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

Abstract

A total of 413 diatom taxa were known for aquatic habitats of the Lena Delta Nature Reserve. We identified 385 taxa in 14 small tundra lakes near the reserve that significantly enriched the diatom diversity of the region (666 taxa including definitions to the genus level). Thus, the species composition of diatoms in the reserve and adjacent territories was increased by 278 species. We showed that the species of the genera Pinnularia (57) and Eunotia (51) have predominance at the family and generic levels. The index of intraspecific variability Ssp./Sp. for the lakes of the reserve was 1.11, and that for the lakes of the Tiksi region 1.14, which is typical for high-latitude and high-mountain communities. The number of rare or endangered species varied in different lakes from 1 to 10, totaling 42 species for the entire study area. Bioindication has shown that potentially threatened species prefer moderate temperatures, and slightly acidic or neutral environments free from organic pollution. A comparative analysis of the species composition of diatoms in the vicinity of the Lena Delta and other northern water bodies of Yakutia and the Arctic Islands showed that the species composition of each lake in the Arctic has a discernably different species distribution. The indicator characteristics show a certain response of the species composition of diatoms to changes in salinity, pH, and organic pollution. Regularities in the spatial distribution of diatoms in the study area were revealed in connection with the environmental variables of their habitat. Statistical mapping of diatom diversity data and bioindicators revealed a pronounced response to point pollution, and also let us assume the influence of summer northeast winds on species composition of the studied lake communities. We suggest that the high diversity inherent in the diatom lakes of the Tiksi coastal zone, which can even be updated in further studies, can be considered as a property of coastal biota inherent in ecotones. Since it is in the coastal Tiksi region 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. The results of the study are important for developing the basis for monitoring biodiversity under the conditions of anthropogenic and climatic changes in 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 study of diatoms of the Eurasian high Arctic aquatic ecosystems has remained in the initial stage but even now results are represented on the Eurasian northern coast of Arctic Ocean [1,2], the Arctic Ocean islands [3,4,5,6], Chukotka [7,8,9], and the Yakutia continental part [10,11].

Our studies of the Northern Yakutia aquatic communities were carried out to assess the impact of anthropogenic and climatic factors on them [12,13,14,15,16,17,18].

The water bodies of the Lena Delta Nature Reserve (Figure 1, green dots) and adjacent territories (black dots) include the lower reaches of the Lena River, the river delta, the close places of the Laptev Sea area and the New Siberian Islands, as well as tundra reservoirs on the Kharaulakh Range. All mentioned waterbodies are located beyond the Arctic Circle in the zone of continuous occurrence of permafrost soils. Algological studies of this area were started almost 100 years ago. The latest summary, including all currently available information on the algoflora of the delta region, was previously published on the GBIF.org portal [19]. Therefore, the diatom flora of the Lena Delta Nature Reserve and the area close to its border coast (Figure 1, green and black dots) included information on 413 taxa below the genus rank before this study. Investigations of diatoms in the lakes of the coastal territory adjacent to the reserve (Figure 1, blue dots) are currently ongoing due to the potential for industrial development of the coastal territory and shelf [18].

Figure 1. Investigated waterbodies in the Lena Delta Nature Reserve (green outline, green dots) and the adjacent territory (black dots), summarized as “delta region” and a recent survey of waterbodies (blue dots, “Tiksi region”) with the wind rose seasonality.

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, as mentioned in previous studies [1,18,20]. However, the detection of species worthy of inclusion in the Red Book of the Arctic [6,21] has not been done so far. Figure 1 shows that the region of the Arctic coast near the Lena River Delta needs 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 and black 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 “delta region” but the environmental data for “Tiksi region” were sufficient [18] to be used for the species–environment relationships analysis.

Our hypothesis was that by studying in detail the relationship between diatom biodiversity and environmental variables in the model zone of the Arctic coast, it is possible to identify the introduction of species from temperate latitudes to the Arctic coast in the context of global climate change.

The aim of this study was to compile a general list of diatoms of the Lena Delta Nature Reserve and the adjacent coastal area, characterize the diversity and species richness, conduct an ecological and geographical analysis, reveal environmental factors influencing the diatom diversity in the studied lakes, 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, and 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 [22,23,24]. The territory belongs to the tundra and mountain-tundra natural zones. The climate is polar maritime, the average annual air temperature is −9–11 °C [25], and 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, and 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⁻¹ (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, Figure 1 and Figure 2).

Table 1. Sampling station parameters and the geographical coordinates of recent survey of waterbodies in “Tiksi region” (blue dots according to Figure 1).

No of Station	Lake Name	Water Temperature	Altitude, m	North	East
1	Lake 1	16.7	25	71°44′44″	128°43′12″
2	Lake 2	15.1	66	71°44′12″	128°41′37″
3	Lake 3	15.0	109	71°43′31″	128°38′31″
4	Lake 4	20.4	38	71°43′48″	128°42′35″
5	Lake 5	20.6	−4	71°43′45″	128°44′36″
6	Lake 6	16.1	76	71°41′10″	128°36′50″
7	Lake 7	14.5	76	71°40′52″	128°37′11″
8	Lake-puddle 8	10.1	55	71°40′26″	128°41′21″
9	Lake 9	15.1	54	71°40′10″	128°43′27″
10	Lake 10	13.3	52	71°35′56″	128°51′70″
11	Lake 11	14.0	38	71°34′33″	128°45′51″
12	Swampy lake 12	-	105	71°33′36″	128°40′26″
13	Lake 13	14.6	85	71°33′17″	128°38′51″
14	Lake 14	14.7	154	71°32′34″	128°34′57″

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

Algae sampling on 14 waterbodies of the adjacent territory was carried out between 3 and 7 July 2021. When taking samples, Apstein’s plankton net (SEFAR NITEX fabric, mesh diameter 15 µm) was used. All samples from 14 lakes were taken by throwing the Apstein net three times. Since the lakes are shallow water bodies, the shores of which are overgrown with tundra vegetation, in the process of sampling, not only the inhabitants of the water mass, but also organisms that were disturbed and torn off from the substrate were collected in the net. So, each sample accumulated both plankton and periphyton. 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 altitudes of the stations were defined by a Garmin eTrex GPS-navigator (Table 1). Water samples of 1 L were collected from each lake for chemical analysis. All samples were transported for determination to the Analytical Chemistry Laboratory of the Institute for Biological Problems of Cryolithozone SB RAS, Yakutsk, Russia.

2.3. Diatom Analysis

Cleaning of diatom shells from organic matter was carried out by burning in 30% hydrogen peroxide with 6 h 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 [9,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51]. 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 to [55], revealing species-specific ecological preferences [56,57]. Statistical maps were constructed as the network analysis in JASP (significant only) on the botnet package in the R Statistica package [58]. The BioDiversity Pro 2.0 program was used for similarity calculation [59].

Table 2. Threat categories for diatom species in the waterbodies of the Lena Delta Nature Reserve and the adjacent area.

IUCN Category	IUCN Code	No of Red List Category	Red List Category	Number of Species
Extinct	EX	1	Extinct or Lost	2
Critically Endangered	CR	2, 3	Threatened with Extinction, Highly Threatened	40
Endangered	EN	4, 5	Threatened, Threat of Unknown Extent	112
Vulnerable	VU	6	Extremely Rare	16
Near Threatened	NT	7	Near Threatened	28
Least Concern	LC	9	Not Threatened	198
Data Deficient	DD	8	Data Deficient	43
Not Evaluated	NE	0, 10	Not established	194

3. Results

3.1. Taxonomical and Floristic Analysis of Diatoms

A significant diversity (385 taxa, Appendix A Figure A1 and 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 updated 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).

Figure 3. Distribution of diatom species over 123 genera (a), ten richest genera (b), ten richest families (c), and Willis’s curve (d) in the Lena Delta Nature Reserve and the adjacent area.

Among the first 10 families out of 47, the Naviculaceae family with 65 species is the most abundant, followed by Pinnulariaceae and Eunotiaceae which 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]. It was found that when the Willis curve is represented by a hyperbolic distribution, it can be used as a criterion for the completeness of the list of algoflora and, therefore, for the subsequent analysis of alpha or gamma diversity. 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 increased 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. As it was revealed earlier [61], the index of intraspecific/species variability of diatom floras of Eurasia decreases from north to south, which may be associated with climate change and therefore can be used as a criterion for future warming. The 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.

Table 3. Floristic parameters of the entire Lena Delta Nature Reserve and the adjacent area as the “Delta region”, and the “Tiksi region”.

Variable	“Delta Region”	“Tiksi Region”
Area, km2	14300	180
Species with intraspecies	666	385
Taxa without sp.	631	356
Species only	569	337
Sp./Area	0.05	2.14
Ssp./Sp.	1.11	1.14

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 above sea level 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.

Figure 4. Distribution of the studied lakes in the territory of the “delta region” (a) and a group of 14 lakes in the “Tiksi region” (d), altitude (b,e) and the number of diatom species (c,f). The top row of graphs is Delta region and bottom row is Tiksi lakes.

The relationship between the morphometry of the studied lakes and the diatom species richness was defined by calculation data for the number of species per lake area represented in Table 4. It can be seen that highest species richness was in lake 6, but the Sp./Area index was highest in 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.

Table 4. Distribution of the diatom species richness of the “Tiksi region” lakes over the lake surface.

No of Station	Lake Name	Lake Surface Area, km2	Coastline Length, m	No of Species	Sp./Area
1	Lake 1	0.075	1618.42	66	881.601
2	Lake 2	0.038	894.56	62	1635.603
3	Lake 3	0.031	763.29	76	2460.437
4	Lake 4	0.008	359.76	72	8891.117
5	Lake 5	0.067	1188.51	33	493.171
6	Lake 6	0.042	902.78	137	3252.128
7	Lake 7	0.586	5716.74	75	128.074
8	Lake-puddle 8	-	-	69	-
9	Lake 9	0.486	3167.26	59	121.281
10	Lake 10	0.077	1153.85	85	1101.333
11	Lake 11	0.124	1800.36	117	946.742
12	Swampy lake 12	-	-	43	-
13	Lake 13	0.158	1639.88	96	609.365
14	Lake 14	0.023	712.85	50	2175.773

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. The indicator species number distribution over the ecological categories is shown in Figure 5. Benthic and planktonic-benthic inhabitants prevail (Figure 5a). Temperate temperature species and indicators of middle oxygenated waters strongly prevail (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, as shown in Figure 5f. Water quality was defined with the relation of the species-specific index saprobity S to 1–5 classes. Figure 5g shows the prevailing of organically unpolluted water indicators of classes 2 and 3. Between nutrition type indicators, the autotrophs (ats and ate) strongly prevail (Figure 5h). Trophic state indicator distribution was irregular, with two peaks in oligotrophic and eutrophic groups (ot and e) that reflected the impact on aquatic ecosystems, which increased the trophicity in some lakes (Figure 5i). The detailed distribution of species indicators over ecological categories is represented in Appendix A Table A3.

Figure 5. Distribution of species indicators of the waterbodies in the entire Lena Delta Nature Reserve and the adjacent areas over ecological groups. The ecological groups order on the axis x follows the increase in the related environmental indicator. (a) Habitat (P—planktonic, P-B—plankto-benthic, B—benthic). (b) Temperature preferences (cool—cool-water, temp—temperate, eterm—eurythermic, warm—warm-water). (c) Oxygen and streaming (st—standing water, str—streaming water, st-str—low streaming water, aer—aerophiles). (d) Salinity ecological groups according to Hustedt (1938–1939) [62] (hb—oligohalobes-halophobes, i—oligohalobes-indifferent, hl—halophiles; mh—mesohalobes, eh—euhalobes, ph—polyhalobes). (e) pH preferences groups (pH) according to Hustedt (1957) [63] (alb—alkalibiontes; alf—alkaliphiles, ind—indifferent; acf—acidophiles; acb—acidobiontes). (f) Organic pollution indicators according to Watanabe et al. (1986) [64]: sx—saproxenes; es—eurysaprobes; sp—saprophiles. (g) Class 1–5 of organic pollution indicators according to species-specific Index saprobity of Sládeček, 1986 [65]. (h) Nutrition type as nitrogen uptake metabolism (Van Dam et al., 1994) [66]: ats—nitrogen-autotrophic taxa, tolerating very small concentrations of organically bound nitrogen; ate—nitrogen-autotrophic taxa, tolerating elevated concentrations of organically bound nitrogen; hne—facultative nitrogen-heterotrophic taxa, needing periodically elevated concentrations of organically bound nitrogen; hce—obligate nitrogen-heterotrophic taxa, needing continuously elevated concentrations of organically bound nitrogen. (i) Trophic state indicators (Van Dam et al., 1994) [66]: (ot—oligotraphentic; om—oligomesotraphentic; m—mesotraphentic; me—mesoeutraphentic; e—eutraphentic; he—hypereutraphentic; o-e—oligo- to eutraphentic (hypereutraphentic)).

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).

The 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 the Threatened species categories of the highest three threat levels, 1–3, from Extinct or Lost to Highly Threatened, showed that 42 species classified as such (Table 5) can be found on the Lena Delta Nature Reserve and the adjacent areas.

Figure 6. Distribution of the number of diatom species in the flora of water bodies of the Lena Delta Nature Reserve and adjacent territories by IUCN Threat Categories. The order of the IUCN categories on the x-axis corresponds to threat reduction.

Table 5. Ecological preferences of diatom species in IUCN Threat Categories (Red Data List) of the Lena Delta Nature Reserve and adjacent areas.

Species in Threat Categories	Hab	T	Oxy	Sal	pH	D	Index S	Sap	Aut-Het	Tro
EXTINCT (Extinct or Lost)
Cymbopleura designata (Krammer) Bahls	B	temp	st-str	i	alf	-	1.8	o-a	ats	m
Encyonema latens (Krasske) D.G.Mann	B	-	-	-	-	-	1.0	o	ats	ot
CRITICALLY ENDANGERED (Threatened with Extinction)
Eunotia elegans Østrup	P-B	-	st-str	hb	acf	-	0.2	x	ats	ot
Eunotia faba Ehrenberg	B	temp	st-str	-	alf	-	-	o	ats	ot
Frustulia krammeri Lange-Bertalot & Metzeltin	B	-	-	-	acf	-	-	-	-	e
Navigeia thingvallae (Østrup) Bukhtiyarova	B	-	-	-	-	-	-	-	-	-
Tetracyclus glans (Ehrenberg) F.W.Mills	P-B	temp	-	i	acf	-	1.0	x-o	-	ot
CRITICALLY ENDANGERED (Highly Threatened)
Boreozonacola hustedtii Lange-Bertalot, Kulikovskiy & Witkowski	-	-	-	-	-	-	-	-	-	-
Brachysira calcicola Lange-Bertalot	B	-	-	-	-	-	1.0	o	-	-
Brachysira procera Lange-Bertalot & Gerd Moser	B	-	-	-	acf	-	-	-	-	-
Brachysira styriaca (Grunow) R.Ross	B	temp	-	i	ind	es	1.0	o	-	ot
Cymbella affinis Kützing	B	temp	st-str	i	alf	sx	1.1	b	ats	e
Cymbella carassius Skvortzov	-	-	-	-	-	-	-	-	-	-
Cymbellafalsa diluviana (Krasske) Lange-Bertalot & Metzeltin	B	-	-	i	alf	-	1.0	o	-	ot
Cymbopleura tynnii (Krammer) Krammer	B	-	-	-	-	-	-	-	-	-
Diploneis ovalis (Hilse) Cleve	B	-	st-str	i	alf	-	0.9	x-b	ate	m
Eucocconeis alpestris (Brun) Lange-Bertalot	B	temp	str	hb	ind	-	-	-	-	-
Eucocconeis austriaca (Hustedt) Lange-Bertalot	B	-	-	i	alf	-	0.2	x	ats	ot
Eucocconeis flexella (Kützing) F.Meister	B	temp	str	mh	ind	-	-	-	-	-
Eunotia bigibba Kützing	B	-	str	i	acf	-	0.4	x-o	-	ot
Eunotia flexuosa (Brébisson ex Kützing) Kützing	B	temp	st-str	i	acf	-	0.4	x-o	-	-
Eunotia praerupta Ehrenberg	P-B	cool	st-str	hb	acf	-	0.3	x	-	-
Eunotia triodon Ehrenberg	B	temp	-	hb	acf	-	1.0	o	-	ot
Gomphonema helveticum Brun	B	-	-	i	ind	-	-	-	-	-
Gomphonema lagerheimii A.Cleve	B	-	str	hb	acf	-	-	-	-	m
Gomphonema ventricosum W.Gregory	B	cool	str	i	ind	-	1.0	o	-	-
Iconella curvula (W.Smith) Ruck & Nakov	B	-	str	hb	acf	-	2.0	b	-	me
Kobayasiella subtilissima (Cleve) Lange-Bertalot	B	temp	st-str	i	acb	-	1.6	b-o	ats	me
Mayamaea disjuncta (Hustedt) J.Y. Li & Y.Z.Qi	B	-	str	i	ind	sp	3.0	a	ate	he
Navicula angusta Grunow	B	-	st-str	i	ind	-	1.0	o	-	-
Navicula gottlandica Grunow	P-B	-	-	hl	alf	es	2.5	b-a	ate	e
Navicula mediocostata E.Reichardt	B	-	-	oh	alf	es	3.0	a	ate	e
Navicula notha J.H.Wallace	B	-	str	i	acf	-	-	-	-	-
Neidium iridis (Ehrenberg) Cleve var. iridis	B	temp	st-str	hb	ind	-	-	-	-	-
Nitzschia frigida Grunow	-	-	-	-	-	-	-	-	-	-
Placoneis opportuna (Hustedt) Chudaev & Gololobova	B	-	-	-	-	es	-	-	-	-
Psammothidium kryophilum (J.B.Petersen) E.Reichardt	P-B	-	str	i	ind	sx	0.5	x-o	ats	ot
Psammothidium levanderi (Hustedt) Bukhtiyarova & Round	B	temp	str	i	ind	sx	2.0	b	ats	om
Psammothidium rechtense (Leclercq) Lange-Bertalot	B	-	str	hb	alf	-	1.0	o	ats	ot
Psammothidium rossii (Hustedt) Bukhtiyarova & Round	B	-	str	hb	ind	-	1.0	o	ats	ot
Psammothidium scoticum (R.J.Flower & V.J.Jones) Bukhtiyarova & Round	B	temp	-	-	-	-	-	-	-	-
Psammothidium ventrale (Krasske) Bukhtiyarova & Round	B	-	str	hb	acf	-	2.0	b	ats	om

Note: “-“, not found. Abbreviations: Habitat (Hab) (P-B—plankto-benthic, B—benthic); temperature (T) preferences (cool—cool-water, temp—temperate, eterm—eurythermic, warm—warm-water); oxygenation and streaming (Oxy) (str—streaming water, st-str—low streaming water); pH preferences groups (pH) according to Hustedt (1957) [63] (alb—alkalibiontes; alf—alkaliphiles, ind—indifferent; acf—acidophiles; salinity ecological groups (Sal) according to Hustedt (1938–1939) [62] (hb—oligohalobes-halophobes, i—oligohalobes-indifferent, hl—halophiles; mh—mesohalobes, oh—oligohalobes of wide spectrum with optimum as indifferent); Index S, species-specific index saprobity according to Sládeček, 1986 [65]; self-purification zone with index of saprobity (Sap) (x/0.0—xenosaprobe; x-o/0.4—xeno-oligosaprobe; x-b/0.8—xeno-betamesosaprobe; o/1.0—oligosaprobe; b-o/1.6—beta-oligosaprobe; o-a/1.8—oligo-alphamesosaprobe; b/2.0—betamesosaprobe; a/3.0—alphamesosaprobe; organic pollution indicators according to Watanabe et al. (1986) [64] (D): sx—saproxenes; es—eurysaprobes; sp—saprophiles; nitrogen uptake metabolism (Aut-Het) (Van Dam et al., 1994) [66]: ats—nitrogen-autotrophic taxa, tolerating very small concentrations of organically bound nitrogen; ate—nitrogen-autotrophic taxa, tolerating elevated concentrations of organically bound nitrogen; Trophic state indicators (Tro) (Van Dam et al., 1994) [66]: (ot—oligotraphentic; om—oligomesotraphentic; m—mesotraphentic; me—mesoeutraphentic; e—eutraphentic; he—hypereutraphentic).

Most of these are species of the genus Psammothidium (6), and there are 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), having low salinity (ind), neutral, and 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 in 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 14 Tiksi lakes, were taken for similarity of diatom community calculation: 9 Yakutia 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 the “Tiksi region” 14 lakes [18] (Appendix A Table A1). The Bray–Curtis calculation of the diatom species composition similarity of the lakes above the Arctic circle latitude of Russia shows strong separation of each group of the lakes. Figure 7 demonstrates three clusters that were marked for North Yakutia (1), Bolshezemelskaya Tundra (2), and 14 Tiksi lakes from current research (3).

Figure 7. Bray–Curtis cluster analysis of diatom list similarity of the Arctic lakes over the Arctic circle in Eurasia. Cluster 1: Nine Yakutia lakes (Y): Aalaah, Kurelah, Sullah, Dyiere, Ynah, Nal Tungulu, L. and S. Tungulu, Abalah, Nidzhili [10]. Cluster 2: Bolshezemelskaya Tundra lakes (BZ) Vanutkiny, Kharbeyskiye, Korotaikha, Vorkuta, Usa, Kara [2]. Cluster 3: Tiksi (T), species from 14 lakes [18] (Appendix A Table A1).

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

Comparison with the JASP program [58] represented results of similarity calculation, as shown in Figure 8. It can be seen that the species composition of each group of the lakes is strongly separated from each other. This high individuality of species composition can be the result of the influence of the geographical position of the lakes group and its climatic features.

Figure 8. JASP network plot of diatom species composition similarity for the small Arctic lakes, p< 0.5. Tiksi (T), species from the Tiksi region 14 lakes [18]. Arctic Chukotka, species from Amguema basin lakes: Ervynaygytgyn, Matachingagytgyn, Ekitiki [7,8]. Bolshezemelskaya Tundra lakes (BZ) Vanutkiny, Kharbeyskiye, Korotaikha, Vorkuta, Usa, Kara [2]. Svalbard (Sv), Hornsund fiord, eight lakes [5]. Yakutia (Y), nine lakes: Aalaah, Kurelah, Sullah, Dyiere, Ynah, Nal Tungulu, Large and Small Tungulu, Abalah, Nidzhili [10].

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 was found to be quite smooth and close to the trend line, thereby indicating that the list of diatoms is sufficiently complete for an adequate flora of the analysis. The Willis curve was not so smooth to allow us to assume that the list of species has yet been exhausted, and the list will be increased with further research. The index of intraspecific variability Ssp./Sp. for the lakes of the “delta region” was 1.11, and for the lakes of the “Tiksi region” it was 1.14, which is typical for high-latitude and high-mountain communities.

We calculated the Sp./Area index as the number of diatom species per whole studied area, which was 0.05 for the “delta region” but 2.14 for the “Tiksi region”, thereby showing differences between biodiversity of both studied areas and confirming that the coastal zone can be the hotspot of the Arctic diatoms, as was revealed for Arctic chrysophytes [67]. Our reasoning boils down to the fact that in the lakes of Northern Europe, as well as in some subarctic and temperate lakes of northwestern Russia and the Baltic states, the species lists of diatoms were proportional to the area of the lakes [68]. In the lakes of the Tiksi region and some lakes of the delta region studied here, the area of lakes does not correlate with species richness. Even though all compared lakes are shallow and have been studied many times in the delta region, and samples were taken once in the Tiksi region, the diversity in the lakes of the Tiksi region was found to be significantly higher. We attempted to remove a possible reason for the high diversity in Tiksi lakes surveyed by SEM and carried out the same study of diatoms in some lakes of the delta, but here the species composition did not increase. Thus, we concluded that the burst of diversity of diatoms in lakes of the same type morphometrically but located in the coastal zone of the lakes of the Tiksi region is associated with the Arctic coastal ecotone. Thus, the geographic factor was found 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, and the influence of such climatic factors such 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 class 2 water, and characterize two trophic types 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, and 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 that one indicator of global climate change may be the introduction of diatom species from temperate latitudes to the Arctic was confirmed. The species richness in the Tiksi coastal lakes was higher than that 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 enriched 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. However, 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]. The revealed record level of species diversity of diatoms and related changes in the structure of diatom communities can be fingerprint evidence of the beginning 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. Our conclusions are in the frame of the Ruth Patrick theory [75] about the relationship between diatom biodiversity and the health of the environment that can be seen in increasing the species diversity in the tundra coastal area of Arctic. So, this type of Arctic wetlands can have high importance because of their high water cleaning capacity by absorbing and assimilating a variety of pollutants.

Therefore, we revealed the important role of climatic and other environmental variables related with geographical position of the waterbody in forming the diatom community composition in the high latitude lakes. We suggest that the results of this study can be used to create a database on the biodiversity of diatoms as indicators of changes in untouched areas, as well as pioneers in monitoring climate change in the Arctic. Their relevance for assessing the consequences of local anthropogenic impact is high.