Icelandic grasslands as long-term C sinks under elevated organic N inputs

About 10% of the anthropogenic CO₂ emissions have been absorbed by northern terrestrial ecosystems during the past decades. It has been hypothesized that part of this increasing carbon (C) sink is caused by the alleviation of nitrogen (N) limitation by increasing anthropogenic N inputs. However, little is known about this N-dependent C sink. Here, we studied the effect of chronic seabird-derived N inputs (47-67 kg N ha⁻¹ year⁻¹) on the net soil organic C (SOC) storage rate of unmanaged Icelandic grasslands on the volcanic Vestmannaeyjar archipelago by using a stock change approach in combination with soil dating. We studied both early developmental (young) soils that had been receiving increased N inputs over a decadal timescale since an eruption in 1963, and well-developed soils, that had been receiving N inputs over a millennial timescale. For the latter, however, the effects on both decadal (topsoil; 40 years) and millennial (total soil profile; 1600 years) SOC storage could be studied, as the age of topsoil and the total soil profile could be determined from volcanic ash layers deposited in 1973 and 395 AD. We found that enhanced N availability-either from accumulation over time, or seabird derived-increased the net SOC storage rate. Under low N inputs, early developmental soils were weak decadal C sinks (0.018 ton SOC ha−1 year−1), but this increased quickly under ca. 30 years of elevated N inputs to 0.29 ton SOC ha⁻¹ year⁻¹, thereby equalling the decadal SOC storage rate of the unfertilized well-developed soils. Furthermore, for the well-developed soils, chronically elevated N inputs not only stimulated the decadal SOC storage rate in the topsoil, but also the total millennial SOC storage was consistently higher. Hence, our study suggests that Icelandic grasslands, if not disturbed, can remain C sinks for many centuries under current climatic conditions and that chronically elevated N inputs can induce a permanent strengthening of this sink

Temperature responses in a subarctic springtail from two geothermally warmed habitats

Common-garden experiments with populations sampled along natural thermal gradients help to reveal local adaptation, disentangle environmental and genetic effects, and ultimately predict, by analogy, future biotic responses to climate change. In this regard, geothermal habitats are useful model systems as they exhibit dramatic changes in soil temperature. The springtail Protaphorura pseudovanderdrifti has apparently coped with such local geothermal warming in Iceland, as this species occurs along a more than half-century-old geothermal gradient in a grassland and persists along a newly emerged temperature gradient in a previously non-geothermal planted spruce forest. We measured thermal reaction norms for development and walking speed and acute cold shock tolerance of P. pseudovanderdrifti originating from the grassland and forest geothermal gradients. Temperature-dependent juvenile development showed little variation among subpopulations from the recently warmed forest, probably due to insufficient evolutionary time, but springtails from the warmed grassland plots had significantly steeper reaction norms than their counterparts from the corresponding unwarmed plot. In contrast, cold tolerance and locomotory activity showed no conclusive clinal pattern despite significant within-habitat variation. There appeared to be significant differences between habitats, as springtails from the forest had more temperature-sensitive developmental rate and locomotory activity, walked faster, and exhibited more variable cold tolerance than grassland springtails did. The planting of a forest, therefore, seems to have exerted a stronger effect on the thermal phenotype of P. pseudovanderdrifti than the emergence of a geothermal gradient. Thus, habitat properties may be no less important in shaping thermal reaction norms than the mean temperature. These local-scale findings suggest that, in addition to warming per se, global transformation of communities may drive the evolution of thermal phenotypes to an extent comparable with the effect of rising environmental temperature

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).This work was supported by Research Foundation–Flanders (FWO) [1293114N to JTW, 12B0716N to SV, 11G1615N to NIWL], Icelandic Research Council [163272-051 to BDS], Climate Change Manipulation Experiments in Terrestrial Ecosystems (ClimMani) COST Action [ES1308], the European Research Council grant ERC-SyG-610028 IMBALANCE-P and the University of Antwerp: University Research Fund (BOF).Peer Reviewe

Coupled carbon and nitrogen losses in response to seven years of chronic warming in subarctic soils

Increasing temperatures may alter the stoichiometric demands of soil microbes and impair their capacity to stabilize carbon (C) and retain nitrogen (N), with critical consequences for the soil C and N storage at high latitude soils. Geothermally active areas in Iceland provided wide, continuous and stable gradients of soil temperatures to test this hypothesis. In order to characterize the stoichiometric demands of microbes from these subarctic soils, we incubated soils from ambient temperatures after the factorial addition of C, N and P substrates separately and in combination. In a second experiment, soils that had been exposed to different in situ warming intensities (+0, +0.5, +1.8, +3.4, +8.7, +15.9 °C above ambient) for seven years were incubated after the combined addition of C, N and P to evaluate the capacity of soil microbes to store and immobilize C and N at the different warming scenarios. The seven years of chronic soil warming triggered large and proportional soil C and N losses (4.1 ± 0.5% °C−1 of the stocks in unwarmed soils) from the upper 10 cm of soil, with a predominant depletion of the physically accessible organic substrates that were weakly sorbed in soil minerals up to 8.7 °C warming. Soil microbes met the increasing respiratory demands under conditions of low C accessibility at the expenses of a reduction of the standing biomass in warmer soils. This together with the strict microbial C:N stoichiometric demands also constrained their capacity of N retention, and increased the vulnerability of soil to N losses. Our findings suggest a strong control of microbial physiology and C:N stoichiometric needs on the retention of soil N and on the resilience of soil C stocks from high-latitudes to warming, particularly during periods of vegetation dormancy and low C inputs

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

Acclimation of Fine Root Systems to Soil Warming: Comparison of an Experimental Setup and a Natural Soil Temperature Gradient

Global warming is predicted to impact high-latitude and high-altitude forests severely, jeopardizing their overall functioning and carbon storage, both of which depend on the warming response of tree fine root systems. This paper investigates the effect of soil warming on the biomass, morphology and colonizing ectomycorrhizal community of spruce fine and absorptive fine roots. We compare the responses of spruce roots growing at a man-made long-term soil warming (+ 4°C) experiment to results obtained from a geothermal soil temperature gradient (+ 1 to + 14°C) extending to the forest die-off edge, to shed light on the generalizability of the warming response and reveal any thresholds in acclimation ability. Trees in warmer soils formed longer and less-branched absorptive roots with higher specific root length and area, and lower root tissue density in both spruce stands, irrespective of warming method and location. Soil warming at the experimental warming site also supported the occurrence of a more varied EcM community and an increase in the abundance of Tomentella spp., indicating a shift in nutrient foraging. Fine and absorptive fine root biomass decreased toward warmer soil, with a sharp reduction occurring between + 4 and + 6°C from the ambient and leading to the collapse of the fine root system at the geothermal gradient. At the experimental warming site, the applied + 4°C warming had no effect on fine and absorptive fine root biomass. The similar fine root responses at the two warming sites suggest that the observations possibly reflect general acclimation patterns in spruce forests to global warming.We thank Krista Lõhmus for valuable discussions, Kessy Abarenkov for guidance with uploading the EcM fungal sequences, and Aale Puri, Aulis Puri, Laura Soon and Marta Arula for assistance in the laboratory. We acknowledge the EU through the European Regional Development Fund (Center of Excellence ENVIRON and EcolChange), the Estonian Ministry of Education, Research projects IUT2-16, IUT34-9 and Lydia and Felix Krabi Scholarship Fund for financial support. We are very grateful to ExpeER for financing the field work of Kaarin Parts and analyses of EcM fungal community samples at the Achenkirch experimental area. This work contributes to the Icelandic ForHot-Forest Project (IRF Fund, No. 163272-051), the CAR-ES Nordic Network, the ClimMani (ES1308) and the Biolink COST Actions (FP1305).Peer Reviewe

Impact of soil warming on the plant metabolome of Icelandic grasslands

Altres ajuts: Scholarly Studies programme of the Smithsonian Institution, projects LM2015061 and LO1415 of the Ministry of Education, Youth and Sports of the Czech Republic, and the Research Foundation-Flanders (FWO aspirant grant to N.L.).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

Twenty-Two Years of Warming, Fertilisation and Shading of Subarctic Heath Shrubs Promote Secondary Growth and Plasticity but Not Primary Growth

Most manipulation experiments simulating global change in tundra were short-term or did not measure plant growth directly. Here, we assessed the growth of three shrubs (Cassiope tetragona, Empetrum hermaphroditum and Betula nana) at a subarctic heath in Abisko (Northern Sweden) after 22 years of warming (passive greenhouses), fertilisation (nutrients addition) and shading (hessian fabric), and compare this to observations from the first decade of treatment. We assessed the growth rate of current-year leaves and apical stem (primary growth) and cambial growth (secondary growth), and integrated growth rates with morphological measurements and species coverage. Primary- and total growth of Cassiope and Empetrum were unaffected by manipulations, whereas growth was substantially reduced under fertilisation and shading (but not warming) for Betula. Overall, shrub height and length tended to increase under fertilisation and warming, whereas branching increased mostly in shaded Cassiope. Morphological changes were coupled to increased secondary growth under fertilisation. The species coverage showed a remarkable increase in graminoids in fertilised plots. Shrub response to fertilisation was positive in the short-term but changed over time, likely because of an increased competition with graminoids. More erected postures and large, canopies (requiring enhanced secondary growth for stem reinforcement) likely compensated for the increased light competition in Empetrum and Cassiope but did not avoid growth reduction in the shade intolerant Betula. The impact of warming and shading on shrub growth was more conservative. The lack of growth enhancement under warming suggests the absence of long-term acclimation for processes limiting biomass production. The lack of negative effects of shading on Cassiope was linked to morphological changes increasing the photosynthetic surface. Overall, tundra shrubs showed developmental plasticity over the longer term. However, such plasticity was associated clearly with growth rate trends only in fertilised plots

Soil carbon loss in warmed subarctic grasslands is rapid and restricted to topsoil

Global warming may lead to carbon transfers from soils to the atmosphere, yet this positive feedback to the climate system remains highly uncertain, especially in subsoils (Ilyina and Friedlingstein, 2016; Shi et al., 2018). Using natural geothermal soil warming gradients of up to +6.4 degrees C in subarctic grasslands (Sigurdsson et al., 2016), we show that soil organic carbon (SOC) stocks decline strongly and linearly with warming (-2.8 t ha(-1) degrees C-1). Comparison of SOC stock changes following medium-term (5 and 10 years) and long-term (> 50 years) warming revealed that all SOC stock reduction occurred within the first 5 years of warming, after which continued warming no longer reduced SOC stocks. This rapid equilibration of SOC observed in Andosol suggests a critical role for ecosystem adaptations to warming and could imply short-lived soil carbon-climate feedbacks. Our data further revealed that the soil C loss occurred in all aggregate size fractions and that SOC stock reduction was only visible in topsoil (0-10 cm). SOC stocks in subsoil (10-30 cm), where plant roots were absent, showed apparent conservation after > 50 years of warming. The observed depth-dependent warming responses indicate that explicit vertical resolution is a prerequisite for global models to accurately project future SOC stocks for this soil type and should be investigated for soils with other mineralogies

The handbook for standardized field and laboratory measurements in terrestrial climate change experiments and observational studies (ClimEx)

1. Climate change is a world‐wide threat to biodiversity and ecosystem structure, functioning and services. To understand the underlying drivers and mechanisms, and to predict the consequences for nature and people, we urgently need better understanding of the direction and magnitude of climate change impacts across the soil–plant–atmosphere continuum. An increasing number of climate change studies are creating new opportunities for meaningful and high‐quality generalizations and improved process understanding. However, significant challenges exist related to data availability and/or compatibility across studies, compromising opportunities for data re‐use, synthesis and upscaling. Many of these challenges relate to a lack of an established ‘best practice’ for measuring key impacts and responses. This restrains our current understanding of complex processes and mechanisms in terrestrial ecosystems related to climate change. 2. To overcome these challenges, we collected best‐practice methods emerging from major ecological research networks and experiments, as synthesized by 115 experts from across a wide range of scientific disciplines. Our handbook contains guidance on the selection of response variables for different purposes, protocols for standardized measurements of 66 such response variables and advice on data management. Specifically, we recommend a minimum subset of variables that should be collected in all climate change studies to allow data re‐use and synthesis, and give guidance on additional variables critical for different types of synthesis and upscaling. The goal of this community effort is to facilitate awareness of the importance and broader application of standardized methods to promote data re‐use, availability, compatibility and transparency. We envision improved research practices that will increase returns on investments in individual research projects, facilitate second‐order research outputs and create opportunities for collaboration across scientific communities. Ultimately, this should significantly improve the quality and impact of the science, which is required to fulfil society's needs in a changing world