Soil fungal and bacterial communities reflect differently tundra vegetation state transitions and soil physico-chemical properties.

Strong disturbances may induce ecosystem transitions into new alternative states that sustain through plant-soil interactions, such as the transition of dwarf shrub-dominated into graminoid-dominated vegetation by herbivory in tundra. Little evidence exists on soil microbial communities in alternative states, and along the slow process of ecosystem return into the predisturbance state. We analysed vegetation, soil microbial communities and activities as well as soil physico-chemical properties in historical reindeer enclosures in northernmost Finland in the following plot types: control heaths in the surrounding tundra; graminoid-dominated; 'shifting'; and recovered dwarf shrub-dominated vegetation inside enclosures. Soil fungal communities followed changes in vegetation, whereas bacterial communities were more affected by soil physico-chemical properties. Graminoid plots were characterized by moulds, pathotrophs and dark septate endophytes. Ericoid mycorrhizal and saprotrophic fungi were typical for control and recovered plots. Soil microbial communities inside the enclosures showed historical contingency, as their spatial variation was high in recovered plots despite the vegetation being more homogeneous. Self-maintaining feedback loops between plant functional types, soil microbial communities, and carbon and nutrient mineralization act effectively to stabilize alternative vegetation states, but once predisturbance vegetation reestablishes itself, soil microbial communities and physico-chemical properties return back towards their predisturbance state.

N-fertilization and disturbance exert long-lasting complex legacies on subarctic ecosystems.

Subarctic ecosystems are subjected to increasing nitrogen (N) enrichment and disturbances that induce particularly strong effects on plant communities when occurring in combination. There is little experimental evidence on the longevity of these effects. We applied N-fertilization (40 kg urea-N ha-1 year-1 for 4 years) and disturbance (removal of vegetation and organic soil layer on one occasion) in two plant communities in a subarctic forest-tundra ecotone in northern Finland. Within the first four years, N-fertilization and disturbance increased the share of deciduous dwarf shrubs and graminoids at the expense of evergreen dwarf shrubs. Individual treatments intensified the other's effect resulting in the strongest increase in graminoids under combined N-fertilization and disturbance. The re-analysis of the plant communities 15 years after cessation of N-fertilization showed an even higher share of graminoids. 18 years after disturbance, the total vascular plant abundance was still substantially lower and the share of graminoids higher. At the same point, the plant community composition was the same under disturbance as under combined N-fertilization and disturbance, indicating that multiple perturbations no longer reinforced the other's effect. Yet, complex interactions between N-fertilization and disturbance were still detected in the soil. We found higher organic N under disturbance and lower microbial N under combined N-fertilization and disturbance, which suggests a lower bioavailability of N sources for soil microorganisms. Our findings support that the effects of enhanced nutrients and disturbance on subarctic vegetation persist over decadal timescales. However, they also highlight the complexity of plant-soil interactions that drive subarctic ecosystem responses to multiple perturbations across varying timescales.

Bacterial and fungal communities in sub-Arctic tundra heaths are shaped by contrasting snow accumulation and nutrient availability.

Climate change is affecting winter snow conditions significantly in northern ecosystems but the effects of the changing conditions for soil microbial communities are not well-understood. We utilized naturally occurring differences in snow accumulation to understand how the wintertime subnivean conditions shape bacterial and fungal communities in dwarf shrub-dominated sub-Arctic Fennoscandian tundra sampled in mid-winter, early, and late growing season. Phospholipid fatty acid (PLFA) and quantitative PCR analyses indicated that fungal abundance was higher in windswept tundra heaths with low snow accumulation and lower nutrient availability. This was associated with clear differences in the microbial community structure throughout the season. Members of Clavaria spp. and Sebacinales were especially dominant in the windswept heaths. Bacterial biomass proxies were higher in the snow-accumulating tundra heaths in the late growing season but there were only minor differences in the biomass or community structure in winter. Bacterial communities were dominated by members of Alphaproteobacteria, Actinomycetota, and Acidobacteriota and were less affected by the snow conditions than the fungal communities. The results suggest that small-scale spatial patterns in snow accumulation leading to a mosaic of differing tundra heath vegetation shapes bacterial and fungal communities as well as soil carbon and nutrient availability.

Reindeer grazing history determines the responses of subarctic soil fungal communities to warming and fertilization.

Composition and functioning of arctic soil fungal communities may alter rapidly due to the ongoing trends of warmer temperatures, shifts in nutrient availability, and shrub encroachment. In addition, the communities may also be intrinsically shaped by heavy grazing, which may locally induce an ecosystem change that couples with increased soil temperature and nutrients and where shrub encroachment is less likely to occur than in lightly grazed conditions. We tested how 4 yr of experimental warming and fertilization affected organic soil fungal communities in sites with decadal history of either heavy or light reindeer grazing using high-throughput sequencing of the internal transcribed spacer 2 ribosomal DNA region. Grazing history largely overrode the impacts of short-term warming and fertilization in determining the composition of fungal communities. The less diverse fungal communities under light grazing showed more pronounced responses to experimental treatments when compared with the communities under heavy grazing. Yet, ordination approaches revealed distinct treatment responses under both grazing intensities. If grazing shifts the fungal communities in Arctic ecosystems to a different and more diverse state, this shift may dictate ecosystem responses to further abiotic changes. This indicates that the intensity of grazing cannot be left out when predicting future changes in fungi-driven processes in the tundra.

Contrasting vegetation states do not diverge in soil organic matter storage: evidence from historical sites in tundra.

Ecosystems where severe disturbance has induced permanent shifts in vegetation and soil processes may represent alternative stable states. To date, little is known on how long-lasting changes in soil processes are following such disturbances, and how the changes in plant and soil processes between the alternative states eventually manifest themselves in soil organic matter (SOM) storage. Here, we analyzed plant density, the shrub : forb ratio, microbial respiration, extracellular enzyme activities and SOM stocks in soils of subarctic tundra and historical milking grounds, where reindeer herding induced a vegetation transition from deciduous shrubs to graminoids several centuries earlier but were abandoned a century ago. This provides the possibility to compare sites with similar topography, but highly contrasting vegetation for centuries. We found that enzymatic activities and N:P stoichiometry differed between control and disturbed sites, confirming that culturally induced vegetation shifts exert lasting impacts on tundra soil processes. Transition zones, where shrubs had encroached into the historical milking grounds during the past 50 yr, indicated that microbial activities for N and P acquisition changed more rapidly along a vegetation shift than those for microbial C acquisition. Although plant and soil processes differed between control and disturbed sites, we found no effect of historical vegetation transition on SOM stock. Across the study sites, soil SOM stocks were correlated with total plant density but not with the shrub : forb ratio. Our finding that SOM stock was insensitive to a centennial difference in plant community composition suggests that, as such, grazing-induced alternative vegetation states might not necessarily differ in SOM sequestration.

Bacterial and fungal communities in boreal forest soil are insensitive to changes in snow cover conditions.

The northern regions are experiencing considerable changes in winter climate leading to more frequent warm periods, rain-on-snow events and reduced snow pack diminishing the insulation properties of snow cover and increasing soil frost and freeze-thaw cycles. In this study, we investigated how the lack of snow cover, formation of ice encasement and snow compaction affect the size, structure and activities of soil bacterial and fungal communities. Contrary to our hypotheses, snow manipulation treatments over one winter had limited influence on microbial community structure, bacterial or fungal copy numbers or enzyme activities. However, microbial community structure and activities shifted seasonally among soils sampled before snow melt, in early and late growing season and seemed driven by substrate availability. Bacterial and fungal communities were dominated by stress-resistant taxa such as the orders Acidobacteriales, Chaetothyriales and Helotiales that are likely adapted to adverse winter conditions. This study indicated that microbial communities in acidic northern boreal forest soil may be insensitive to direct effects of changing snow cover. However, in long term, the detrimental effects of increased ice and frost to plant roots may alter plant derived carbon and nutrient pools to the soil likely leading to stronger microbial responses.

Gender Dimorphism Does Not Affect Secondary Compound Composition in Juniperus communis After Shoot Cutting in Northern Boreal Forests.

Due to a difference in plant resource allocation to reproduction, the males of dioecious plants may be more growth-orientated, whereas females may allocate more resources for synthesizing secondary compounds. This mechanism is considered to cause gender-specific differences in the plant responses to the loss of plant biomass. Here, we tested gender dimorphism in the responses of common juniper (Juniperus communis) to shoot cutting in four juniper populations located in northern boreal forests in Finland. We collected shoots from uncut junipers and from junipers subjected to shoot cutting in the previous year, and analyzed them for their shoot growth as well as phenolic and terpenoid concentrations. There were no differences in foliar phenolic or terpenoid concentrations between the males and the females. Shoot cutting increased phenolic but not terpenoid concentrations, similarly, in both males and females. Our study reveals that the nature of gender dimorphism may differ among species and locations, which should be considered in theories on plant gender dimorphism. Given the similar phenolic and terpene concentrations in both genders, the different sexes in the northern juniper populations might experience equal levels of herbivory. This lack of gender dimorphism in biotic interactions could result from the high need of plant secondary metabolites (PSM) against abiotic stresses, which is typical for juniper at high latitudes.

The Snow Must Go On: Ground Ice Encasement, Snow Compaction and Absence of Snow Differently Cause Soil Hypoxia, CO2 Accumulation and Tree Seedling Damage in Boreal Forest.

At high latitudes, the climate has warmed at twice the rate of the global average with most changes observed in autumn, winter and spring. Increasing winter temperatures and wide temperature fluctuations are leading to more frequent rain-on-snow events and freeze-thaw cycles causing snow compaction and formation of ice layers in the snowpack, thus creating ice encasement (IE). By decreasing the snowpack insulation capacity and restricting soil-atmosphere gas exchange, modification of the snow properties may lead to colder soil but also to hypoxia and accumulation of trace gases in the subnivean environment. To test the effects of these overwintering conditions changes on plant winter survival and growth, we established a snow manipulation experiment in a coniferous forest in Northern Finland with Norway spruce and Scots pine seedlings. In addition to ambient conditions and prevention of IE, we applied three snow manipulation levels: IE created by artificial rain-on-snow events, snow compaction and complete snow removal. Snow removal led to deeper soil frost during winter, but no clear effect of IE or snow compaction done in early winter was observed on soil temperature. Hypoxia and accumulation of CO2 were highest in the IE plots but, more importantly, the duration of CO2 concentration above 5% was 17 days in IE plots compared to 0 days in ambient plots. IE was the most damaging winter condition for both species, decreasing the proportion of healthy seedlings by 47% for spruce and 76% for pine compared to ambient conditions. Seedlings in all three treatments tended to grow less than seedlings in ambient conditions but only IE had a significant effect on spruce growth. Our results demonstrate a negative impact of winter climate change on boreal forest regeneration and productivity. Changing snow conditions may thus partially mitigate the positive effect of increasing growing season temperatures on boreal forest productivity.

Vegetation shift from deciduous to evergreen dwarf shrubs in response to selective herbivory offsets carbon losses: evidence from 19 years of warming and simulated herbivory in the subarctic tundra.

Selective herbivory of palatable plant species provides a competitive advantage for unpalatable plant species, which often have slow growth rates and produce slowly decomposable litter. We hypothesized that through a shift in the vegetation community from palatable, deciduous dwarf shrubs to unpalatable, evergreen dwarf shrubs, selective herbivory may counteract the increased shrub abundance that is otherwise found in tundra ecosystems, in turn interacting with the responses of ecosystem carbon (C) stocks and CO2 balance to climatic warming. We tested this hypothesis in a 19-year field experiment with factorial treatments of warming and simulated herbivory on the dominant deciduous dwarf shrub Vaccinium myrtillus. Warming was associated with a significantly increased vegetation abundance, with the strongest effect on deciduous dwarf shrubs, resulting in greater rates of both gross ecosystem production (GEP) and ecosystem respiration (ER) as well as increased C stocks. Simulated herbivory increased the abundance of evergreen dwarf shrubs, most importantly Empetrum nigrum ssp. hermaphroditum, which led to a recent shift in the dominant vegetation from deciduous to evergreen dwarf shrubs. Simulated herbivory caused no effect on GEP and ER or the total ecosystem C stocks, indicating that the vegetation shift counteracted the herbivore-induced C loss from the system. A larger proportion of the total ecosystem C stock was found aboveground, rather than belowground, in plots treated with simulated herbivory. We conclude that by providing a competitive advantage to unpalatable plant species with slow growth rates and long life spans, selective herbivory may promote aboveground C stocks in a warming tundra ecosystem and, through this mechanism, counteract C losses that result from plant biomass consumption.

Phenolic responses of mountain crowberry (Empetrum nigrum ssp. hermaphroditum) to global climate change are compound specific and depend on grazing by reindeer (Rangifer tarandus).

Mountain crowberry (Empetrum nigrum ssp. hermaphroditum) is a keystone species in northern ecosystems and exerts important ecosystem-level effects through high concentrations of phenolic metabolites. It has not been investigated how crowberry phenolics will respond to global climate change. In the tundra, grazing by reindeer (Rangifer tarandus) affects vegetation and soil nutrient availability, but almost nothing is known about the interactions between grazing and global climate change on plant phenolics. We performed a factorial warming and fertilization experiment in a tundra ecosystem under light grazing and heavy grazing and analyzed individual foliar phenolics and crowberry abundance. Crowberry was more abundant under light grazing than heavy grazing. Although phenolic concentrations did not differ between grazing intensities, responses of crowberry abundance and phenolic concentrations to warming varied significantly depending on grazing intensity. Under light grazing, warming increased crowberry abundance and the concentration of stilbenes, but decreased e.g., the concentrations of flavonols, condensed tannins, and batatasin-III, resulting in no change in total phenolics. Under heavy grazing, warming did not affect crowberry abundance, and induced a weak but consistent decrease among the different phenolic compound groups, resulting in a net decrease in total phenolics. Our results show that the different phenolic compound groups may show varying or even opposing responses to warming in the tundra at different levels of grazing intensity. Even when plant phenolic concentrations do not directly respond to grazing, grazers may have a key control over plant responses to changes in the abiotic environment, reflecting multiple adaptive purposes of plant phenolics and complex interactions between the biotic and the abiotic factors.

Phenolic composition and antioxidant capacity of bilberry (Vaccinium myrtillus) leaves in Northern Europe following foliar development and along environmental gradients.

Bilberry is a characteristic field layer species in the boreal forests and is an important forage plant for herbivores of the North European ecosystem. Bilberry leaves contain high levels of phenolic compounds, especially hydroxycinnamic acids, flavonols, catechins, and proanthocyanidins. We investigated the phenolic composition of bilberry leaves in two studies, one following foliar development in forest and open areas, and the other along a wide geographical gradient from south to north boreal forests in Finland. An analysis of bilberry leaves collected in open and forest areas showed that major phenolic changes appeared in the first stages of leaf development, but, most importantly, synthesis and accumulation of flavonoids was delayed in the forest compared to the high light sites. Sampling along a geographical gradient in the boreal zone indicated that leaves from higher latitudes and higher altitudes had greater soluble phenolic and flavonol levels, higher antioxidant capacity, and lower contents of chlorogenic acid derivatives. The ecological significance of the results is discussed.

Effect of latitude and altitude on the terpenoid and soluble phenolic composition of juniper (Juniperus communis) needles and evaluation of their antibacterial activity in the boreal zone.

The demand for dry juniper (Juniperus communis) needles as a raw material for the food, pharmaceutical, and cosmetic industries has increased rapidly in recent years. Juniper needles are known to be rich in terpenoids and phenolics, but their chemical composition and antibacterial properties have not been well-characterized. In this study, we describe the soluble phenolic and terpenoid composition of juniper needles collected in Finland (n = 125) and demonstrate that the concentration of these compounds clearly increased with latitude and altitude with, however, a stronger latitudinal effect (a higher content of monoterpenoids, proanthocyanidins, and flavonols in northern latitudes). Analysis of methanolic extracts showed quite good activity against both antibiotic-sensitive and -resistant Staphylococcus aureus strains and suggested an important role of the soluble phenolic fraction. Finally, we demonstrate the relative lack of toxicity of juniper extracts on keratinocytes and fibroblastic cells, raising the possibility of their use in preventing bacterial skin infection.

Links between plant community composition, soil organic matter quality and microbial communities in contrasting tundra habitats.

Plant communities, soil organic matter and microbial communities are predicted to be interlinked and to exhibit concordant patterns along major environmental gradients. We investigated the relationships between plant functional type composition, soil organic matter quality and decomposer community composition, and how these are related to major environmental variation in non-acid and acid soils derived from calcareous versus siliceous bedrocks, respectively. We analysed vegetation, organic matter and microbial community compositions from five non-acidic and five acidic heath sites in alpine tundra in northern Europe. Sequential organic matter fractionation was used to characterize organic matter quality and phospholipid fatty acid analysis to detect major variation in decomposer communities. Non-acidic and acidic heaths differed substantially in vegetation composition, and these disparities were associated with congruent shifts in soil organic matter and microbial communities. A high proportion of forbs in the vegetation was positively associated with low C:N and high soluble N:phenolics ratios in soil organic matter, and a high proportion of bacteria in the microbial community. On the contrary, dwarf shrub-rich vegetation was associated with high C:N and low soluble N:phenolics ratios, and a high proportion of fungi in the microbial community. Our study demonstrates a strong link between the plant community composition, soil organic matter quality, and microbial community composition, and that differences in one compartment are paralleled by changes in others. Variation in the forb-shrub gradient of vegetation may largely dictate variations in the chemical quality of organic matter and decomposer communities in tundra ecosystems. Soil pH, through its direct and indirect effects on plant and microbial communities, seems to function as an ultimate environmental driver that gives rise to and amplifies the interactions between above- and belowground systems.

Concentrations of foliar quercetin in natural populations of white birch (Betula pubescens) increase with latitude.

We investigated latitudinal and regional variations in the composition and concentrations of foliar flavonoids and condensed tannins in wild populations of white birch (Betula pubescens EHRH) in a large climatic transect in Finland. Concentrations of quercetin derivatives were correlated positively with latitude. By contrast, the concentrations of apigenin and naringenin derivatives were correlated negatively with latitude. These compound-specific latitudinal gradients compensated each other, resulting in no changes in the concentration of total flavonoids. Our results thus demonstrate a qualitative, but not quantitative, latitude-associated gradient in the foliar flavonoids in white birch. Due to higher antioxidant capacity of the quercetin derivatives in relation to other flavonoids, the qualitative change can reflect higher adaptation to light in the north than south. An investigation on a regional scale in the northern boreal zone showed that the temperature sum was correlated positively and soil P concentration was correlated negatively with the concentrations of foliar flavonoid, while the concentration of condensed tannins was correlated with slope. The variation in concentrations of flavonoids at large-scale geographical patterns is in line with the conjecture that foliar flavonoids are synthesized for protection against photooxidative stress.

The phenolic compounds in Cladonia lichens are not antimicrobial in soils.

According to classic text books on lichen biology, the phenolic secondary chemicals in lichens have antibiotic effects on soil microorganisms and mycorrhizal fungi in ecosystems. However, the experimental evidence for this under natural conditions is still relatively scarce. We examined some of the assumptions behind the concept of antimicrobial effects of lichen secondary substances: (1) the secondary substances of Cladonia stellaris, usnic and perlatolic acids, are leached out from the lichens by rainwater; (2) these substances inhibit the microbial activity of soil, and; (3) since they are extremely resistant to microbial decomposition, the soil underneath a continuous lichen mat is enriched in usnic and perlatolic acids. Our results did not support any of these assumptions. The evidence for the antimicrobial activity of lichen secondary substances seems to be weak in comparison to other suggested functions such as light filtering and herbivore protection. We suggest that it is time to re-evaluate the evidence for the antimicrobial ecological role of lichen secondary substances in natural systems.

Ecological role of reindeer summer browsing in the mountain birch (Betula pubescens ssp. czerepanovii) forests: effects on plant defense, litter decomposition, and soil nutrient cycling.

Mammalian herbivores commonly alter the concentrations of secondary compounds in plants and, by this mechanism, have indirect effects on litter decomposition and soil carbon and nutrient cycling. In northernmost Fennoscandia, the subarctic mountain birch (Betula pubescens ssp. czerepanovii) forests are important pasture for the semidomestic reindeer (Rangifer tarandus). In the summer ranges, mountain birches are intensively browsed, whereas in the winter ranges, reindeer feed on ground lichens, and the mountain birches remain intact. We analyzed the effect of summer browsing on the concentrations of secondary substances, litter decomposition, and soil nutrient pools in areas that had been separated as summer or winter ranges for at least 20 years, and we predicted that summer browsing may reduce levels of secondary compounds in the mountain birch and, by this mechanism, have an indirect effect on the decomposition of mountain birch leaf litter and soil nutrient cycling. The effect of browsing on the concentration of secondary substances in the mountain birch leaves varied between different years and management districts, but in some cases, the concentration of condensed tannins was lower in the summer than in the winter ranges. In a reciprocal litter decomposition trial, both litter origin and emplacement significantly affected the litter decomposition rate. Decomposition rates were faster for the litter originating from and placed into the summer range. Soil inorganic nitrogen (N) concentrations were higher in the summer than in the winter ranges, which indicates that reindeer summer browsing may enhance the soil nutrient cycling. There was a tight inverse relationship between soil N and foliar tannin concentrations in the winter range but not in the summer range. This suggests that in these strongly nutrient-limited ecosystems, soil N availability regulates the patterns of resource allocation to condensed tannins in the absence but not in the presence of browsing.