Advertisement

  • Loading metrics

Open Access

Review

Effects of reduced snowpack due to climate warming on abiotic and biotic soil properties in alpine and boreal forest systems

  • Anastasiia Kosolapova,

    Roles Conceptualization, Investigation, Writing – original draft, Writing – review & editing

    Affiliation MACE Laboratory, Environmental Engineering Institute (IIE), Alpine and Polar Environmental Research Centre (ALPOLE), School of Architecture, Civil and Environmental Engineering (ENAC), École Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland

    ⨯
  • Ianina Altshuler

    Roles Conceptualization, Investigation, Writing – review & editing

    ianina.altshuler@epfl.ch

    Affiliation MACE Laboratory, Environmental Engineering Institute (IIE), Alpine and Polar Environmental Research Centre (ALPOLE), School of Architecture, Civil and Environmental Engineering (ENAC), École Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland

    ⨯

Abstract

Reduction in snow cover, depth, onset, and duration of seasonal snow in mid-latitude regions due to climate warming has multiple global and local scale ecosystem impacts. These effects include modulations of the hydrological cycles and increases in land surface solar radiation absorption due to decreased albedo. Changes in snow cover characteristics also affect underlying soils. Snow has an insulating effect on soils by decoupling air and soil temperatures, thus seasonal snow cover reduction leads to overall lower soil temperatures and an increase in freeze-thaw cycles. This is especially prominent during the fall and spring thaw seasons when the snow cover is not as extensive. This in turn has downstream impacts on soil physical, chemical, and biological properties. Among these impacts are soil moisture reduction, temperature, frost regimes, soil pH shifts, and alteration in nutrient flux dynamics during winter, snowmelt period and the following summer growing season. These changes in soil physicochemical properties due to snowpack reduction can then impact the biological soil properties via increased plant root mortality, reduced abundance and diversity of soil arthropods, and shifts in composition, abundance and activity of soil microbial communities. All these soil biotic factors can in turn alter the dynamics of soil nutrient fluxes and future greenhouse gas emissions. Here, we integrate data on the effects of snow cover reduction on abiotic and biotic soil properties, with focus on temperate alpine and forest ecosystems and with an outlook on future impacts.

Citation: Kosolapova A, Altshuler I (2024) Effects of reduced snowpack due to climate warming on abiotic and biotic soil properties in alpine and boreal forest systems. PLOS Clim 3(5): e0000417. https://doi.org/10.1371/journal.pclm.0000417

Editor: Masayuki Yokozawa, Waseda University: Waseda Daigaku, JAPAN

Published: May 7, 2024

Copyright: © 2024 Kosolapova, Altshuler. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: The author(s) received no specific funding for this work.

Competing interests: The authors have declared that no competing interests exist.

1. Introduction

In temperate and mountain ecosystems, seasonal snow covers the ground from several weeks to months during the cold season [1]. In the Northern Hemisphere, up to one-third of the land area is covered with snow for at least three months per year [2–4]. Seasonal snowpack is highly sensitive to climate change, with warming being a major factor affecting seasonal snow cover [1]. Snow cover extent has decreased by 13% per decade for the last fifty years and continues to decrease across the Northern Hemisphere [5,6], while the duration of the snow cover period is also declining, mainly due to the earlier onset of snowmelt [7,8]. Moreover, since 1950`s the overall mean and maximum snow depths have reduced across Europe, including mountainous regions, with the acceleration of the trend after the 1980`s (with notable exception at the higher latitudes) [9–11]. Warmer winter temperatures and the increase in precipitation, both due to climate change, have opposing effects on seasonal snow cover [9]. However, increase in winter precipitation appears to have a significant impact on snow cover in high-altitude areas, whereas in mid- and low-altitude regions, temperature has the principal impact on snow cover [12].

Seasonal snow cover has multiple effects on these ecosystems contributing to energy balance by cooling the Earth’s surface and reducing ground heat losses [13]. Firstly, as snow has a high surface albedo, it reflects 60–90% of solar radiation (lower values for wet spring snow) [14–16], resulting in lowering of the surface temperature [17,18]. Secondly, snow has a low thermal conductivity [19] which allows the snowpack to act as an insulator, decoupling underlying soils from freezing air temperatures and reducing heat loss from the ground [15]. The stable snow cover decreases the fluctuations in soil temperatures and minimizes the number of soil freeze-thaw events [20]. This, in turn, influences the activity and viability of soil-inhabiting organisms throughout the cold season and has downstream impacts during the growing season [21,22]. Another major effect of the seasonal snowpack on ecosystems is its role in hydrological cycles as it acts as a seasonal water reservoir. In the Northern Hemisphere, snowmelt water is dominate source of runoff [23], recharging freshwater and groundwaters resources [24,25]. On local the scale, meltwater is a source of moisture and nutrients for the underlying soil [2], thus the timing of snowmelt affects the growing season productivity and activity of the soil microbiome [26,27].

Here we review the effect of climate change on the seasonal snow cover with focus on temperate and mountain ecosystems, while still utilizing knowledge from higher latitude habitats. In addition, we focus on the impacts of reduced seasonal snow cover on the underlying soils in the context of their physical and biogeochemical properties as well as soil-associated biomes.

2. Effects of snow cover reduction on physical properties of soils

Seasonal snow cover has a significant influence on underlying soil physical characteristics, mainly soil temperatures [15,28]. The key property of the snow affecting soil temperature is snow’s low thermal conductivity [19]. Low thermal conductivity makes snow an excellent insulator decoupling the atmosphere and ground surface, which in turn lowers the impact of air temperature on the soil thermal regime. The magnitude of the snow insulation effect varies with the extent of snow cover, depth, density and structure, timing, and duration of the seasonal snow cover [15]. Snow depth is one of the major factors affecting the soil thermal regime during the cold season. The insulating effect of snow is greater in thicker snowpack [15,29], with complete decoupling of ground and atmosphere occurring at around 30–40 cm of snow [30]. In addition, late season dense/melting snow has greater thermal conductivity compared to fresh early winter snow [15,29]. Timing of snow cover deposition is important, as areas where snow cover is established before ground freezing, the snow insulating effect allows soil temperature to be maintained above 0°C, i.e., the soil remains unfrozen throughout the winter [31].

With climate warming, snow cover undergoes reduction in spatial distribution, reduction in depth, delayed deposition, and earlier snowmelt [32–34]. Snow cover reduction leads to greater exposure of soil to cold air temperatures which may result in “colder soils in a warmer world” and increase soil freezing [22,35] (Fig 1). This leads to reduced liquid water availability in winter soils [36] and reduced solute infiltration rates during the snowmelt period [2,37]. The thinner snowpack or its complete absence also may lead to a greater amplitude of soil temperature fluctuations throughout the cold season and an increased number of freeze-thaw events [38,39], due to the lack of the decoupling from air temperatures. For example, to simulate a reduction in snow cover depth due to climate warming, Broadbent et al. (2021) conducted snow removal experiments in the European Alps, demonstrating an increased number of freeze-thaw events in plots with shallower snow depth [40]. Similar results were obtained in snow removal experiments conducted in the alpine forest ecosystem of the Tibetan Plateau [41,42].

thumbnail
Download:
Fig 1. Snow cover reduction and its effect on soil biome.

https://doi.org/10.1371/journal.pclm.0000417.g001

3. Snow manipulation experiments

To assess the effects of snow cover reduction on underlying soils several overarching strategies are possible, including i) sampling of naturally heterogeneous snow accumulation sites [43], ii) long-term monitoring [44], iii) snow manipulation experiments which are the most utilized approach in ecological and biogeochemical studies assessing the impacts of climate change [45]. Snow manipulation experiments can include snow addition, partial or full snow removal, and snow compaction [45]. Snow removal plots are created by either manual periodical snow removal or physical cover of the experimental plot which prevents snow accumulation [41,46]. Another manipulation approach is the installation of a snow fence, that alters snow accumulation creating a snow depth gradient with zones of deep, moderate, and shallow snowpack [47,48].

Several reviews and meta-analyses were published in the last 15 years summarizing the results of snow manipulation experiments, including a review by Wipf and Rixen (2010), focused on snow manipulation experiments in Arctic and alpine tundra ecosystems from a plant phenology perspective [49], and a meta-analysis by Zhao et al. (2022), summarizing results of 99 snow manipulation experiments with the focus on physicochemical characteristics and biotic properties of soil [45]. However, direct synthesis of data obtained through snow manipulation experiments results is complicated as there is heterogeneity in experimental designs (snow manipulation strategy and sampling timing), as well as heterogeneity in the type of analyzed soil properties.

Alpine habitats are highly sensitive to warming and subsequent greening with spatial, temperature, and snow cover heterogeneity resulting from steep altitudinal gradients [50,51]. To draw conclusions of the effects of snow cover changes with climatic warming in these sensitive habitats, we summarize the results of snow manipulation experiments in subalpine and alpine ecosystems with focus on soil biogeochemical properties and effects on the soil microbiome (Table 1).

thumbnail
Download:
Table 1. Snow removal experiments conducted in subalpine and alpine ecosystems.

https://doi.org/10.1371/journal.pclm.0000417.t001

In most of the studies performed in subalpine and alpine environments, snow removal consistently resulted in decreased soil temperatures during the winter, increased frost formation in topsoil, and an increase in the number of freeze-thaw cycles (Table 1). However, some of the studies have not detected any significant influence of snow removal on these characteristics. For example, Bombonato and Gerdol (2012) conducted a study in the European Alp peatland, where they removed snow only once in late winter/early spring, which resulted earlier snowmelt but had no effect on soil temperature or frost formation [52]. Contrariwise, Gavazov et al. (2017) conducted a similar snow removal experiment at the same elevation in the European Alp grassland, again snow was removed only once in the late winter, however, this led to increased frost formation in soil [36]. This difference can potentially be explained by higher spring air temperatures or ecosystem type in the experiment performed by Bombonato and Gerdol [52].

Overall, across the studies, snow removal experiments performed in subalpine and alpine environments have not demonstrated any clear and unified effect on the geochemical properties of soils (Table 1). This mostly originates from the limited number of available works and a diversity of measured chemical parameters. In the meta-analysis performed by Zhao et al. [45], snow removal had a significant effect only on ammonification and nitrification rates in winter soils, though only a few works have analyzed these parameters [46]. In the growing season, Zhao et al. revealed a significant increase in C, DOC, NH4+ and DON, though these results face the same problem, as the measurements of these parameters were available only for a very limited number (2–3 experiments) of studies [45]. However, alpine centric studies (Table 1) overall do not align with these conclusions. For example, Bombonato and Gerdol (2012) demonstrated no effect on DOC [52], and Freppaz et al. (2012) exhibited that in zones with reduced snow cover (via snow fence manipulation) there was a decrease in TN (37.37%), NH4+(49.19%), TOC (33.38%) in alpine grassland of the Rocky Mountains [48]. From a biological perspective, snow removal often resulted in a reduction of microbial biomass and enzymatic activity, as well as a shift towards higher abundance of fungal taxa in winter soil microbial communities (Table 1) (see section 4). For example, both Freppaz et al. (2012) and Gavazov et al. (2017) demonstrated loss of microbial biomass in snow reduction experiments [36,48].

In order to estimate overall effect of snow cover reduction on different soil geochemical and biological properties in alpine ecosystems, we quantitatively synthesised available data from studies focusing on snow removal experiments in alpine (high-altitude) ecosystems (Supplementary Table 1). Overall, we extracted data from six studies performed in Tibetan plateau [41,42,55–58] and two studies performed in the European Alps [40,53]. The majority of studies performed in Tibetan plateau were performed in alpine forest ecosystem [41,42,56–58] whereas all studies from the European alps were performed in high alpine grasslands [40,53]. To estimate the magnitude of the observed effects we calculated log response ratio (lnRR) [59], the most-used effect size metric for assessment of ecological studies results [60]. To estimate the weighted effect sizes across the studies we ran mixed intercept-only models, with lnRR as response variable and the paper ID as a random-effect factor to reduce collinearities between data extracted from the same study. The weighted effect sizes were reported as percent of changes [45] (Fig 2).

thumbnail
Download:
Fig 2. Effect of snow cover reduction on biochemical properties of alpine soils in snow removal experiments.

Effects shown as percent of change with 95% confidence intervals. N obs.–number of observations, Ref.–data source references, MBN–microbial nitrogen, * - 95% confidence interval of [0.93%, 4.05%].

https://doi.org/10.1371/journal.pclm.0000417.g002

Overall, we calculated weighted effect sizes for parameters that were measured in at least three studies (Fig 2). In winter alpine soils, we revealed a significant decrease in water content (8.04%, p<0.001) and mean soil temperature (0.6°C decrease, p <0.001) in snow removal experimental plots. During snowmelt period we demonstrated increase in microbial nitrogen content (51.52%, p = 0.022) and decrease in phosphatase activity (19.64%, P = 0.014) as well as presence of fungal PFLA (15.35%, p<0.001). Among bacteria, only Firmicutes demonstrated significant change in relative abundance at phylum level (2.48% increase in growing period, p = 0.0016). What is more, no significant effect on bacterial alpha-diversity was detected.

To estimate ecosystem-specific effects we focused on alpine forests in winter and during the snowmelt period due to limited number of measurements available for alpine grasslands and inconsistency in measured parameters between studies (S1 Table). We revealed significant decrease in soil water content in winter (9.47%, p<0.001) whereas during snowmelt period increase was demonstrated in DON (68.96%, p = 0.007) and nitrate content (36.7%, p<0.001). At the same time, no significant effects were demonstrated for ammonium content and urease activity neither in winter nor during snowmelt period in alpine forest soils (Fig 3).

thumbnail
Download:
Fig 3. Effect of snow cover reduction on biochemical properties of soils in alpine forests in snow removal experiments.

Effects shown as percent of change with 95% confidence intervals. N obs.–number of observations, Ref.–data source references, DON–dissolves organic nitrogen, * - 95% confidence interval of [-66.65%, 6184,74%].

https://doi.org/10.1371/journal.pclm.0000417.g003

4. Microbial activity and nutrient cycling

Seasonal snowpack affects soil biogeochemical state through changes in soil physical properties and input of water and nutrients during the snowmelt events [45]. However, it is difficult to develop a unified model of snow cover reduction effects on soil biogeochemical processes, as there are limited number of studies spanning different ecosystem types with inconsistent variables measured (nutrient levels, vegetation, and microbial community composition).

In general, insulation of soil via seasonal snowpack leads to an increased stabilization of soil temperatures facilitating microbial activity and respiration in winter soils [2,61]. Microbial biomass can even reach its annual peak values under the snowpack during winter [2,61]. More severe freezing of soils and an increased number of freeze-thaw events (under decreased snowpack) has a negative effect on microbial biomass and leads to the release of DOC and DON [62,63]. For example, microbial biomass carbon decreased in response to an increase of freeze-thaw cycles, which was also linked to reduced abundance of fungi in the community [64]. A similar decrease of microbial C (and decrease in microbial C:N) was demonstrated by Freppaz et al. (2008) for subalpine soils under reduced snow cover [46]. A more complicated dynamic in microbial biomass was revealed by Tan et al. (2014) in snow removal experiments, performed in the Tibetan Plateau alpine forest. The study demonstrated an initial decrease in microbial (C and N) biomass (16.92% and 52.91% decrease respectively) followed by an increase in microbial biomass later in the winter (32.88% increase in MBN) and during snowmelt period (66.21% increase MBC and 102.99% increase in MBN) in snow removed plots [57]; these results were corroborated by a separate Tibetan alpine forest study [41]. This late-winter increase in biomass may be explained by the increased activity of survived microorganisms which are stimulated by the input of nutrients from lysed cells [65,66]. As microbial biomass can act as a nitrogen sink in alpine catchments, loss of biomass from increased mortality due to increased freeze thaw cycles, could lead to higher nitrogen deposition to streams and downstream lakes during snowmelt period [67,68].

The activity of microorganisms in winter soils can be traced by measuring soil respiration levels [69]. Winter soil respiration under the snowpack was demonstrated in various ecosystems, including boreal and alpine forests [70,71], arctic and alpine tundra [72,73], and agricultural fields [74]. In alpine forests, respiration rates remain high during the winter and may contribute to the loss of up 50% of C assimilated by photosynthesis in the preceding growing season [71,75]. Therefore, with snowpack reduction, microbial activity and respiration may be expected to decrease. This pattern was demonstrated for alpine forest ecosystems in a snow manipulation experiment performed in the Tibetan Plateau [76] and long-term observations in the Rocky Mountains [77]. This results in a decrease of CO2 emission during winter, leading to enhancement of carbon sequestration in forest ecosystems [71,78]. However, this is not always consistent, as no effect on winter soil CO2 efflux rates was detected in snow removal experiments performed in subalpine grassland [36] and boreal forest [79].

Another proxy for microbial activity and cycling of carbon (C) and nitrogen (N) in soils under snowpack is evidence of extracellular enzymatic activity [80]. The activity of urease and invertase in soils are often used to infer microbial C and N cycling dynamics in biogeochemical studies [80]. Urease catalyzes the hydrolysis of urea (an organic N substrate) into NH4+, thus urease activity can be used as an index of N mineralization rate in soils [80,81], while carbon cycling can be accessed via invertase activity–an enzyme, that catalyzes the hydrolysis of sucrose to monosaccharides [82]. Tan et al (2014) demonstrated that reduction in snow cover resulted in decreased soil activity of both urease (56.94% decrease) and invertase (32.24% decrease) [57]. Similarly, Sorensen et al. (2016) demonstrated reduced overall enzymatic activity in mixed-hardwood forest soils as a result of an increase in soil frost formation [83]. A similar decrease in soil enzymatic activity during winter as a result of snow removal was reported in the alpine forest in the Tibetan Plateau and subalpine grassland in the European Alps [41,53,57,76]. During snowmelt period, we estimated 19.64% (p = 0.014) decrease in phosphatase activity in alpine soils in response snow cover removal (See 3. Snow manipulation experiments). The decrease in enzymatic activity may be associated with a reduction in net nitrification and N mineralization as was demonstrated in snow removal experiments in forest and subalpine grassland ecosystems [36,63,84]. However, Li et al. (2017) demonstrated an increase in N mineralization rate and N availability in snow removal plots in subalpine forest [41], while snow cover reduction and an increase in the number of freeze-thaw cycles led to increased ammonification rates in forests [41,58,85].

5. Microbial community structure

In ecosystems exhibiting strong seasonality, soil microbial community composition undergoes seasonal turnover [86]. For example, strong seasonal dynamics in soil microbial community structure was demonstrated for an alpine grassland and arctic tundra where high biomass winter communities were fungi-dominated, while lower biomass summer communities where bacteria-dominated [86–88]. The transition to summer communities can be abrupt during the snowmelt, as this period is marked by changes in soil temperature and shifts in liquid water availability and nutrients, as these environmental conditions favor the rapid propagation of bacteria [55,89]. With snow cover reduction, this transition is expected to happen earlier in the season, which can potentially disrupt seasonal nutrient exchange between soil microbiome and plants [90]. The snowmelt period is also associated with the exposure of soils to increased free-thaw cycles leading to microbial cells lysis, this provides an additional pulse of nutrients in the snowmelt period and potential shifts in microbial community composition [65,66].

In boreal forests, soil microbial community is dominated by frost-resistant taxa, such as Acidobacteria, insensitive to intensified freeze-thaw cycles [91,92]. In these communities, the winter-to-spring transition may have a reduced effect on bacterial and fungal composition [92]. However, this is not universal, as Gavazov et al. (2017) demonstrated that in European subalpine grasslands both winter and summer communities were dominated by bacteria, with a higher proportion of Gram-positive bacteria in winter compared to summer [36], incidentally, this study demonstrated no effect of snow removal on microbial community composition [36]. Isobe et al. (2022) demonstrated a declined richness of soil microbial community, but an increased abundance of Acidobacteria, Proteobacteria, Verrumicrobia, Planctomycetes and Actinobacteria in response to snow removal in cool-temperate forests (Japan), though this effect was diminished in growing season [93]. In contrast, in alpine ecosystems we reveled the increase in relative abundance of Firmicutes in growing period soils in response to snow removal (See 3. Snow manipulation experiment). In the Tibetan alpine forest, snow removal led to an increase in alpha-diversity during the late winter period. However, this had no legacy effect on the same soil community during the growing season [56]. Similarly, in a temperate North American forest, while there were initial differences in winter soil community composition between snow removal and control plots, revealed with PLFA fingerprinting, these differences were diminished by spring [94]. In general, the influence of snow cover reduction on soil microbial community composition has been rarely addressed and was assessed mostly with low taxonomic resolution techniques such as PLFA analysis [36,94], however as PLFA analysis is quantitative it can be used as a proxy of biomass of each microbial group [95]. The combination of 16S/18S/ITS rRNA amplicon sequencing with PLFA analysis can provide deeper understanding of microbial community structure allowing both higher taxonomic resolution along with quantification of biomass [40]. The application of metatransriptomics or metaproteomics can be used to assess physiological state and functional activity of the soil microbiome and its response to changes in snow cover regime.

6. Snowpack microbiome

Snow serves as an interface between the ground and the atmosphere, accumulating dust, microorganisms and other biological particles on its surface. Microorganisms are deposited on the snow surface via aerial transport of aerosol particles and precipitation [96]. The microorganisms can originate both from local sources [97] and from transport over long distances [98–101], depending on seasonal and meteorological conditions [102]. The origin of microorganisms in the atmosphere varies greatly with geography and may include different aquatic, terrestrial, animal, and plant surface sources [102].

Snow microbiome could act as a source of microbial species for colonization of underlying soils following the snowmelt [103,104], but more so because rapid seasonal shift during snow melt could constitute as an ecosystem disturbance which can favor colonization by new species [103,104]. This colonization potential of snow microorganisms was assessed by Mallard et al. (2022, 2023) in Arctic soils, where taxa originally unique to the snow medium were able to persist and establish in the soils following snowmelt [105,106]. Finally, since the snow microbiomes undergo post-deposition selection, favoring psychrotrophic stress-resistant microorganisms [107], future snow cover reduction/duration may result in reduced colonization of frost resistant microorganisms into the soils. This can then have a compounding negative effect on the biomass due to higher frost-induced mortality in soil microbes over time (speculative).

7. Plant root mortality

With the reduction of winter snow cover, plants are more exposed to freeze-thaw events that can lead to plant root damage and mortality followed by compensatory root regrowth in spring [108]. Fine root mortality leads to the release of organic matter that results in higher rates of soil N mineralization and inorganic N soil losses [109,110]. Such an effect was demonstrated in northern forests, where an increased number of freeze-thaw events led to root damage, increased soil ammonium in the early growing season, and reduction in root nitrogen uptake capacity [111]. Snow cover reduction also results in alternate snowmelt timing and reduced runoff volume [112], which has a downstream impact on plant phenology and plant growth rates during the snowmelt period [49,113,114]. For example, Bokhorst er al. (2008), demonstrated that mid-winter snow loss resulted in delayed bud development and reduced flower production of Vaccinium myrtillus L. [115]. Compounding this, reduced snow cover leads to drier soils in spring and summer resulting in potential water limitation in plants during the late growing season [26,43,116].

8. Soil fauna

The effect of snow cover reduction on soil-inhabiting fauna is not as widely studied as its influence on plants and microorganisms [117]. For terrestrial arthropods, winter snow-insulating properties are vital as a large proportion of arthropods hibernate in soil overlayed by snow [118]. Therefore, increased soil frost formation as well as the number of freeze-thaw events may lead to temperature-related arthropod injury and mortality [119,120]. For example, in snow-removal in the northern North American hardwood forest reduced arthropod richness and diversity during the growing season due to increased frost [121]. The microarthropod species richness as well as the population of enchytraeids (earthworms) was reduced in response to snow removal in pine forests, Finland [122]. Furthermore, this decline in soil-inhabiting fauna also has a direct impact on the biogeochemical soil cycles as meso- and microfauna contribute to via litter decomposition [123], and as the act as both decomposers of organic matter and grazers of bacteria and fungi [124].

9. Synthesis and future perspectives

With climate change, seasonal snow cover experiences a general negative trend in its depth, duration, and extent, which has a downstream effect on ecosystems (Fig 1) [2] (though climate change has uneven influence and may lead to a local increase in snowpack [12]). Though, snowpack reduction diminishes the insulating properties of snow, leading to a decrease in soil temperature, increased frost formation and freeze-thaw events. However, these effects can be diminished by the continual increase in air temperatures, which may lead to a decrease in the extent of seasonally frozen soil and higher soil temperatures [9,125]. The prevailing effect will rely on the degree of climate change and vary between ecosystems depending on multiple factors including their geographical location and local microclimate.

Changes in the physical properties of soil affect soil-inhabiting organisms including bacteria, fungi, plants, and animals. These effects may comprise of a decrease in microbial biomass and activity, microbiome composition changes, and increase in the mortality of plant roots and soil fauna [45,122,126]. This, in turn, is reflected in changes in soil geochemical cycles in winter and during the growing season [45]. However, these negative effects were not consistent across experimental studies, which may be partially explained by the adaptation of the soil inhabitants [91,92,118]. As soil biogeochemical interactions are complex and vary between ecosystems, it is hard to reveal a general pattern of soil response to snow cover reduction [36,92,93]. This is further complicated by the overall limited number of studies and the inconsistency of methodologies [46,52,55]. In this review, we synthesized data available for high-altitude ecosystems: alpine grasslands and alpine forests. In snow cover removal experiments, snow cover reduction had several general effects on alpine soils including decrease in water content and soil mean temperatures in winter that align with global meta-analysis performed by Zhao et al. (2022) [45]. At the same time, we identified increase in microbial nitrogen during snowmelt period and decrease in phosphatase activity. In addition, in alpine forests the snow cover removal affected nitrogen in soil during snowmelt period as the increase in nitrate and dissolved organic nitrogen was observed. These increase in DON and nitrate content in alpine forests soils during snowmelt may promote microbial activity in soils but also lead to loss of nutrients in early spring.

Snowpack reduction also has an indirect effect on soil microbiomes via reduced colonization potential of frost-resistant taxa from snow to soils, however, there are no studies assessing this potential effect. In general, in-depth winter soil community characterization has been performed in a limited number of studies, with only a few assessing the impact of snowpack reduction on soil microbiome composition and functioning [125]. The potential shifts in microbiome function may be addressed in future with the utilization of modern approaches (metatranscriptomics and metaproteomics). These studies would allow to acquire a complex view on the processes underlying alterations in geochemical cycles and, in broad, adaptation of soil microbiome to changing environments. Moreover, winter and the following growing season communities are rarely examined alongside in the same experiment. Often studies focus on the effect of snow cover removal over short periods which do not span across the winter, spring melt, and growing seasons. A systematic and multi-year monitoring of soil microbial communities under varied snow cover regimes could capture shifts and bigger trends in soil microbiome dynamics in response to climate change and subsequent snow cover reduction.

Supporting information

S1 Table. Data extracted from snow removal studies performed in high-altitude ecosystems.

List of used abbreviations: Exp–data for snow removal plots, contr–corresponding control plots, SD–standard deviation; IN–inorganic nitrogen, TN–total nitrogen, DOC–dissolved organic carbon, DON–dissolved organic nitrogen, MBC–microbial carbon, MBN–microbial nitrogen, MBC_MBN–MBC:MBN ratio. Bacterial abundances are present as relative abundances.

https://doi.org/10.1371/journal.pclm.0000417.s001

(CSV)

References

  1. 1. Vaughan DG, Comiso JC, Allison I, Carrasco J, Kaser G, Kwok R, et al. Observations: cryosphere. Clim Change. 2013;2103:317–82.
  2. 2. Edwards AC, Scalenghe R, Freppaz M. Changes in the seasonal snow cover of alpine regions and its effect on soil processes: A review. Quat Int. 2007 Mar 1;162–163:172–81.
  3. 3. Mudryk LR, Kushner PJ, Derksen C. Interpreting observed northern hemisphere snow trends with large ensembles of climate simulations. Clim Dyn. 2014 Jul 1;43(1):345–59.
  4. 4. Kunkel KE, Robinson DA, Champion S, Yin X, Estilow T, Frankson RM. Trends and Extremes in Northern Hemisphere Snow Characteristics. Curr Clim Change Rep. 2016 Jun 1;2(2):65–73.
  5. 5. Pulliainen J, Luojus K, Derksen C, Mudryk L, Lemmetyinen J, Salminen M, et al. Patterns and trends of Northern Hemisphere snow mass from 1980 to 2018. Nature. 2020 May;581(7808):294–8. pmid:32433620
  6. 6. Pörtner HO, Roberts DC, Masson-Delmotte V, Zhai P, Tignor M, Poloczanska E, et al. The ocean and cryosphere in a changing climate. IPCC Spec Rep Ocean Cryosphere Chang Clim. 2019;1155.
  7. 7. Allchin MI, Déry SJ. A spatio-temporal analysis of trends in Northern Hemisphere snow-dominated area and duration, 1971–2014. Ann Glaciol. 2017 Jul;58(75pt1):21–35.
  8. 8. Allchin MI, Déry SJ. The Climatological Context of Trends in the Onset of Northern Hemisphere Seasonal Snow Cover, 1972–2017. J Geophys Res Atmospheres. 2020;125(17):e2019JD032367.
  9. 9. Fontrodona Bach A, Van der Schrier G, Melsen L, Klein Tank A, Teuling A. Widespread and accelerated decrease of observed mean and extreme snow depth over Europe. Geophys Res Lett. 2018;45(22):12–312.
  10. 10. Fontrodona-Bach A, Schaefli B, Woods R, Teuling AJ, Larsen JR. NH-SWE: Northern Hemisphere Snow Water Equivalent dataset based on in situ snow depth time series. Earth Syst Sci Data. 2023 Jun 23;15(6):2577–99.
  11. 11. López-Moreno JI, Fassnacht SR, Heath JT, Musselman KN, Revuelto J, Latron J, et al. Small scale spatial variability of snow density and depth over complex alpine terrain: Implications for estimating snow water equivalent. Adv Water Resour. 2013 May;55:40–52.
  12. 12. Wang H, Zhang X, Xiao P, Zhang K, Wu S. Elevation-dependent response of snow phenology to climate change from a remote sensing perspective: A case survey in the central Tianshan mountains from 2000 to 2019. Int J Climatol. 2022;42(3):1706–22.
  13. 13. Thackeray CW, Derksen C, Fletcher CG, Hall A. Snow and Climate: Feedbacks, Drivers, and Indices of Change. Curr Clim Change Rep. 2019 Dec 1;5(4):322–33.
  14. 14. Wendler G, Kelley J. On the Albedo of Snow in Antarctica: A Contribution to I.A.G.O. J Glaciol. 1988 Jan;34(116):19–25.
  15. 15. Zhang T. Influence of the seasonal snow cover on the ground thermal regime: An overview. Rev Geophys. 2005;43(4).
  16. 16. Barry RG, Gan TY, editors. Snowfall and snow cover. In: The Global Cryosphere: Past, Present, and Future [Internet]. 2nd ed. Cambridge: Cambridge University Press; 2022 [cited 2023 Sep 6]. p. 15–86. Available from: https://www.cambridge.org/core/books/global-cryosphere/snowfall-and-snow-cover/8A95F9D0CFA9D3BDDCCE1A52C06E7C6C.
    • 17. Frei A, Tedesco M, Lee S, Foster J, Hall DK, Kelly R, et al. A review of global satellite-derived snow products. Adv Space Res. 2012 Oct 15;50(8):1007–29.
    • 18. Barry RG. The Role of Snow and Ice in the Global Climate System: A Review. Polar Geogr. 2002 Jul 1;26(3):235–46.
    • 19. Sturm M, Holmgren J, König M, Morris K. The thermal conductivity of seasonal snow. J Glaciol. 1997 Jan;43(143):26–41.
    • 20. Henry HAL. Climate change and soil freezing dynamics: historical trends and projected changes. Clim Change. 2008 Apr 1;87(3):421–34.
    • 21. Sorensen PO, Finzi AC, Giasson MA, Reinmann AB, Sanders-DeMott R, Templer PH. Winter soil freeze-thaw cycles lead to reductions in soil microbial biomass and activity not compensated for by soil warming. Soil Biol Biochem. 2018 Jan 1;116:39–47.
    • 22. Groffman PM, Driscoll CT, Fahey TJ, Hardy JP, Fitzhugh RD, Tierney GL. Colder soils in a warmer world: A snow manipulation study in a northern hardwood forest ecosystem. Biogeochemistry. 2001 Nov 1;56(2):135–50.
    • 23. Barnett TP, Adam JC, Lettenmaier DP. Potential impacts of a warming climate on water availability in snow-dominated regions. Nature. 2005 Nov;438(7066):303–9. pmid:16292301
    • 24. Mankin JS, Viviroli D, Singh D, Hoekstra AY, Diffenbaugh NS. The potential for snow to supply human water demand in the present and future. Environ Res Lett. 2015 Nov;10(11):114016.
    • 25. Hayhoe K, Cayan D, Field CB, Frumhoff PC, Maurer EP, Miller NL, et al. Emissions pathways, climate change, and impacts on California. Proc Natl Acad Sci. 2004 Aug 24;101(34):12422–7. pmid:15314227
    • 26. Berdanier AB, Klein JA. Growing Season Length and Soil Moisture Interactively Constrain High Elevation Aboveground Net Primary Production. Ecosystems. 2011 Sep 1;14(6):963–74.
    • 27. Slatyer RA, Umbers KDL, Arnold PA. Ecological responses to variation in seasonal snow cover. Conserv Biol. 2022;36(1):e13727. pmid:33636757
    • 28. Goncharova OYu Matyshak GV, Epstein HE Sefilian AR, Bobrik AA. Influence of snow cover on soil temperatures: Meso- and micro-scale topographic effects (a case study from the northern West Siberia discontinuous permafrost zone). CATENA. 2019 Dec 1;183:104224.
    • 29. Goodrich LE. The influence of snow cover on the ground thermal regime. Can Geotech J. 1982 Nov;19(4):421–32.
    • 30. Cline DW. Snow surface energy exchanges and snowmelt at a continental, midlatitude Alpine site. Water Resour Res. 1997;33(4):689–701.
    • 31. Rindt O, Rosinger C, Bonkowski M, Rixen C, Brüggemann N, Urich T, et al. Biogeochemical dynamics during snowmelt and in summer in the Alps. Biogeochemistry. 2023;162(2):257–66.
    • 32. Wang X, Chen R. Influence of snow cover on soil freeze depth across China. Geoderma. 2022 Dec 15;428:116195.
    • 33. Lievens H, Demuzere M, Marshall HP, Reichle RH, Brucker L, Brangers I, et al. Snow depth variability in the Northern Hemisphere mountains observed from space. Nat Commun. 2019 Oct 11;10(1):4629. pmid:31604957
    • 34. Guo H, Yang Y, Zhang W, Zhang C, Sun H. Attributing snow cover extent changes over the Northern Hemisphere for the past 65 years. Environ Res Commun. 2021 Jun;3(6):061001.
    • 35. Hardy JP, Groffman PM, Fitzhugh RD, Henry KS, Welman AT, Demers JD, et al. Snow depth manipulation and its influence on soil frost and water dynamics in a northern hardwood forest. Biogeochemistry. 2001 Nov 1;56(2):151–74.
    • 36. Gavazov K, Ingrisch J, Hasibeder R, Mills RTE, Buttler A, Gleixner G, et al. Winter ecology of a subalpine grassland: Effects of snow removal on soil respiration, microbial structure and function. Sci Total Environ. 2017 Jul 15;590–591:316–24. pmid:28279534
    • 37. Hazlett P w., English M c., Foster N w. Ion Enrichment of Snowmelt Water by Processes within a Podzolic Soil. J Environ Qual. 1992;21(1):102–9.
    • 38. Edwards AC, Cresser MS. Freezing and Its Effect on Chemical and Biological Properties of Soil. In: Stewart BA, editor. Advances in Soil Science: Volume 18 [Internet]. New York, NY: Springer; 1992 [cited 2023 Oct 5]. p. 59–79. (Advances in Soil Science). Available from: https://doi.org/8_2
      • 39. Choi G, Robinson DA, Kang S. Changing Northern Hemisphere Snow Seasons. J Clim. 2010 Oct 1;23(19):5305–10.
      • 40. Broadbent AAD, Bahn M, Pritchard WJ, Newbold LK, Goodall T, Guinta A, et al. Shrub expansion modulates belowground impacts of changing snow conditions in alpine grasslands. Ecol Lett. 2022;25(1):52–64. pmid:34708508
      • 41. Li Z, Yang W, Yue K, Justine MF, He R, Yang K, et al. Effects of snow absence on winter soil nitrogen dynamics in a subalpine spruce forest of southwestern China. Geoderma. 2017 Dec 1;307:107–13.
      • 42. Yang K, Yin R, Peñuelas J, Li Z, Tan B, You C, et al. Divergent effects of snow exclusion on microbial variables across aggregate size classes. CATENA. 2021 Nov 1;206:105481.
      • 43. Litaor M, Williams M, Seastedt T. Topographic controls on snow distribution, soil moisture, and species diversity of herbaceous alpine vegetation, Niwot Ridge, Colorado. J Geophys Res Biogeosciences. 2008;113(G2).
      • 44. Petriccione B, Bricca A. Thirty years of ecological research at the Gran Sasso d’Italia LTER site: climate change in action. Nat Conserv. 2019 Mar 5;34:9–39.
      • 45. Zhao Z, De Frenne P, Peñuelas J, Van Meerbeek K, Fornara DA, Peng Y, et al. Effects of snow cover-induced microclimate warming on soil physicochemical and biotic properties. Geoderma. 2022 Oct 1;423:115983.
      • 46. Freppaz M, Celi L, Marchelli M, Zanini E. Snow removal and its influence on temperature and N dynamics in alpine soils (Vallée d’Aoste, northwest Italy). J Plant Nutr Soil Sci. 2008;171(5):672–80.
      • 47. Larsen KS, Grogan P, Jonasson S, Michelsen A. Respiration and Microbial Dynamics in Two Subarctic Ecosystems during Winter and Spring Thaw: Effects of Increased Snow Depth. Arct Antarct Alp Res. 2007 May 1;39(2):268–76.
      • 48. Freppaz M, Williams MW, Seastedt T, Filippa G. Response of soil organic and inorganic nutrients in alpine soils to a 16-year factorial snow and N-fertilization experiment, Colorado Front Range, USA. Appl Soil Ecol. 2012 Nov 1;62:131–41.
      • 49. Wipf S, Rixen C. A review of snow manipulation experiments in Arctic and alpine tundra ecosystems. Polar Res. 2010 Jan 1;29(1):95–109.
      • 50. Barry RG. Mountain Weather and Climate [Internet]. 3rd ed. Cambridge: Cambridge University Press; 2008 [cited 2023 Nov 30]. Available from: https://www.cambridge.org/core/books/mountain-weather-and-climate/AB88E7CA8DE0FD36123922EBBCBF3B1E.
        • 51. Lamprecht A, Semenchuk PR, Steinbauer K, Winkler M, Pauli H. Climate change leads to accelerated transformation of high-elevation vegetation in the central Alps. New Phytol. 2018;220(2):447–59. pmid:29938796
        • 52. Bombonato L, Gerdol R. Manipulating snow cover in an alpine bog: effects on ecosystem respiration and nutrient content in soil and microbes. Clim Change. 2012 Sep 1;114(2):261–72.
        • 53. Broadbent AAD, Snell HSK, Michas A, Pritchard WJ, Newbold L, Cordero I, et al. Climate change alters temporal dynamics of alpine soil microbial functioning and biogeochemical cycling via earlier snowmelt. ISME J. 2021 Aug;15(8):2264–75. pmid:33619353
        • 54. Robroek BJM, Heijboer A, Jassey VEJ, Hefting MM, Rouwenhorst TG, Buttler A, et al. Snow cover manipulation effects on microbial community structure and soil chemistry in a mountain bog. Plant Soil. 2013 Aug 1;369(1):151–64.
        • 55. Ade LJ, Hu L, Zi HB, Wang CT, Lerdau M, Dong SK. Effect of snowpack on the soil bacteria of alpine meadows in the Qinghai-Tibetan Plateau of China. CATENA. 2018 May 1;164:13–22.
        • 56. Ren Y, Zhang L, Yang K, Li Z, Yin R, Tan B, et al. Short-term effects of snow cover manipulation on soil bacterial diversity and community composition. Sci Total Environ. 2020 Nov 1;741:140454. pmid:32610243
        • 57. Tan B, zhong Wu F, i Yang W, hua He X. Snow removal alters soil microbial biomass and enzyme activity in a Tibetan alpine forest. Appl Soil Ecol. 2014 Apr 1;76:34–41.
        • 58. Yang F, Ni X, Zeng X, Li H, Tan B, Liang Z, et al. Short-term winter snow reduction stimulates soil nutrient leaching without changing the microbial biomass in an alpine fir forest. Glob Ecol Conserv. 2021 Jan 1;25:e01434.
        • 59. Hedges LV, Gurevitch J, Curtis PS. The Meta-Analysis of Response Ratios in Experimental Ecology. Ecology. 1999;80(4):1150–6.
        • 60. Nakagawa S, Noble DWA, Lagisz M, Spake R, Viechtbauer W, Senior AM. A robust and readily implementable method for the meta‐analysis of response ratios with and without missing standard deviations. Ecol Lett. 2023 Feb;26(2):232–44. pmid:36573275
        • 61. Isobe K, Oka H, Watanabe T, Tateno R, Urakawa R, Liang C, et al. High soil microbial activity in the winter season enhances nitrogen cycling in a cool-temperate deciduous forest. Soil Biol Biochem. 2018 Sep 1;124:90–100.
        • 62. Clein JS, Schimel JP. Microbial activity of tundra and taiga soils at sub-zero temperatures. Soil Biol Biochem. 1995 Sep 1;27(9):1231–4.
        • 63. Hosokawa N, Isobe K, Urakawa R, Tateno R, Fukuzawa K, Watanabe T, et al. Soil freeze–thaw with root litter alters N transformations during the dormant season in soils under two temperate forests in northern Japan. Soil Biol Biochem. 2017 Nov 1;114:270–8.
        • 64. Larsen KS, Jonasson S, Michelsen A. Repeated freeze–thaw cycles and their effects on biological processes in two arctic ecosystem types. Appl Soil Ecol. 2002 Oct 1;21(3):187–95.
        • 65. Buckeridge KM, Grogan P. Deepened snow alters soil microbial nutrient limitations in arctic birch hummock tundra. Appl Soil Ecol. 2008 Jun 1;39(2):210–22.
        • 66. Buckeridge KM, Grogan P. Deepened snow increases late thaw biogeochemical pulses in mesic low arctic tundra. Biogeochemistry. 2010 Dec 1;101(1):105–21.
        • 67. Bilbrough CJ, Welker JM, Bowman WD. Early Spring Nitrogen Uptake by Snow-Covered Plants: A Comparison of Arctic and Alpine Plant Function under the Snowpack. Arct Antarct Alp Res. 2000 Nov 1;32(4):404–11.
        • 68. Sickman JO, Leydecker A, Chang CCY, Kendall C, Melack JM, Lucero DM, et al. Mechanisms underlying export of N from high-elevation catchments during seasonal transitions. Biogeochemistry. 2003 Jun 1;64(1):1–24.
        • 69. Grogan P, Jonasson S. Temperature and substrate controls on intra-annual variation in ecosystem respiration in two subarctic vegetation types. Glob Change Biol. 2005;11(3):465–75.
        • 70. Winston GC, Sundquist ET, Stephens BB, Trumbore SE. Winter CO2 fluxes in a boreal forest. J Geophys Res Atmospheres. 1997;102(D24):28795–804.
        • 71. Monson RK, Sparks JP, Rosenstiel TN, Scott-Denton LE, Huxman TE, Harley PC, et al. Climatic influences on net ecosystem CO2 exchange during the transition from wintertime carbon source to springtime carbon sink in a high-elevation, subalpine forest. Oecologia. 2005 Nov 1;146(1):130–47. pmid:16091970
        • 72. Fahnestock JT, Jones MH, Welker JM. Wintertime CO2 efflux from Arctic soils: Implications for annual carbon budgets. Glob Biogeochem Cycles. 1999;13(3):775–9.
        • 73. Brooks PD, Williams MW, Schmidt SK. Microbial activity under alpine snowpacks, Niwot Ridge, Colorado. Biogeochemistry. 1996 Feb 1;32(2):93–113.
        • 74. van Bochove E, Jones HG, Bertrand N, Prévost D. Winter fluxes of greenhouse gases from snow-covered agricultural soil:intra-annual and interannual variations. Glob Biogeochem Cycles. 2000;14(1):113–25.
        • 75. Hubbard RM, Ryan MG, Elder K, Rhoades CC. Seasonal patterns in soil surface CO2 flux under snow cover in 50 and 300 year old subalpine forests. Biogeochemistry. 2005 Mar 1;73(1):93–107.
        • 76. Yang K, Peng C, Peñuelas J, Kardol P, Li Z, Zhang L, et al. Immediate and carry-over effects of increased soil frost on soil respiration and microbial activity in a spruce forest. Soil Biol Biochem. 2019 Aug 1;135:51–9.
        • 77. Monson RK, Lipson DL, Burns SP, Turnipseed AA, Delany AC, Williams MW, et al. Winter forest soil respiration controlled by climate and microbial community composition. Nature. 2006 Feb;439(7077):711–4. pmid:16467835
        • 78. Yu Z, Wang J, Liu S, Piao S, Ciais P, Running SW, et al. Decrease in winter respiration explains 25% of the annual northern forest carbon sink enhancement over the last 30 years. Glob Ecol Biogeogr. 2016;25(5):586–95.
        • 79. Groffman PM, Hardy JP, Driscoll CT, Fahey TJ. Snow depth, soil freezing, and fluxes of carbon dioxide, nitrous oxide and methane in a northern hardwood forest. Glob Change Biol. 2006;12(9):1748–60.
        • 80. Bai Y, Li F, Yang G, Shi S, Dong F, Liu M, et al. Meta-analysis of experimental warming on soil invertase and urease activities. Acta Agric Scand Sect B—Soil Plant Sci. 2018 Feb 17;68(2):104–9.
        • 81. Pettit NM, Smith ARJ, Freedman RB, Burns RG. Soil urease: Activity, stability and kinetic properties. Soil Biol Biochem. 1976 Jan 1;8(6):479–84.
        • 82. Frankenberger WT, Johanson JB. Factors affecting invertase activity in soils. Plant Soil. 1983 Oct 1;74(3):313–23.
        • 83. Sorensen PO, Templer PH, Finzi AC. Contrasting effects of winter snowpack and soil frost on growing season microbial biomass and enzyme activity in two mixed-hardwood forests. Biogeochemistry. 2016 Mar 1;128(1):141–54.
        • 84. Hishi T, Urakawa R, Tashiro N, Maeda Y, Shibata H. Seasonality of factors controlling N mineralization rates among slope positions and aspects in cool-temperate deciduous natural forests and larch plantations. Biol Fertil Soils. 2014;50(2):343–56.
        • 85. Patel KF, Tatariw C, MacRae JD, Ohno T, Nelson SJ, Fernandez IJ. Repeated freeze–thaw cycles increase extractable, but not total, carbon and nitrogen in a Maine coniferous soil. Geoderma. 2021 Nov 15;402:115353.
        • 86. Buckeridge KM, Banerjee S, Siciliano SD, Grogan P. The seasonal pattern of soil microbial community structure in mesic low arctic tundra. Soil Biol Biochem. 2013 Oct 1;65:338–47.
        • 87. Lipson DA, Schadt CW, Schmidt SK. Changes in Soil Microbial Community Structure and Function in an Alpine Dry Meadow following Spring Snow Melt. Microb Ecol. 2002;43(3):307–14. pmid:12037609
        • 88. Schadt CW, Martin AP, Lipson DA, Schmidt SK. Seasonal Dynamics of Previously Unknown Fungal Lineages in Tundra Soils. Science. 2003 Sep 5;301(5638):1359–61. pmid:12958355
        • 89. Fierer N, Schimel JP. A Proposed Mechanism for the Pulse in Carbon Dioxide Production Commonly Observed Following the Rapid Rewetting of a Dry Soil. Soil Sci Soc Am J. 2003;67(3):798–805.
        • 90. Bardgett RD, Bowman WD, Kaufmann R, Schmidt SK. A temporal approach to linking aboveground and belowground ecology. Trends Ecol Evol. 2005 Nov 1;20(11):634–41. pmid:16701447
        • 91. Stres B, Philippot L, Faganeli J, Tiedje JM. Frequent freeze–thaw cycles yield diminished yet resistant and responsive microbial communities in two temperate soils: a laboratory experiment. FEMS Microbiol Ecol. 2010 Nov 1;74(2):323–35. pmid:20735477
        • 92. Männistö M, Vuosku J, Stark S, Saravesi K, Suokas M, Markkola A, et al. Bacterial and fungal communities in boreal forest soil are insensitive to changes in snow cover conditions. FEMS Microbiol Ecol. 2018 Sep 1;94(9):fiy123. pmid:29939247
        • 93. Isobe K, Oka H, Watanabe T, Tateno R, Senoo K, Shibata H. Soil microbial community response to winter climate change is phylogenetically conserved and highly resilient in a cool-temperate forest. Soil Biol Biochem. 2022 Feb 1;165:108499.
        • 94. Aanderud ZT, Jones SE, Schoolmaster DR, Fierer N, Lennon JT. Sensitivity of soil respiration and microbial communities to altered snowfall. Soil Biol Biochem. 2013 Feb 1;57:217–27.
        • 95. Lewe N, Hermans S, Lear G, Kelly LT, Thomson-Laing G, Weisbrod B, et al. Phospholipid fatty acid (PLFA) analysis as a tool to estimate absolute abundances from compositional 16S rRNA bacterial metabarcoding data. J Microbiol Methods. 2021 Sep 1;188:106271. pmid:34146605
        • 96. Xiang SR, Shang TC, Chen Y, Yao TD. Deposition and postdeposition mechanisms as possible drivers of microbial population variability in glacier ice. FEMS Microbiol Ecol. 2009 Nov;70(2):9–20. pmid:19796140
        • 97. Azzoni RS, Tagliaferri I, Franzetti A, Mayer C, Lambrecht A, Compostella C, et al. Bacterial diversity in snow from mid-latitude mountain areas: Alps, Eastern Anatolia, Karakoram and Himalaya. Ann Glaciol. 2018 Dec;59(77):10–20.
        • 98. Chuvochina MS, Marie D, Chevaillier S, Petit JR, Normand P, Alekhina IA, et al. Community Variability of Bacteria in Alpine Snow (Mont Blanc) Containing Saharan Dust Deposition and Their Snow Colonisation Potential. Microbes Environ. 2011;26(3):237–47. pmid:21666389
        • 99. Dastrup DB, Carling GT, Collins SA, Nelson ST, Fernandez DP, Tingey DG, et al. Aeolian dust chemistry and bacterial communities in snow are unique to airshed locations across northern Utah, USA. Atmos Environ. 2018 Nov 1;193:251–61.
        • 100. Greilinger M, Schauer G, Baumann-Stanzer K, Skomorowski P, Schöner W, Kasper-Giebl A. Contribution of Saharan dust to ion deposition loads of high alpine snow packs in Austria (1987–2017). Front Earth Sci. 2018;6:126.
        • 101. Meola M, Lazzaro A, Zeyer J. Bacterial composition and survival on Sahara dust particles transported to the European Alps. Front Microbiol. 2015;6:1454. pmid:26733988
        • 102. Margesin R, Miteva V. Diversity and ecology of psychrophilic microorganisms. Res Microbiol. 2011 Apr 1;162(3):346–61. pmid:21187146
        • 103. Liu M, Bjørnlund L, Rønn R, Christensen S, Ekelund F. Disturbance Promotes Non-Indigenous Bacterial Invasion in Soil Microcosms: Analysis of the Roles of Resource Availability and Community Structure. PLOS ONE. 2012 Oct 2;7(10):e45306. pmid:23056198
        • 104. De Roy K, Marzorati M, Negroni A, Thas O, Balloi A, Fava F, et al. Environmental conditions and community evenness determine the outcome of biological invasion. Nat Commun. 2013 Jan 22;4(1):1383.
        • 105. Malard LA, Pearce DA. Bacterial colonisation: from airborne dispersal to integration within the soil community. Front Microbiol. 2022;13:782789. pmid:35615521
        • 106. Malard LA, Bergk-Pinto B, Layton R, Vogel TM, Larose C, Pearce DA. Snow Microorganisms Colonise Arctic Soils Following Snow Melt. Microb Ecol [Internet]. 2023 Mar 20 [cited 2023 Mar 21]; Available from: pmid:36939866
        • 107. Maccario L, Carpenter SD, Deming JW, Vogel TM, Larose C. Sources and selection of snow-specific microbial communities in a Greenlandic sea ice snow cover. Sci Rep. 2019 Feb 19;9(1):2290. pmid:30783153
        • 108. Tierney GL, Fahey TJ, Groffman PM, Hardy JP, Fitzhugh RD, Driscoll CT. Soil freezing alters fine root dynamics in a northern hardwood forest. Biogeochemistry. 2001 Nov 1;56(2):175–90.
        • 109. Campbell JL, Socci AM, Templer PH. Increased nitrogen leaching following soil freezing is due to decreased root uptake in a northern hardwood forest. Glob Change Biol. 2014;20(8):2663–73.
        • 110. Fitzhugh RD, Driscoll CT, Groffman PM, Tierney GL, Fahey TJ, Hardy JP. Effects of soil freezing disturbance on soil solution nitrogen, phosphorus, and carbon chemistry in a northern hardwood ecosystem. Biogeochemistry. 2001 Nov 1;56(2):215–38.
        • 111. Sanders-DeMott R, Sorensen PO, Reinmann AB, Templer PH. Growing season warming and winter freeze–thaw cycles reduce root nitrogen uptake capacity and increase soil solution nitrogen in a northern forest ecosystem. Biogeochemistry. 2018 Feb 1;137(3):337–49.
        • 112. Beniston M. Climatic Change in Mountain Regions: A Review of Possible Impacts. Clim Change. 2003 Jul 1;59(1):5–31.
        • 113. Löffler J. The influence of micro-climate, snow cover, and soil moisture on ecosystem functioning in high mountains. J Geogr Sci. 2007 Feb 1;17(1):3–19.
        • 114. Rammig A, Jonas T, Zimmermann NE, Rixen C. Changes in alpine plant growth under future climate conditions. Biogeosciences. 2010 Jun 24;7(6):2013–24.
        • 115. Bokhorst S, Bjerke JW, Bowles FW, Melillo J, Callaghan TV, Phoenix GK. Impacts of extreme winter warming in the sub-Arctic: growing season responses of dwarf shrub heathland. Glob Change Biol. 2008;14(11):2603–12.
        • 116. Zhang R, Zhang R, Zuo Z. Impact of Eurasian Spring Snow Decrement on East Asian Summer Precipitation. J Clim. 2017 May 1;30(9):3421–37.
        • 117. Green K, Slatyer R. Arthropod community composition along snowmelt gradients in snowbeds in the Snowy Mountains of south-eastern Australia. Austral Ecol. 2020;45(2):144–57.
        • 118. ávila-Jiménez ML, Coulson SJ, Solhøy T, Sjöblom A. Overwintering of terrestrial Arctic arthropods: the fauna of Svalbard now and in the future. Polar Res. 2010 Jan 1;29(1):127–37.
        • 119. Bale JS, Hayward SAL. Insect overwintering in a changing climate. J Exp Biol. 2010 Mar 15;213(6):980–94. pmid:20190123
        • 120. Johnston AN, Christophersen RG, Beever EA, Ransom JI. Freezing in a warming climate: Marked declines of a subnivean hibernator after a snow drought. Ecol Evol. 2020 Dec 29;11(3):1264–79. pmid:33598129
        • 121. Templer PH, Schiller AF, Fuller NW, Socci AM, Campbell JL, Drake JE, et al. Impact of a reduced winter snowpack on litter arthropod abundance and diversity in a northern hardwood forest ecosystem. Biol Fertil Soils. 2012 May 1;48(4):413–24.
        • 122. Sulkava P, Huhta V. Effects of hard frost and freeze-thaw cycles on decomposer communities and N mineralisation in boreal forest soil. Appl Soil Ecol. 2003 Mar 1;22(3):225–39.
        • 123. Coq S, Ibanez S. Soil fauna contribution to winter decomposition in subalpine grasslands. SOIL Org. 2019 Dec 1;91(3):107–12.
        • 124. Hartshorn J. A Review of Forest Management Effects on Terrestrial Leaf Litter Inhabiting Arthropods. Forests. 2021 Jan;12(1):23.
        • 125. Dahl MB, Kreyling J, Petters S, Wang H, Mortensen MS, Maccario L, et al. Warmer winters result in reshaping of the European beech forest soil microbiome (bacteria, archaea and fungi)—With potential implications for ecosystem functioning. Environ Microbiol. 2023;25(6):1118–35. pmid:36752534
        • 126. Rixen C, Høye TT, Macek P, Aerts R, Alatalo JM, Anderson JT, et al. Winters are changing: snow effects on Arctic and alpine tundra ecosystems. Arct Sci. 2022 Sep;8(3):572–608.