New desmid records from high mountain lakes in Artabel Lakes Nature Park, Gümüşhane, Turkey

: The algal flora of 17 lakes and 1 pond in the Artabel Lakes Nature Park were investigated during two summer seasons (2013 and 2016). In total, 26 desmid taxa were found and identified as new records for the desmid flora of Turkey based on their morphotaxonomic characteristics and ecological preferences. The taxa identified belong to the genera Actinotaenium (1), Closterium (1), Cosmarium (15), Micrasterias (1), Spondylosium (1), Staurastrum (5), Teilingia (1), and Tetmemorus (1). Morphotaxonomy, ecology, and distribution of each species were discussed in detail.


Introduction
Desmid habitats are exclusively freshwater (Coesel and Meesters, 2007;Kouwets, 2008). Desmids usually prefer acidic or pH-circumneutral, nutrient-poor, and clear waters (Lenzenweger, 1996;Coesel and Meesters, 2007). It is well known that members of order Desmidiales exhibit great diversity in their external morphology and also have remarkably complex cell symmetry (Lee, 2015). That is why they attract the attention of researchers. To date, about 3250 different desmid species have been identified worldwide (Guiry and Guiry, 2019). Desmids are also considered excellent bioindicators in terms of the stability of ecosystems (Coesel, 1998). In recent years, eutrophication, acidification, desiccation, and cultivation have been identified as processes that could negatively affect desmid habitats (Lenzenweger, 1996;Šimek, 1997;Coesel et al., 1978;Štastný, 2009). Therefore, these processes have played a part in affecting the most endangered group of aquatic microorganisms (Coesel, 1998).
According to phylogenetic studies, Conjugatophyceae is one of the most important classes within the Charophyta and is associated with land plants (Gontcharov, 2008a). However, recent molecular phylogenetic studies have shown a disagreement between the traditional taxonomic structure of Conjugatophyceae and the pattern of phylogenetic relationships between the class members (Gontcharov, 2008a).
Desmids are an integral part of benthic habitats of high mountain lakes; in particular, those of the Northern Hemisphere (Medvedeva, 2001;Sterlyagova, 2008). In the period from 1998 to 2014, 43 new records of desmid species from high mountain lakes in the eastern Black Sea Region were identified and published (Şahin, 1998, 2000, 2002, 2007Şahin and Akar, 2007;Akar and Şahin, 2014). Some of them [e.g., Actinotaenium cruciferum (De Bary) Teiling, A. cucurbita (Brébisson ex Ralfs) Teiling, Micrasterias americana Ehrenberg ex Ralfs, M. denticulata Brébisson ex Ralfs, M. rotata Ralfs, Netrium digitus (Brébisson ex Ralfs) Itzigsohn & Rothe, and Spondylosium planum (Wolle) West & G.S.West] were remarkable, because they were the first representatives of their genera in Turkey. These findings are considered unsurprising for this interesting and unexplored mountain region of Turkey. The high mountain lakes in this region contain many boreal and arctic-alpine desmid species, and in-depth survey studies on species composition and biogeographical distribution of the hidden desmid flora of these unique habitats are still an important prerequisite for expanding our scant knowledge.
Artabel Lakes Nature Park is one of the important nature parks in Turkey and contains 23 high mountain lakes. The first data published on the algal flora of this mountain nature habitat was presented by Atıcı (2018). In general, 96 algal species belonging to Bacillariophyta, regions of 17 lakes and 1 pond and then transported to the laboratory for further investigation. Epipelic algae were taken with a glass tube from the surface of the sediment. Epilithic samples were scraped from randomly chosen stones with the toothbrush and washed into plastic bottles. Epiphytic species were collected by squeezing out the moss [Hygrohypnum luridum (Hedw.) Jenn.] and filamentous green alga (Microspora sp.). All samples were preserved with 4% (v/v) formaldehyde in 100 mL plastic bottles. In the lab, temporary slides were prepared using the appropriate methods (Round, 1953;Sládečková, 1962) and identified under a light microscope (Leica DM 2500). The desmid taxa were photographed using a Leica DFC 290 camera attached to the microscope. Dissolved oxygen, water temperature, pH, and conductivity of lake waters were measured in situ using Thermo Orion-4-Star pH and YSI-55 portable meters.
Ecology and distribution: Very rare (VR) and found only in the epiphytic samples of the lake IL. Lake IL is located at an elevation of 2668 m a.s.l. and is characterized by a pH value of 6.78. This taxon is known for its wide ecological valence and occurs in acidic (pH 4.8-6) and alkaline (pH 8) habitats with Sphagnum and among other algae and mosses, in oligo-mesotrophic water bodies, and in arctic and alpine waters (the Alps, 2680 m a.s.l.; China, 3000 m a.s.l.; and the Himalayas, about 5000 m a.s.l.) (Huber-Pestalozzi, 1982;John et al., 2003;Coesel and Meesters, 2007).
Description: Cells longer than breadth; sinus slightly open and not deep; semicells truncate-pyramidate; sides very slightly concave; apex truncate; upper and lower angels rounded; cell wall is smooth.
Ecology and distribution: We found this species in the epiphytic samples of lake YL2. It was very rare (VR). Lake YL2 is located at an elevation of 2980 m a.s.l. and is characterized by a pH value of 6.89. According to West and West (1908) and Lenzenweger (1999), this species is a very characteristic alpine and subalpine species. It usually occurs in acidic and slightly acidic waters (pH 6.5) and in the littoral zone of high mountain lakes (2550 m a.s.l.). However, Coesel and Meesters (2007) reported that this species also occurs, rarely, in mesotrophic fen hollows and temporary pools. Description: Cells slightly longer than breadth; sinus deep, linear and closed for the greater part; semicells hexagonal in shape and semicell margins between the broadly rounded angles concave. Cell wall is smooth.
Ecology and distribution: C. boitierense was very rare (VR) and found only in the epipelic samples of lake BL4. Lake BL4 is located at an elevation of 2924 m a.s.l. and is characterized by a pH value of 7.04. Although it used to be bound to meso-eutrophic and mesotrophic habitats (Kouwets, 1998;Coesel and Meesters, 2007), we found it in circumneutral and oligo-mesotrophic water.

C. botrytis var. gemmiferum (Brébisson) Nordstedt (Figures 2F and 2G)
West and West (1912)  Description: Cells longer than breadth; sinus deep and linear; semicells ovate-pyramidal in shape; angles broadly rounded; lateral margins convex; cell wall uniformly granulated. It differs from the typical species in that the semicells have a central granulated protuberance surrounded by a smooth area of small extent. In the vertical view, there is a small inflation at the midregion on each side.
Ecology and distribution: This variety was very rare (VR) and found in the epipelic and epiphytic samples of lakes YL1 and YL2. Lakes YL1 and YL2 are located at an elevation of 2980 m a.s.l. and are characterized by pH values of 6.85 and 6.89, respectively. According to Lenzenweger (1999), the ecological characteristics of this variety are like the type species. It is a well-adapted species that prefers oligotrophic and slightly eutrophic waters but can also occur in Sphagnum ponds and peat bogs and is found in the Alps up to 2500 m a.s.l.

C. cucumis Corda ex Ralfs (Figure 2H)
West and West (1905)  Description: According to Figure 2H, the shapes of the semicells exhibit differences. It is likely that this species was observed after cell division, and that this is why one of the semicells had not completed its development. Cell 1.5 times longer than breadth; cell moderately constricted; sinus narrowly linear; semicell semielliptic; angles round and apex convex. Cell wall finely and closely punctate.
Ecology and distribution: This species was recorded in the epiphytic habitat in lake YL2. It was very rare (VR). Lake YL2 is located at an elevation of 2980 m a.s.l. and is characterized by a pH value of 6.89. According to Lenzenweger (1999) and John et al. (2003), this is a cosmopolitan taxon and widespread in slightly acidic waters in the Alps up to 2000 m a.s.l. and in acidic (pH 4.8-6.8) pools.
Ecology and distribution: This was a very rare (VR) element in the epiphytic samples of lake YL2. It was found in slightly acidic water (pH 6.89) located at an elevation of 2980 m a.s.l. According to Lenzenweger (1999), this variety is acidophilic.
Ecology and distribution: It was found in the epilithic and epiphytic samples of lakes ACL1 and IL. It was very rare (VR). Lakes ACL1 and IL are located at average elevations of 2980 m a.s.l. and 2668 m a.s.l., respectively, and are characterized by pH values of 7.04 and 6.89, respectively. Lenzenweger (1999) reported that this variety occurs in the benthic zone of mountain lakes up to 2500 m a.s.l.
Ecology and distribution: It was found in the epipelic and epiphytic samples of lakes ARL1 and ACL2. This variety was very rare (VR). Lakes ARL1 and ACL2 are located at average elevations of 2687 m a.s.l. and 2712 m a.s.l., respectively, and are characterized by pH values of 6.19 and 7.09, respectively. This species belongs to desmids that have a wide ecological valence and can occur in slightly acidic, slightly alkaline, alkaline (pH 8-9; optimum pH 6-7), oligotrophic, mesotrophic, tropic, and alpine (2400 m a.s.l.) waters (Huber-Pestalozzi, 1982;Lenzenweger, 1999;Coesel and Meesters, 2007).
Ecology and distribution: Cosmarium notabile var. subnotabile was found in the epilithic samples of lake BL2. It was very rare (VR). Lake BL2 is located at an elevation of 2863 m a.s.l. and is characterized by a pH value of 6.75. According to Coesel and Meesters (2007), this variety is mesotrophic.
Ecology and distribution: This variety was found in the epipelic and epiphytic samples of lakes ARL1 and ARL5. It was very rare (VR). Lakes ARL1 and ARL5 are located at average elevations of 2687 m a.s.l. and 2930 m a.s.l., respectively, and are characterized by pH values of 6.16 and 7.02, respectively. Cosmarium paragranatoides var. dickii was previously reported from waters at 1200 m a.s.l. with a pH value of 6.8 in Austria (Lenzenweger, 1999).
Ecology and distribution: We found this taxon in the epiphytic samples of a circumneutral habitat. It was very rare (VR). Lake YL3 is located at an elevation of 2980 m a.s.l. and is characterized by a pH value of 7.01. West and West (1905) noted that this species is principally found among mosses on wet limestone rocks in subalpine habitats. Lenzenweger (1999), on the other hand, stated that this species occurs in mountain lakes up to 2400 m a.s.l. According to Coesel and Meesters (2007), Cosmarium pokornyanum is mesotrophic.
Ecology and distribution: It was found in the epiphytic samples of lake ARL1. It was very rare (VR). Lake RL1 is located at an elevation of 2687 m a.s.l. and is characterized by a pH value of 6.19. This variety has only been reported by Lenzenweger from alpine lakes of the Central Alps (1999). Description: Cell longer than breadth; sinus deep, linear, and a large part closed; semicells trapeziform; lateral margins convex; basal and apex angles rounded. Cell wall is smooth.
Ecology and distribution: This species was found in the epiphytic samples of lake ARL1. It was very rare (VR). Lake ARL1 is located at an elevation of 2687 m a.s.l. and is characterized by a pH value of 6.19. Lenzenweger (1999) found it in a lake (pH 6.8-7) at an elevation of 1400 m in the Northern Alps of Austria. According to Coesel and Meesters (2007), this species is mesotrophic and occurs in slightly acidic and slightly alkaline waters. Description: Cell slightly longer than breadth; sinus deep, narrow, closed in the middle, but open widely to outside and inside; semicells kidney-shaped and depressed. The median parts of the apex slightly truncate. Cell walls have granules which are rounded, disposed in obliquely decussating series.
Ecology and distribution: C. reniforme var. compressum was found in the epiphytic samples of lake ACL3. It was very rare (VR). Lake ACL3 is located at an elevation of 2711 m a.s.l. and is characterized by a pH value of 7.52. This variety is one of the desmids with large ecological valance. It is rather common in slightly acidic and in slightly alkaline (pH 6-8.6) waters and in slightly brackish waters (West and West, 1908;Lenzenweger, 1999;John et al., 2003;Coesel and Meesters, 2007).
C. subspeciosum var. transiens Messikommer ( Figure  3K) Lenzenweger (1999)  Description: Cell about 1.3 times as long as breadth; cells roughly elliptical; sinus moderately deep and linearly closed; semicells rounded-trapezoidal; basal angles broadly rounded; sides flat convex. There are 6 nongranulated waves (crenate) on each side. Apex truncate and flat convex. Cell wall with radially extending rows of outgoing side waves, paired on the outside, to the center of the cell to form simple wads.
Ecology and distribution: Spondylosium papillosum was found in the epiphytic samples of lake ARL1. It was very rare (VR). Lake ARL1 is located at an elevation of 2687 m a.s.l. and is characterized by a pH value of 6.89. It occurs in peat waters (Lenzenweger, 1997).
Ecology and distribution: Staurastrum dilalatum was found in the epipelic and epiphytic samples of lakes YL1 and IL. It was very rare (VR). Lakes YL1 and IL are located at average elevations of 2980 m a.s.l. and 2670 m a.s.l., respectively, and are characterized by pH values of 6.85 and 6.78, respectively. According to the literature (John et al., 2003;Coesel and Meesters, 2013), this species is cosmopolitan and occurs in acidic and oligo-mesotrophic water bodies.
Ecology and distribution: Staurastrum dybowskii was found in the epipelic samples of lake ARL4. It was very rare (VR). Lake ARL4 is located at an elevation of 2890 m a.s.l. and is characterized by a pH value of 6.73. According to Coesel and Meesters (2013), this species occurs in plankton of oligo-mesotrophic and slightly acidic water bodies.
S. glaronense Messikommer ( Figure 4F) Coesel and Meesters (2013)  Description: This species was identified based on morphotaxonomic features only available in the apical view. Semicells in apical view 5-radiate the short, thick-set processes rounded-truncate at their apex. Semicell body with a cluster of granules near the base of each process.
Ecology and distribution: It was found in the epiphytic samples of lake YL3. This variety was very rare (VR). Lake YL3 is located at an elevation of 2980 m a.s.l. and is characterized by a pH value of 7.1. S. punctulatum var. pygmaeum occurs in small waters (pH 6.5) (Lenzenweger, 1997).
Ecology and distribution: This variety was found in the epipelic and epiphytic samples of lakes ARL1 and BL4. It was very rare (VR). Lakes ARL1 and BL4 are located at average elevations of 2687 m a.s.l. and 2924 m a.s.l., respectively, and are characterized by pH values of 6.19 and 7.04, respectively. The ecological characteristics of this variety are similar to the type species (Teilingia excavata), which is common in acidic Sphagnum marshes (pH 5-5.8) and in peatlands (2300 m a.s.l., the Alps) (Lenzenweger, 1997 Dillard (1990) p. 144, pl. 51, fig. 3; Lenzenweger (1996)  Description: Cells longer than breadth, with a slight median constriction; cells in front view from the midregion toward the ends moderately tapering, with convex to concave lateral sides; semicells very gradually attenuated to the apices; apex fairly broad and rounded, with a deep median incision; in side view strongly attenuated; cell wall minutely punctate and colorless.
In total, 26 desmid species were described herein as new records for the freshwater algal flora of Turkey. Qualitatively, Cosmarium was the most dominant and diverse genus with 15 species (57.69%), followed by the subdominant Staurastrum (5 species; 19.23%); whereas the other genera were only represented by 1 species (3.84%). The dominance of the genus Cosmarium in these mountain nature park habitats is highly congruent with previous studies on similar ecosystems in the Northern Hemisphere (Medvedeva, 2001;Sterlyagova, 2008;Šovran et al., 2013;Briškaite et al., 2016). Cosmarium is the genus that typifies desmids (Lee, 2015). According to recent phylogenetic data, Gontcharov and Melkonian (2008b) showed that Cosmarium is polyphyletic in origin, and its species are distributed within 11 well-supported clades.
To date, Cosmarium polygonum var. hexagonum and Staurastrum glaronense have only been reported by Lenzenweger (1999) and Coesel and Meesters (2013) from the Central Alps and Swiss Alps. There is no information regarding distribution of these species in the Algaebase (Guiry and Guiry, 2019). Therefore, our results will be the second published for these interesting species.
On the basis of the hydrochemical data, the lakes and the pond in Artabel Lakes Nature Park are characterized by relatively acidic to circumneutral waters. Furthermore, our results show that desmids are not merely one of the main freshwater microalgae groups that occur in highmountain lakes biotopes in Turkey; they also inhabit microhabitats with oligotrophic conditions characterized by relatively acidic to weakly alkaline waters with low conductivity (Saber et al., 2018). Geographical and ecological analyses also showed that the desmid flora is typical, with a predominance of cosmopolitan species, planktic-benthic forms, acidophilic and pH-indifferent species, and halophobic-to-salinity-indifferent species.
In conclusion, the investigated lakes can be classified as relatively pristine habitats in good ecological condition based on their hydrochemical and desmid biodiversity characteristics.