Biological soil crusts (BSCs) represent a community of various organisms associated with soil particles within and on top of the upper few millimeters of the soil. Algae, cyanobacteria, lichens, bacteria, microfungi, and bryophytes in different proportions form a thin layer on the soil surface, where filamentous algae, and cyanobacteria stick together with soil particles by their mucilaginous sheaths and excreted extracellular polymeric substances (EPS) (Belnap et al., 2001). These EPS consist of sticky polysaccharides and proteins, and are typically released by abundant BSC green algae, such as members of the genera Coccomyxa and Klebsormidium, which leads to adhesion to soil particles (Barberousse et al., 2006). Some of the EPS adhesives exhibit strong intrinsic mechanical properties (Mostaert et al., 2009), and their producers were frequently observed in BSCs of Antarctica (Pfaff et al., 2016).

The composition and development of BSCs can be very different and hence, various types are distinguished by macroscopic as well as microscopic characteristics (Belnap et al., 2001; Büdel et al., 2009; Williams et al., 2016). BSC types of Arctic Svalbard and Livingston Island, Antarctica were recently described based on visible features, such as the presence/absence of functional groups, their dominance and topography (Williams et al., 2016). The establishment and development of these cryptogamic communities is influenced by several biotic as well as abiotic parameters like pedological properties, climatic factors, and intervention by animals and humans (Elster et al., 1999; Büdel et al., 2009; Langhans et al., 2009; Pushkareva et al., 2016). BSCs are pioneer communities and have important ecological functions in soil stabilization against water and wind erosion (Van Den Ancker and Jungerius, 1985; Eldridge and Greene, 1994; Belnap and Gillette, 1998), change in hydrology as water retention (reviewed in Belnap, 2006; Breen and Lévesque, 2008), primary production and nitrogen fixation (Evans and Lange, 2001; Belnap, 2002; Bhatnagar et al., 2008; Zhang et al., 2009), biogeochemistry as well as geomorphology (Evans and Belnap, 1999) and in nutrient cycles (Wu et al., 2013; Baumann et al., 2017). Furthermore, BSCs have positive influence on the seed germination and plant growth because they enrich nutrients in the soil (Belnap et al., 2001; Evans and Lange, 2001; Harper and Belnap, 2001; Belnap, 2003; Breen and Lévesque, 2008; Ghiloufi et al., 2016).

BSCs are distributed worldwide in all climatic zones and occur mostly in extreme and nutrient-poor habitats, such as hot and cold, semiarid and arid areas, and can be the only vegetation in these landscapes (Belnap and Lange, 2003). Colesie et al. (2014) reported BSCs in continental Antarctica and Borchhardt et al. (2017) in maritime Antarctica. The latter authors also provided for the first time a comprehensive species list of microalgae and lichens of BSCs. Furthermore, a comparative geo-ecological study described various BSC types of Antarctic Livingston Island and Arctic Svalbard, but without any information on biodiversity (Williams et al., 2016). BSCs are generally poorly studied in the Polar Regions until now (Green and Broady, 2001), and a recent review by Pushkareva et al. (2016) summarized all information on Arctic BSCs and concluded that much more studies on the biodiversity of BSCs at high latitudes are needed because of ongoing climate change. In addition, a considerable high areal coverage of BSCs (up to 90%) on Svalbard was recently reported by Williams et al. (2016) which indicated that BSCs might be the prevailing vegetation type at such high latitudes. It is assumed that the BSC composition as well as their distribution will shift or BSCs will even be displaced by invasive species due to climate change in the Polar Regions (Frenot et al., 2005; Pushkareva et al., 2016). Consequently, deeper investigations on the biodiversity of Polar BSCs are urgently required and will enable better prediction of future vegetation development at high latitudes.

Therefore, in the present study two major scientific questions were addressed. Firstly, the microalgal diversity of Arctic BSCs was investigated. Secondly, local habitat differences were analyzed with a major focus on soil characteristics and precipitation, as these factors might have a strong effect on microalgal species composition in BSCs.

BSCs host a variety of different organisms (reviewed in Belnap et al., 2003; Weber et al., 2016). Compared to former literature, the data presented in this study point to a surprisingly high species richness of microalgae in BSCs of Arctic Svalbard (102 species). Studies on terrestrial microflora are rare in comparison to aquatic investigations (Elster et al., 1999) and also BSCs are generally poorly studied in the Polar Regions (Green and Broady, 2001). Previous studies reported different species numbers of microalgae in BSCs which ranged from only few to about 100 taxa depending on habitat. A study about the algal species composition of continental Antarctica reported only 10 chlorophytes in soil samples (Broady and Weinstein, 1998) although they were not associated with a BSC community. In contrast, 78 eukaryotic algal species in soil (Zidarova, 2008) and 106 species in BSCs (Borchhardt et al., 2017) of maritime Antarctica were reported. Kim et al. (2008) identified 23 eukaryotic algal species and (Kaštovská et al., 2005) 33 taxa in soil samples from Arctic Svalbard partly covered by vascular plants and mosses which point to a rather low diversity. In addition, Elster et al. (1999) found 84 eukaryotic soil algae in the Arctic desert of central Ellesmere Island, Canada which is similar to the data presented in this study. However, a comparison of both species lists revealed less matches, only 33 taxa (29 green algae, 4 xanthophytes) were determined in both study sites.

The proportion of xanthophyte species was 5 fold higher (20 species) in the present study compared to the reported number in BSCs from coastal dunes at the Baltic Sea (Schulz et al., 2016, 4 species). This conspicuous biogeographic pattern for xanthophytes was already indicated by Büdel et al. (2016), who assumed that the species richness of xanthophytes increases with cooler habitats. These authors mentioned members of Botrydiopsis, Tribonema, Xanthonema, and Heterococcus as most common species which all occurred in the Arctic BSCs of the present study. Lower species numbers of xanthophytes were determined in the Arctic desert of Canada (4 species, Elster et al., 1999) and Maritime Antarctica (7 species, Borchhardt et al., 2017).

Unfortunately, some aspects are impeding detailed comparison with previous studies. On one hand more investigations on the biodiversity of BSCs at high latitudes are needed and on the other hand sometimes only species numbers without taxonomic information were provided and thus verification was not possible. Furthermore, identification by morphology is often difficult and depends on experience, methods, equipment and taxonomic state of the organisms, or cryptic species. Therefore, we suggest to use an integrative approach including several methods such as direct microscopy and cultivation with different media and additionally genetic analyses. Metagenomic approaches for Arctic BSCs were not conducted yet, because of still unsolved problems with optimum primers and available sequences in database. On the other hand comprehensive data based on morphology exist in the literature which enabled a comparison with our results.

Fortunately, a direct comparison of species richness and biodiversity of Arctic as well as Antarctic BSCs could be performed because the identifications were done by the same authors using exactly the same methods. These analyses revealed approximately equal β-diversity based on very similar species numbers (Arctic: 102, Antarctic: 106) and therefore, we conclude that the species richness of BSCs in the Polar Regions are congruent. Moreover, MDS as well as ANOSIM analysis showed no significant grouping by Polar Regions which indicated that many BSC taxa (40 species) are bipolar distributed. Some of these bipolar taxa are also known as cosmopolitans, for example, member of Chlamydomonas, Coccomyxa, and Klebsormidium (Ettl and Gärtner, 2014).

Surprisingly, Klebsormidium sp. (Streptophyta) belonging to G clade (according to Rindi et al., 2011) was found at 5 sampling stations on Arctic Svalbard. In general, the genus Klebsormidium is distributed worldwide as a typical member of BSC communities, and exhibits a high level of morphological plasticity which is shown as differences in ultrastructure and cell wall texture (Mikhailyuk et al., 2014). Due to this peculiarity, the delimitation of species by morphology usually is very difficult and therefore, genetic analysis are necessary. In contrast, the G lineage is genetically relatively isolated from all other Klebsormidium species and additionally, also distinguished from the other lineages by a unique morphology. Therefore, it is possible to unambiguously identify members of G clade using light microscopy only. Most interesting, species belonging to G clade were so far mainly found in BSCs of hot dryland regions of South Africa (Rindi et al., 2011; Karsten et al., 2015; Mikhailyuk et al., 2015). All these authors characterized members of clade G as African group and Ryšánek et al. (2015) confirmed that an investigation of 200 Klebsormidium strains from Europe, Asia and North America revealed no single species belonging to clade G. South Africa, where the strains of clade G were isolated for the first time, constitutes a xerophytic habitat which is characterized by very low annual precipitation of 56 mm with only 0–14 monthly rainfall days and hence by the occurrence of desiccation-tolerant microalgae such as Klebsormidium clade G members (Karsten et al., 2015). Statistical analysis of the biogeography of several Klebsormidium species from different regions showed clear separation of the African from the remaining groups and hence very high dissimilarity (Mikhailyuk et al., 2015). For the first time in the present study 5 clade G Klebsormidium strains could be identified in samples mainly collected around Longyearbyen which has also low annual precipitation (205 mm), and hence can be characterized as dry Tundra climate ET according the climate classification by Köppen and Geiger (1930–1939). A study on the biodiversity of Klebsormidium taxa along elevational gradients of the Alps demonstrated that members of all known lineages (B, C, D, E, and F) could be morphologically and genetically verified except members of clade G (Mikhailyuk et al., 2015). Data of this investigation indicated that the key driver for the occurrence of Klebsormidium clade G is rather water availability than the temperature which coincides with our results.

Although the species composition of all sampled BSCs from Svalbard highly varied, our results showed no significant differences between the two investigated localities Ny-Alesund and Longyearbyen. Therefore the biodiversity data might be representative for a larger area of Arctic Svalbard.

No correlations between BSC species composition and analyzed chemical soil properties could be outlined, although Schulz et al. (2016) reported the TP content as the main driver for the BSC microalgal species composition collected at coastal dunes of the Baltic Sea. This might be explained by generally higher P contents and dominant optimal soil pH for high bioavailability of P (Table 4) in these Arctic soils, which suggest a sufficient P supply instead of P limited growth. A comparison with the soil TP concentrations measured by Schulz et al. (2016) showed noticeable lower values, with TP contents ranging between 90 and 310 mg kg⁻¹ soil with a median value of 110 mg kg⁻¹. In contrast, our analysis resulted in about 3 fold higher TP contents (median of 366 mg kg⁻¹) with a remarkable maximum value of 753 mg kg⁻¹. Mann et al. (1986) analyzed soils from different locations around Kongsfjorden which corresponded to the sampling stations “Geo” and “London” located near Ny-Ålesund. The TP contents of the soil directly underneath the BSCs in the present study revealed about 10-fold increased P amounts compared to the bulk topsoil data presented by Mann et al. (1986). Our TP concentrations are confirmed by results of Beraldi-Campesi et al. (2009), who also described increased P contents under BSCs of the Colorado Plateau highlands and the Sonoran Desert lowlands (USA) compared to the bulk soil without BSCs, as well as by increased P concentrations with BSC growth (Wu et al., 2013). Chemical data of soil underneath BSCs presented in this study revealed noticeable higher contents of organic matter, which might be promoted by decreased decomposition activity of soil organic matter in Arctic climate conditions, which is confirmed by observations in Arctic and Antarctic BSCs (Williams et al., 2016).

The determined pH values varied between 4.2 and 7.4 but significant correlation with BSC algal species composition was not confirmed statistically. However, Kaštovská et al. (2007) reported that the abundance of microalgae increased with lower pH, and data of statistical analysis presented in our study showed a p-value very close to significance threshold which might indeed reflect such a relationship between pH and species composition. It should be pointed out that our results were based on presence-absence data, and that pH might affect more the abundance of organisms than species richness.

Only precipitation could be identified as one key factor which controlled BSC species composition and it is known that the availability of water is an important environmental factor for the occurrence of soil algae (Hoffmann, 1989; Ohtani et al., 1991; reviewed in Broady, 1996; Adams et al., 2006). Borchhardt et al. (2017) also showed that soil moisture content of various Antarctic microhabitats affected the specific species composition in BSCs.

Another abiotic factor, which controls BSC composition, might be substrate and soil texture. Results by Kaštovská et al. (2005) and Schulz et al. (2016) indicated that the soil particle size influenced the abundance as well as diversity of BSC organisms.

The discrepancy of missing correlation between species compositions and environmental factors (except water availability) can be explained by the heterogeneity of the studied habitats. Both microclimatic (e.g., diurnal variations) and macroclimatic factors (e.g., precipitation and temperature) might affect species diversity. However, more studies are needed to evaluate which environmental factors control species composition and biodiversity in Arctic BSCs. These results in combination with the provided species lists would offer a basis for understanding the functions of BSCs which constitute the main vegetation of Arctic Svalbard.

UK conceived and designed the study. UK and NB collected the samples. NB cultivated as well as isolated all microalgae, took light micrographs, made hand drawings, created figures and tables, calculated biodiversity indices, did statistical analyses and wrote the first draft of the manuscript. NB and TM identified species. CB did all soil analyses and wrote part of the section Material and Methods. All authors edited and revised the manuscript and approved the publication.