature of the process of eutrophication of aquatic ecosystems and allowed identifying natural physical, landscape, and hydrochemical factors shaping the zooplankton abundance and diversity.
Contemporary features of the planktonic fauna of lakes are determined by the natural and climatic conditions of the subarctic region. Zooplankton communities were represented by species typical of cold-water oligotrophic reservoirs of northern latitudes. Low species diversity and quantitative characteristics were noted for zoocenoses. A specific feature of the trophic structure of these ecosystems is the dominance of large filtrators and predators that forage in the water column, which indicates the predominance of pasture trophic food chains in reservoirs.
The main factors influencing the structural characteristics of communities were the mineralization and acidity of water, the area of lakes, as well as the degree of overgrowth of the territory of lakes by macrophytes. The biodiversity, abundance, and biomass of zooplankton in lakes increased with increasing pH values. With an increase in the acidity of the lakes, a restructuring of the zooplankton communities was observed. With an increase in water mineralization, the species composition of zooplankton communities became more diverse.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/w15030511/s1, Table S1: Zooplankton species composition of the studied thermokarst lakes of the Bolshezemelskaya Tundra (Accepted abbreviations: NM-Naryan-Mar site, SH-Shapkino site, KV-Khorey-Ver site).

Author Contributions

Conceptualization, E.I.S.; methodology, L.S.S.; field investigation and sampling, A.V.C., S.A.Z., N.V.S., O.Y.M., A.A.C. and T.Y.V.; data formal analysis, S.I.K.; writing—original draft and text, E.I.S. and L.S.S. All authors have read and agreed to the published version of the manuscript.

Funding

The study was mainly funded by RSF No 22-17-00253 and also received partial support from the FNIR «Comprehensive studies of biotic and abiotic components of aquatic ecosystems of the Subarctic and Arctic in a changing natural environment» N° 122011800149-3. LS Acknowledges partial support from TSU Program “Priority 2030”. The selection and analysis of materials was carried out with the funding of RSF No. 22-17-00253, the processing of materials with the support of the FNIR theme and partially with the support of the TSU Development Programme “Priority 2030”.

Data Availability Statement

All data used in this study are available upon request from the corresponding author.

Acknowledgments

The authors express their gratitude to the candidate of biological sciences, senior researcher of the Laboratory of Biology of Aquatic Invertebrates Limnological Institute of the Siberian Branch of the Russian Academy of Sciences N. G. Sheveleva for assistance in determining the species composition of copepods. LS acknowledges partial support from the TSU Program “Priority 2030”.

Conflicts of Interest

The authors declare no conflict of interest.

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Water 15 00511 g001 550
Figure 1. Map of studied sites.
Figure 1. Map of studied sites.
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Water 15 00511 g002 550
Figure 2. Contribution of major zooplankton groups to the total abundance in the zooplankton communities of various sites (August 2016).
Figure 2. Contribution of major zooplankton groups to the total abundance in the zooplankton communities of various sites (August 2016).
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Figure 3. Contribution of major zooplankton groups to the total biomass in zooplankton communities of various sites (August 2016).
Figure 3. Contribution of major zooplankton groups to the total biomass in zooplankton communities of various sites (August 2016).
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Water 15 00511 g004a 550Water 15 00511 g004b 550
Figure 4. Biomass (a), abundance (b,d) and number of zooplankton species (c) depending on pH, mineralization and lakes area.
Figure 4. Biomass (a), abundance (b,d) and number of zooplankton species (c) depending on pH, mineralization and lakes area.
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Table
Table 1. Characteristics of the studied lakes by hydrochemical indicators (average values).
Table 1. Characteristics of the studied lakes by hydrochemical indicators (average values).
ParameterStudy Area Degree of Overgrowth of the Lake
District Khorey-Ver District Shapkino District Naryan-Mar Lightly OvergrownOvergrown
pH5.8 ± 0.36.2 ± 0.35.8 ± 0.66.1 ± 0.15.6 ± 0.1
Dissolved O2, mg/L 8.0 ± 0.68.7 ± 1.58.4 ± 1.18.5 ± 0.37.9 ± 0.2
Conductivity, µS 14.1 ± 3.433.0 ± 11.420.6 ± 6.220.3 ± 3.116.1 ± 2.2
Color, °Cr-Co133 ± 28143 ± 23190 ± 7.8135 ± 5.7178 ± 19
DOC, ppm13.6 ± 2.419.0 ± 3.417.5 ± 7.9––
Fe, µg L−1
(min–max)		204
(74–388)		519
(141–1220) 		290
(107–706)		––
Total-P, µg L−1
(min–max) 		21.2
(6.9–64)		18.4
(12.9–29)		14.3
(8.8–18)		––
Total-N, µg L−1
(min–max) 		617
(263–923)		420
(321–625)		367
(136–488)		––
Number of lakes 16761514
Table
Table 2. General characteristics of zooplankton communities of thermokarst reservoirs in three study sites.
Table 2. General characteristics of zooplankton communities of thermokarst reservoirs in three study sites.
ParameterDistrict Naryan-Mar
(n = 6)		District Shapkino
(n = 7)		District Khorey-Ver
(n = 16)
Number of species11.3 ± 1.010.1 ± 1.07.8 ± 0.6
Average (min–max) abundance, thousand ind./m322.35 (2.04–33.88)19.61 (7.00–39.76)21.58 (27.44–77.86)
Average biomass (min–max), g/m30.44 (0.04–0.79)2.94 (0.21–8.25)0.61 (0.03–1.87)
N Rot:Clad:Cop,%20:73:74:72:2423:22:55
B Rot:Clad:Cop,%6:71:231:74:253:19:78
Nclad/Ncop9.102.300.43
Bcycl/Bcal0.020.050.02
B3/B20.340.080.17
W, mg0.020 ± 0.0060.130 ± 0.0460.040 ± 0.005
Shannon index
by abundance (HN)		2.50 ± 0.122.27 ± 0.161.92 ± 0.18
Index of uniformity Pielou (I)0.71 ± 0.030.69 ± 0.040.62 ± 0.05
Berger–Parker
dominance index (Ib/p)		2.75 ± 0.292.06 ± 0.091.96 ± 0.18
Simpson index by
abundance (Is)		0.23 ± 0.020.28 ± 0.030.39 ± 0.05
N Rot:Clad:Cop and B Rot:Clad:Cop represent the percentage of major groups Rotifera, Cladocera and Copepoda by abundance and biomass, respectively; Nclad/Ncop represents the ratio of Cladocera to Copepoda abundance; Bcycl/Bcal stays for the ratio of Cyclopoida and Calanoida biomass; B3/B2 represents the ratio of the biomass of predatory and herbivorous zooplankton; and W correspond to the values of the average individual zooplankton mass.
Table
Table 3. Correlation analysis of zooplankton structural indicators with hydrological and hydrochemical factors.
Table 3. Correlation analysis of zooplankton structural indicators with hydrological and hydrochemical factors.
ParameterStructural Indicators
N CopB CopN
Clad		B CladN
Rot		B
Rot		Total Abundance, ind./m3Total Biomass, g/m3Number of Species
Area (S)0.130.13−0.01−0.070.400.290.420.12−0.13
Water temperature 0.140.04−0.21−0.300.030.10−0.08−0.19−0.11
pH0.250.300.310.37−0.05−0.140.440.50.00
Dissolved O2 0.000.040.110.10−0.08−0.110.130.050.11
Mineralization 0.290.150.650.70−0.34−0.270.040.250.45
Color Cr-Co0.330.260.110.14−0.10−0.13−0.15−0.140.06
Bold indicates reliable correlations (significance level-0.05), n = 29; N Cop, N Clad, N Rot—abundance groups Copepoda, Cladocera and Rotifera; B Cop, B Clad, B Rot—biomass groups Copepoda, Cladocera and Rotifera.
Table
Table 4. Correlation analysis of the number of dominant zooplankton species in tundra lakes with abiotic and biotic factors.
Table 4. Correlation analysis of the number of dominant zooplankton species in tundra lakes with abiotic and biotic factors.
ParameterThe Dominant Species of Zooplankton
E. gracilisP. pediculusD. middendorffianaB. longispinaC. unicornisK. longispina
Area (S)0.34−0.26−0.270.030.410.15
pH0.110.180.600.570.1−0.34
Mineralization−0.210.700.560.67−0.37−0.14
Water temperature 0.24−0.450.250.020.040.06
E. gracilis −0.56−0.09−0.280.270.12
P. pediculus 0.150.55−0.25−0.09
D. middendorffiana 0.560.00−0.15
B. longispina −0.28−0.05
C. unicornis 0.06
Notes: bold indicates reliable correlations (significance level—0.05), n = 29.
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Sobko, E.I.; Shirokova, L.S.; Klimov, S.I.; Chupakov, A.V.; Zabelina, S.A.; Shorina, N.V.; Moreva, O.Y.; Chupakova, A.A.; Vorobieva, T.Y. Environmental Factors Controlling Zooplankton Communities in Thermokarst Lakes of the Bolshezemelskaya Tundra Permafrost Peatlands (NE Europe). Water 2023, 15, 511. https://doi.org/10.3390/w15030511

AMA Style

Sobko EI, Shirokova LS, Klimov SI, Chupakov AV, Zabelina SA, Shorina NV, Moreva OY, Chupakova AA, Vorobieva TY. Environmental Factors Controlling Zooplankton Communities in Thermokarst Lakes of the Bolshezemelskaya Tundra Permafrost Peatlands (NE Europe). Water. 2023; 15(3):511. https://doi.org/10.3390/w15030511

Chicago/Turabian Style

Sobko, Elena I., Liudmila S. Shirokova, Sergey I. Klimov, Artem V. Chupakov, Svetlana A. Zabelina, Natalia V. Shorina, Olga Yu. Moreva, Anna A. Chupakova, and Taissia Ya. Vorobieva. 2023. "Environmental Factors Controlling Zooplankton Communities in Thermokarst Lakes of the Bolshezemelskaya Tundra Permafrost Peatlands (NE Europe)" Water 15, no. 3: 511. https://doi.org/10.3390/w15030511

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