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Rhizosphere microbiome assembly is essential for plant health, but the temporal dimension of this process remains unexplored. We used a chronosequence of 150 years of the retreating Hallstätter glacier (Dachstein, Austria) to disentangle this exemplarily for the rhizosphere of three pioneer alpine plants. Time of deglaciation was an important factor shaping the rhizosphere microbiome. Microbiome functions, i.e. nutrient uptake and stress protection, were carried out by ubiquitous and cosmopolitan bacteria. The rhizosphere succession along the chronosequence was characterized by decreasing microbial richness but increasing specificity of the plant-associated bacterial community. Environmental selection is a critical factor in shaping the ecosystem, particularly in terms of plant-driven recruitment from the available edaphic pool. A higher rhizosphere microbial richness during early succession compared to late succession can be explained by the occurrence of cold-acclimated bacteria recruited from the surrounding soils. These taxa might be sensitive to changing habitat conditions that occurred at the later stages. A stronger influence of the plant host on the rhizosphere microbiome assembly was observed with increased time since deglaciation. Overall, this study indicated that well-adapted, ubiquitous microbes potentially support pioneer plants to colonize new ecosystems, while plant-specific microbes may be associated with the long-term establishment of their hosts.
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Microbiota , Rizosfera , Camada de Gelo/microbiologia , Áustria , Microbiologia do Solo , Bactérias/genética , Solo , PlantasRESUMO
Complex links between biotic and abiotic constituents are fundamental for the functioning of ecosystems. Although non-monotonic interactions and associations are known to increase the stability, diversity, and productivity of ecosystems, they are frequently ignored by community-level standard statistical approaches. Using the copula-based dependence measure qad, capable of quantifying the directed and asymmetric dependence between variables for all forms of (functional) relationships, we determined the proportion of non-monotonic associations between different constituents of an ecosystem (plants, bacteria, fungi, and environmental parameters). Here, we show that up to 59% of all statistically significant associations are non-monotonic. Further, we show that pairwise associations between plants, bacteria, fungi, and environmental parameters are specifically characterized by their strength and degree of monotonicity, for example, microbe-microbe associations are on average stronger than and differ in degree of non-monotonicity from plant-microbe associations. Considering directed and non-monotonic associations, we extended the concept of ecosystem coupling providing more complete insights into the internal order of ecosystems. Our results emphasize the importance of ecological non-monotonicity in characterizing and understanding ecosystem patterns and processes. Supplementary Information: The online version contains supplementary material available at 10.1007/s10021-023-00867-9.
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Substrate geochemistry is an important factor influencing early microbial development after glacial retreat on nutrient-poor geological substrates in the High Arctic. It is often difficult to separate substrate influence from climate because study locations are distant. Our study in the retreating Nordenskiöldbreen (Svalbard) is one of the few to investigate biogeochemical and microbial succession in two adjacent forefields, which share the same climatic conditions but differ in their underlying geology. The northern silicate forefield evolved in a classical chronosequence, where most geochemical and microbial parameters increased gradually with time. In contrast, the southern carbonate forefield exhibited high levels of nutrients and microbial biomass at the youngest sites, followed by a significant decline and then a gradual increase, which caused a rearrangement in the species and functional composition of the bacterial and fungal communities. This shuffling in the early stages of succession suggests that high nutrient availability in the bedrock could have accelerated early soil succession after deglaciation and thereby promoted more rapid stabilization of the soil and production of higher quality organic matter. Most chemical parameters and bacterial taxa converged with time, while fungi showed no clear pattern.
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Camada de Gelo , Solo , Solo/química , Svalbard , Camada de Gelo/microbiologia , Microbiologia do Solo , Bactérias/genética , MineraisRESUMO
Glacier retreat caused by global warming may result in the variation of soil organic carbon and nutrient cycling. Yet, the dynamic change of soil microbial functional profiles, especially C metabolism-related, with soil development following glacier retreat are still unclear. In the present study, we investigated the soil microbial communities, metagenomic functioning, and metabolomic profiles along the Hailuogou Glacier forefield representing a 120-year chronosequence. The alpha diversity indices of soil bacteria, protozoa and nifH genes showed an upward trend with increased soil ages, and the beta diversity of soil archaea, bacteria, fungi, protozoa, nifH and nirS genes were significantly correlated with soil ages, in which increasing soil C and P while decreased C/N and pH significantly contributed to the differences of soil microbial communities among the analyzed environmental variables. The metagenomic functional genes related to the metabolisms of Glycogen and Cellulosome, Iron Acquisition and Metabolism were significantly decreased with chronosequence, while the utilization of Xylose and Lactate, Potassium Metabolism, Sulfur Metabolism showing an upward trend with soil ages, in which soil C/N ratios and pH were the most influential factors. In addition, soil C and C/N ratios were also significantly correlated to metabolomic compositions, in which the complexity of the metabolite structure increased with soil ages. Our results indicate that glacier retreat may lead to the asynchronous C and N accumulation along the chronosequence, thereby affecting the metagenomic and metabolomic functioning of soil microbial communities related to C metabolisms during soil development following glacier retreat.
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Camada de Gelo , Solo , Solo/química , Camada de Gelo/microbiologia , Carbono/metabolismo , Microbiologia do Solo , Bactérias/genética , Bactérias/metabolismoRESUMO
Soils in glacier forefields have a significant capacity for atmospheric CH4 uptake, but this pattern could be changed by high soil water content (SWC). The Hailuogou Glacier in SW China is a typical temperate monsoon glacier on siliceous bedrock, where a forefield soil chronosequence has developed with progressive glacier recession. To understand CH4 dynamics and their potential regulatory factors, we measured the concentrations and stable carbon (C) isotope compositions of CH4 and CO2, soil physicochemical properties, and perfromed a high-throughput sequencing. Among nine sampling sites, soil CH4 concentrations of six sites were below atmospheric levels and δ13C-CH4 values were similar to atmospheric levels. The average value was approximately -48.6 and without obvious fractionation. The soil CH4 concentrations exceeded atmospheric levels for the remaining three sites, and the δ13C-CH4 values were more enriched with increasing soil CH4 concentration. We calculated the soil-atmosphere CH4 flux (Jatm) using the concentration gradient method based on the soil CH4 concentration, sampling depth, and soil porosity. Jatm ranges from -0.08 to -0.52 mg m-2 d-1, acting as an atmospheric CH4 sink. It also shows that the correlation with soil exposure age or vegetation succession was insignificant. But the CH4 emission shows a larger variation changing from 0.05 to 1.8 mg m-2 d-1, which could result from local CH4 production differences catalyzed by aceticlastic methanogens. The results showed that not all sites acted as a net CH4 sink. SWC may have an important influence on CH4 dynamics in the Hailuogou Glacier forefield (HGF).
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Camada de Gelo , Metano , Atmosfera , China , SoloRESUMO
Community assembly is a result of dispersal, abiotic and biotic characteristics of the habitat as well as stochasticity. A direct comparison between the assembly of microbial and 'macrobial' organisms is hampered by the sampling of these communities in different studies, at different sites or on different scales. In a glacier forefield in the Austrian Alps, we recorded the soil and plant microbiome (bacteria and fungi) and plants that occurred in the same landscape and in close proximity in the same plots. We tested five predictions deduced from assembly processes and revealed deviating patterns of assembly in these community types. In short, microbes appeared to be less dispersal limited than plants and soil microbes, and plants strongly responded to abiotic factors whereas the leaf microbiome was plant species specific and well buffered from environmental conditions. The observed differences in community assembly processes may be attributed to the organisms' dispersal abilities, the exposure of the habitats to airborne propagules and habitat characteristics. The finding that assembly is conditional to the characteristics of the organisms, the habitat and the spatial scale under consideration is thus central for our understanding about the establishment and the maintenance of biodiversity.
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Microbiota , Solo , Biodiversidade , Camada de Gelo , Plantas , Microbiologia do SoloRESUMO
Polar glacier forefields offer an unprecedented framework for studying community assembly processes in regions that are geographically and climatically isolated. Through amplicon sequence variant (ASV) inference, we compared the composition and structure of soil bacterial communities from glacier forefields in Iceland and Antarctica to assess overlap between communities and the impact of established cryptogamic covers on the uniqueness of their taxa. These pioneer microbial communities were found to share only 8% of ASVs and each taxonomic group's contribution to the shared ASV data subset was heterogeneous and independent of their relative abundance. Although the presence of ASVs specific to one glacier forefield and/or different cryptogam cover values confirms the existence of habitat specialist bacteria, our data show that the influence of cryptogams on the edaphic bacterial community structure also varied also depending on the taxonomic group. Hence, the establishment of distinct cryptogamic covers is probably not the only factor driving the uniqueness of bacterial communities at both poles. The structure of bacterial communities colonising deglaciated areas seems also conditioned by lineage-specific limitations in their dispersal capacity and/or their establishment and persistence in these isolated and hostile regions.
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Bactérias/genética , Biodiversidade , Camada de Gelo/microbiologia , Microbiologia do Solo , Regiões Antárticas , Regiões Árticas , Bactérias/classificação , RNA Ribossômico 16S/genéticaRESUMO
In this study, the early ecological succession patterns of Forni Glacier (Ortles-Cevedale group, Italian Alps) forefield along an 18-year long chronosequence (with a temporal resolution of 1 year) has been reported. Bacterial and fungal community structures were inferred by high-throughput sequencing of 16S rRNA gene and ITS, respectively. In addition, the occurrence of both herbaceous and arboreous plants was also recorded at each plot. A significant decrease of alpha-diversity in more recently deglaciated areas was observed for both bacteria and plants. Time since deglaciation and pH affected the structure of both fungal and bacterial communities. Pioneer plants could be a major source of colonization for both bacterial and fungal communities. Consistently, some of the most abundant bacterial taxa and some of those significantly varying with pH along the chronosequence (Polaromonas, Granulicella, Thiobacillus, Acidiferrobacter) are known to be actively involved in rock-weathering processes due to their chemolithotrophic metabolism, thus suggesting that the early phase of the chronosequence could be mainly shaped by the biologically controlled bioavailability of metals and inorganic compounds. Fungal communities were dominated by ascomycetous filamentous fungi and basidiomycetous yeasts. Their role as cold-adapted organic matter decomposers, due to their heterotrophic metabolism, was suggested.
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Microbiologia do Solo , Solo , Bactérias/genética , Fungos/genética , Camada de Gelo , Itália , Plantas , RNA Ribossômico 16S/genéticaRESUMO
Glaciers are constantly retreating because of global warming. In this study, three soil samples along the forefield of Urumqi Glacier No. 1 were collected. The effects of warming on the microbial community in the glacier forefield were investigated through a 150-day laboratory experiment. In this experiment, two temperature treatments were performed at 5âand 15â. The results showed that with increasing deglaciation age, the concentrations of carbon and nitrogen increased and the abundance and alpha diversity of microbial communities increased in the original samples. The 150-day laboratory experiment indicated that warming insignificantly changed the copy number of archaea and bacteria. Furthermore, it changed the microbial community composition, and the changes varied in different sampling sites. Based on the analysis of abundant OTUs changing significantly with warming, the sampling sites with shorter deglaciation age had stronger response with warming, representing an increase in the abundance of genus Thiobacillus. Furthermore, these results revealed that warming caused different effects on microbes along glacier forefield and thus, it could provide important characteristics of the microbial community with warming in alpine glacier regions.
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Camada de Gelo , Microbiota , Bactérias , Solo , Microbiologia do SoloRESUMO
Mountain glaciers are retreating at an unprecedented rate due to global warming. Glacier retreat is widely believed to be driven by the physiochemical characteristics of glacier surfaces; however, the current knowledge of such biological drivers remains limited. An estimated 130 Tg of organic carbon (OC) is stored in mountain glaciers globally. As a result of global warming, the accelerated microbial decomposition of OC may further accelerate the melting process of mountain glaciers by heat production with the release of greenhouse gases, such as carbon dioxide (CO2 ) and methane. Here, using short-term aerobic incubation data from the forefield of Urumqi Glacier No. 1, we assessed the potential climate feedback mediated by soil microbiomes at temperatures of 5°C (control), 6.2°C (RCP 2.6), 11°C (RCP 8.5), and 15°C (extreme temperature). We observed enhanced CO2 -C release and heat production under warming conditions, which led to an increase in near-surface (2 m) atmospheric temperatures, ranging from 0.9°C to 3.4°C. Warming significantly changed the structures of the RNA-derived (active) and DNA-derived (total) soil microbiomes, and active microbes were more sensitive to increased temperatures than total microbes. Considering the positive effects of temperature and deglaciation age on the CO2 -C release rate, the alterations in the active microbial community structure had a negative impact on the increased CO2 -C release rate. Our results revealed that glacial melting could potentially be significantly accelerated by heat production from increased microbial decomposition of OC. This risk might be true for other high-altitude glaciers under emerging warming, thus improving the predictions of the effects of potential feedback on global warming.
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Gases de Efeito Estufa , Microbiota , Aquecimento Global , Camada de Gelo , SoloRESUMO
Cyanobacteria are important colonizers of recently deglaciated proglacial soil but an in-depth investigation of cyanobacterial succession following glacier retreat has not yet been carried out. Here, we report on the successional trajectories of cyanobacterial communities in biological soil crusts (BSCs) along a 100-year deglaciation gradient in three glacier forefields in central Svalbard, High Arctic. Distance from the glacier terminus was used as a proxy for soil age (years since deglaciation), and cyanobacterial abundance and community composition were evaluated by epifluorescence microscopy and pyrosequencing of partial 16S rRNA gene sequences, respectively. Succession was characterized by a decrease in phylotype richness and a marked shift in community structure, resulting in a clear separation between early (10-20 years since deglaciation), mid (30-50 years), and late (80-100 years) communities. Changes in cyanobacterial community structure were mainly connected with soil age and associated shifts in soil chemical composition (mainly moisture, SOC, SMN, K, and Na concentrations). Phylotypes associated with early communities were related either to potentially novel lineages (< 97.5% similar to sequences currently available in GenBank) or lineages predominantly restricted to polar and alpine biotopes, suggesting that the initial colonization of proglacial soil is accomplished by cyanobacteria transported from nearby glacial environments. Late communities, on the other hand, included more widely distributed genotypes, which appear to establish only after the microenvironment has been modified by the pioneering taxa.
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Cianobactérias/classificação , Camada de Gelo/microbiologia , Filogenia , Microbiologia do Solo , Regiões Árticas , Biodiversidade , Cianobactérias/genética , DNA Bacteriano , Genótipo , Sequenciamento de Nucleotídeos em Larga Escala , RNA Ribossômico 16S/genética , Solo/química , SvalbardRESUMO
Past research demonstrating the importance plant-microbe interactions as drivers of ecosystem succession has focused on how plants condition soil microbial communities, impacting subsequent plant performance and plant community assembly. These studies, however, largely treat microbial communities as a black box. In this study, we sought to examine how emblematic shifts from early successional Alnus viridus ssp. sinuata (Sitka alder) to late successional Picea sitchensis (Sitka spruce) in primary succession may be reflected in specific belowground changes in bacterial community structure and nitrogen cycling related to the interaction of these two plants. We examined early successional alder-conditioned soils in a glacial forefield to delineate how alders alter the soil microbial community with increasing dominance. Further, we assessed the impact of late-successional spruce plants on these early successional alder-conditioned microbiomes and related nitrogen cycling through a leachate addition microcosm experiment. We show how increasingly abundant alder select for particular bacterial taxa. Additionally, we found that spruce leachate significantly alters the composition of these microbial communities in large part by driving declines in taxa that are enriched by alder, including bacterial symbionts. We found these effects to be spruce specific, beyond a general leachate effect. Our work also demonstrates a unique influence of spruce on ammonium availability. Such insights bolster theory relating the importance of plant-microbe interactions with late-successional plants and interspecific plant interactions more generally.
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Global change contributes to the retreat of glaciers at unprecedented rates. The deglaciation facilitates biogeochemical processes on glacial deposits with initiating soil formation as an important driver of evolving ecosystems. The underlying mechanisms of soil formation and the association of soil organic matter (SOM) with mineral particles remain unclear, although further insights are critical to understand carbon sequestration in soils. We investigated the microspatial arrangement of SOM coatings at intact soil microaggregate structures during various stages of ecosystem development from 15 to >700 years after deglaciation in the proglacial environment of the Damma glacier (Switzerland). The functionally important clay-sized fraction (<2 µm) was separated into two density fractions with different amounts of organo-mineral associations: light (1.6-2.2 g/cm3 ) and heavy (>2.2 g/cm3 ). To quantify how SOM extends across the surface of mineral particles (coverage) and whether SOM coatings are distributed in fragmented or connected patterns (connectivity), we developed an image analysis protocol based on nanoscale secondary ion mass spectrometry (NanoSIMS). We classified SOM and mineral areas depending on the 16 O- , 12 C- , and 12 C14 N- distributions. With increasing time after glacial retreat, the microspatial coverage and connectivity of SOM increased rapidly. The rapid soil formation led to a succession of patchy distributed to more connected SOM coatings on soil microaggregates. The maximum coverage of 55% at >700 years suggests direct evidence for SOM sequestration being decoupled from the mineral surface, as it was not completely masked by SOM and retained its functionality as an ion exchange site. The chemical composition of SOM coatings showed a rapid change toward a higher CN:C ratio already at 75 years after glacial retreat, which was associated with microbial succession patterns reflecting high N assimilation. Our results demonstrate that rapid SOM sequestration drives the microspatial succession of SOM coatings in soils, a process that can stabilize SOM for the long term.
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Carbono/química , Camada de Gelo , Solo/química , Ecossistema , Minerais/química , Suíça , Fatores de TempoRESUMO
Glacier forefield soils can provide a substantial sink for atmospheric CH4, facilitated by aerobic methane-oxidizing bacteria (MOB). However, MOB activity, abundance, and community structure may be affected by soil age, MOB location in different forefield landforms, and temporal fluctuations in soil physical parameters. We assessed the spatial and temporal variability of atmospheric-CH4 oxidation in an Alpine glacier forefield during the snow-free season of 2013. We quantified CH4 flux in soils of increasing age and in different landforms (sandhill, terrace, and floodplain forms) by using soil gas profile and static flux chamber methods. To determine MOB abundance and community structure, we employed pmoA gene-based quantitative PCR and targeted amplicon sequencing. Uptake of CH4 increased in magnitude and decreased in variability with increasing soil age. Sandhill soils exhibited CH4 uptake rates ranging from -3.7 to -0.03 mg CH4 m-2 day-1 Floodplain and terrace soils exhibited lower uptake rates and even intermittent CH4 emissions. Linear mixed-effects models indicated that soil age and landform were the dominating factors shaping CH4 flux, followed by cumulative rainfall (weighted sum ≤4 days prior to sampling). Of 31 MOB operational taxonomic units retrieved, â¼30% were potentially novel, and â¼50% were affiliated with upland soil clusters gamma and alpha. The MOB community structures in floodplain and terrace soils were nearly identical but differed significantly from the highly variable sandhill soil communities. We concluded that soil age and landform modulate the soil CH4 sink strength in glacier forefields and that recent rainfall affects its short-term variability. This should be taken into account when including this environment in future CH4 inventories.IMPORTANCE Oxidation of methane (CH4) in well-drained, "upland" soils is an important mechanism for the removal of this potent greenhouse gas from the atmosphere. It is largely mediated by aerobic, methane-oxidizing bacteria (MOB). Whereas there is abundant information on atmospheric-CH4 oxidation in mature upland soils, little is known about this important function in young, developing soils, such as those found in glacier forefields, where new sediments are continuously exposed to the atmosphere as a result of glacial retreat. In this field-based study, we investigated the spatial and temporal variability of atmospheric-CH4 oxidation and associated MOB communities in Alpine glacier forefield soils, aiming at better understanding the factors that shape the sink for atmospheric CH4 in this young soil ecosystem. This study contributes to the knowledge on the dynamics of atmospheric-CH4 oxidation in developing upland soils and represents a further step toward the inclusion of Alpine glacier forefield soils in global CH4 inventories.
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Microbial communities in the glacier forefield of Styggedalsbreen, Norway, were investigated along a chronosequence from newly exposed soil to vegetated soils using next-generation sequencing of the 16S rRNA gene. In order to monitor the short-term effect of temperature on community successions along the soil gradient, the soil samples were incubated at three different temperatures (5°C, 10°C and 22°C). The microbial community composition along the chronosequence differed according to distance from the glacial terminus and incubation temperature. Samples close to the glacier terminus were dominated by Proteobacteria at 5°C and 10°C, while at 22°C members of Chloroflexi, Acidobacteria and Verrucomicrobia in addition to Proteobacteria accounted for most of the diversity, indicating that sites close to the glacier terminus are more closely related to former subglacial environments. Within the Archaea domain, members of the phylum Euryarchaeota dominated in samples closer to the glacier terminus with a shift to members of the phyla Thaumarchaeota-Crenarchaeota with increased soil age. Our data indicate that composition and diversity of the microbial communities along the glacier forefield depend not only on exposure time but are also to a large degree influenced by soil surface temperature and soil maturation.
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DNA Arqueal/genética , DNA Bacteriano/genética , Aquecimento Global , Camada de Gelo/microbiologia , Microbiota/genética , Acidobacteria/genética , Acidobacteria/isolamento & purificação , Regiões Árticas , Sequência de Bases , Chloroflexi/genética , Chloroflexi/isolamento & purificação , Crenarchaeota/classificação , Crenarchaeota/genética , Crenarchaeota/isolamento & purificação , Meio Ambiente , Sequenciamento de Nucleotídeos em Larga Escala , Líquens/classificação , Noruega , Proteobactérias/classificação , Proteobactérias/genética , Proteobactérias/isolamento & purificação , RNA Ribossômico 16S/genética , Análise de Sequência de DNA , Solo/química , Microbiologia do Solo , Temperatura , Verrucomicrobia/genética , Verrucomicrobia/isolamento & purificaçãoRESUMO
Three sampling sites were established at increasing distance from the Morteratsch glacier to investigate lichen communities on soil in the glacier forefield. The survey yielded 13 lichen species and one lichenicolous fungus. Peltigera extenuata (Nyl. ex Vain.) Lojka (Peltigerales) is new to the canton of Graubünden.
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The investigation of lichens on soil, plant debris and terricolous mosses in the glacier forefield of the Pasterze yielded 35 lichen species. Placidiopsis oreades Breuss (Verrucariales) is new to Austria. Three sampling sites were established at increasing distance from the glacier, in order to compare species diversity, abundance and composition within the forefield and with four other glacier forefields of the Eastern Alps.
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The investigation of lichens on soil, plant debris and terricolous mosses in the glacier forefield of the Rötkees yielded 31 lichen taxa (29 species and 2 varieties) and one lichenicolous fungus. Micarea incrassata Hedl. (Lecanorales) is new to Italy. Three sampling sites were established at increasing distance from the glacier, in order to compare species diversity, abundance and composition.
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The investigation of lichens on soil, plant debris and terricolous mosses in the glacier forefield of the Gaisbergferner yielded 41 lichen taxa (39 species and 2 varieties) and one lichenicolous fungus. Three sampling sites were established at increasing distance from the glacier, in order to compare species diversity, abundance and composition.