# Carbon, nutrient and metal controls on phytoplankton concentration and biodiversity in thermokarst lakes of latitudinal gradient from isolated to continuous permafrost

Oleg Pokrovsky, Rinat Manasypov, Oksana Pavlova, Liudmila Shirokova, Sergey Vorobeyev

► To cite this version:

Oleg Pokrovsky, Rinat Manasypov, Oksana Pavlova, Liudmila Shirokova, Sergey Vorobeyev. Carbon, nutrient and metal controls on phytoplankton concentration and biodiversity in thermokarst lakes of latitudinal gradient from isolated to continuous permafrost. Science of the Total Environment, 2022, 806 (Pt 3), pp.151250. 10.1016/j.scitotenv.2021.151250. hal-04843259

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# Carbon, nutrient and metal controls on phytoplankton concentration and biodiversity in thermokarst lakes of latitudinal gradient from isolated to continuous permafrost

Oleg S. Pokrovsky¹*, Rinat M. Manasypov², Oksana A. Pavlova³,

Liudmila S. Shirokova¹,⁴, Sergey N. Vorobyev²

*corresponding author. Email: oleg.pokrovsky@get.omp.eu

Submitted to *Science of the Total Environment*, after revision September 2021

Key words: phytoplankton, thermokarst, permafrost, gradient, thaw, climate warming
Abstract

Shallow thaw (thermokarst) lakes abundant in regions of permafrost-affected peatlands represent important sources of carbon dioxide and methane emission to the atmosphere, however the quantitative parameters of phytoplankton communities which control the C cycle in these lakes remain poorly known. This is especially true considering the roles of permafrost, hydrochemical composition of lakes, lake sizes and season as major governing factors on phytoplankton abundance and biodiversity. In this work, we quantified phytoplankton characteristics of 27 thermokarst lakes (sizes ranging from 115 m² to 1.24 km²) sampled in spring, summer and autumn across a permafrost gradient (isolated, sporadic, discontinuous and continuous zone) in the Western Siberia Lowland (WSL). The biodiversity indices were highest during all seasons in lakes of the continuous permafrost zone and rather similar in lakes of isolated, sporadic and discontinuous permafrost zone. Considering all seasons and permafrost zones, the biomass and cell number of phytoplankton correlated with Dissolved Organic Carbon (DOC), phosphate, and some metal micro-nutrients (Ni, Zn). The strongest correlations were observed for *Cyanophycea* during summer, with pH, Ni, Cu, Zn, Sr, Ba (cell number) and Cu, Zn, Ba (biomass), and during autumn, with DOC, K, Cr, Cu, Zn, Ba, Cd, Pb (biomass). Using a substituting space for time approach for climate warming and permafrost thaw and suggesting a shift in permafrost boundaries northward, we foresee an increase in cell number and biomass in continuous permafrost zone in spring and summer, and a decrease in phytoplankton abundance in the discontinuous and sporadic permafrost zones. The biodiversity of phytoplankton in the continuous permafrost zone might decrease whereas in other zones, it may not exhibit any sizably change. However, in case of strong deepening of the active layer down to underlaying mineral horizons, and the release of some limiting nutrients (Si, P) due to enhanced connectivity of the lake with groundwater, the share of cyanobacteria and diatoms may increase.
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INTRODUCTION

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The change of aquatic biota in the Arctic under climate trends and permafrost thaw is at the forefront of environmental studies in high latitudes (Prowse et al., 2006; Roberts et al., 2017). Arctic warming is anticipated to result in massive carbon (C) mobilization from permafrost peat to atmosphere, rivers and lakes, thereby potentially worsening global warming via greenhouse gases (GHG) emissions (Vachon et al., 2021). The role of biotic component of inland waters, notably phytoplankton, is of crucial importance to understand whether the climate change can switch the lakes of permafrost zone from net source of carbon dioxide (CO₂) emission to C sinks (Elder et al., 2018; Bogard et al., 2019; Shirokova et al., 2020). In this regard, C-rich permafrost peatlands are especially important as they occupy around 3.7 million km² of Arctic and subarctic territories, mostly in Northern Eurasia, and contain huge amount of highly vulnerable carbon (415 Pg C) in soil and surface waters (Hugelius et al., 2020). In all, the frozen peatlands of Northern Hemisphere (Bolshezemelskaya Tundra, 0.25×10⁶ km²; western Siberia 1.05×10⁶ km²; Hudson Bay Lowlands (1.1×10⁶ km²); Northern Siberia and Eastern Siberia lowlands, 0.5×10⁶ km²) account for 14 % of overall permafrost-affected regions worldwide and remain very poorly explored. These peatlands exhibit a disproportionally high contribution to C storage and exchange fluxes and present a prominent exception to well-studied aquatic and soil ecosystems on mineral substrates such as those investigated in Alaska and Scandinavia because the frozen peatlands 1) are developed on flat, low runoff terrain with long water residence time in lakes and ponds; 2) act as important C stock in the form of organic-rich histosols (peat soils); 3) emit substantial amount of CO₂ and methane (CH₄) to the atmosphere from the surface of inland waters (Karlsson et al., 2021) and 4) exhibit high DOC and low pH in waters in contact with peat soils (Shirokova et al., 2021). These factors determine highly specific and still poorly known aquatic communities in dystrophic to mesotrophic peatland waters. Due to lack of nutrients and shallow photic layer, aquatic ecosystems of frozen
peatlands are likely to be very sensitive to permafrost thaw and can respond in totally unknown way to ongoing climate warming in terms in change of their C, nutrient and metal storage as well biodiversity and organisms adaptation strategies. However, in contrast to wide use of plant communities (i.e., Loiko et al., 2020; Yue et al., 2020) or microbial abundances (Song et al., 2021) as ecological indicators of permafrost development, the aquatic organisms are strongly understudied.

Western Siberia falls into the category of key targeting regions outlined in perspectives of biogeochemical studies in the Arctic (Vonk et al., 2019) as this region includes a continuous-discontinuous permafrost transition and experiences substantial thermokarst. As a result, this high-priority region is most susceptible to permafrost thaw thus affecting the biotic population of aquatic systems. The permafrost peatlands of WSL present unique hydrogeochemical surface water features that are capable shaping the abundance and diversity of the planktonic population. The majority of thaw ponds and lakes are located within the flat mound palsa of watershed divides and are thermokarst originated, i.e., formed after thawing of peat and mineral soil ice (Polishchuk et al., 2017, 2018). The thermokarst lakes are isolated, do not have distinct inlets and outlets and possess very small catchments, typically comparable to or less than the water's surface area. All lakes are shallow (< 1–1.5 m), devoid of fish and freeze solid during winter (Manasypov et al., 2015). Due to the dominance of peat rather than mineral deposits within the active (unfrozen) layer, the soil supra-permafrost water delivers high amount of allochthonous Dissolved Organic Matter (DOM) to these lakes (Raudina et al., 2018). This leads to a very shallow photic layer, restricted to the first few decimeters of the water column, due to high concentration of DOC ranging from 10 to 50 mg·L⁻¹ depending on lake size. Moreover, the concentration of dissolved inorganic carbon (DIC) is on average ten times lower than that of DOC and rarely exceeds several mg·L⁻¹. This provides a very low buffering capacity for the lake waters. Finally, the acidic character of terrestrial organic matter subjected to water
102 leaching within the lake watershed (oligotrophic peat, moss biomass) leads to quite acidic
103 waters ($3 \le \text{pH} \le 6$), typically unfavorable for the phytoplankton development, although some
104 acid-tolerant picocyanobacteria can thrive in humic waters (Jasser and Arvola, 2003; Jasser et
105 al., 2009, 2013).

106 These environmental factors (acidic pH, high DOC, lack of stratification, total freeze in
107 winter and peatland context) make the thermokarst lakes of western Siberia peatlands very
108 different from other high-latitude or permafrost-affected lakes of Scandinavia (Forsström et al.,
109 2005, 2007, 2009; Hay et al., 2000; Rautio et al., 2011; Albert et al., 2012), Northern European
110 Russia (Trifonova, 1998; Laing & Smol, 2000), Qinghai Tibet Plateau (Jia et al., 2021; Li et
111 al., 2021; Liang et al., 2021) and North America (Moore, 1978; Vincent, 2000; Milot-Roy &
112 Vincent, 1994; Tang & Vincent, 1999; Tang et al., 1997; Sheath et al., 1986, 1996; Sheath &
113 Steinman, 1982; Douglas & Small, 1994, 1995; Bergeron & Vincent, 1997; Bonilla et al., 2005;
114 Thompson et al., 2012; Paterson et al., 2014; Lougheed et al., 2015; Lewis et al., 2016;
115 Przytulska et al., 2017). Overall, compared to oligotrophic clearwater arctic lake waters,
116 dystrophic, highly acidic and organic-rich lakes are still poorly studied from the view point of
117 phytoplankton population with the exception of very few recent works on picoplankton
118 (Przytulska et al., 2016) or periphyton (Bouchard et al., 2018) in subarctic Quebec. The poor
119 knowledge on phytoplankton abundance and diversity in thermokarst lakes contrasts the
120 increasing amount of work on bacterial and viral population and metabolism in these inland
121 waters (i.e., Comte et al., 2016; Roiha et al., 2016; Crevecoeuret al., 2017; Vigneron et al.,
122 2019, 2020; Levesque et al., 2019). At the same time, the role of photosynthetic microorganisms
123 may be crucial in determining the net C balance of thermokarst lakes in terms of C
124 emission/uptake. On the annual scale, the thermokarst lakes of permafrost peatlands are strong
125 $CO_2$ emitters (i.e., Serikova et al., 2019). However, during summer, phytoplankton $CO_2$ uptake
126 can reduce the $pCO_2$ in both nutrient-rich and nutrient-poor boreal lakes (i.e., Engel et al., 2019).
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In order to estimate the relative importance of this processes in thermokarst lakes of frozen peatlands, quantitative measurements of phytoplankton abundance are needed.

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In previous work, we investigated 20 thermokarst lakes located in discontinuous permafrost zones over 3 seasons demonstrating high phytoplankton biodiversity, dominated by green algae (Pavlova et al., 2016). The number of cells and biomass of cyanobacteria were partially controlled by DIC, whereas the number of diatoms and green algae was linked to DOC, Fe and Si concentration. However, permafrost (and climate) control on phytoplankton abundance and diversity in the thermokarst lakes remains totally unknown. This does not allow prediction of the possible evolution of phytoplankton communities under climate change scenarios. Here we present results of an extended study of 27 lakes located along the permafrost gradient, from isolated/sporadic zones in the forest-tundra, discontinuous (peat palsas) to continuous permafrost zone of polygonal tundra, sampled over three main hydrological seasons.

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We aimed at inventorying their phytoplankton population and testing environmental factors possibly controlling the microorganism population number and biomass as well as the abundance of individual taxons. We hypothesize primary control of lake water hydrochemistry on phytoplankton abundance and we expected a decrease in biomass and biodiversity northward, from isolated to continuous permafrost zone, following a decrease of the water temperature. At the same time, because studied lakes exhibit the highest pH and DIC in the continuous permafrost zone (Manasypov et al., 2020), this trend can be reversed in case of water acidity control on phytoplankton development. It is important to note that there is no latitudinal trend in DOC and nutrient concentrations in thermokarst water bodies across the permafrost gradient of the WSL (Manasypov et al., 2020). We further attempted a 'substituting space for time' approach to foresee possible changes in phytoplankton population induced by a permafrost boundary shift northward. Obtained results should help constrain hydrochemical factors controlling autotrophic processes in the water column. Eventually, this should allow

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evaluation the capacity of thermokarst lakes to act as source or sink of CO₂ under a climate warming scenario in western Siberia.

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## 2. STUDY SITE AND METHODS

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### 2.1. Thermokarst lakes of western Siberia

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The thermokarst (thaw) lakes of the Western Siberia Lowland are developed on palsa peat bogs across the isolated, sporadic, discontinuous and continuous permafrost zones within the northern taiga, forest-tundra and tundra biomes (Fig. 1). The substrate of the lake watersheds is Late Pleistocene sand and clay deposits that are covered by a layer of peat 1 to 2 m thick. The physio-geographical and climatic conditions of studied sites are summarized in Table 1.

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Water bodies ranged from 115 m² to 1.24 km² in diameter and had a similar depth of 1.0 ± 0.5 m as measured in the field (Manasypov et al., 2020). The morphology, hydrology and the water balance of thermokarst lakes have been extensively studied in June, August, and October (Manasypov et al., 2015, 2020). Further hydrochemical characterization of thermokarst lakes and their overall abundance in western Siberia are provided elsewhere (Polishchuk et al., 2017, 2018; Serikova et al., 2019). Given their dissolved nutrient concentration, the lakes can be considered as oligotrophic to weakly mesotrophic. However, small water bodies (< 1000 m²) are quite acidic (3 ≤ pH ≤ 4), and humic (> 20–30 mg·L⁻¹ of DOC) and thus can be considered as dystrophic. No thermal and redox stratification was detected during open water seasons in these shallow fully oxygenated water bodies. The development of thermokarst lakes of western Siberia follows a sequence of maturation stages, from permafrost depressions and subsidences (< 10 m²) to small, actively growing (via peat abrasion at the borders) thaw ponds (10-10,000 m²) and large thermokarst lakes (> 10,000 m²) with stable shoreline (Audry et al., 2011; Pokrovsky et al., 2014). Large lakes (> 100,000 m²) are often subjected to drainage which occurs due to the thawing of the permafrost and the formation of soil subsidences in the valley

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through which lake water flows. The soil stability decreases, which causes a deepening of the flow and the formation of erosion channels, through which the lake water is discharged. The thawed ground is washed away by a stream, which leads to a decrease in the water table of the lake. As a result, lacustrine sediments become exposed. Pioneer plant species colonize the relatively warm and nutrient-rich sediments, thus initiating the succession of vegetation and soil (see Loiko et al., 2020 and references therein for details). The initial herbs are replaced by mosses, and a new cycle "depression → thaw pond → thermokarst lake" initiates. Along this sequence of aquatic ecosystems, there is a systematic increase in pH and DIC and a decrease in pCO₂ and nutrients with an increase in the size of the water body (Shirokova et al., 2013, 2020; Manasypov et al., 2020; Zabelina et al., 2021).

Similar to previous design of the field work (Pavlova et al., 2016), 27 lakes have been sampled during three main hydrological seasons in 2016: 20 May–13 June, 8–24 August and 25 September–8 October. The beginning of June, right after a massive ice break corresponded to “biological spring”; the middle of August exhibited the highest water temperatures and thus corresponded to biological “summer”, and the end of September - beginning of October corresponded to the beginning of the ice formation and can be considered as biological “autumn.” During our sampling campaign, we followed the change of seasons and moved from the south to the north in spring and from the north to the south in autumn, thus collecting lake water at approximately the same hydrological stage and biological season. Sampling and analyses of pH, Specific Conductivity (S.C.), Specific UV absorbance at 254 nm (SUVA), DOC, CO₂, CH₄, DIC, major anions (Cl and SO₄), major cations (Na, Mg, Ca, K), macro-nutrients (Pₜot, P-PO₄, N-NO₃⁻, N-NH₄⁺, Si) and selected micro-nutrients (B, Mn, Fe, Co, Ni, Cu, Zn, Rb, Mo, Ba) were performed as described elsewhere (Manasypov et al., 2020; Serikova et al., 2019).

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## 2.2. Phytoplankton sampling and analyses

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For phytoplankton analyses, a 500-mL bottle of lake water was collected from the central part of the lake (or the deepest part if it was close to the border) using a rubber boat, from the depth of 30 ± 10 cm and immediately fixed with 4 % formalin Lugol's solution. The phytoplankton was concentrated by sedimentation (10-14 days for 500-mL volume). To insure that this pre-concentration allowed total recovery of all species, including the small-sized ones, the biomass yield was verified by centrifugation at 3500 g during 20 min. For consistency with previous studies of thermokarst lakes of permafrost peatlands (cf., Getsen et al., 1994; Trifonova et al., 1998; Patova et al., 2014), the phytoplankton was counted in a sedimentation plankton counting chamber (Guseva, 1959) analogous to commonly used Utermöhl technique (Lund et al., 1958), using AxioLab A1 and Axiovert 40 CFL trinocular inverted fluorescence phase contrast microscopes (Zeiss). The biomass was determined as algal volume for each lake and converted to wet weight assuming a density of 1 g·cm⁻³ after approximating the geometry of the cell (Makarova & Pichkily, 1970). The phytoplankton diversity was evaluated using the Shannon-Weaver's index (SH) and Pielou's index (P) based on the biomass (Odum, 1971) and Simpson and Simpson's equitability indices (SI and SE) (Odum, 1971). The Saprobiity index (S) was evaluated according to Sládecek (1973) and Barinova et al. (2006). In this study, we used classical taxonometric approach to represent phytoplankton variability across lakes and seasons, to insure the consistency with previous studies of phytoplankton in thermokarst (Trfonova, 1998; Bouchard et al., 2018; Paterson et al., 2014) and humic boreal (Forsström et al., 2005; Engel et al., 2019) lakes. Classification of identified algae into functional groups (i.e., Reynolds et al., 2002; Salmaso and Padisak, 2007; Kruk et al., 2010; Salmaso et al., 2015) was not possible because the studied habitats (shallow, non-stratified, non-turbid, acidic, dystrophic humic lakes) belong to none of the established codon except Q (small acidic, humic lakes). However, none of the representative of this codon (Gonyostromum spp, Heterosigma
spp; Padisak et al., 2009) has been identified in thermokarst lakes of western Siberia (Pavlova et al., 2016 and this study).

The data on the taxon concentrations were analyzed with best fit functions based on the Pearson correlation and one-way ANOVA with the STATISTICA version 8 software (StatSoft Inc., Tulsa, OK). Regressions and power functions were used to examine the relationships among the cell number, the biomass, the pH, DIC, DOC and nutrient concentration in the lake water. A criterion for a significant correlation between chemical and biological parameters was that the Pearson coefficients is at p < 0.05. Further identification of phytoplankton drivers in thermokarst lake waters included a Principal Component Analysis which allowed to test the effect of various hydrochemical parameters on total phytoplankton cell number and biomass and those of individual taxons. In addition to PCA, a Redundancy analysis (RDA) was used to extract and summarize the variation in a set of response variables in phytoplankton composition that can be explained by a set of explanatory variables (environmental climatic and hydrochemical factors). The RDA combines a PCA and multiple regression analysis and it was run in XLSTAT is a statistical software that works as an add-on to Excel.

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## 3. RESULTS

### 3.1. Biodiversity of the phytoplankton

The list of sampled lakes together with main hydrochemical parameters is provided in **Table S1 of the Supplement**. The dominant species during each period, representing more than 10 % of total species number, are listed in **Table S2**, whereas the taxa distribution in lakes during three observation seasons, averaged over 4 permafrost zones are summarized in **Table 2**. Based on the three sampling campaigns conducted in 27 lakes across four permafrost zones, 279 taxa of algae species were found. In June, August and October, we identified 42, 24 and 26
252 taxa in the isolated zone, 61, 48 and 39 taxa in the sporadic zone, 32, 71 and 45 taxa in the discontinuous zone and 75, 130 and 111 taxa in the continuous permafrost zone, respectively.
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254 The highest biodiversity was recorded among Charophyta (85 taxa representing from 13.7 % to 35.2 % of total encountered forms in different permafrost zones), green algae (52 taxa corresponding to 12.4–22.2 % of total forms in different permafrost zones) and Cyanobacteria (40 taxa of 9.6 to 14.2 % forms in different permafrost zones). Although the sampling was always performed from the water column (20-40 cm depth), notable components of the identified algae were represented by benthic and periphytic forms of the classes Zygnematophyceae, Chlorophyceae, Cyanophyceae, Bacillariophyceae and others.
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261 The measured biomass and biodiversity indices for individual lakes of each permafrost zones are illustrated in **Figure 2** whereas integral values (averaged over 4–10 lakes in each permafrost zone) of total cell number, biomass, Shannon, Pielu Simpson and Saproblity indices for each permafrost zone during three main seasons are shown in **Figure 3**. The total phytoplankton biomass was dominated by Chlorophyta, Cryptophyta and Dinophyta (30 %, 22 % and 13 %, respectively) (Figure 4).
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267 The biodiversity Shannon's index was the highest in the continuous permafrost zone, during all three season and it was rather similar across isolated, sporadic and discontinuous permafrost zones. This indicates the high species diversity and high and equal species cell number in thermokarst lakes of continuous permafrost zone during all seasons. The Simpson's index of diversity was also the highest in the continuous permafrost zones during spring and summer periods. In contrast, the Simpson's index of equitability was the lowest in the continuous zone and the highest in the discontinuous one (only in summer and autumn). This indicates 1) a low share of individual species in the total community structure of continuous permafrost lakes, consistent with Shannon indices, and 2) an enhanced influence of typical dominant species on the community structure in lakes of discontinuous permafrost zone.
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## 3.2. Phytoplankton cell number, biomass and their possible link to lake size and hydrochemistry of thermokarst lakes across the seasons and permafrost gradient.

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The lake surface area (which reflected the degree of lake maturity) correlated with neither biomass nor the cell number of phytoplankton ($p < 0.05$), as illustrated for each season across all four permafrost zones in **Figure 5**. An overall lack of lake area impact on quantitative parameters of phytoplankton allowed consideration of the effect of other environmental parameters, notably the pH, $pCO_2$, major ions, macro- and micro-nutrients via averaging all lakes in each region and season.

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The mean value of the phytoplankton biomass ranged from 0.2 to 5 $mg_{wet}·L^{-1}$ and exhibited a local maximum in the sporadic to discontinuous permafrost zone in spring and summer and in the sporadic zone in autumn (**Fig. 3**). The cell number varied from 500 $cell·mL^{-1}$ in spring and autumn to 15,000 $cell·mL^{-1}$ in summer, had a maximum in sporadic to discontinuous permafrost zone in spring, and increased northward in summer and autumn.

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A Pearson pairwise correlation allowed to test possible control of major components ($pH$, DOC, $CO_2$), macro-nutrients (P, N, Si, K), micro-nutrients and toxicants on the total biomass and cell number of phytoplankton and those of individual taxons (**Table S3**). Considering total phytoplankton number and biomass across all seasons and permafrost zones, DOC, macro-nutrients ($PO_4$, K), some lithogenic elements (Al, Cr), micro-nutrients (Zn, Ba) and potential toxicant (Cd) exhibited significant positive impact. The total cell number positively ($R > 0.2$) correlated with water temperature, $pH$, $PO_4$, $P_{tot}$ and Ni concentrations. The most pronounced effects were observed in summer and autumn, and the minimal impact was revealed in spring. Thus, in summer, total cell number strongly ($R \ge 0.48$) correlated with $PO_4$, P, Co, Ni, Cu, Zn and Ba. Such correlations were mostly pronounced for Cyanophyceae ($pH$, Ni, Cu, Zn, Sr, Ba with cell number and Cu, Zn and Ba with biomass). In autumn, Cryptophyta demonstrated the highest ($R \ge 0.41$) correlations with DOC, $PO_4$, K, Cr, Cu, Zn, Sr, Ba, and

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Pb. The biomass of Cyanophycea strongly ($R \ge 0.58$, p < 0.01) correlated with DOC, SUVA, K, Cr, Cu, Zn, Cd, Ba, Pb. Furthermore, during this period of the year, the biomass of Chlorophyta strongly increased with lake area, $NO_3$ and V concentration. Overall, in autumn, total phytoplankton biomass sizably correlated ($R \ge 0.42$) with DOC, nutrients ($PO_4$, $NH_4$, K), lithogenic elements (Al, Cr), micro-nutrients (Cu, Zn, Ba) and potential toxicant (Pb).

In contrast to other seasons, the spring period did not reveal sizable links between phytoplankton quantitative parameters and lake water hydrochemistry (Table S3). Among all trace elements, only Pb exhibited significant ($R \ge 0.55$, p < 0.01) control on Bacillariophyta and Charophyta biomass and cell number, and strong control on the biomass of cyanobacteria ($R = 0.98$, p < 0.001). The latter was also positively correlated with $CO_2$, $PO_4$, $NO_3$ and K concentration.

Principal Component Analysis (PCA) demonstrated a general lack of control of environmental parameters (lake depth, area (S), $T_{water}$, macro- and micro-nutrients) on total abundance and biomass of phytoplankton and of individual taxons. The PCA identified two factors that had generally low ability to describe the variance (10 to 5%).

In spring, the 2nd factor acted on cell number, biomass, Bacillariophyta, Charophyta and Pb concentration (Fig. 6). The phytoplankton parameters were not associated to any factor in autumn, and in summer, the 2nd factor acted on cell number. None of the major and minor dissolved components of the lake water were linked to phytoplankton.

The RDA treatment did not provide additional insights into environmental control of phytoplankton concentration and biodiversity across the lakes, seasons and permafrost zones. After normalization, the main result was that the analyses are not statistically significant (p > 0.05). For example, during spring period, the biomass contributes < 30 % to the data inertia but it is linked to none of the predicting factor including the permafrost zones.
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## 4. DISCUSSION

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### 4.1. General features of cell number and biodiversity evolution as a function of lake size and permafrost zone

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The lake area exhibited negligible control on both the biomass and the cell number of total phytoplankton and those of individual taxons. This contrasts the behavior of major hydrochemical parameters such as acidity, DOC, and $pCO_2$ that decreased with an increase in thermokarst lake size (Shirokova et al., 2013, 2020; Zabelina et al., 2020; Manasypov et al., 2020). This result suggests a rather homogeneous distribution of phytoplankton across all stages of lake growth and maturation, from small thaw ponds to large thermokarst lakes. Note that the water temperature at the lake bottom is unlikely to be a controlling factor of the phytoplankton development. Indeed, the shallow, well-mixed WSL lakes present no sizable thermal and chemical stratification (Shirokova et al., 2013; Manasypov et al., 2015, 2020). In addition, the photic layer depth of humic lakes sampled in this work (at 20-40 cm depth) rarely exceeds 0.5 m; in this layer, the temperature was quite homogeneous.

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Consistent with the generally weak control of lake size on phytoplankton abundance, the majority of hydrochemical parameters, including DOC, macro- and micro-nutrient concentration exhibited a rather weak effect on the total microorganisms number and biomass as well as those of individual taxons. The most pronounced control was revealed in autumn, when DOC, macro-nutrients ($PO_4$, $NH_4$, K) and some micro-nutrients (Cu, Zn, Cr, Ba) significantly correlated with the total biomass of phytoplankton, and in particular that of Cyanobacteria and Cryptophyta. For example, lakes from isolated permafrost zone (the most southern Kogalym site), dominated by Cryptomonadaceae, Peridiniaceae and Flagellata, demonstrated a 5-fold decrease in both cell number and biomass with a lake size increase over two orders of magnitude. In this zone, the active layer is very thick and a large amount of unfrozen peat is capable of interacting with lake water, thereby enriching it with limiting

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nutrients. This was especially pronounced for small thaw ponds (≤ 1000 m² in size) which were subjected to maximal impact of peat abrasion at the border and fed by shallow (subsurface, supra-permafrost) water.

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A pronounced impact of certain macro-nutrients (N, P, K) and trace elements on the phytoplankton development in autumn could be originated from vegetation litter (K, N, P), peat (Cu, Zn, Ba, Pb), and deep soil mineral horizons (Al, Cr). This may be linked to enhanced mobilization of these elements from decaying plant litter at the surface and from deep (frozen) peat and mineral horizons, when the active layer was at its maximum. Another example is CO₂, PO₄, NO₃, K and Pb control on Cyanophyceae biomass during the spring. It is possible that this reflects the release of CO₂, P, N, K from vegetation biomass by melted snow (Broder and Biester, 2017; Manasypov et al., 2020), and delivery of atmospherically-originated Pb from snow. The importance of snowmelt on Pb delivery to lakes is known from elemental mass balance estimation in the WSL (Shevchenko et al., 2017).

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A first-order explanation of low environmental control on thermokarst lake phytoplankton abundance is the action of two factors: 1) inhibition of phytoplankton development by acidic, organic-rich peat waters (Pavlova et al., 2016 and references therein) and 2) promotion of possible bloom due to nutrient delivery from surface vegetation and thawing peat horizons (Shirokova et al., 2015). The latter is fairly well known from laboratory experiments on cyanobacterial growth on organic substrates obtained from moss and peat leachates (Shirokova et al., 2017). Overall, harsh conditions at the beginning of thaw in small water bodies (low pH, high DOC and shallow photic layer) were counterbalanced by enhanced delivery of nutrients, notably P and N, but also some micro-nutrients. Upon progressive lake size increase, initial dystrophic conditions are replaced by higher pH and lower DOC, thus leading to an increase in the photic layer. However, the delivery of main nutrients also drastically decreases as the ratio of lake circumference (and lake watershed) to lake volume

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decreases, given very small watershed area of thermokarst lakes in western Siberia (Manasypov et al., 2020).

A tentative explanation of the association, in spring, between the 2nd PCA factor and cell number, biomass, Bacillariophyta, Charophyta and Pb concentration (Fig. 6 A) is that these algae (diatoms and chara) are delivered to the lakes from submerged supports (grass, mosses) of the lake watershed and within the lake border. During this period, Pb is massively delivered to the lakes due to its presence in melted snow and within the snow-water leached lichens and mosses (Shevchenko et al., 2017).

One of the hypotheses of this study was a decrease of biomass and biodiversity northward, from isolated to continuous permafrost zone. However, we discovered rather reverse trends, with maximal phytoplankton cell number (in summer) observed in the continuous permafrost zone. Most likely, elevated pH in this zone and sufficiently high water temperature during summer (16–17 °C, see Table S1) allowed for strong development of Chlorophyta, Cryptophyta, Cyanophyceae and Flagellata. In contrast, we do not have a straightforward explanation for local maxima of biomass in spring and autumn, observed in the sporadic permafrost zone (Fig. 3 B). One possibility is a maximal delivery of limiting macro- and micro-nutrients from the watershed to the lake in this permafrost zone. Indeed, it is known that the watershed export fluxes of some components (Particulate Organic Carbon (POC), DOC, Si, Fe, total dissolved phosphorus (Ptot) and phosphate (PO4)) also exhibit a maximum at the permafrost front boundary, in the discontinuous to the sporadic zone (Krickov et al., 2018; Pokrovsky et al., 2020). It is thus not excluded that freshly delivered from the lake watershed essential components are quickly consumed by autotrophic microorganisms and thus no correlations between phytoplankton parameters and these component concentrations are encountered in thermokarst lake waters.

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## 4.2. Comparison with other Arctic and subarctic lakes

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Among thermokarst lakes studied all over the world, such as from the Kolyma lowland (Walter Anthony et al., 2014), the Lena Delta (Boike et al., 2013), Northern Siberia (Khaliullina et al., 2016), Mackenzie Delta plain (Tank et al., 2009, 2011; Grosse et al., 2013; Walter Anthony & Anthony, 2013), Qinghai Tibet Plateau (Mu et al., 2016; Chen et al., 2021) and those north of Quebec (Laurion et al., 2010; Negandhi et al., 2013), only lakes of Canadian permafrost peatlands (Prsytulska et al., 2016; Wauthy & Rautio, 2020) can serve as a first order analogue of WSL thermokarst lakes. However, such an analogy should be considered with caution given much higher DOC concentration and lower pH in the western Siberia lakes compared to the more oligotrophic Canadian water bodies. These factors create quite hostile environments in the WSL lakes for most phytoplankton, including cyanobacteria and diatoms.

Furthermore, due to their very shallow (0.5–1.5 m) depth and good wind mixing, WSL lakes are not stratified and do not exhibit prolonged hypoxia or anoxia in the bottom waters during summer (Manasypov et al., 2015). This is unlike the Canadian thaw lakes (northern Québec) which are sizably deeper and influenced by underlaying mineral deposits (Prsytulska et al., 2016). The main source of solutes for thermokarst lakes of the WSL is thawed peat and surface vegetation (moss and lichen, Manasypov et al., 2017; Payandi-Rolland et al., 2020; Shirokova et al., 2021). This leads to acidic, Si-poor, and humic-rich nature of the lake water, which is not suitable for diatoms compared to the oligotrophic or ultra-oligotrophic lakes of other Arctic and subarctic regions on mineral substrates, including those of the Bolshezemelskaya tundra (Trifonova, 1998; Patova, 2014). For example, in most thermokarst lakes investigated in this study, the diatoms constituted only 6 to 10 % of the total taxon number (Table 2) and contributed only 7 % to the total biomass (Fig. 4). Low diatom abundance is consistent with quite low Si concentration in lakes across the WSL permafrost gradient (typically 200 µg·L⁻¹
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in isolated to discontinuous permafrost zone; 300 to 400 µg·L⁻¹ in the continuous permafrost zone, Manasypov et al., 2020).

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Similar to previous study of phytoplankton in the discontinuous permafrost zone during three seasons (Pavlova et al., 2016), the acidic environment of these lakes brought about the dominance of green algae (Chlorophyta) desmids which are typical for low pH boreal waters (Kosinskaya, 1960) and include a variety of genera *Botryococcus*, *Dictyospaerium*, *Monoraphidium*, *Pseudosphaerocystis* and others). These results are in general agreement with prevalence of eukaryotic over prokaryotic picophytoplankton in shallow eutrophic lakes (Craig, 1987; Mozés et al., 2006), boreal humic lakes (Jasser & Arvola, 2003), and in acidic dystrophic lakes (Stockner & Shortreed, 1991) which is partially linked to strong light extinction (Pick & Agbeti, 1991).

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The majority of studied lakes in sporadic to discontinuous permafrost zone exhibited a pH range between 4 and 6. In contrast, the lakes of the continuous permafrost zone (Tazovsky) exhibited the highest pH (up to 7.5–7.6) and were also accompanied by much higher cell number, Shannon's and Simpson's indices of diversity. Presumably, elevated pH and more abundant bicarbonate ions are beneficial for phytoplankton development. Indeed, the proportion of cyanobacteria and diatoms in the phytoplankton population (biomass) of western Siberia thermokarst lakes from isolated to discontinuous permafrost zone ranged from 3.5 % to 2.3 % and 3.6 % to 12 %, respectively (Fig. 4). Only in less acidic thermokarst lakes from the continuous permafrost zone lakes, the proportion of cyanobacteria and diatoms in the phytoplankton biomass raised to 7 ± 6 % (max. 48 %) and 11 ± 9 % (max. 43 %), respectively. Such a low proportion of cyanobacteria and diatoms in thermokarst lakes of the WSL contrasts their dominance in other subarctic and High Arctic lakes and ponds (Milot-Roy & Vincent, 1994; Sheath et al., 1996; Vézina & Vincent, 1997; Vincent, 2000; Vincent et al., 2000; Ratté-Fortin et al., 2020), including thermokarst lakes of Yakutia (Kopyrina et al., 2020). This can be

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explained primarily by the pH regime. In fact, neutral pH, eutrophic shallow tundra lakes of the
Bolshezemelskaya tundra (Trifonova, 1998) demonstrated dominance of cyanobacteria (75 %
of the total biomass). The latter habitats are represented by a peat bog palsa permafrost-bearing
region that can be considered as most similar to thermokarst lakes of western Siberia, although
the pH of the Bolshezemelskaya tundra permafrost lakes is 1 to 2 units higher and the DOC is
a factor of 2 to 3 lower than those of thermokarst lakes studied in this work. Consistent with
this observation, in the WSL lakes the pH exerted positive control on the number of
Cyanophyceae, which was especially pronounced during summer (R = 0.49, p < 0.01).

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4.3. *Consequences for CO₂ regime, DOC quality and permafrost boundary shifts*

Considering the range of phytoplankton biomass concentration in the thermokarst lakes
during summer (0.5 to 3 mg wet L⁻¹), together with the assumption of a doubling of the cell
population every 2 days (as measured in the field, Shirokova et al., 2009) and the wet:dry ratio
of 10:1, the primary productivity in the water column is equal to 0.012 to 0.075 mg·C·L⁻¹·day⁻¹.
This is significantly lower than the heterotrophic bacterioplankton respiration in thermokarst
lakes of western Siberia (~0.3 mg·C·L⁻¹·day⁻¹, Shirokova et al., 2013). Such a difference
suggests net heterotrophic status of thermokarst lakes, i.e., CO₂ emission due to heterotrophic
mineralization of allochthonous DOM. Indeed, all WSL lakes act as a strong CO₂ source for
the atmosphere as indicated by a field study of the CO₂ emission in the WSL thermokarst lakes
across a permafrost gradient (Serikova et al., 2019). However, in summer period, the day time
CO₂ fluxes of large lakes may switch from emission to absorbance (Shirokova et al., 2020).
The most likely reason for CO₂ uptake is photosynthesis of lake macrophytes and aquatic
vegetation (i.e., submerged mosses) rather than the phytoplankton activity of the water column.

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Another interesting results of phytoplankton quantification performed in the present
work is an assessment of autochthonous DOC production (phytoplankton capacity to release

475
DOC into the lake water). It is known that the extracellular release of soluble $C_{org}$ ranges from 10 to 20 % of the particulate $C_{org}$ produced by phytoplankton (Baines and Pace, 1991). Given the typical range of phytoplankton biomass concentration in thermokarst lakes of the WSL (0.5 to 5 $mg·L^{-1}$), the autochthonous DOC production is between 0.05 and 0.6 $mg·L^{-1}$. This is a negligibly small number relative to the allochthonous DOC reservoir in these lakes across the studied permafrost gradient (10 to 30 $mg·L^{-1}$, Manasypov et al., 2020). High concentration of allochthonous carbon is consistent with dominance of soil (humic and fulvic) chromoforic DOM in thermokarst lakes of western Siberia, as also reflected in the high value of $SUVA_{254}$ (4.0 ± 0.7 $L·mg^{-1}·m^{-1}$, averaged over all permafrost zones; Manasypov et al., 2020).

Assuming that climate warming and permafrost thaw will produce a northward shift in the permafrost zones and applying a substituting space for time scenario, already tested for river, lake water, soil solutions and the GHG regime in the WSL (Krickov et al., 2018; Manasypov et al., 2014, 2020; Raudina et al., 2017, 2018; Serikova et al., 2019; Vorobyev et al., 2017), results of the present study suggest that phytoplankton biomass, cell number and community diversity in "southern" (isolated and sporadic zones) will not appreciably change. If the continuous permafrost zone disappears and discontinuous shifts northward, then one can expect a decrease in the cell number and biodiversity. An alternative scenario is that, due to thickening of the active layer, there will be an increase in groundwater connectivity leading primarily to thawing of currently frozen peat down to underlying mineral horizons. This may happen both at the lake border and in the lake sediments. As a result of enhanced mineral - lake water interaction across all permafrost zones, the pH of thermokarst lakes and ponds, determined by connectivity of lake water with mineral horizons, might increase upon the permafrost thaw. This, together with enhanced release of limiting nutrients (P, Si, Fe) from previously frozen soil minerals, may create favorable conditions for cyanobacterial and diatomous phytoplankton development in all permafrost regions.
501 CONCLUSIONS

502 A study of 27 shallow, acidic and organic-rich thermokarst lakes and thaw ponds across
503 four permafrost zones of western Siberia permafrost peatlands, sampled over 3 main
504 hydrological seasons demonstrated a lack of effect of the water body size on phytoplankton
505 biomass and cell number. The dominant taxa in total biomass were Chlorophyta, Cryptophyta
506 and Dinophyta, whereas Charophyta, Chlorophyta and Cyanophyceae accounted for the majority
507 of species number without distinct control of season, lake size and permafrost zone. The
508 biodiversity was the highest in the lakes of continuous permafrost zone and rather similar
509 among other zones. The former exhibited the highest pH (across all seasons) and sufficiently
510 high water temperature (during the sammer), favorable for the phytoplankton development.

511 The phytoplankton biomass ranged from 0.2 to 5 mgwet·L⁻¹ and exhibited a local
512 maximum in the sporadic to discontinuous permafrost zone in spring and summer and in the
513 sporadic zone in autumn. The cell number varied from 500 to 15,000 cell·mL⁻¹, had a maximum
514 in the sporadic to discontinuous permafrost zone in spring, and increased northward in summer
515 and autumn. There was an overall low controlling effect of lake water hydrochemistry on
516 quantitative parameters of phytoplankton abundance. We hypothesize that rather harsh
517 conditions at the beginning of thaw (low pH, high DOC and shallow photic layer) were
518 counterbalanced by enhanced delivery of macro- and micro-nutrients from thawing peat and
519 surface vegetation.

520 Thermokarst lakes of the WSL act as strong CO₂ emitters to the atmosphere due to the
521 dominance of heterotrophic bacterial degradation of allochthonous DOM over the primary
522 productivity of phytoplankton. Under a climate warming scenario, a thawing of peat permafrost
523 and thickening of the active layer down to mineral horizons will lead to an increase in
524 connectivity between the groundwater (mineral soils) and the lake. This may increase the lake
525 water pH and some currently limiting nutrient concentrations. Such changes in lake
526 hydrochemistry may favor development of cyanobacteria and diatoms which are currently
527 subordinate taxons relative to green and chara algae.

528

529 Acknowledgements

530 We acknowledge support from RFBR grants № 20-05-00729_a and 19-55-15002-cnrs. Partial
531 support from RSF 18-17-00237-P, a Belmont Forum project VULCAR-FATE and RFBR No
532 21-54-75001 BF_soils is also acknowledged. The study was carried out using the research
533 equipment of the Unique Research Installation “System of experimental bases located along
534 the latitudinal gradient” TSU.

535

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904

<table><caption>**Table 1.** The physio-geographical and climatic conditions of thermokarst lakes in four study sites of the Western Siberian Lowland. MAT is mean annual air temperature.</caption><thead><tr><th>Site</th><th>Coordinates</th><th>Permafrost zone</th><th>MAAT, °C</th><th>Mean annual precipitation, mm</th><th>Mineral substrate</th><th>Peat thickness, m</th><th>Seasonal thaw depth, cm</th><th>Lake average depth (summer), cm</th><th>Mean annual ice-free period, days</th><th>Melting date</th><th>Freeze-up date</th><th>Vegetation period, days</th></tr></thead><tbody><tr><td>Tazovsky</td><td>67.4°N 78.7°E</td><td>Continuous</td><td>-9.1</td><td>363</td><td>clay loam and loam</td><td>0.2-1.5</td><td>44</td><td>90±35</td><td>111</td><td>25.05-10.06</td><td>12.09-30.09</td><td>93 (07.06-10.09)</td></tr><tr><td>Urengoy</td><td>66.0°N 78.3°E</td><td>Discontinuous</td><td>-7.8</td><td>453</td><td>loam and silt loam</td><td>0.3-1.2</td><td>49</td><td>36±25</td><td>118</td><td>20.05-05.06</td><td>20.09-05.10</td><td>96 (07.06-11.09)</td></tr><tr><td>Khanymey</td><td>63.8°N 75.6°E</td><td>Discontinuous/ Sporadic</td><td>-5.6</td><td>540</td><td>sand</td><td>0.7-1.1</td><td>40-90</td><td>45±27</td><td>137</td><td>15.05-05.06</td><td>25.09-07.10</td><td>107 (31.05-15.09)</td></tr><tr><td>Kogalym</td><td>62.3°N; 74.2°E</td><td>Isolated/ Sporadic</td><td>-4.0</td><td>594</td><td>sand</td><td>1.0-1.5</td><td>-</td><td>125±77</td><td>141</td><td>20.04-10.05</td><td>25.09-15.10</td><td>111 (29.05-17.09)</td></tr></tbody></table>

905
<table><caption>**Table 2.** Taxa distribution in lakes during three observation seasons across the four permafrost zones.</caption><thead><tr><th colspan="8">CONTINUOUS</th></tr><tr><th></th><th colspan="2">Spring</th><th colspan="2">Summer</th><th colspan="2">Autumn</th><th colspan="2">Total content</th></tr><tr><th></th><th></th><th>%</th><th></th><th>%</th><th></th><th>%</th><th></th><th>%</th></tr></thead><tbody><tr><td>Cyanophycea</td><td>8</td><td>10.7</td><td>25</td><td>19.2</td><td>12</td><td>10.8</td><td>30</td><td>14.2</td></tr><tr><td>Cryptophyta</td><td>8</td><td>10.7</td><td>8</td><td>6.2</td><td>10</td><td>9.0</td><td>19</td><td>9.0</td></tr><tr><td>Dinophyta</td><td>6</td><td>8.0</td><td>7</td><td>5.4</td><td>3</td><td>2.7</td><td>10</td><td>4.7</td></tr><tr><td>Chrysophyta</td><td>5</td><td>6.7</td><td>3</td><td>2.3</td><td>3</td><td>2.7</td><td>9</td><td>4.2</td></tr><tr><td>Bacillariophyta</td><td>8</td><td>10.7</td><td>6</td><td>4.6</td><td>11</td><td>9.9</td><td>14</td><td>6.6</td></tr><tr><td>Chlorophyta</td><td>17</td><td>22.7</td><td>31</td><td>23.8</td><td>25</td><td>22.5</td><td>47</td><td>22.2</td></tr><tr><td>Xanthophyta</td><td>1</td><td>1.3</td><td>2</td><td>1.5</td><td>1</td><td>0.9</td><td>4</td><td>1.9</td></tr><tr><td>Charophyta</td><td>18</td><td>24.0</td><td>36</td><td>27.7</td><td>35</td><td>31.5</td><td>61</td><td>28.8</td></tr><tr><td>Flagellata</td><td>1</td><td>1.3</td><td>1</td><td>0.8</td><td>2</td><td>1.8</td><td>2</td><td>0.9</td></tr><tr><td>Euglenozoa</td><td>3</td><td>4.0</td><td>11</td><td>8.5</td><td>9</td><td>8.1</td><td>16</td><td>7.5</td></tr><tr><td>Rhodophyta</td><td>0</td><td>0.0</td><td>0</td><td>0.0</td><td>0</td><td>0.0</td><td>0</td><td>0.0</td></tr><tr><td><strong>Total taxons</strong></td><td><strong>75</strong></td><td></td><td><strong>130</strong></td><td></td><td><strong>111</strong></td><td></td><td><strong>212</strong></td><td></td></tr><tr><th colspan="8">DISCONTINUOUS</th></tr><tr><th></th><th colspan="2">Spring</th><th colspan="2">Summer</th><th colspan="2">Autumn</th><th colspan="2">Total content</th></tr><tr><th></th><th></th><th>%</th><th></th><th>%</th><th></th><th>%</th><th></th><th>%</th></tr><tr><td>Cyanophycea</td><td>3</td><td>9.4</td><td>9</td><td>12.7</td><td>2</td><td>4.4</td><td>14</td><td>13.3</td></tr><tr><td>Cryptophyta</td><td>4</td><td>12.5</td><td>6</td><td>8.5</td><td>3</td><td>6.7</td><td>8</td><td>7.6</td></tr><tr><td>Dinophyta</td><td>3</td><td>9.4</td><td>4</td><td>5.6</td><td>5</td><td>11.1</td><td>8</td><td>7.6</td></tr><tr><td>Chrysophyta</td><td>2</td><td>6.3</td><td>5</td><td>7.0</td><td>3</td><td>6.7</td><td>8</td><td>7.6</td></tr><tr><td>Bacillariophyta</td><td>6</td><td>18.8</td><td>5</td><td>7.0</td><td>4</td><td>8.9</td><td>9</td><td>8.6</td></tr><tr><td>Chlorophyta</td><td>3</td><td>9.4</td><td>7</td><td>9.9</td><td>8</td><td>17.8</td><td>13</td><td>12.4</td></tr><tr><td>Xanthophyta</td><td>1</td><td>3.1</td><td>1</td><td>1.4</td><td>0</td><td>0.0</td><td>2</td><td>1.9</td></tr><tr><td>Charophyta</td><td>6</td><td>18.8</td><td>29</td><td>40.8</td><td>17</td><td>37.8</td><td>37</td><td>35.2</td></tr><tr><td>Flagellata</td><td>2</td><td>6.3</td><td>2</td><td>2.8</td><td>1</td><td>2.2</td><td>2</td><td>1.9</td></tr><tr><td>Euglenozoa</td><td>2</td><td>6.3</td><td>3</td><td>4.2</td><td>2</td><td>4.4</td><td>4</td><td>3.8</td></tr><tr><td>Rhodophyta</td><td>0</td><td>0.0</td><td>0</td><td>0.0</td><td>0</td><td>0.0</td><td>0</td><td>0.0</td></tr><tr><td><strong>Total taxons</strong></td><td><strong>32</strong></td><td></td><td><strong>71</strong></td><td></td><td><strong>45</strong></td><td></td><td><strong>105</strong></td><td></td></tr><tr><th colspan="8">SPORADIC</th></tr><tr><th></th><th colspan="2">Spring</th><th colspan="2">Summer</th><th colspan="2">Autumn</th><th colspan="2">Total content</th></tr><tr><th></th><th></th><th>%</th><th></th><th>%</th><th></th><th>%</th><th></th><th>%</th></tr><tr><td>Cyanophycea</td><td>7</td><td>11.5</td><td>4</td><td>8.3</td><td>2</td><td>5.1</td><td>9</td><td>9.6</td></tr><tr><td>Cryptophyta</td><td>6</td><td>9.8</td><td>3</td><td>6.3</td><td>3</td><td>7.7</td><td>7</td><td>7.4</td></tr><tr><td>Dinophyta</td><td>6</td><td>9.8</td><td>1</td><td>2.1</td><td>2</td><td>5.1</td><td>6</td><td>6.4</td></tr><tr><td>Chrysophyta</td><td>5</td><td>8.2</td><td>1</td><td>2.1</td><td>1</td><td>2.6</td><td>5</td><td>5.3</td></tr><tr><td>Bacillariophyta</td><td>6</td><td>9.8</td><td>6</td><td>12.5</td><td>3</td><td>7.7</td><td>10</td><td>10.6</td></tr><tr><td>Chlorophyta</td><td>10</td><td>16.4</td><td>9</td><td>18.8</td><td>9</td><td>23.1</td><td>20</td><td>21.3</td></tr><tr><td>Xanthophyta</td><td>0</td><td>0.0</td><td>1</td><td>2.1</td><td>0</td><td>0.0</td><td>1</td><td>1.1</td></tr><tr><td>Charophyta</td><td>17</td><td>27.9</td><td>18</td><td>37.5</td><td>16</td><td>41.0</td><td>30</td><td>31.9</td></tr><tr><td>Flagellata</td><td>2</td><td>3.3</td><td>1</td><td>2.1</td><td>2</td><td>5.1</td><td>2</td><td>2.1</td></tr><tr><td>Euglenozoa</td><td>2</td><td>3.3</td><td>3</td><td>6.3</td><td>1</td><td>2.6</td><td>3</td><td>3.2</td></tr><tr><td>Rhodophyta</td><td>0</td><td>0.0</td><td>1</td><td>2.1</td><td>0</td><td>0.0</td><td>1</td><td>1.1</td></tr><tr><td><strong>Total taxons</strong></td><td><strong>61</strong></td><td></td><td><strong>48</strong></td><td></td><td><strong>39</strong></td><td></td><td><strong>94</strong></td><td></td></tr><tr><th colspan="8">ISOLATED</th></tr><tr><th></th><th colspan="2">Spring</th><th colspan="2">Summer</th><th colspan="2">Autumn</th><th colspan="2">Total content</th></tr><tr><th></th><th></th><th>%</th><th></th><th>%</th><th></th><th>%</th><th></th><th>%</th></tr><tr><td>Cyanophycea</td><td>8</td><td>19.0</td><td>2</td><td>8.3</td><td>0</td><td>0.0</td><td>10</td><td>13.7</td></tr><tr><td>Cryptophyta</td><td>5</td><td>11.9</td><td>4</td><td>16.7</td><td>4</td><td>15.4</td><td>10</td><td>13.7</td></tr><tr><td>Dinophyta</td><td>3</td><td>7.1</td><td>0</td><td>0.0</td><td>4</td><td>15.4</td><td>6</td><td>8.2</td></tr><tr><td>Chrysophyta</td><td>3</td><td>7.1</td><td>1</td><td>4.2</td><td>1</td><td>3.8</td><td>4</td><td>5.5</td></tr><tr><td>Bacillariophyta</td><td>7</td><td>16.7</td><td>4</td><td>16.7</td><td>6</td><td>23.1</td><td>13</td><td>17.8</td></tr><tr><td>Chlorophyta</td><td>6</td><td>14.3</td><td>7</td><td>29.2</td><td>4</td><td>15.4</td><td>13</td><td>17.8</td></tr><tr><td>Xanthophyta</td><td>3</td><td>7.1</td><td>1</td><td>4.2</td><td>0</td><td>0.0</td><td>3</td><td>4.1</td></tr><tr><td>Charophyta</td><td>5</td><td>11.9</td><td>4</td><td>16.7</td><td>3</td><td>11.5</td><td>10</td><td>13.7</td></tr><tr><td>Flagellata</td><td>2</td><td>4.8</td><td>1</td><td>4.2</td><td>2</td><td>7.7</td><td>2</td><td>2.7</td></tr><tr><td>Euglenozoa</td><td>0</td><td>0.0</td><td>0</td><td>0.0</td><td>2</td><td>7.7</td><td>2</td><td>2.7</td></tr><tr><td>Rhodophyta</td><td>0</td><td>0.0</td><td>0</td><td>0.0</td><td>0</td><td>0.0</td><td>0</td><td>0.0</td></tr><tr><td><strong>Total taxons</strong></td><td><strong>42</strong></td><td></td><td><strong>24</strong></td><td></td><td><strong>26</strong></td><td></td><td><strong>73</strong></td><td></td></tr></tbody></table>
<figure><img src="image_2.png" /><figcaption>**Figure 1.** Map of the study site. The area around the Tazovsky settlement (Continuous permafrost zone), the area around the Urengoy settlement (Discontinuous permafrost zone), the area around the Khanymey settlement (Sporadic permafrost zone) and the area around the Kogalym city (Isolated permafrost zone).</figcaption></figure>

910

911

912

913

914

915
<figure><img src="image_3.png" /><figcaption>**Figure 2.** Quantitative parameters of phytoplankton abundance and biodiversity of individual lakes across four permafrost zones studied in spring (May), summer (August) and autumn (September). Abbreviations LKg, LKh, LU and LT stand for lakes sampled in isolated (Kogalym), sporadic (Khanymey), discontinuous (Urengoy) and continuous (Tazovsky) permafrost zones. See Table S1 for identification of lakes and their hydrochemical features.</figcaption></figure>

916

917

918

919

920

921

922
<figure><img src="image_4.png" /><figcaption>**Figure 3.** Integral values (averaged from 4 to 10 lakes in each permafrost zone) of total cell number (A), biomass (B), Shannon (C), Pielu (D), Simpson (E) and Saprobiity (F) indices for each permafrost zone during three main seasons.</figcaption></figure>
<figure><img src="image_5.png" /><figcaption>B</figcaption></figure>

**Figure 4.** Share of different taxons in overall phytoplankton biomass, averaged over all permafrost zones for different seasons (left column, **A**) and averaged over all seasons for four different permafrost zones (right column, **B**).

932

933

934

935

936

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938
SPRING

<figure><img src="image_6.png" /></figure>

SUMMER

<figure><img src="image_7.png" /></figure>

AUTUMN

<figure><img src="image_8.png" /></figure>

939

940

941 **Figure 5.** Lack of lake size impact on phytoplankton biomass and cell number in thermokarst lakes of western Siberia. The symbols represent the study sites of the four permafrost zones: 942 Kogalym (isolated), Khanymey (sporadic), Urengoy (discontinuous) and Tazovsky 943 (continuous). 944

945
<figure><img src="image_9.png" /></figure>

<figure><img src="image_10.png" /></figure>

<figure><img src="image_11.png" /><figcaption>**Figure 6.** Results of PCA treatment of the whole database (all lakes, all permafrost zones) for spring (A), summer (B) and autumn (C). The red color denotes significant (p < 0.05) link to the factor. Red ovals designate the components mostly affected by 1st or 2nd factor (based on statistical criterion).</figcaption></figure>

946

947

948

949

950
Environmental control on phytoplankton in thermokarst lakes of permafrost peatlands

<figure><img src="image_12.png" /></figure>

DOC, macro-nutrients, lithogenic elements (Al, Cr) micro-nutrients (Zn, Ba) exhibited positive impact on phytoplankton abundance

<figure><img src="image_13.png" /></figure>

<figure><img src="image_14.png" /></figure>