Significance The Arctic is warming rapidly, causing permafrost soils to thaw. Vast stocks of nitrogen (>67 billion tons) in the permafrost, accumulated thousands of years ago, could now become available for decomposition, leading to the release of nitrous oxide (N 2 O) to the atmosphere. N 2 O is a strong greenhouse gas, almost 300 times more powerful than CO 2 for warming the climate. Although carbon dynamics in the Arctic are well studied, the fact that Arctic soils store enormous amounts of nitrogen has received little attention so far. We report that the Arctic may become a substantial source of N 2 O when the permafrost thaws, and that N 2 O emissions could occur from surfaces covering almost one-fourth of the entire Arctic.

Abstract Permafrost in the Arctic is thawing, exposing large carbon and nitrogen stocks for decomposition. Gaseous carbon release from Arctic soils due to permafrost thawing is known to be substantial, but growing evidence suggests that Arctic soils may also be relevant sources of nitrous oxide (N 2 O). Here we show that N 2 O emissions from subarctic peatlands increase as the permafrost thaws. In our study, the highest postthaw emissions occurred from bare peat surfaces, a typical landform in permafrost peatlands, where permafrost thaw caused a fivefold increase in emissions (0.56 ± 0.11 vs. 2.81 ± 0.6 mg N 2 O m−2 d−1). These emission rates match those from tropical forest soils, the world’s largest natural terrestrial N 2 O source. The presence of vegetation, known to limit N 2 O emissions in tundra, did decrease (by ∼90%) but did not prevent thaw-induced N 2 O release, whereas waterlogged conditions suppressed the emissions. We show that regions with high probability for N 2 O emissions cover one-fourth of the Arctic. Our results imply that the Arctic N 2 O budget will depend strongly on moisture changes, and that a gradual deepening of the active layer will create a strong noncarbon climate change feedback.

Arctic land areas are predicted to warm up to 5.6–12.4 °C by the end of this century (1), likely leading to widespread permafrost degradation (2⇓⇓–5) and substantial changes in ecosystem functioning (6). With thawing, a vast pool of immobile C stored in permafrost (7) becomes available for decomposition and remobilization, triggering greenhouse gas emissions of carbon dioxide (CO 2 ) and methane (CH 4 ). Thus, gaseous C release from thawing permafrost is being studied extensively to evaluate the magnitude of the permafrost–carbon feedback to the climate (8, 9). Often overlooked, however, is the fact that permafrost soils are also large N reservoirs, with a conservative estimate of 67 billion tons of total N in the upper 3 m (10). Thus, the permafrost N stocks are more than 500 times larger than the annual N load added as fertilizer to soils globally (11, 12). Upon thawing, organically bound N is subject to mineralization, leading to a release of mineral N. Mineral N forms, predominantly ammonium (NH 4 +) and nitrate (NO 3 −), fuel nitrification and denitrification, respectively, the two dominant processes generating the strong greenhouse gas nitrous oxide (N 2 O) in soils (13).

Mounting evidence shows that Arctic soils may produce (14, 15) and release (16, 17) substantial amounts of N 2 O. In previous studies, we identified patches of bare peat in permafrost peatlands as hot spots for N 2 O emissions in subarctic tundra (16, 17). Furthermore, an increase in growing season temperature without causing permafrost thaw not only increases N 2 O emissions from these hot spots, but also triggers N 2 O emissions from vegetated tundra peatlands (18), which cover large areas of the Arctic. This highlights the important role that peatlands may play in promoting Arctic N 2 O emissions in the future.

So far, soil moisture, soil organic matter (SOM) content, C/N ratio, and plant growth have been identified as the key regulators of Arctic N 2 O emissions (17, 18). The great unknown, however, is how permafrost thaw will affect N 2 O emissions by potentially unlocking the vast N stocks currently stored in Arctic soils (10). Evidence for an N 2 O pulse from thawing permafrost is scarce, and up to now based solely on laboratory incubations with external N input (15). Field experiments, or mesocosm studies at near-field conditions, are lacking.

To assess whether permafrost thaw will increase N 2 O release to the atmosphere, we measured N 2 O fluxes from 16 intact peat mesocosms (diameter, 10 cm; length, 80 cm) during a 33-wk experiment. The mesocosms were collected in a typical subarctic permafrost peatland (68°89′N, 21°05′E) in Finnish Lapland (SI Appendix, Fig. S1) and originated from vegetated and naturally bare parts of a palsa mound (17, 19) (SI Appendix, Fig. S2), a reported N 2 O source (17). Some of the bare peat surfaces exhibited a sporadic lichen cover, but vascular plants, with roots penetrating into the peat profile, were absent. The mesocosms included living plants, when present, and the full peat profile from the surface of the active layer (soil layer above the permafrost subjected to seasonal thawing; 0–∼65 cm) to the upper permafrost layer (∼65–∼80 cm). On these bare and vegetated surfaces, we applied two distinct moisture treatments, representing possible postthaw conditions: an unaltered water table level (>55 cm below the surface; “dry” scenario), simulating gradual active layer deepening, and an artificially raised water table level (5–10 cm below the surface; “wet” scenario), simulating conditions after palsa collapse. Transport and storage of mesocosms took place in mild freezing temperatures (−5 °C minimum), imitating natural winter conditions. After a 5-mo preincubation period, the mesocosms were set up in a climate-controlled growth chamber (air temperature 10 °C) and then sequentially thawed, stepwise, by lowering the level of a saltwater bath (−4 °C) (SI Appendix, Figs. S3 and Fig. S4 and Table S1).

Conclusions Here we present strong evidence for a substantial thawing-induced N 2 O release from Arctic peatlands. We also show that vegetated peat soils may turn from a negligible to a small but significant N 2 O source, with significant implications for pan-Arctic emission budgets. Furthermore, the positive climate change feedback of N 2 O will be stronger under aerobic conditions than under anaerobic conditions. Because N 2 O has an almost 300 times stronger global warming potential than CO 2 on a 100-y time horizon (12), a postthaw N 2 O release would further enhance the radiative forcing stemming from C gases (8, 9).

Materials and Methods Study Site. Peat mesocosms for this study were collected from a palsa mire (68°89’N, 21°05’E; SI Appendix, Fig. S1) located in the subarctic permafrost zone in Finnish Lapland. Underlain by discontinuous permafrost, the palsa complex was uplifted by frost heave ∼3 m above the surrounding mire area. The vegetation cover on the palsa surface is dominated by dwarf shrubs and herbaceous plants, such as Empetrum nigrum subsp. hermaphroditum, Vaccinium vitis-idaea L., Betula nana L., Rubus chamaemorus L., lichens, and mosses (e.g., Dicranum spp., Polytrichum spp., Pleurozium spp.) in the wetter areas. Patches of bare peat, naturally free of vascular plants, are scattered among the vegetated areas. More details are provided in SI Appendix. Sampling and Transport of Peat Mesocoms. We sampled 16 intact peat mesocosms from vegetated and naturally bare (absent of vascular plants) parts of the palsa. A steel corer (∼1 m length) with a removable steel cap was hammered into the soil using a pneumatic drill (SI Appendix, Fig. S2). The soil cores were collected within plastic tubes (polypropylene, 10 cm diameter; SI Appendix, Fig. S3), which were inserted into the steel corer before drilling. A chain connected to a pulley and tripod was used to retrieve the peat cores. The sampling occurred at maximum seasonal thaw depth at the end of September 2012. The peat cores were frozen immediately after sampling. Great care was taken to keep the cores frozen at gentle minus temperatures (−5 °C minimum) at all times during the transport and the 5-mo preincubation period (= artificial winter), until the start of the experiment in March 2013. Details of mesocosm collection are provided in SI Appendix. Climate Chamber Setup and Replication. The cores were set up in a climate-controlled chamber (BDR16 Reach-in plant growth chamber; Conviron, Winnipeg, Canada), providing constant humidity and air temperature (+10 °C) and the ability to regulate the light level. To simulate thawing, we placed the mesocosms in two replicate saltwater baths (water temperature −3 to −4 °C), and sequentially thawed the peat mesocosms from top to bottom, by gradually lowering the saltwater level, during six thawing stages (SI Appendix, Figs. S3 and S4 and Table S1). One-half of the cores from vegetated and bare parts of the palsa were left under natural soil moisture conditions, and the water table level of the other half of the cores was artificially raised to 5–10 cm below the surface. The four treatments that we used in this study, each with four replicates, are referred to as dry bare (DB), dry vegetated (DV), wet bare (WB), and wet vegetated (WV). Details are provided in SI Appendix. N 2 O Fluxes. For gas flux measurements, the peat mesocosms were permanently covered with 6-mm transparent Plexiglas chambers (diameter, 120 mm; height, 250 mm; volume, 2.8 L), fixed around the plastic tubes with the peat monoliths with two rubber rings. A layer of distilled water on top of the rubber rings further ensured the gas tightness of the chambers. N 2 O samples were taken manually two to three times per week from each mesocosm. More information is provided in SI Appendix. Soil Profile Concentration of N 2 O. To determine the concentration of N 2 O along the soil profile, we installed five soil gas collectors horizontally in each core at the following depths: 5, 20, and 40 cm below the soil surface; 10 cm above the measured thaw depth (∼55 cm); and 5 cm below the measured thaw depth (∼70 cm) (SI Appendix). Nutrient Profile in Soil Pore Water. For soil water sampling, we used Rhizon pore water samplers (Rhizosphere, Wageningen, The Netherlands) installed at depths of 5–10 cm, 35–40 cm below the surface, and 0–5 cm below the maximum seasonal thaw depth (∼65–70 cm). Amounts of NO 3 − and NH 4 + in the pore water were determined using spectrophotometric methods, as described in detail in SI Appendix. Soil Analyses and Statistical Methods. Detailed descriptions of soil analyses, hyperspectral imaging of peat profiles, GIS mapping, and statistical analyses are provided in SI Appendix.

Acknowledgments We thank Igor Marushchak, Timo Oksanen, Maxim Dorodnikov, Hanne Säppi, Tatiana Trubnikova, Ville Närhi, and Kateřina Diáková for their help with practical work, and two anonymous reviewers for their valuable comments that helped improve the manuscript. This study was funded by the Nordic Center of Excellence DEFROST. We gratefully acknowledge financial support from the Academy of Finland project CryoN (decision no. 132045), the European Union FP7-ENV project PAGE21 (contract no. 282700), and the Joint Programming Initiative Climate project “Constraining Uncertainties in the Permafrost-Climate Feedback” (COUP; decision no. 291691). C.V. received personal funding from the University of Eastern Finland’s doctoral program in Environmental Physics, Health, and Biology, and travel support from European Cooperation in Science and Technology (COST) Action ABBA (ES0804), Nordic Network for Stable Isotope Research (NordSIR), and NORDFLUX.

Footnotes Author contributions: C.V., M.E.M., M.J.-K., M.M., T.R.C., P.J.M., and C.B. designed research; C.V., M.E.M., R.E.L., M.J.-K., A.L., L.G., and T.T. performed research; L.G. contributed new reagents/analytic tools; C.V. analyzed data; and C.V., M.E.M., P.J.M., and C.B. wrote the paper.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

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