Snow algal communities on glaciers in the Suntar-Khayata Mountain Range in eastern Siberia, Russia

Polar Science xxx (2016) 1e12

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Snow algal communities on glaciers in the Suntar-Khayata Mountain Range in eastern Siberia, Russia Sota Tanaka a, *, Nozomu Takeuchi a, Masaya Miyairi a, Yuta Fujisawa a, Tsutomu Kadota b, Tatsuo Shirakawa c, Ryo Kusaka c, Shuhei Takahashi c, Hiroyuki Enomoto d, Tetsuo Ohata b, Hironori Yabuki b, Keiko Konya b, Alexander Fedorov e, Pavel Konstantinov e a

Chiba University, Yayoicho 1-33, Inageku, Chiba, 263-8522, Japan Japan Agency for Marine-Earth Science and Technology, Natsushimacho 2-15, Yokosukashi, Kanagawa, 237-0061, Japan Kitami Institute of Technology, Koencho 165, Kitami, 090-8507, Japan d National Institute of Polar Research, Midori-cho, Tachikawa, Tokyo, 190-8518, Japan e Melnikov Permafrost Institute, Merzlotnaya St., 36, Yakutsk, 677010, Russia b c

a r t i c l e i n f o

a b s t r a c t

Article history: Received 1 October 2015 Received in revised form 18 February 2016 Accepted 15 March 2016 Available online xxx

Snow and ice algal communities were investigated on four glaciers in the Suntar-Khayata Mountain Range in eastern Siberia in Russia over three melting seasons from 2012 to 2014. Two taxa of green algae and five taxa of cyanobacteria were observed on the glaciers. The algal community was dominated by green algae: Ancylonema nordenskioldii in the lower bare ice area and Chloromonas sp. in the upper snow area. The total algal bio-volume showed altitudinal variation, ranging from 0.03 to 4.0 mL m
2, and was greatest in the middle of the glaciers. The altitudinal variations in the algal community were similar on all studied glaciers, suggesting that they are typical in this region. Observations over the three years revealed that there was no significant change in the community structure, but a significant change in the total biomass. Since the mean summer air temperature was significantly higher in 2012 when algal biomass was greater, the difference in algal biomass among the years is probably due to the duration of surface melting. The community structure on the studied glaciers is similar to those on glaciers in Arctic and sub-Arctic regions. © 2016 Elsevier B.V. and NIPR. All rights reserved.

Keywords: Ice algae Snow algae Mountain glacier Eastern Siberia Algal community

1. Introduction Snow and ice algae are photosynthetic microbes growing on snow and ice, and they have been reported on glaciers, snow fields, and sea ice in many parts of the world. They appear on glaciers during the melting season since they need liquid water for their growth. Their community is usually composed of green algae and cyanobacteria, but occasionally of diatoms and charophytes in some regions (e.g., Daily, 1961; Watanabe, 1982). They play an important role as primary producers in glacier ecosystems (Hodson et al., 2008; Anesio et al., 2009), and they and their products sustain heterotrophic organisms living on glaciers, such as bacteria, tardigrades, rotifers, midges, stoneflies, collembolans, and ice worms (e.g., Kohshima, 1987; Aitchison, 2001; Hoham and Duval, 2001; Murakami et al., 2015).

* Corresponding author. E-mail address: [email protected] (S. Tanaka).

Since algal cells in snow and ice can efficiently absorb solar radiation, they can affect the melting of snow and ice (e.g., Takeuchi et al., 2015). Blooms of algae can change the color of snow or ice to green, red, brown, or black since the algal cells are usually filled with light-absorbing pigments. For example, the melting snow surface often appears to be red due to the red-pigmented algal cells of Chlamydomonas nivalis or Chloromonas sp. (e.g., Hoham and Mullet, 1977; Kol and Eurola, 1974; Takeuchi et al., 2006; Lutz et al., 2015). Glacial ice surfaces in Svalbard and Greenland are often patchily colored blown or grey due to the dark-reddish algal cells of Ancylonema nordenskioldii (Remias et al., 2012; Yallop et al., 2012; Lutz et al., 2014). These snow or ice surfaces with algae can absorb more solar radiation due to their lower reflectivity, and thus melt faster than surfaces without algae (e.g., Takeuchi et al., 2001a; Takeuchi, 2009). Filamentous cyanobacteria, which often grow on ice surfaces, also have a large effect on surface albedo because they can entangle with mineral and organic particles and form darkcolored aggregates called cryoconite granules (e.g., Takeuchi et al.,

http://dx.doi.org/10.1016/j.polar.2016.03.004 1873-9652/© 2016 Elsevier B.V. and NIPR. All rights reserved.

Please cite this article in press as: Tanaka, S., et al., Snow algal communities on glaciers in the Suntar-Khayata Mountain Range in eastern Siberia, Russia, Polar Science (2016), http://dx.doi.org/10.1016/j.polar.2016.03.004

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S. Tanaka et al. / Polar Science xxx (2016) 1e12

2001b). The granules are particularly abundant on Asian mountain glaciers, and have been reported to substantially accelerate ice melting compared to a clean surface on a Himalayan glacier (Kohshima et al., 1993). Thus, spatial and geographical variations in these snow and ice algae are important in evaluating their impact on glacier melting. Algal communities on glaciers usually vary with altitude. During the melting season, the lower part of glaciers has a bare ice surface and is dominated by algae that are ice environment specialists, which prefer the conditions on ice for their growth (Yoshimura et al., 1997). In contrast, the upper part of glaciers has a snow surface and is dominated by the algae of snow environment specialists. The area around the snow line, which is the border between snow and bare ice areas on glaciers, is dominated by generalist algae. The total algal biomass also varies with altitude on glaciers. It generally decreases as altitude increases on Asian glaciers, but reaches a maximum in the middle of Arctic and sub-Arctic glaciers (e.g., Yoshimura et al., 1997; Takeuchi, 2001). The factors affecting these altitudinal changes in algal communities have been explained by altitudinal gradients in snow cover frequency, solar radiation, and the amount of running meltwater on the surface (e.g., Yoshimura et al., 1997). Algal communities also vary around the world (e.g., Takeuchi et al., 2006). For example, algal communities on the bare ice surface of glaciers are usually dominated by filamentous cyanobacteria in central Asia (e.g., Takeuchi and Li, 2008; Takeuchi et al., 2010), but by green algae in Arctic and sub-Arctic regions including Alaska, Greenland, and the Altai Mountains (Takeuchi et al., 2006). The geographical variation suggests that the effect of algae on the surface albedo of glaciers differs among the regions, and the variations are probably caused by the physical and chemical characteristics of glaciers in each region, and by the limited extent of algal dispersal. Recent climate warming has substantially affected the physical and chemical conditions on glaciers, which possibly affect snow algal communities and their geographical distribution on glaciers. For example, climate warming can extend the duration of melting on glaciers, causing more algal growth. It might also affect atmospheric circulation, changing the nutrient supply via aerial deposition on glaciers. These environmental changes possibly affect algal growth on glaciers and the geographical extent of the algal communities. Eastern Siberia is a glacierized mountainous area in the Arctic and sub-Arctic regions. There are many glaciers in mountain ranges of the region such as the Suntar-Khayata, Cherskiy, and Kodar Mountain Ranges. Some of the glaciers have been glaciologically studied since the 1950s, but there is a lack of information on the snow and ice algal community on glaciers in this region. Furthermore, a rise of mean annual and summer temperature has been reported in Suntar-Khayata region during the past 40 years (e.g. Takahashi et al., 2011; Chapin et al., 2005). Descriptions of the algal community in the region could support our understanding of the biogeography of snow and ice algae over the circum-Arctic area and are important for evaluating the impacts of climate change on glacier ecosystems in the Arctic. In this paper, we aim to describe for the first time the snow and ice algal communities on four glaciers in the Suntar-Khayata Mountain Range in eastern Siberia in Russia. We collected samples of surface snow and ice from sites at different elevations on four glaciers and showed the spatial variation in the algal community. We also collected the samples over three melting seasons from 2012 to 2014 and showed the inter-annual variability in the algal community. Results are compared with those of other Arctic and Asian regions and their spatial and annual variations are discussed along with the physical and chemical conditions of the glaciers.

2. Study site and methods The investigation was carried out on four glaciers in the SuntarKhayata region in eastern Siberia. This region is located in a mountain range from 62 N to 63 N and from 140 220 E to 142 E (Fig. 1). The area was mostly vegetated with boreal forest or tundra below approximately 1900 m a.s.l., and with epilithic lichen communities around glaciers. This mountain region consists of two catchments: the Indigirka River and south-oriented drainages. The former drains into the Arctic Ocean and the latter drains into the Sea of Okhotsk. A total of 195 glaciers with a combined area of 163 km2 have been listed in this mountain range. The total area has been reduced by 20.8% since 1945, and the average rate of loss is 0.75 km2 per year (Ananicheva et al., 2006). Glaciers in this range can be grouped into three main massifs: the northern massifs, the central massifs, and the southern massifs. The southern massifs are closer to the Sea of Okhotsk and therefore more influenced by the Okhotsk air mass than the northern massifs, and its glaciers are retreating faster (Takahashi et al., 2011). We selected four glaciers: Glaciers No. 31, 29, 32, and 33, for this study in the central massifs. The field investigations were carried out on these glaciers from July 2 to September 3 in 2012, from July 29 to August 24 in 2013, and from July 30 to August 10 in 2014. We accessed this area by a helicopter in 2012 and 2013 and by an off-road vehicle in 2014 from the city of Yakutsk, located approximately 500 km west of the region. On the way to the area, several forest fires were observed, as were many longicorn beetles, which may have been burnt out from the forests and were observed on glaciers in 2012 and 2013. The mass balance of Glacier No. 31 has been monitored since the 1950s. The first glaciological and meteorological observations on the glacier were conducted during the International Geophysical Year (IGY, 1957e58) by Russian researchers. Then, the glacier was resurveyed in 2001 and in 2004/2005 by Russian/Japanese joint research groups. According to these studies, this glacier retreated by approximately 200 m in length from 1959 to 2001 (Yamada et al., 2002). Snow fall mainly occurs from April to September. The equilibrium line was located at approximately 2300 m a.s.l. in 2009 (Takahashi et al., 2011). Glaciers No. 31, 29, and 32 face the northwest, with areas of 3.20, 4.05, and 4.25 km2 and lengths of 3.85, 4.50, and 4.90 km, respectively. Glacier No. 33 faces southeast, with an area of 2.00 km2 and a length of 2.30 km (Koreisha, 1963). The highest peak in this area is approximately 2960 m a.s.l. All of the glaciers terminated at approximately 2030 m a.s.l. The surfaces of the glaciers were mostly debris-free bare ice or snow. Dark-colored cryoconite was observed in cryoconite holes and on the bare ice surface of the glaciers, and it appeared to be more abundant in the middle part of the glaciers. Sections of red colored snow and ice were also observed in the middle parts of Glacier No. 29 (around 2370 m a.s.l.) and No. 31 (around 2390 m a.s.l.). Collections of surface ice or snow were carried out at a total of 20 sites on the four glaciers. We collected samples at six sites ranging in altitude from 2120 to 2540 m a.s.l. (A1eA6: Fig. 1). on Glacier No. 31; five sites on Glacier No. 29 (B1eB5 from 2100 to 2509 m a.s.l.), four sites on Glacier No. 32 (C1eC4 from 2184 to 2463 m a.s.l.), and five sites on Glacier No. 33 (D1eD5 from 2325 to 2496 m a.s.l.). The sites where we collected samples in each year are listed in Table 1. When we collected samples, the snow line in 2012 was located between A5 and A6, B4 and B5, and D4 and D5, and above C4 on Glaciers No. 31, 29, 33, and 32, respectively, while it was located above all of the study sites in 2013 and 2014. In order to know whether snow and ice algae can survive the winter under the snow cover, we collected the ice surface below the snow cover at the upper snow site (D5 of Glacier No. 33) in 2012. The snow depth was 18 cm at the site.

Please cite this article in press as: Tanaka, S., et al., Snow algal communities on glaciers in the Suntar-Khayata Mountain Range in eastern Siberia, Russia, Polar Science (2016), http://dx.doi.org/10.1016/j.polar.2016.03.004

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Lena river

Siberia Suntar Khayata Mts.

Yakutsk

60˚N

Magadan

Sampling site

Sea of Okhotsk

Glacier 50˚N

Mountain ridge

Pacific Ocean 130˚E

Glacier flow

170˚E

150˚E

No.34

No.31 No.29

A1 (2120m)

B1 (2100 m)

Mt. MusKhaya (2959 m)

C1 (2184 m) C2 (2275 m)

A2 (2158 m)

C3 (2350 m) C4 (2463 m)

A3 (2257m) A4 (2354 m)

B2 (2210 m)

B4 (2400 m)

D5 (2496 m)

A5 (2446 m)

B3 (2297 m)

A6 (2540 m)

D4 (2474 m)

N

D3 (2422 m)

D2 (2377 m)

D1 (2325 m)

No.33

No.30 B5 (2509 m)

No.32

1 km

Fig. 1. Locations of Glaciers No. 31, 29, 32, and 33 in the Suntar-Khayata Mountain Range, Russia, and maps of the glaciers showing the study sites.

Samples were collected with a stainless-steel scoop at three to five surfaces randomly selected at each site. We measured the collected area to calculate the algal biomass per unit area. The samples were melted and then preserved as a 3% formalin solution in 30 mL clean polyethylene bottles. For the microscopy of algal cell morphology, another set of samples was collected and kept frozen without formalin. All samples were transported to a laboratory in

Chiba University, Japan, for analysis. The algal biomass at each site was represented by the cell number per unit melt water volume and by the algal cell volume (bio-volume) per unit area. The samples were ultrasonicated for 10 min to loosen sedimentary particles. Then, 2e100 mL of the sample water was filtered through a hydrophilic membrane filter (pore size 0.45 mm, Millipore JHWP01300) and the number of algae

Please cite this article in press as: Tanaka, S., et al., Snow algal communities on glaciers in the Suntar-Khayata Mountain Range in eastern Siberia, Russia, Polar Science (2016), http://dx.doi.org/10.1016/j.polar.2016.03.004

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Table 1 List of study sites, sampling dates, and surface conditions from 2012 to 2014 on glaciers in the Suntar-Khayata Mountain range. Glacier

Site

Altitude (m a.s.l.)

2012

2013

No. 31

A1 A2 A3 A4 A5 A6 B1 B2 B3 B4 B5 C1 C2 C3 C4 D1 D2 D3 D4 D5

2120 2158 2257 2354 2446 2540 2100 2210 2297 2400 2509 2184 2275 2350 2463 2325 2377 2422 2474 2496

12 July, ice 18 July, ice 12 July, ice 12 July, ice 18 July, ice 18 July, snow 15 July, ice 15 July, ice 15 July, ice 15 July, ice 15 July, snow 10 July, ice 10 July, ice 10 July, ice 10 July, ice 9 July, ice

1 August, ice 1 August, ice 1 August, ice 3 August, ice 3 August, ice 3 August, ice 30 July, ice

No. 29

No. 32

No. 33

9 July, ice 9 July, snow

2014 6 August, ice 7 August, ice

30 July, ice 30 July, ice 8 August, ice 8 August, ice 8 August, ice 8 August, ice 7 August, ice 7 August, ice 7 August, ice 7 August, ice 7 August, ice

on the filter was counted (1e3 lines on the filter) with an optical microscope (OLYMPUS BX51, Japan). We counted only algal cells which showed chlorophyll autofluorescence as active cell. Each sample was counted three times. From the mean results of cell counts and the filtered volume of sample water, the cell concentration (cells mL
1) of the sample was obtained. Mean cell volume was estimated by measuring the size of 50 cells for each taxon. From these analyses, we estimated the total algal biomass (mL m
2). Community structure was represented by the mean proportion of each taxon to the total algal biomass at each sampling site. The mean and standard deviation were obtained based on the results from surfaces at each site. Electrical conductivity (EC), pH, and the amount of mineral particles on the glacier surface were measured at each site in 2012. We collected surface ice or snow with a stainless-steel scoop melted it in Whirl-Pak bags, and then measured the EC and pH of the melted water with a portable measuring device (HORIBA D54SE, Japan). After the measurement, the particulate sediment in each sample was transported to Chiba University, Japan, and then dried and weighed. After the samples were combusted for 3 h at 500  C in an electric furnace (ISUZU SS-K-1200, Japan) to remove organic matter in the samples, we weighed the remained mineral particles and estimated the amount of mineral particles per unit area (g m
2). 3. Results 3.1. Snow and ice algae observed on Suntar-Khayata glaciers Microscopy revealed two major taxa of green algae and five taxa of cyanobacteria on the glaciers (Fig. 2). Their descriptions are as follows: Chlorophyta (green algae). Chloromonas sp. (Fig. 2a). Cells round, green or red-orange pigmented. Chloroplast without pyrenoids. Two distinct cell sizes: smaller cells 11.1 ± 2.8 mm (mean ± SD) in diameter, larger cells 18.4 ± 2.1 mm. Most cells round-shaped resting cells. Dominant on visible red snow at site B5 and on ice surfaces at sites B4 and A5. Ancylonema nordenskioldii Berggren (Fig. 2b). Filaments straight or slightly curved, ordinarily consisting of 1e10 cells. Cell sap usually dark brown. Chloroplast with one or two

pyrenoids. Cylindrical cells 18.0 ± 3.8 mm long, 9.8 ± 0.73 mm wide. Cells per filament differed among study sites. Most algae consisted of single cell at site near glacier terminus, but multiple cells from middle part of glacier (A3eA4). Single-cell type 20.8 ± 3.9 mm long, 10.1 ± 0.87 mm wide. Dominant at lower part of glaciers, accounting for 92% of cells at site A1, but 41% at site A2 and 9e16% at sites A3 and A4. Cyanobacteria (blue-green algae). Oscillatoriaceae (Osc.) cyanobacterium 1 (Fig. 2c). Trichome blue-green and 13e125 mm long. Cells 1.9 ± 1.1 mm wide. Oscillatoriaceae cyanobacterium 2 (Fig. 2d). Trichome blue-green and 13e195 mm long. Cells 3.7 ± 0.56 mm wide, 4.0 ± 1.3 mm long. Cells about 1.1-fold longer than wide. Oscillatoriaceae cyanobacterium 3 (Fig. 2e). Trichome blue-green or brownish and 11e65 mm long. Cells 5.0 ± 0.51 mm wide, 2.5 ± 0.59 mm long. Cells about 2-fold wider than long. Calothrix parietina Thuret (Fig. 2f). Filaments sinuous, cylindrical, long-tapering at end, 6.4 ± 0.94 mm wide. Trichome blue-green, cylindrical, 35e115 mm long. Sheath brown, 1.0 ± 0.26 mm thick. Chroococcaceae (Chr.) cyanobacterium (Fig. 2g). Cells spherical, with thin outer envelopes. Two distinct types of cell size. Smaller cells 2.6 ± 0.51 mm in diameter, larger cells 5.5 ± 1.2 mm in diameter. 3.2. Quantitative analyses of snow algal community on glaciers in 2012 Each algal taxon had a different altitudinal distribution pattern (Fig. 3). Ancylonema nordenskioldii, Chr. cyanobacterium, and Osc. cyanobacterium 1 were observed on the entire ice surface of the glaciers, but they reached maximums at different elevations. A. nordenskioldii was most abundant at middle-elevation sites (e.g., site A4 on Glacier No. 31), while Chr. cyanobacterium and Osc. cyanobacterium 1 showed two peaks in abundance, at the middle and lowest sites (sites A4 or A5, and A1). Chloromonas sp. was observed on both ice and snow surfaces and was most abundant at the site near the snow line (site A5). Osc. cyanobacteria 2 and 3 and Calothrix parietina were observed at some, but not all, of the sites from the ice area. These three taxa were most abundant on middleelevation sites. The altitudinal distributions of each algal taxon were similar on the other three glaciers (Glaciers No. 29, 32, and 33; Supplement. 1). The total algal cell volume showed altitudinal variations on the four glaciers. On Glaciers No. 31, 29, 32, and 33 it ranged from 0.03 to 4.0 mL m
2; 0.17e2.1 mL m
2; 0.40e3.1 mL m
2; and 0.01e16 mL m
2, respectively (Fig. 4a). On all four glaciers, the biomass was highest in the middle part of each glacier and gradually decreased with increasing or decreasing altitude. Statistical analyses (one-way analysis of variance (ANOVA)) revealed that the altitudinal variation in the biomass was significant on all four glaciers (F ¼ 2.62, P ¼ 0.00004 < 0.01 for Glacier No. 31; F ¼ 3.12, P ¼ 0.0058 < 0.01 for No. 29; F ¼ 3.49, P ¼ 0.00001 < 0.01 for No. 32; and F ¼ 3.98, P ¼ 0.000008 < 0.01 for No. 33). The algal community structure showed that green algae were dominant on all four glaciers (Fig. 5). The ice area of the glaciers was dominated by A. nordenskioldii, while the snow area was dominated by Chloromonas sp. On Glacier No. 31, A. nordenskioldii accounted for 65e95% of the total biomass in the ice area and Chloromonas sp. accounted for 82% in the snow area. Although site B4 on Glacier No. 29 had a bare ice surface, the site was exceptionally dominated by Chloromonas sp. (80%) and secondly by A. nordenskioldii (15%). Site D3 on Glacier No. 33 was also exceptionally dominated by coccoid

Please cite this article in press as: Tanaka, S., et al., Snow algal communities on glaciers in the Suntar-Khayata Mountain Range in eastern Siberia, Russia, Polar Science (2016), http://dx.doi.org/10.1016/j.polar.2016.03.004

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Fig. 2. Photographs of snow algae observed on glaciers in the Suntar-Khayata Mountain Range: (A) Chloromonas sp.; (B) Ancylonema nordenskioldii; (C) Oscillatoriaceae cyanobacterium 1; (D) Oscillatoriaceae cyanobacterium 2; (E) Oscillatoriaceae cyanobacterium 3; (F) Calothrix parietina; and (G) Chroococcaceae cyanobacterium. All photographs were taken with a phase contrast microscope. Scale bar ¼ 10 mm.

cyanobacteria (Chr. cyanobacterium), which accounted for 90% of the total biomass. This site was the only surface that was dominated by cyanobacteria instead of green algae on the four glaciers. Algal cells which showed chlorophyll autofluorescence were observed in the samples from the ice surface collected below the snow at site D5 in 2012. The average value of the total algal cell biomass was 0.74 mL m
2 and the dominant taxon was A. nordenskioldii (87%). Chloromonas sp., Osc. cyanobacteria, and Chr. cyanobacterium comprised 8%, 2%, and 2% of the biomass, respectively.

3.3. EC, pH, and abundance of mineral particles on the glaciers The EC of the surface snow and ice was generally low and varied slightly among the study sites (Table 2). On Glacier No. 31, it ranged from 2.82 to 6.26 mS cm
1 (mean: 3.91 mS cm
1), and was highest at the middle part (site A3) and lowest at the upper part (site A6). The range and mean value were generally similar on the other glaciers: it ranged from 3.24 to 7.14 mS cm
1 (mean: 5.07 mS cm
1) for Glacier No. 29, from 2.89 to 7.73 mS cm
1 (mean: 5.11 mS cm
1) for No. 32, and from 2.78 to 8.36 mS cm
1 (mean: 6.50 mS cm
1) for No. 33. The pH of the surface snow and ice also slightly varied among the study sites (Table 2). It ranged from 6.22 to 8.17 (mean: 7.12), and was highest at the lower site (site A1) and lowest at the middle site (site A4) on Glacier No. 31. There was no significant difference in pH among the four glaciers. It ranged from 5.92 to 7.19 (mean: 6.49) for Glacier No. 29, from 4.82 to 6.84 (mean: 6.20) for No. 32,

and from 7.64 to 8.58 (mean: 8.17) for No. 33. The abundance of mineral particles showed altitudinal variations for the four glaciers (Fig. 6). The mean abundance on the ice area of Glaciers No. 31, 29, 32, and 33 was 39 g m
2, 59 g m
2, 8 g m
2, and 67 g m
2, respectively. It was relatively abundant at sites B3 (131 g m
2) and D3 (116 g m
2). A t-test revealed that the abundance of mineral particles at site B3 was significantly greater than at lower ice sites on Glacier No. 29 (B3 and B1: t ¼ 3.127, P ¼ 0.02 < 0.05; B3 and B2: t ¼ 3.722, P ¼ 0.02 < 0.05). The abundance at site D3 was also significantly greater than at other sites on Glacier No. 33 (D3 and D1: t ¼ 4.915, P ¼ 0.001 < 0.01). Although the abundance at site A5 was also greater, it was not significantly different from at other sites on Glacier No. 31 (A5 and A1: t ¼ 1.677, P ¼ 0.13 > 0.05; A5 and A2: t ¼ 1.970, P ¼ 0.08 > 0.05; A5 and A3: t ¼
0.819, P ¼ 0.44 > 0.05; A5 and A4: t ¼ 1.810, P ¼ 0.11 > 0.05).

3.4. Inter-annual changes in the snow algal community from 2012 to 2014 The analysis of the algal community on the glaciers over the three years revealed that the species composition did not change, but the proportions of each taxon in the community slightly changed (Fig. 5). The bare ice area of Glacier No. 31 was always dominated by A. nordenskioldii over all three years. The altitudinal distribution of total algal biomass, which was highest at the middle part and lower at the lower and upper sites of the glacier, was also

Please cite this article in press as: Tanaka, S., et al., Snow algal communities on glaciers in the Suntar-Khayata Mountain Range in eastern Siberia, Russia, Polar Science (2016), http://dx.doi.org/10.1016/j.polar.2016.03.004

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S. Tanaka et al. / Polar Science xxx (2016) 1e12

Fig. 3. Altitudinal distribution of the cell number per unit area (103 cells mL
2) of each algal taxon on Glacier No. 31 in 2012. Dotted lines show the altitude of the snow line.

(0.76 mL m
2 for A2 and 3.8 mL m
2 for A4), but lowest in 2013 (0.04 mL m
2 for A2 and 0.09 mL m
2 for A4) and intermediate in 2014 (0.11 mL m
2 for A2 and 0.36 mL m
2 for A4) on Glacier No. 31. A t-test revealed that the biomass in 2012 was significantly greater than in other years at A2 (2012 and 2013: t ¼ 3.849, P ¼ 0.009 < 0.01; 2012 and 2014: t ¼ 3.375, P ¼ 0.03 < 0.05; 2013 and 2014: t ¼
1.618, P ¼ 0.18 > 0.05) and A4 (2012 and 2013: t ¼ 4.468, P ¼ 0.011 < 0.05; 2012 and 2014: t ¼ 4.114, P ¼ 0.014 < 0.05; 2013 and 2014: t ¼
2.037, P ¼ 0.11 > 0.05). The results for Glaciers No. 29 and 32 over two seasons from 2012 to 2013 showed similar patterns to those on Glacier No. 31. The bare ice surfaces on both glaciers were dominated by A. nordenskioldii, and the snow surface on Glacier No. 29 was dominated by Chloromonas sp. in both years (Fig. 5). The total algal biomass was greatest at the middle part of the glaciers and gradually decreased with increasing or decreasing altitude in both years. The mean total biomass in the bare ice area was generally smaller in 2013 than in 2012 at each site (mean of No. 29: 1.1 vs. 0.01 mL m
2; mean of No. 32: 1.2 vs. 0.12 mL m
2; Fig. 4), as was observed on Glacier No. 31. A change in the dominant taxon was observed at the lowest site, site B1, on Glacier No. 29. It was A. nordenskioldii in 2012, but Chloromonas sp. in 2013 (Sup. 1b). The proportion of A. nordenskioldii to the total algal biomass at the site decreased from 58% in 2012 to 25% in 2013. The dominant taxon of the algal community on Glacier No. 33 was A. nordenskioldii in both 2012 and 2013 at the lowest site, site D1, while it changed at the middle and upper sites, sites D3 and D5 (Fig 5). The algal community at site D3, which was the only site dominated by Chr. cyanobacterium in 2012, was dominated by A. nordenskioldii in 2013. The proportion of A. nordenskioldii to the total algal biomass at site D3 was 1% in 2012, but increased to 35% in 2013. The proportion of Chr. cyanobacterium was 90% in 2012, but decreased to 17% in 2013. At site D5, the community was dominated by Chloromonas sp. (57%) in 2012, but was dominated by A. nordenskioldii (73%) in 2013. The mean total biomass in the bare ice area greatly decreased from 8.8 mL m
2 in 2012 to 0.84 mL m
2 in 2013. A t-test showed that there was a significant difference in the algal biomass between 2012 and 2013 on sites D1 (t ¼ 4.85,

Fig. 4. The altitudinal change in the total algal biomass of Glaciers No. 31, 29, 32, and 33 in 2012 (A) and 2013 (B). Solid and open marks indicate bare ice and snow-covered areas, respectively. Error bar ¼ standard deviation.

similar over the three years. In contrast, the total algal biomass at each site in the bare ice area changed greatly from year to year. It was highest in 2012

P ¼ 0.008 < 0.01) and D3 (t ¼ 5.91, P ¼ 0.01 < 0.01).

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Fig. 5. Altitudinal change in the structure of the algal community on glaciers in Suntar-Khayata from 2012 to 2014; (A) No. 31 in 2012; (B) No. 31 in 2013; (C) No. 31 in 2014; (D) No. 29 in 2012; (E) No. 29 in 2013; (F) No. 32 in 2012; (G) No. 32 in 2013; (H) No. 33 in 2012; and (I) No. 33 in 2013. Dotted lines show the altitude of the snow line and white upwardpointing triangles show the altitude of the terminus of each glacier.

Table 2 The EC and pH (range and mean) of surface melt water measured on each glacier of Suntar-Khayata in 2012. Glacier

EC mS cm
1

pH

No. No. No. No.

2.82e6.26 3.24e7.14 2.89e7.73 2.78e8.36

6.22e8.17 5.92e7.19 4.82e6.84 7.64e8.58

31 29 32 33

(3.91) (5.07) (5.11) (6.50)

(7.12) (6.49) (6.20) (8.17)

4. Discussion 4.1. Snow and ice algal community on glaciers of the SuntarKhayata region The taxa of green algae and cyanobacteria observed on the glaciers in this study have been commonly found on glaciers in other Asian and Arctic regions. For example, Chloromonas sp. or its close relative has been commonly reported on the snow surface of glaciers in both the Northern and Southern Hemispheres (e.g.,

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Fig. 6. Altitudinal change in the abundance of mineral particles per unit area on glaciers in Suntar-Khayata in 2012. Solid and open marks indicate bare ice and snowcovered areas, respectively. Error bar ¼ standard deviation.

Takeuchi and Kohshima, 2004; Takeuchi et al., 2006). Oscillatoriaceae and Chroococcaceae are also common families of cyanobacteria on glaciers reported from all over the world (e.g., Takeuchi et al., 2009). C. parietina and A. nordenskioldii are typical algae of glaciers in the Arctic region. C. parietina has been reported only on glaciers in Arctic and sub-Arctic regions, including Greenland, the Canadian Arctic, and the Russian Altai (e.g., Gerdel and Drouet, 1960; Takeuchi et al., 2006). A. nordenskioldii is a common taxon in the Northern Hemisphere, and is dominant in the algal community on glaciers and sea ice in the Arctic region, including West Russia, Alaska, Canada, and Greenland (e.g., Melnikov, 1997), while it was rarely observed on glaciers in Central Asia (e.g., Yoshimura et al., 1997; Segawa and Takeuchi, 2010). A green alga, Mesotaenium berggrenii, which is a common taxon on glaciers in the Arctic region (e.g., Takeuchi, 2001), was rarely observed on the glaciers. The lack of this taxon may be due to the higher pH of the glacial melt water. The pH of glaciers in Alaska and the Russian Altai, where the alga was observed, ranged from approximately 5 to 6, while the pH of glaciers in the Canadian Arctic, sea ices in the Arctic Ocean, and glaciers in Central Asia, where the alga was not observed (Melnikov, 1997; Takeuchi et al., 2001c; Segawa and Takeuchi, 2010), ranged from 8 to 9 (Table 3). The pH of the glaciers in this study was also relatively high, ranging from 5 to 9 (Table 2). These facts suggest that the high pH of the glacier surface does not allow M. berggrenii to grow on the glaciers. The altitudinal distribution of each algal taxon on the four glaciers agreed well with those reported on other glaciers. Yoshimura et al. (1997) classified algae on glaciers into four specialized types: snow-environment specialists (observed on the snow surface), iceenvironment specialists (observed on the ice surface), generalists (observed on both snow and ice surfaces), and opportunists (observed on only a specific area on a snow or ice surface). A. nordenskioldii, Osc. cyanobacterium 1, and Chr. cyanobacterium

can be classified as ice-environment specialists because they were observed at all of the study sites in the ice areas. Chloromonas sp. is an opportunist or snow-environment specialist because it was observed in all of the snow areas and in some of the ice surface areas near the snowlines. Osc. cyanobacterium 2 and 3 and C. parietina are opportunists because they were only observed in the ice areas of the middle-parts of the glaciers. These altitudinal distributions may reflect favorable surface conditions for each alga. The altitudinal changes in total algal biomass on the four glaciers showed similar trends and agreed well with those reported in previous studies in Arctic regions. The results showed that the biomass was higher at the middle part of glaciers and lower at the upper snow area and lower ice area. A similar trend has been reported from glaciers in Alaska and the Russian Altai, and Greenland (Takeuchi, 2001; Takeuchi et al., 2006; Uetake et al., 2010). The decrease in biomass in the upper part of the glaciers can be explained by an increase in the snow-cover frequency with altitude reducing the light intensity of the algal habitats (Yoshimura et al., 1997). Since winter snow cover disappears from lower to higher elevations during the melting season, more sunlight and meltwater can be available to algae in the lower ice area than in the higher snow area. On the other hand, the decrease in biomass in the lower area has been explained by the amount of running meltwater on the glacier surface (Takeuchi, 2001). Since the meltwater was more abundant at the lower area, it can wash algae out from the glacier, and then the algal biomass would decrease as altitude decreased. The community structures of snow and ice algae were mostly similar on the four studied glaciers, indicating that they are typical in this region. The algal communities on bare ice and snow areas were dominated by A. nordenskioldii and Chloromonas sp., respectively. There were only the exceptional algal communities at site B4 on Glacier No. 29 and at site D3 on Glacier No. 33. Although the surface at site B4 was bare ice, the dominant taxon was not A. nordenskioldii but Chloromonas sp., which usually dominated in the snow area. The dominance of Chloromonas sp. is probably due to the location of the snow line, which was just above the site when we collected the samples. Furthermore, patchy winter snow remained at the site, so the bare ice at this site was probably just exposed and A. nordenskioldii had not yet grown at the time of sample collection. The dominant taxon on the bare ice surface at site D3 was Chr. cyanobacteria; 90% of the total algal biomass at the site was dominated by this alga, 6% was filamentous cyanobacteria, and 4% was other green algae. This was the only site where the algal community was dominated by cyanobacteria instead of green algae. Although the reason for this is uncertain, it may be due to the topography of Glacier No. 33, which is the only glacier that flows on the south side of the mountain, while the other glaciers flow on the north side. As previous studies suggested, the pH and EC on the glacier surface may also affect the algal community (e.g., Jones, 1991; Hoham and Duval, 2001). For example, cyanobacteria tend to prefer a higher pH (Bano and Siddiqui, 2004), while green algae prefer a lower pH (Hoham and Mohn, 2004; Stibal et al., 2006). As compared with the bare ice surfaces of Arctic and Asian glaciers (Table 3), the pH on glaciers in Suntar-Khayata tended to be higher

Table 3 The pH and mean biomass of cyanobacteria on bare ice area of glaciers in the Northern Hemisphere. Data are from Takeuchi et al. (2006) for Akkem, Takeuchi (2001) and NADP (2000) for Gulkana, and Segawa and Takeuchi (2010) and Wu et al. (2008) for Qiyi. Glacier

Biomass of cyanobacteria mL m
2

pH

No. 31 (Eastern Siberia, this study) Akkem (Russian Altai) Gulkana (Alaska, USA) Qiyi (Qilian Mts, China)

0.11 0.04 Less than 0.01 1.9

6.22e8.17 2.9e5.2 4.4e5.6 8.05e8.79

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S. Tanaka et al. / Polar Science xxx (2016) 1e12

(mean: 7.1 for No. 31); however, the algal community was dominated by green algae rather than cyanobacteria (Fig. 5). There was no correlation between pH and the biomass of cyanobacteria at each site on the studied glaciers (r ¼
0.14, P > 0.05), but there was a significant negative correlation between pH and the biomass of green algae (r ¼
0.57, P < 0.05). This correlation is consistent with previous findings that the propagation of green algae is inhibited under alkaline conditions (e.g., Hoham and Mohn, 2004). The reason for the higher pH of Suntar-Khayata glaciers is still uncertain, but may be due to the effect of windblown ash from forest fires, which were ubiquitous in the surrounding areas, particularly in 2012. Mineral particles on the glacier surface might also affect the algal community or biomass since they can provide nutrients to the algae and allow filamentous cyanobacteria to form cryoconite granules (Takeuchi et al., 2001b). However, there was no correlation between the abundance of mineral particles and the total algal biomass on the glacier surface (r ¼ 0.09), a greater abundance of Osc. cyanobacteria and C. parietina was observed at sites B3 and D3, where there were greater amounts of mineral particles. The abundant mineral particles at the sites may support the growth of these cyanobacteria, since these two taxa are filamentous and can grow as they form cryoconite granules with mineral particles. 4.2. Inter-annual variations in snow algal communities from 2012 to 2014 The observation of the algal community over the three melting seasons from 2012 to 2014 suggested that the algal community structure did not change inter-annually on the studied glaciers. All of the algal taxa observed in 2012, two taxa of green algae and five of cyanobacteria, appeared on the glaciers every melting season. The community structure also did not change at most of the studied sites from year to year, i.e., the algal community on the bare ice surface was dominated by A. nordenskioldii and that on the snow surface was dominated by Chloromonas sp. A change in the dominant taxon was observed at only three sites. On Glacier No. 31, the dominant algae at the upper site, site A6, changed from Chloromonas sp. in 2012 to A. nordenskioldii in 2013. The location of the snow line changed between years due to meteorological conditions, such as the accumulation of winter snow and melting rate in the summer of each year; therefore, this change is probably due to the upward shift in the location of the snow line in 2013. The dominant taxon at the lowest site, site B1 on Glacier No. 29, was A. nordenskioldii in 2012, but was Chloromonas sp. in 2013 (Sup. 1b). This change may be due to the remaining snow patches at the site in 2013, which could delay the growth of A. nordenskioldii. At site D3 on Glacier No. 33, which was the only site dominated by Chr. cyanobacterium in 2012, A. nordenskioldii dominated in 2013. Although the reason for this change is uncertain, it may be due to the physical or chemical conditions at this site, which locally affect the algal community. In contrast with community structure, the total algal biomass at each site significantly differed over the three melting seasons, although the altitudinal pattern of the total algal biomass reached a maximum at the middle part of the glaciers in every year. For Glacier No. 31, the biomass was largest in 2012, intermediate in 2014, and smallest in 2013 (Fig. 7). Although the data were available for only the two seasons of 2012 and 2013 on the other three glaciers, the biomass changed similarly over the two seasons. These variations in total algal biomass are likely due to the meteorological conditions in each year. Algal biomass can increase if the duration of the melting period is longer since algae can keep growing on melting snow or ice as long as other conditions, such as nutrients and solar radiation, are not limiting for their growth. In fact, a

9

Fig. 7. Change in mean algal biomass of sites A2 and A4 on Glacier No. 31 from 2012 to 2014. Error bar ¼ standard deviation.

continuous biomass increase during the melting season has been reported for an Alaskan glacier (Takeuchi, 2013). Thus, the algal biomass on glaciers is likely to be greater in warmer years. Fig. 8 shows the NCEP/NCAR reanalysis data of air temperature and precipitation in this region from May to August for the three years. The methods and set-up employed for the reanalysis project are described in Kalnay et al. (1996). We selected the nearest gridpoint to Glacier No. 31, 62 N and 140 E, and used the daily average temperature and precipitation. The data show that these conditions in 2012 were distinctive from the other two years. The mean air temperature in this period was higher in 2012 (7.7, 7.0, and 6.5  C for 2012, 2013, and 2014, respectively). The sum total of the daily mean temperature above 0  C (positive degree day sum) from May to August of each year was also highest in 2012 and relatively low in 2013 and 2014 (989.4, 888.0, and 875.0 degree days for 2012, 2013, and 2014, respectively). The total July precipitation in 2012 was approximately half of those in 2013 and 2014 (36.4, 88.2, and 93.4 mm for 2012, 2013, and 2014, respectively), which can cause more solar radiation on the surface. The warmer temperature and lower precipitation likely caused the significantly greater growth of algae in 2012. 4.3. Comparison with glaciers in other Arctic and Asian regions According to previous research, the algal biomass on glaciers is generally greatest in Asia (Yoshimura et al., 1997; Segawa and Takeuchi, 2010), intermediate in polar and central Siberia (Takeuchi, 2001; Takeuchi et al., 2006), and smallest in Patagonia (Takeuchi and Kohshima, 2003; Fig. 9a). The mean algal biomass on Glacier No. 31 (A1eA5) in this study was different between 2012 and 2013 (1.9 mL m
2 and 0.17 mL m
2, respectively). As compared with those glaciers, the biomass in 2012 was greater than those at glaciers in Alaska, central Siberia, and the Himalayas, and comparable to that of a glacier in the Qilian Mountains in China (1.9 mL m
2 for Qiyi Glacier). On the other hand, the biomass in 2013 was close to that of a Patagonian glacier (0.074 mL m
2 for Tyndall Glacier), and generally smaller than all other glaciers investigated in previous studies (e.g., Takeuchi, 2001). This suggests that the inter-annual variation of the snow algal biomass on the Siberian glacier is comparable to the geographical variations of algal biomass on glaciers; however, since the biomass data on these glaciers were based on a single year observation, inter-annual variation on each glacier should be carefully studied to compare the biomass among the different glaciers. The algal community structure of the Suntar-Khayata region was

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Fig. 8. Daily mean temperature and precipitation in the Suntar-Khayata Mountain Range from 2012 to 2014; (A) in 2012; (B) in 2013; (C) in 2014, and (D) the positive degree day sum of each year. Data are from the NCEP/NCAR Reanalysis of daily mean temperature and precipitation rate from 2012 to 2014.

similar to those of other Arctic regions. It was dominated by Chloromonas sp. in the upper snow area and by A. nordenskioldii in the lower bare ice area of the glaciers. Although the species of Chloromonas sp. has not been exactly identified from the glaciers or regions, algae of genus Chloromonas or Chlamydomonas were dominant in snow areas of glaciers widely from Central Asia to the Arctic region. In particular, a visible red snow surface caused by the bloom of red-pigmented Chloromonas or Chlamydomonas sp. commonly occurred on glaciers in Alaska, Greenland, Svalbard, and Altai, and on other Arctic glaciers (e.g., Takeuchi et al., 2006). The red snow was visible on glaciers in this study, indicating that it is a typical phenomenon over the Arctic region, including Siberia. The

dominance of A. nordenskioldii in the bare ice area is not common in the low latitude glaciers. Fig. 9b shows the comparison of community structure on the bare ice area of glaciers in various regions. A. nordenskioldii accounted for 87% of the total biomass in SuntarKhayata, 53% in Alaska, and 57% in the Russian Altai, but less than 10% in the Himalayas and Qilian Mountains in Asia. The abundance of cryoconite on the glaciers in Suntar-Khayata region is comparable to those of other Arctic or sub-Arctic glaciers, but is significantly smaller than those of Asian glaciers. For example, the abundance ranged from 0.84 to 97.8 g m
2 (mean: 23 g m
2) for Gulkana Glacier in Alaska (Takeuchi, 2001), from 0.59 to 118 g m
2 (mean: 20.1 g m
2) for Greenland (Takeuchi et al., 2014) and from 0.32 to 550 g m
2 (mean: 124 g m
2) for Akkem Glacier in the Russian Altai (Takeuchi et al., 2006), and is comparable to those on the studied glaciers (from 12.3 to 114.4 g m
2; mean: 47.1 g m
2). In contrast, the abundance ranged from 30.4 to 873 g m
2 (mean: 292 g m
2) for Qiyi Glacier in the Qilian Mountains in China (Takeuchi et al., 2005), and ranged from 50 to 900 g m
2 (mean: 300 g m
2) in Yala Glacier in the Nepali Himalayas (Takeuchi et al., 2000), values significantly greater than those in this study. The biomass of filamentous cyanobacteria is a possible factor determining the abundance of cryoconites on the glacier surface since they play a role in forming cryoconite granules. For example, the biomass of filamentous cyanobacteria on Glacier No. 31 (2012) was 0.089 mL m
2, which is smaller than that of Asian glaciers (1.9 mL m
2 for Qiyi Glacier; Segawa and Takeuchi, 2010). Furthermore, the dominant cyanobacterial taxon on Glacier No. 31 seems not to form cryoconite granules efficiently. Most of the filamentous cyanobacteria on the glaciers in Suntar-Khayata were C. parietina (69% in biomass), which has a larger cell size with a thick sheath (thick filament: 6.4 mm) and appears not to be effective at entangling particles, while those in Asian glaciers were Oscillatoriaceae cyanobacterium, which has a smaller cell size and thinner filament (approximately: 1.5e2.0 mm) and is likely to effectively form cryoconite granules. A smaller supply of air-blown mineral particles compared with those on Asian glaciers in arid regions may also cause the smaller abundance of cryoconite on the Suntar-Khayata glaciers. The results suggest that the effect of cryoconite on surface albedo may be rather small, although the surface albedo on Asian glaciers is substantially reduced by the cryoconite. On Suntar-Khayata glaciers, pigmented algal cells may have a greater effect on the surface albedo, as reported for other Arctic glaciers (e.g., Yallop et al., 2012). In terms of algal community structure, the glaciers in SuntarKhayata can be classified as the Arctic type; there are many common characteristics with those on other Arctic and sub-Arctic glaciers, although this region is geographically isolated from other glacierized regions in the Arctic. This suggests that the algae composing the community can disperse over the circum-Arctic areas, although further phylogenic analysis of algae on each glacier is necessary. As many studies have predicted, significant climate warming is expected in the Arctic region in this century, and is likely to have an impact on Arctic glaciers physically and chemically. Glaciers in the Suntar-Khayata region are no exception, as there have already been reports of mass loss from the glaciers (Ananicheva et al., 2005). Therefore, it is important to evaluate future changes to glacier ecosystems and the interactions between glaciers and supraglacial microbes on the glaciers. Further studies on algae on these glaciers may provide insight into the geographical distribution of each algal species and dispersal processes over the Arctic region. 5. Conclusions The snow and ice algal communities on glaciers in the Suntar-

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Fig. 9. Comparison of total biomass (A) and community structure (B) of the algal community in bare ice areas of glaciers in the world. Solid and open marks indicate data from different sites and the mean of the data from each glacier, respectively. Sources of the data are Takeuchi et al. (2006) for Akkem, Takeuchi (2001) for Gulkana, Segawa and Takeuchi (2010) for Qiyi, Yoshimura et al. (1997) for Yala, and Takeuchi and Kohshima (2004) for Tyndall.

Khayata region of eastern Siberia were revealed to consist of two green algae and five cyanobacteria. A green alga, Chloromonas sp., was dominant in the upper snow area, while another green alga, A. nordenskioldii, was dominant in the lower bare ice area. Cyanobacteria comprised less than 10% of the algal biomass across most of the surface of the glaciers. The total algal biomass reached a maximum at the middle part of the glaciers, and was smaller in the lower ice area and the upper snow area. Observations over the three melting seasons from 2012 to 2014 revealed that the total algal biomass at each study site differed from year to year, although the algal community structure did not generally change. The differences in algal biomass among the years are probably due to the meteorological conditions of each year, but this should be carefully studied. Although this region is geographically isolated from other glacierized regions in the Arctic, there are many similar characteristics with algal communities reported from other Arctic and sub-Arctic glaciers rather than those from Asian glaciers; thus, the algal community of the Suntar-Khayata region can be classified as ‘Arctic type’. Further studies are necessary to evaluate the impact of expected climate warming in the Arctic region in the coming century on the microbial community on the glaciers. Although this study is mostly based on microscopic analysis, further phylogenic analyses using DNA molecular techniques on the algae would help to understand the geographical distribution and dispersal processes of snow and ice algae on Arctic and sub-arctic glaciers.

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Please cite this article in press as: Tanaka, S., et al., Snow algal communities on glaciers in the Suntar-Khayata Mountain Range in eastern Siberia, Russia, Polar Science (2016), http://dx.doi.org/10.1016/j.polar.2016.03.004