Decadal soil warming decreased vascular plant above and belowground production in a subarctic grassland by inducing nitrogen limitation.

Below and aboveground vegetation dynamics are crucial in understanding how climate warming may affect terrestrial ecosystem carbon cycling. In contrast to aboveground biomass, the response of belowground biomass to long-term warming has been poorly studied. Here, we characterized the impacts of decadal geothermal warming at two levels (on average +3.3°C and +7.9°C) on below and aboveground plant biomass stocks and production in a subarctic grassland. Soil warming did not change standing root biomass and even decreased fine root production and reduced aboveground biomass and production. Decadal soil warming also did not significantly alter the root-shoot ratio. The linear stepwise regression model suggested that following 10 yr of soil warming, temperature was no longer the direct driver of these responses, but losses of soil N were. Soil N losses, due to warming-induced decreases in organic matter and water retention capacity, were identified as key driver of the decreased above and belowground production. The reduction in fine root production was accompanied by thinner roots with increased specific root area. These results indicate that after a decade of soil warming, plant productivity in the studied subarctic grassland was affected by soil warming mainly by the reduction in soil N.

Sensitivity of soil carbon fractions and their specific stabilization mechanisms to extreme soil warming in a subarctic grassland.

Terrestrial carbon cycle feedbacks to global warming are major uncertainties in climate models. For in-depth understanding of changes in soil organic carbon (SOC) after soil warming, long-term responses of SOC stabilization mechanisms such as aggregation, organo-mineral interactions and chemical recalcitrance need to be addressed. This study investigated the effect of 6 years of geothermal soil warming on different SOC fractions in an unmanaged grassland in Iceland. Along an extreme warming gradient of +0 to ~+40 °C, we isolated five fractions of SOC that varied conceptually in turnover rate from active to passive in the following order: particulate organic matter (POM), dissolved organic carbon (DOC), SOC in sand and stable aggregates (SA), SOC in silt and clay (SC-rSOC) and resistant SOC (rSOC). Soil warming of 0.6 °C increased bulk SOC by 22 ± 43% (0-10 cm soil layer) and 27 ± 54% (20-30 cm), while further warming led to exponential SOC depletion of up to 79 ± 14% (0-10 cm) and 74 ± 8% (20-30) in the most warmed plots (~+40 °C). Only the SA fraction was more sensitive than the bulk soil, with 93 ± 6% (0-10 cm) and 86 ± 13% (20-30 cm) SOC losses and the highest relative enrichment in 13 C as an indicator for the degree of decomposition (+1.6 ± 1.5‰ in 0-10 cm and +1.3 ± 0.8‰ in 20-30 cm). The SA fraction mass also declined along the warming gradient, while the SC fraction mass increased. This was explained by deactivation of aggregate-binding mechanisms. There was no difference between the responses of SC-rSOC (slow-cycling) and rSOC (passive) to warming, and 13 C enrichment in rSOC was equal to that in bulk soil. We concluded that the sensitivity of SOC to warming was not a function of age or chemical recalcitrance, but triggered by changes in biophysical stabilization mechanisms, such as aggregation.

Phenological responses of Icelandic subarctic grasslands to short-term and long-term natural soil warming.

The phenology of vegetation, particularly the length of the growing season (LOS; i.e., the period from greenup to senescence), is highly sensitive to climate change, which could imply potent feedbacks to the climate system, for example, by altering the ecosystem carbon (C) balance. In recent decades, the largest extensions of LOS have been reported at high northern latitudes, but further warming-induced LOS extensions may be constrained by too short photoperiod or unfulfilled chilling requirements. Here, we studied subarctic grasslands, which cover a vast area and contain large C stocks, but for which LOS changes under further warming are highly uncertain. We measured LOS extensions of Icelandic subarctic grasslands along natural geothermal soil warming gradients of different age (short term, where the measurements started after 5 years of warming and long term, i.e., warmed since ≥50 years) using ground-level measurements of normalized difference vegetation index. We found that LOS linearly extended with on average 2.1 days per °C soil warming up to the highest soil warming levels (ca. +10°C) and that LOS had the potential to extend at least 1 month. This indicates that the warming impact on LOS in these subarctic grasslands will likely not saturate in the near future. A similar response to short- and long-term warming indicated a strong physiological control of the phenological response of the subarctic grasslands to warming and suggested that genetic adaptations and community changes were likely of minor importance. We conclude that the warming-driven extension of the LOSs of these subarctic grasslands did not saturate up to +10°C warming, and hence that growing seasons of high-latitude grasslands are likely to continue lengthening with future warming (unless genetic adaptations or species shifts do occur). This persistence of the warming-induced extension of LOS has important implications for the C-sink potential of subarctic grasslands under climate change.

A systemic overreaction to years versus decades of warming in a subarctic grassland ecosystem.

Temperature governs most biotic processes, yet we know little about how warming affects whole ecosystems. Here we examined the responses of 128 components of a subarctic grassland to either 5-8 or >50 years of soil warming. Warming of >50 years drove the ecosystem to a new steady state possessing a distinct biotic composition and reduced species richness, biomass and soil organic matter. However, the warmed state was preceded by an overreaction to warming, which was related to organism physiology and was evident after 5-8 years. Ignoring this overreaction yielded errors of >100% for 83 variables when predicting their responses to a realistic warming scenario of 1 °C over 50 years, although some, including soil carbon content, remained stable after 5-8 years. This study challenges long-term ecosystem predictions made from short-term observations, and provides a framework for characterization of ecosystem responses to sustained climate change.

Prolonged exposure does not increase soil microbial community compositional response to warming along geothermal gradients.

Global change is expected to affect soil microbial communities through their responsiveness to temperature. It has been proposed that prolonged exposure to elevated temperatures may lead to progressively larger effects on soil microbial community composition. However, due to the relatively short-term nature of most warming experiments, this idea has been challenging to evaluate. The present study took the advantage of natural geothermal gradients (from +1°C to +19°C above ambient) in two subarctic grasslands to test the hypothesis that long-term exposure (>50 years) intensifies the effect of warming on microbial community composition compared to short-term exposure (5-7 years). Community profiles from amplicon sequencing of bacterial and fungal rRNA genes did not support this hypothesis: significant changes relative to ambient were observed only starting from the warming intensity of +9°C in the long term and +7°C/+3°C in the short term, for bacteria and fungi, respectively. Our results suggest that microbial communities in high-latitude grasslands will not undergo lasting shifts in community composition under the warming predicted for the coming 100 years (+2.2°C to +8.3°C).

Microbial temperature sensitivity and biomass change explain soil carbon loss with warming.

Soil microorganisms control carbon losses from soils to the atmosphere1-3, yet their responses to climate warming are often short-lived and unpredictable4-7. Two mechanisms, microbial acclimation and substrate depletion, have been proposed to explain temporary warming effects on soil microbial activity8-10. However, empirical support for either mechanism is unconvincing. Here we used geothermal temperature gradients (> 50 years of field warming)11 and a short-term experiment to show that microbial activity (gross rates of growth, turnover, respiration and carbon uptake) is intrinsically temperature sensitive and does not acclimate to warming (+ 6 ºC) over weeks or decades. Permanently accelerated microbial activity caused carbon loss from soil. However, soil carbon loss was temporary because substrate depletion reduced microbial biomass and constrained the influence of microbes over the ecosystem. A microbial biogeochemical model12-14 showed that these observations are reproducible through a modest, but permanent, acceleration in microbial physiology. These findings reveal a mechanism by which intrinsic microbial temperature sensitivity and substrate depletion together dictate warming effects on soil carbon loss via their control over microbial biomass. We thus provide a framework for interpreting the links between temperature, microbial activity and soil carbon loss on timescales relevant to Earth's climate system.

Impact of Soil Warming on the Plant Metabolome of Icelandic Grasslands.

Climate change is stronger at high than at temperate and tropical latitudes. The natural geothermal conditions in southern Iceland provide an opportunity to study the impact of warming on plants, because of the geothermal bedrock channels that induce stable gradients of soil temperature. We studied two valleys, one where such gradients have been present for centuries (long-term treatment), and another where new gradients were created in 2008 after a shallow crustal earthquake (short-term treatment). We studied the impact of soil warming (0 to +15 °C) on the foliar metabolomes of two common plant species of high northern latitudes: Agrostis capillaris, a monocotyledon grass; and Ranunculus acris, a dicotyledonous herb, and evaluated the dependence of shifts in their metabolomes on the length of the warming treatment. The two species responded differently to warming, depending on the length of exposure. The grass metabolome clearly shifted at the site of long-term warming, but the herb metabolome did not. The main up-regulated compounds at the highest temperatures at the long-term site were saccharides and amino acids, both involved in heat-shock metabolic pathways. Moreover, some secondary metabolites, such as phenolic acids and terpenes, associated with a wide array of stresses, were also up-regulated. Most current climatic models predict an increase in annual average temperature between 2-8 °C over land masses in the Arctic towards the end of this century. The metabolomes of A. capillaris and R. acris shifted abruptly and nonlinearly to soil warming >5 °C above the control temperature for the coming decades. These results thus suggest that a slight warming increase may not imply substantial changes in plant function, but if the temperature rises more than 5 °C, warming may end up triggering metabolic pathways associated with heat stress in some plant species currently dominant in this region.