Diversity and distribution of lichens in recently deglaciated areas of southeastern Spitsbergen

The diversity and distribution of lichen species were investigated in recently deglaciated areas of the borderland between Sørkapp Land and Torell Land (southeastern Spitsbergen, Svalbard). A total of 15 sites representing various habitat types specific to the area were evaluated. Sampling sites were characterized by a very diverse composition of lichens and species richness ranging from as few as two species to as many as 53. None of the species was ubiquitous among the investigated sampling sites; conversely, most were recorded only once or twice indicating a high heterogeneity in species distribution. Eighty species are reported for the first time from southeastern Spitsbergen. The terricolous lichen Verrucaria xyloxena is reported for the first time from the Svalbard archipelago. The influence of the selected abiotic and biotic environmental factors on the occurrences and distributions of lichen species is discussed in this paper.


Introduction
Spitsbergen is the largest island of the Svalbard archipelago in the Norwegian Arctic. The southeastern part of the island encompasses the mountainous areas of the borderland between Sørkapp Land and Torell Land (Fig. 1) that sharply descend to the coast of the Barents Sea. This part of Spitsbergen is characterized by a much colder climate with more sunshine and lower humidity compared to that in the western coast of the island [1]. Weather conditions, e.g., insolation, wind direction, and near-ground temperature are significantly affected by the local orography [2]. The harsh climate is primarily the result of strong and gusty winds from the east, the presence of the cold East Spitsbergen Current, and extensive inland glaciation [3]. Consequently, the area experiences a very short growing season and its soils are commonly poorly developed. The landscape is mostly barren and devoid of continuous vegetation, which is limited only to few small "oases" [4,5]. The limited vegetation and dominance of cryptogams, mainly lichens and mosses, is typical for the high Arctic polar deserts [3,6].

Field survey and sampling
The Fieldwork and sampling were carried out in July and August 2016 during a research expedition organized by the Institute of Geography and Spatial Management of Jagiellonian University as part of the project "Southeastern Spitsbergen landscape-seascape and biodiversity dynamics under current climate warming".
A total of 15 sites ( Digital signature This PDF has been certified using digital signature with a trusted timestamp to assure its origin and integrity. A verification trust dialog appears on the PDF document when it is opened in a compatible PDF reader. Certificate properties provide further details such as certification time and a signing reason in case any alterations made to the final content. If the certificate is missing or invalid it is recommended to verify the article on the journal website. The selected sites represented a broad range of arbitrarily determined habitats differing in physiognomic types of tundra, geomorphology, and microclimate. Their brief characteristics are provided in Tab. 1.

Species identification
Identification in the field was practiced only when taxonomically nonproblematic specimens were concerned. However, specimens of all the observed taxa were collected for detailed taxonomic evaluation in the laboratory. The collected specimens were identified using routine microscopic and laboratory techniques based on the following keys and taxonomic treatments: Thomson [19,20], Brodo et al. [21], Øvstedal et al. [6], Smith et al. [22], and Wirth [23]. In addition, chemical analyses of lichen substances were also   Gentle slope of the Geologtoppen massif, exposed to the west, covered by coarsegrained layer of debris, dry. Lack of soil. Very poor habitat.   Wide flattening of the Tvillingtoppen slope which passes up into the high (almost vertical) rock wall exposed to the east. On the surface, a thick cover of rock rubble of various fractions, from silt to large rocky blocks (Fig. 2E). Very dry, soil-forming processes are very slow. Individual bundles of mosses grow in the hollows and rock crevices. Epilithic lichens dominate. More luxuriant vegetation grows only in a few patches, near the rock walls with very small bird colonies.
High-located slope of the Tvillingtoppen massif, exposed to the west, covered by dusty and fine-grained debris weathering material. Dry and lack of soils. Very poor habitat, only with epilithic lichens.
conducted when necessary and according to the method summarized by Orange et al. [24]. Taxonomic classification and nomenclature follow the Index of Fungorum [25] and MycoBank [26]. The collected specimens were deposited in the herbarium of the W. Szafer Institute of Botany, Polish Academy of Sciences in Cracow (KRAM-L).

Habitat variability
To evaluate the degree of habitat environmental variability across sampling sites, the following ten factors were estimated using a 4-grade scale. The environmental characteristics were estimated based on the field observations, available topographic maps, and published data [3,4,14], and are summarized in Tab >500 m a.s.l.); ■ Substrate texture (Sub-1: sand and fine gravel; Sub-2: thick gravel and small rock blocks; Sub-3: massive rock blocks; Sub-4: substrate with highly variable texture); ■ Intensity of geomorphological processes (Geo-1: no visible changes; Geo-2: small intensity of changes mostly due to wind and frost movements; Geo-3: intensive changes due to destructive hydrological impacts and mass movements; Geo-4: very strong and notorious changes); Steep rock-waste talus cone at the foot of the Hedgehogfjellet massif, which passes up into the vertical rock wall exposed to the east. There are visible development of soils (Lithic Leptosols, Regosols) and succession of vascular plants (mainly Cerastium arcticum, Saxifraga cernua, Oxyria dygina) in the rock crevices and siltyloamy hollows. Weak ornithogenic fertilization.
Narrow mountain ridge covered with a layer of the weathered rock debris (a boulder-field), mainly with small and medium-size rocky blocks (Fig. 2F). Only epilithic vegetation (mainly lichens).

Species occurrences across habitat classes
Seriation of an absence-presence (0/1) matrix using the algorithm described by Brower and Kile [27] was used to analyze the occurrences of lichen species across particular habitat classes. A constrained optimization algorithm was applied and all recorded species were included in seriation. In addition, the number of species in all habitat classes was calculated to reveal differences in species richness between the classes and to determine the direction of changes in biodiversity.

Results
A total of 114 lichen species (γ diversity) were recorded in 14 of the 15 study sites. The site containing no lichen species (i.e., site No. 14, which is regularly modified by the Tab. 2 Environmental characteristics of the study sites.  Only two species of Stereocaulon were recorded there: Stereocaulon glareosum, found exclusively at this locality, and S. capitellatum, which was also noted at other localities. Their juvenile forms were found on a soil film on stable rock blocks. Differences in species compositions among the sites (β diversity) were also considerable (Tab. 3). Most species were recorded only once (46 species) or twice (35 species) and none of the species was found at all sampling sites. This indicates high heterogeneity in species distribution. Among the observed species were reputedly rare species, for example, Staurothele arctica, which has only been reported in Spitsbergen twice, including in this study, and Caloplaca tornoënsis, which has been sporadically recorded from Svalbard. Furthermore, the terricolous lichen Verrucaria xyloxena is reported here for the first time from the Svalbard archipelago. Only 10 species were relatively widely distributed in the study area (number of occurrences is shown in parentheses): Candelariella vitellina (7), Cladonia borealis (7), Lecanora polytropa (13), Lecidea atrobrunnea (7), Porpidia tuberculosa (9), Rhizocarpon geographicum (11), Tremolecia atrata (13), Umbilicaria cylindrica (12), U. hyperborea (10), and U. torrefacta (7). From the above species, Lecanora polytropa and Tremolecia atrata are considered to occur frequently across the entire study area, being absent only in extremely harsh habitats, such as areas notoriously flooded by the sea or areas recently freed from ice (see Fig. 3).
Analyses of the seriation graphs (Fig. 3) demonstrate that the aforementioned common species occurred across most of the sampling sites, suggesting they exhibit wide ecological tolerances. Similarly, some of the more uncommon lichens also demonstrate a tolerance of variation in some environmental factors. These species were observed in habitats spanning all the scale degrees of the specified habitat factor. Conversely, other species were associated with specific habitat parameters (see Fig. 3).
Most species (90% of listed lichens) were found in habitats 100-500 m from the coast (Dis-3) and at elevations ranging from 5-150 m a.s.l. (Alt-2). None of the lichens was observed at sites directly by the sea (Dis-1) (Fig. 3A). A minute intensity of geomorphological processes (Geo-2) was preferred by 92 lichen species. A stable rocky substrate and substrates of varied textures (Sub-2 and Sub-4) were preferred by almost 100% of the recorded lichens. The more common species and/or terricolous lichens (around 20% of all species) sporadically occurred in habitats whose substrates were classified into the two other substrate categories (Sub-1 and Sub-3). Humidity (Moi) and wind factor (Win) appear to be the least important parameters in determining lichen distribution (Fig. 3B). The amount of time since glacier retreat (Ice) turned out to be an important factor influencing the quantitative and qualitative diversity of lichens that determines the development of various communities (Fig. 3A). Only 10% of the recorded lichens were exclusively noted in sites classified into the Ice-1 and Ice-2 categories. Seventy lichen species were noted in areas classified into the Ice-3 category, including 18 species occurring exclusively in Ice-3 habitats. Similarly, 77 lichen species were noted in sites classified into the Ice-4 category, including 29 species occurring exclusively in these habitats. The biotic factors, including vegetation cover (Cov), ornithogenic fertilization intensity (Fer), and dominant vegetation type (Veg) mainly grouped the lichen species into two classes (Class 1 and Class 4). The lichen species found in habitats classified into either Class 2 or Class 3 of Cov, Fer, and Veg were observed sporadically (Fig. 3B). Fig. 4 shows variation in patterns of species richness across the considered environmental variables. The most pronounced changes in species richness appear to be related to variation in abiotic factors, including the time since deglaciation (Ice), distance from the shoreline (Dis), elevation (Alt), and intensity of geomorphological and hydrological processes (Geo). For instance, species richness clearly increased as time since glacier retreat also increased. Patterns related to the distance of habitats from the sea coast and habitat elevation indicate that mountain ridges and slopes up to the altitude of 150 m a.s.l. hosted considerably larger numbers of species than lower, coastal areas or steeper mountain slopes and peaks. Other factors were also important and often strongly affected species richness. Unstable sands and fine gravels were poorly colonized by lichens. Contrasting patterns were identified in the effects of biotic factors on lichen richness, as extreme values of ornithogenic fertilization, moisture, and the abundance of mosses and vascular plants seemingly promoted lichen species richness, while lower species richness were associated with habitats exhibiting less extreme values.

Discussion
Taking into account the number of lichen taxa known from the Svalbard archipelago (>740) [6] and the ca. 200 taxa reported from the western part of Sørkapp Land [15][16][17][18], a total species richness of 128 species (114 reported in the current study and 14 species previously reported by Krzewicka and Maciejowski [14] but not recorded here) can be considered as relatively low. However, it is worth noting that the relatively low lichen species richness in the study area is analogous to prior reports on the diversity of vascular plants, which reported richness of only 20-25 species [3] (also personal data). In contrast, 82 species are known from western Sørkapp Land [28,29]. These patterns of low diversity are likely related to differences in glaciation history between study areas, with the current study area being almost completely covered by glaciers during the Little Ice Age but having recently been the subject of considerable deglaciation [3,5]. Increases in the severity of climatic conditions are also likely an important factor limiting biological colonization and ecosystem development processes [1].
One of the goals of our study was to provide insights into the factors that are responsible for the local distribution and diversity of lichens. Therefore, the sampling design covered a broad range of habitats that are typical for the deglaciated areas of southeastern Spitsbergen. Significant differences in the environmental characteristics of the sampling sites are related primarily to their geological and climatological history [5,30]. From a lichenological point of view, the foot of Koval'skijfjella and areas in the vicinity of the Daudbjørnpynten headland are the most interesting since both sites are characterized by high lichen diversity (39 and 53 species, respectively). These sites are generally similar in terms of their environmental conditions, including distance from the sea, elevation, intensity of geomorphological processes, moisture content, and ornithogenic fertilization (see Tab. 2). Nevertheless, the sites differed considerably in their glaciation history. The Daudbjørnpynten headland was ice-free during the Little Ice Age while the site at the foot of Koval'skijfjella was covered by ice until the beginning of the twentieth century when the glacier began to retreat [3,8]. In spite of this, both sites are, at present, overgrown by a well-developed moss-lichen tundra with a large number of vascular plants. This is likely due to the high moisture regime and strong ornithogenic fertilization at these sites, both of which are crucial factors in the development of nutrient-rich soil [31,32].
The rich lichen biota of both sites, in addition to numerous epilithic taxa, also consists of epigeic and epibryophytic species, among which patches of Flavocetraria nivalis, Cetraria islandica, Sphaerophorus globosus, and Cladonia spp. were the most common. Whereas on rocks and boulders, Umbilicaria spp., foliose lichens common in some polar and alpine regions [33,34], grow abundantly forming the main visual component of the epilithic biota. High variation in the stages of lichen thalli development is symptomatic among encountered lichens. This variability is often associated with older deglaciation events and substratum stability, which appear to be decisive factors controlling lichen development in Svalbard [6,18,35].
Many species were found across the other sampling sites, and only a few, i.e., Cladonia mitis, C. pocillum, Flavocetraria nivalis, and Rhizoplaca melanophthalma, seemed to be restricted in their distribution. All of these species are either foliose or fruticose macrolichens and also occur frequently on the opposite side of the island on its west coast [6]. The species richness of Koval'skijfjella and areas in the vicinity of Daudbjørnpynten is comparable with that of some areas of the west coast, for example 43 species of lichens were noted on the Longyearbreen moraine and 60 on the Irenebreen moraine [18].
Considering the importance of glaciation history in determining lichen species distribution and richness, it is not surprising that the lowest species richness is associated with recently deglaciated habitats (i.e., Sykorabreen peripheries) or the recent presence of permanent snowfields (i.e., Tvillingtoppen summit). On the other hand, substratum instability due to intensive geomorphological and/or hydrological processes (i.e., at the Daudbjørnpynten headland and the foot of Geologtoppen) are responsible for the limitation of the development of lichen biotas.
It should be mentioned that a remarkable number of the recorded species appeared to be seemingly rare in the investigated area. Unfortunately, inaccessible but important habitats, such as vertical rock cliffs, can be accidentally omitted during field research. Thus, the actual species richness in the area can still be considerably underestimated.
Considering the current rapid climate change and related ecological implications, further targeted studies are needed to provide a complete assessment of tundra vegetation diversity and a baseline for the monitoring of environmental changes in the area.

Conclusions
■ One hundred fourteen species of lichen were identified in the study area and 80 of them are reported for the first time from southeastern Spitsbergen. ■ The terricolous species Verrucaria xyloxena has been recorded for the first time from Svalbard. ■ The species richness at sampling sites is highly variable. None of the lichens was recorded from every site while most of them were recorded only once or twice. This indicates a high heterogeneity in species distribution. ■ Comparisons between lichenological data from 2005 and 2016 provide evidence for the phenomenon of rapid succession in the lichen biotas of the studied area. ■ Local abiotic environmental factors have the greatest impact on the occurrence of some patterns of lichens. The most important are: geomorphological processes (including cryogenic, frost, slope, wind, and marine-coastal processes), proprieties of bedrock (mainly granulation and degree of soil formation, usually conditioned by intensity of ornithogenic fertilization), as well as the amount of time since deglaciation.