Diversity of Diatom Algae in the Lena Delta Nature Reserve and the Adjacent Territory in the Specific Ecological Factors of the Arctic

1. Introduction

The diatom algae of Bacillariophyta Karsten are a common group of colonial or single-celled organisms characterized by an exogenous siliceous shell. The study of the ecology and species diversity of diatoms in the Arctic is of particular importance in connection with the phenomena of global climate change.

The diatoms study of the Eurasian high Arctic aquatic ecosystems stays in the initial stage but even now represented results on Eurasian northern coast of Arctic Ocean [1,2], the islands of the Arctic Ocean [3-6], Chukotka [7-9], and the continental part of Yakutia [10-11].

Our studies of aquatic communities in Northern Yakutia were carried out to assess the impact of climatic and anthropogenic factors on them [12-18].

The water bodies of the Lena Delta Nature Reserve and adjacent territories are located beyond the Arctic Circle in the zone of continuous occurrence of permafrost soils. Algological studies of this area, including the lower reaches of the Lena River, its delta, the vast water area of the Laptev Sea, tundra reservoirs of the spurs of the Kharaulakh Range and the New Siberian Islands, were started almost 100 years ago. The latest summary, including all currently available information on the algoflora of the delta region was published as a database on the GBIF.org portal [19]. In accordance with it, the diatom flora of the Lena Delta Nature Reserve and close to it coastal area includes information on 413 taxa below the genus rank. Research in the area adjacent to the reserve is currently ongoing due to the potential for industrial development of the coastal territory and shelf [18].

Previously, it was shown that the species composition and diversity of diatoms in Arctic water bodies is influenced by several regional features: the area of the reservoir, the direction of the prevailing winds, water temperature, salinity, and pH [1, 18, 20]. However, identification of species in the category of the Red Book of the Arctic region [21, 6] has not been done so far. Figure 1 shows that the region of the Arctic coast near the Lena River Delta needed to be studied more. As a basis for this study, we chose the data on the species composition of diatoms of the Lena Delta Nature Reserve and the adjacent territory (green dots) hereinafter referred to as “delta region” [19] and a recent survey of 14 water bodies in the vicinity of Tiksi settlement (blue dots) hereinafter referred to as “Tiksi region” [18]. Unfortunately, there is very little data available on the habitat for water bodies in the “delta region” but the environmental data for the “Tiksi region” was sufficient [18].

Our hypothesis is that, by studying the relationship of biodiversity and indicator properties of diatoms with sufficiently studied environmental indicators in the adjacent territory, we can extrapolate these relationships to the diversity of the entire studied flora of diatoms in the coastal zone, including the reserve. So, we collected diatom samples to enrich study biodiversity in this area of the Arctic coast and defined environmental variables of its habitats.

The purpose of this study was to compile a general list of diatoms of the Lena Delta Nature Reserve and the adjacent territory, characterize the diversity and species richness, conduct an ecological and geographical analysis, identify environmental factors that affect the diversity of this group of aquatic organisms in the studied water bodies and identify potentially threatened species worthy of inclusion in the Red Book of the Arctic region.

2. Materials and Methods

2.1. Description of study area

The study area is located north of the Arctic Circle on the coast of the Laptev Sea of the Arctic Ocean and includes the Lena River Delta and reservoirs on the eastern spur of the Kharaulakh Range of the Verkhoyansk Mountain system. The maximum height reaches 400 m above sea level. The underlying rocks are mainly shales, sandstones, limestones, as well as effusive rocks that were formed because of removal by the Lena River or accumulated because of catastrophic outbursts of a glacier-dammed lake in the late Pleistocene-early Holocene [22-24]. The territory belongs to the tundra and mountain-tundra natural zones. The climate is polar maritime, the average annual air temperature is -9-11 °С [25], the average frost-free period is 45 days [26]. The depth of seasonal thawing of permafrost soils is 0.2–1.2 m [27]. The average annual precipitation reaches 212 mm, of which the bulk falls from June to August. The phenomena of a polar day in summer and a polar night in winter are characteristic. Strong winds are frequent, the warmest month of the year, July, is characterized by the lowest average hourly wind speed of the year, which is 15.5 km/h (Figure 1, wind roses). The delta and coastal areas are characterized by an abundance of small tundra reservoirs due to limited drainage due to the low thickness of the seasonally thawed permafrost layer [28]. Our work on the territory adjacent to the reserve was carried out on 14 different types of water bodies, which are shallow tundra lakes, small reservoirs, and a hollow in the swampy tundra (Table 1, Figures 1, 2).

Figure 2. Natural landscape of investigated waterbodies in the Lena Delta Nature Reserve and the adjacent area. (a) Arctic tundra with small waterbodies; (b) phytoplankton sampling.

Figure 2. Natural landscape of investigated waterbodies in the Lena Delta Nature Reserve and the adjacent area. (a) Arctic tundra with small waterbodies; (b) phytoplankton sampling.

2.2. Sampling

Phytoplankton sampling on 14 waterbodies of the adjacent territory was carried out between 3 and 7 July 2021. When taking plankton samples, Apstein's plankton net (SEFAR NITEX fabric, mesh diameter 15 µm) was used. One sample from lake 10 was taken by washing off the biofilm from the surface of a submerged rock using a brush. Fixation with 4% neutral formaldehyde solution was carried out immediately after collection. The temperature of water and the morphometric parameters of each lake were determined during the collection of phytoplankton. Coordinates and altitude of the stations were defined by Garmin eTrex GPS-navigator (Table 1). Water samples of 1 L were collected from each lake for chemical analysis. All samples were transported to the determination in the Institute of Problem of the North, Yakutsk.

2.3. Diatom analysis

Cleaning of diatom shells from organic matter was carried out by burning in 30% hydrogen peroxide with 6-hour heat treatment in a thermostat at 85°C [29]. Diatoms in prepared permanent preparations were examined using a JSM-6510 LV (JEOL Ltd.; Tokyo, Japan) scanning electron microscope.

Handbooks and individual articles were used for the diatom species determinations [30-46, 9, 47-51]. The modern species names were adopted using algaebase.org [52]. Rare and endangered species are marked based on data on the distribution of well-studied diatoms in Central Europe [53] in comparison with IUCN [54] (The International Union for Conservation of Nature) criteria (Table 2). Bioindicator analysis was performed according [55] with species-specific ecological preferences of revealed [56-57]. Statistical maps were constructed as the network analysis in JASP (significant only) on the botnet package in R Statistica package of [58]. The BioDiversity Pro 2.0 program was used for similarity calculation [59].

3. Results

3.1. Taxonomical and floristic analysis of diatoms

A significant diversity (385 taxa, Appendix A Figure A1 and Appendix A Figure A2) of diatoms was found for 14 small tundra shallow lakes in “Tiksi region” [18], which, together with the identified previously diatom species in the Nature Reserve itself of the “delta region” [19], makes up a general floristic list of 666 taxa (including definitions to the genus level) (Appendix A Table A1). Thus, the species composition of diatoms in the reserve and adjacent protected areas was replenished by 278 species.

For the diatom flora of the habitats of this Arctic coast, a wide range of generic richness of 123 genera was revealed, including from 1 to 57 species (Figure 3a) with a predominance of species of the Pinnularia (57) and Eunotia (51) genera (Figure 3b).

Among the first 10 Families out of 47, the Naviculaceae Family with 65 species moves in first place, while Pinnulariaceae and Eunotiaceae move to 2nd and 5th place, respectively (Figure 3c). Floristic data were checked by us for completeness of knowledge by constructing a Willis curve comparing the number of species in genera [60].

Figure 3d shows that the distribution of the number of species over the number of genera is a smooth enough line, almost coinciding with the trend line. This is evidence that the diatom flora of the Lena Delta Nature Reserve and the adjacent area is sufficiently studied to allow a systematic and ecological analysis of its species composition. However, irregularities on the distribution line indicate that the list of species has not yet been exhausted and will be replenished with further research.

Floristic properties may be characteristic of the region under study. For this purpose, the Index of intraspecific variability was calculated for the floristic composition of lakes in the Tiksi region. The index was defined as the quotient of the total number of identified taxa with a rank below the genus divided by the number of species [61]. Index Ssp./Sp. for the entire Lena Delta Nature Reserve and the adjacent area, which includes the “Tiksi region” and “delta region”, was 1.11, and for the study area of the “Tiksi region”, the index was 1.14, typical for high-latitude and high-altitude communities (Table 3). The number of diatom species per area of the reserve and the “Tiksi region” differed markedly, amounting to 0.05 and 2.14 species per area, respectively.

Figure 4 makes it possible to compare the distribution of the studied lakes in the “delta region” and a group of 14 lakes in the “Tiksi region”. Both studied areas have a significant number of the investigated lakes evenly distributed over the territory, the altitude of which is within 0-140 m a.s.l. and the number of species in individual lakes varies in a wider range on the territory of the reserve than on the territory of Tiksi. That is, environmental properties are similar, and differences are observed in the number of species in lakes. In this regard, it should be noted that the lakes in the delta were visited repeatedly over several years, while 14 lakes in the “Tiksi region” were examined only once.

We also tried to find a relationship between the morphometry of the studied lakes and the diatom species richness. Table 4 presents the calculation data for the number of species per lake area, which shows that the species richness was the highest in lake 6, however, the Sp./Area index has the highest value for lake 4. The calculation of correlations of this index with the morphometric parameters of a group of lakes showed a significant correlation (p-value = 0.04), which is -0.502 for Sp./Area and Coastline length.

3.2. Bioindicators and ecological preferences of diatoms

Ecological preferences of revealed species in “Tiksi region” and “delta region” are presented in Appendix A Table A2. Distribution of the indicator numbers in ecological categories can be seen in Figure 5. Benthic and planktonic-benthic inhabitants prevail (Figure 5a). Temperate temperature species and indicators of middle oxygenated waters were strongly prevailed (Figure 5b, c). Indicators of low salinity group of indifferents (i) prevail in the studied area on the seacoast (Figure 5d). Indicators of water pH distribution show prevalence of groups of alkaliphiles and neutral waters (Figure 5e). Organic pollution indicators according to Watanabe demonstrated clear waters with sx and es groups in Figure 5f. Water quality was defined with relation of species-specific index saprobity S to 1-5 class. Figure 5g shows the prevailing of organically unpolluted water indicators of class 2 and 3. Between nutrition type indicators the autotrophs (ats and ate) strongly prevail (Figure 5h). Trophic state indicators distribution was irregular with two peaks in oligotrophic and eutrophic groups (ot and e) that reflected the impact to aquatic ecosystems, which increased some the lakes in trophicity (Figure 5i). Detailed distribution of species indicators over ecological categories is represented in Appendix A Table A3.

3.3. Species in Threat Categories

Appendix A Table A1 shows that the number of diatom species in the entire Lena Delta Nature Reserve and the adjacent areas is extremely high, which forces us to analyze the degree of their endemism and rarity, as well as the threat of extinction. Unfortunately, there is no mention of endangered diatom species in the Protected Areas of Russia [6]. Therefore, we used Germany's most developed red data book diatom species resource [53] as a basis for identifying potentially threatened species in the Lena Delta Nature Reserve and the adjacent areas (Table 2).

Distribution of the revealed species over threat categories can be seen in Figure 6. Analysis of the revealed species composition of diatoms in relation to Threatened species categories of the highest three threat levels 1-3 from Extinct or Lost to Highly Threatened showed that 42 species can be classified as such (Table 5) found on the Lena Delta Nature Reserve and the adjacent areas.

The most of them are species of the genus Psammothidium (6), and three species each from the genera Brachysira and Navicula. Among the list of species there are both newly described (Boreozonacola hustedtii) taxa without studied ecology and distribution, and widespread species (Neidium iridis). We have summarized the known ecological preferences (Appendix A Table A2) of these endangered species in Table 5 and found that they inhabit waters of moderate temperature (temp), well supplied with oxygen (str), low salinity (ind), neutral waters, weakly saturated with organic substances (es, o). These species are characterized by an autotrophic type of nutrition (ats) and living in communities of oligotrophic water bodies (ot). It follows that clean, fresh, pH-neutral, and unpolluted water communities are under threat.

3.4. Comparative floristic

We can see the sufficient role of climatic, morphometric, and other environmental variables to the high latitude lakes community composition because of this calculation. Therefore, we decided to compare diatom community composition in morphometrically similar lakes which were located at the north of Eurasia. Altogether 40 lakes including Tiksi 14 lakes were taken for similarity of diatom community calculation: Yakutia 9 lakes (Y) Aalaah, Kurelah, Sullah, Dyiere, Ynah, Nal Tungulu, Large and Small Tungulu, Abalah, Nidzhili [10]; Bolshezemelskaya Tundra lakes (BZ) Vanutkiny, Kharbeyskiye, Korotaikha, Vorkuta, Usa, Kara [2]; Tiksi (T), species from “Tiksi region” 14 lakes [18] (Appendix A Table A1). Bray-Curtis calculation of diatom species composition similarity of the lakes above the Arctic circle latitude of Russia show strong separation of each group of the lakes. Figure 7 demonstrates three clusters that marked for North Yakutia (1), Bolshezemelskaya Tundra (2) and Tiksi 14 lakes from current research (3).

We have expanded the list of diatom floras for the next step of comparison that including: Arctic Chukotka from Amguema basin lakes Ervynaygytgyn, Matachingagytgyn, Ekitiki [7,8], Bolshezemelskaya Tundra lakes Vanutkiny, Kharbeyskiye, Korotaikha, Vorkuta, Usa, Kara [2], Svalbard, Hornsund fiord 10 lakes [5], Yakutia 9 lakes Aalaah, Kurelah, Sullah, Dyiere, Ynah, Nal Tungulu, Large and Small Tungulu, Abalah, and Nidzhili [10].

Comparison with the JASP program represented results of calculation in Figure 8. Can be seen that species composition of each group of the lakes is strongly separated from each other. This high individuality of species composition can be result of influence of geographical position of the lakes group and its climatic features.

4. Discussion

The subject of our study was the flora of diatoms found in the lakes of the “Tiksi region” in the vicinity of Tiksi settlement and the delta on the territory of the “delta region” of the Lena Delta Nature Reserve. The general list was compiled from our studies of the “delta region” [19] including 413 taxa and 385 taxa of the “Tiksi region”, [18] and amounted to 666 taxa of diatoms (including definitions to the genus level), 278 of which were enriched the regional flora. The floristic analysis was carried out after constructing the Willis curve, which turned out to be quite smooth and close to the trend line, which indicates that the list of diatoms is sufficiently complete for an adequate flora of the analysis region. Willis’s curve was not so smooth that allows us to assume that the list of species has not yet been exhausted and will be replenished with further research. Index of intraspecific variability Ssp./Sp. for the lakes of the “delta region” was 1.11, and for the lakes of the “Tiksi region” was 1.14, which is typical for high-latitude and high-mountain communities.

We calculated the Index Sp./Area as number of diatom species per whole studied area that was for the “delta region” 0.05 but for the “Tiksi region”2.14 that show differences between biodiversity of both studied areas and confirm that coastal zone can be the hotspot of the Arctic diatoms as was revealed for Arctic chrysophytes [67]. It also confirms the idea that the most important factor for diatom species richness can be the lake morphometry [68]. Thus, the geographic factor turned out to be significant for the formation of diatom communities in the Arctic floras, in addition to this, the association with individual river runoff basins on the coast, elevated habitats, as well as the influence of such climatic factors as summer northeast winds on the species composition was previously revealed [18].

The Arctic deltas are responsible for nutrient transport to the sea, which varies by delta and season, and it is estimated that the Lena Delta retains about 15% of the input load, the largest in the Arctic Ocean [69]. At the same time, the deposition of nitrates by the tundra landscape in the spring and their subsequent accumulation in lakes and wetlands adjacent to river channels contributes to the enrichment of lake water with a nutrient base [69]. This makes the water of the Lena River a source of nutrients [17, 70] on the one hand, but on the other hand, stimulates the diversity of algae, as has been shown in the lakes of the Tiksi coastal region [18]. Despite this, the current diatom flora shows clean, organically uncontaminated waters, although there is a diversity burst response to a one-time nutrient point impact in the Tiksi area.

Whole flora bioindicators analysis shows that the diatoms identified in the “delta region” and the coastal “Tiksi region” were mainly benthic autotrophs, preferring temperate, middle oxygenated, low saline, low alkalic clear water class 2 and characterize two trophic type of waterbodies - oligotrophic and eutrophic.

The high individuality of diatom communities was revealed both for the entire Lena Delta and its adjacent areas, and in a comparative analysis with the lacustrine floras of Yakutia and the High Arctic of Eurasia. For the first time for the Arctic regions of Eurasia, a preliminary analysis of the threat of diatom species was carried out and 42 species of the IUCN categories were identified. These rare or threatened species prefer moderate temperatures, slightly acidic or neutral environments free from organic pollution. Thus, the lake communities in clean, fresh, pH-neutral, and unpolluted waters in the coastal zone of the Arctic Ocean with the highest diversity are the most vulnerable.

As a result of comparing the properties of the natural environment of the “delta region” and the coastal zone of the “Tiksi region”, our hypothesis is confirmed about the possibility of extrapolating the patterns identified for the territory of Tiksi to the diversity of the entire studied flora of diatoms because the conditions were similar, but differences were significant in the diatom species content of the lakes. The species richness in the Tiksi coastal lakes was higher than in the delta lakes even though the lakes in the delta were sampled many times over several years, and 14 lakes in the “Tiksi region” were surveyed only once. This allows us to suggest that the high diversity inherent in the diatom lakes of the Tiksi coastal zone, which can even be replenished in further studies, can be considered as a property of coastal biota inherent in ecotones. Since it is in the coastal region of Tiksi that a surge in the number of species is observed, this region can be considered not only an ecotone, but also a hotspot of diatom diversity. Ecotones are border areas of different landscapes where there is a marked increase in the diversity of organisms [71]. Until now, the landscapes of the coast of the Arctic Ocean have not been considered as ecotones for diatom communities. But for the diversity of algae, this term was used, for example, for communities of river habitats [72]. The diversity of diatoms in the coastal area of the “Tiksi region” may be due to several factors. As known, studies of diatoms in a scanning electron microscope give a higher percentage of certain species [73].

We have formed a hypothesis about the introduction of species from temperate latitudes into Arctic waters under the conditions of global climate change [20].

Then the record level of species diversity of these hydrobionts and the change in the structure of their communities reflect the beginning of manifestations of climate warming. On the other hand, there is an opinion that the similarity between the algal communities of the northern and temperate regions may be more apparent than real [74]. This is confirmed by the sharp predominance of species of the genera Pinnularia and Eunotia, not only in our studied lakes, but also in a comparative analysis with other Arctic floras. Moreover, the further north the flora, the more saturated with species are these two genera. This may be one of the decisive signs for assessing the impact of climate change on the aquatic communities of the Arctic.

Therefore, we revealed the important role of climatic, morphometric, and other environmental variables related with geographical position of the waterbody in forming the diatom community composition in the high latitude lakes. The results of the study are important for developing the basis for monitoring the biodiversity of non-impact, ecologically sensitive territories, and climate change in the future. Their relevance for assessing the consequences of local anthropogenic impact is high.