Environmental drivers of increased ecosystem respiration in a warming tundra

S.L. Maes; J. Dietrich; G. Midolo; S. Schwieger; M. Kummu; V. Vandvik; R. Aerts; I.H.J. Althuizen; C. Biasi; R.G. Björk; H. Böhner; M. Carbognani; G. Chiari; C.T. Christiansen; K.E. Clemmensen; E.J. Cooper; J.H.C. Cornelissen; B. Elberling; P. Faubert; N. Fetcher; T.G.W. Forte; J. Gaudard; K. Gavazov; Z. Guan; J. Guðmundsson; R. Gya; S. Hallin; B.B. Hansen; S.V. Haugum; J.-S. He; C. Hicks Pries; M.J. Hovenden; M. Jalava; I.S. Jónsdóttir; J. Juhanson; J.Y. Jung; E. Kaarlejärvi; M.J. Kwon; R.E. Lamprecht; M. Le Moullec; H. Lee; M.E. Marushchak; A. Michelsen; T.M. Munir; E.M. Myrsky; C.S. Nielsen; M. Nyberg; J. Olofsson; H. Óskarsson; T.C. Parker; E.P. Pedersen; M. Petit Bon; A. Petraglia; K. Raundrup; N.M.R. Ravn; R. Rinnan; H. Rodenhizer; I. Ryde; N.M. Schmidt; E.A.G. Schuur; S. Sjögersten; S. Stark; M. Strack; J. Tang; A. Tolvanen; J.P. Töpper; M.K. Väisänen; R.S.P. van Logtestijn; C. Voigt; J. Walz; J.T. Weedon; Y. Yang; H. Ylänne; M.P. Björkman; J.M. Sarneel; E. Dorrepaal

doi:10.1038/s41586-024-07274-7

Environmental drivers of increased ecosystem respiration in a warming tundra

S.L. Maes, J. Dietrich, G. Midolo, S. Schwieger, M. Kummu, V. Vandvik, R. Aerts, I.H.J. Althuizen, C. Biasi, R.G. Björk, H. Böhner, M. Carbognani, G. Chiari, C.T. Christiansen, K.E. Clemmensen, E.J. Cooper, J.H.C. Cornelissen, B. Elberling, P. Faubert, N. FetcherT.G.W. Forte, J. Gaudard, K. Gavazov, Z. Guan, J. Guðmundsson, R. Gya, S. Hallin, B.B. Hansen, S.V. Haugum, J.-S. He, C. Hicks Pries, M.J. Hovenden, M. Jalava, I.S. Jónsdóttir, J. Juhanson, J.Y. Jung, E. Kaarlejärvi, M.J. Kwon, R.E. Lamprecht, M. Le Moullec, H. Lee, M.E. Marushchak, A. Michelsen, T.M. Munir, E.M. Myrsky, C.S. Nielsen, M. Nyberg, J. Olofsson, H. Óskarsson, T.C. Parker, E.P. Pedersen, M. Petit Bon, A. Petraglia, K. Raundrup, N.M.R. Ravn, R. Rinnan, H. Rodenhizer, I. Ryde, N.M. Schmidt, E.A.G. Schuur, S. Sjögersten, S. Stark, M. Strack, J. Tang, A. Tolvanen, J.P. Töpper, M.K. Väisänen, R.S.P. van Logtestijn, C. Voigt, J. Walz, J.T. Weedon, Y. Yang, H. Ylänne, M.P. Björkman, J.M. Sarneel, E. Dorrepaal

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

Arctic and alpine tundra ecosystems are large reservoirs of organic carbon1,2. Climate warming may stimulate ecosystem respiration and release carbon into the atmosphere3,4. The magnitude and persistency of this stimulation and the environmental mechanisms that drive its variation remain uncertain5–7. This hampers the accuracy of global land carbon–climate feedback projections7,8. Here we synthesize 136 datasets from 56 open-top chamber in situ warming experiments located at 28 arctic and alpine tundra sites which have been running for less than 1 year up to 25 years. We show that a mean rise of 1.4 °C [confidence interval (CI) 0.9–2.0 °C] in air and 0.4 °C [CI 0.2–0.7 °C] in soil temperature results in an increase in growing season ecosystem respiration by 30% [CI 22–38%] (n = 136). Our findings indicate that the stimulation of ecosystem respiration was due to increases in both plant-related and microbial respiration (n = 9) and continued for at least 25 years (n = 136). The magnitude of the warming effects on respiration was driven by variation in warming-induced changes in local soil conditions, that is, changes in total nitrogen concentration and pH and by context-dependent spatial variation in these conditions, in particular total nitrogen concentration and the carbon:nitrogen ratio. Tundra sites with stronger nitrogen limitations and sites in which warming had stimulated plant and microbial nutrient turnover seemed particularly sensitive in their respiration response to warming. The results highlight the importance of local soil conditions and warming-induced changes therein for future climatic impacts on respiration.

Original language	English
Pages (from-to)	105-113
Journal	Nature
Volume	629
Issue number	8010
DOIs	https://doi.org/10.1038/s41586-024-07274-7
Publication status	Published - 2 May 2024

Funding

We wish to thank the Abisko Scientific Research Station for hospitality and logistic support. For feedback on the statistical analyses, we are grateful to the R-sig-meta-analysis mailing list. We also wish to acknowledge CSC\u2014IT Center for Science, Finland, for computational resources and the many students and field assistants involved in the monitoring, measurements and sample processing at the tundra sites over the decades of data collection included in this study. Thank you to U. Molau and O. Khitoun for data contribution from the SWE_12, 14, 15 sites and to Dries VDL for permanent support. We acknowledge that some of the fieldwork has been conducted on traditional lands. We deeply regret the passing of J. Tang, one of our co-authors, during the writing of the manuscript and wish to highlight the fundamental contributions he has made as an ecosystem ecologist to the field of carbon cycle science. During the preparation of the manuscript, S.L.M. was funded by the Flemish Research Foundation (FWO grant no. 12ZZV21N) and E.D. was funded by the Swedish Research Council VR (grant no. 2018-04004) and Knut and Alice Wallenberg Foundation (grant no. KAW 2020.0126). We also want to thank the following funding agencies for support in field- or laboratory-work or salaries as part of the in situ data collection and data synthesis: Climate Impact Research Centre, European Research Council (grant no. 819202 awarded to M.K. and grant no. 77102 to I.R.), Academy of Finland (grant nos. N-PERM 341348 to C.B., THAW-N 349503 and ACCC 337550 to M.E.M., and no. 347188 to E.K.), the \u00D6sterreichischer Wissenschaftsfonds FWF (Lise Meitner grant no M-3335 to C.B.), the Research Council of Finland\u2019s Flagship Programme under project Digital Waters (grant no. 359248 to M.K.), European Commission Directorate-General for Research (grant no. EVK2-2001-00235 to E.J.C. and grant no. 771012 to R.R.), Danish National Research Foundation (grant no. CENPERM DNRF 100 awarded to B.E. and A.M. and C.S.N.), National Science Foundation of United States (grant nos. PLR 1418010 to N.F., PLR 1417763 to T.C.P. and ANS-2113641 supported M. Petit Bon), Norwegian Research Council (FRIMEDBIO grant no. 274712 to J.G. and J.P.T. and V.V., grant no. 274712 to R.G. and S.V.H., grant nos. 276080 and 343398 to B.B.H., grant no. SFF-III 223257 to Norwegian University of Science and Technology to M.L.M., grant nos. FEEDBACK, 250740 and EMERALD, 294948 to H.L. and Arctic Field grant no. 269957 to M. Petit Bon), Greenland Ecosystem Monitoring funds to K.R., ARCUM, Stiftelsen Ymer-80 and SNSF (grant no. PZ00P2_174047 to K.G.), Swedish Research Council FORMAS (grant nos. 2013-655 to S.H. and 2021-02449 to J.M.S.), Alberta Innovates Technology Futures and Canada Research Chairs programme to M.S., Australian Research Council Discovery Projects (grant no. DP220100915 to M.J.H.), Icelandic Research Fund (to I.S.J.), National Research Foundation of Korea (grant nos. NRF-2021M1A5A1075508 and KOPRI-PN22012 to J.Y.J.), Svalbard Environmental Protection Fund (grant no. 15/128 to M. Petit Bon and grant no. 16/113 to B.B.H.), Danish Environmental Protection Agency (for funding N.M.S.), Academy of Finland (grant no. MUFFIN 332196 to C.V.), Maj and Tor Nessling Foundation (for funding H.Y.), Maaja vesitekniikan tukiry (to M.J.), European Union\u2019s Horizon 2020 research and innovation programme under the Marie Sk\u0142odowska-Curie agreement (grant no. 657627 to M.P. Bj\u00F6rkman), FORMAS Swedish Research Council for Sustainable Development (for funding M.P. Bj\u00F6rkman), Climate-ecological Observatory for Arctic Tundra-COAT and UNIS (logistical support for fieldwork M.L.M. and B.B.H.). The strategic research environment BECC\u2014Biodiversity and Ecosystem Services in a Changing Climate (to M. P. Bj\u00F6rkman) and for funding T.S., we thank the US Department of Energy, Office of Biological and Environmental Research (Terrestrial Ecosystem Science Program nos. DE-SC0006982, DE-SC0014085 and DE-SC0020227 and the Permafrost Carbon Network (NSF project nos. 1331083 and 1931333).

Funders	Funder number
Alberta Innovates Technology Futures and Canada Research Chairs
BECC
Permafrost Carbon Network
ARCUM
Biodiversity and Ecosystem services in a Changing Climate
Danmarks Grundforskningsfond
Horizon 2020 Framework Programme
FORMAS Swedish Research Council for Sustainable Development
U.S. Department of Energy
Icelandic Centre for Research
Maj ja Tor Nesslingin Säätiö
Universitetssenteret på Svalbard
Austrian Science Fund	M-3335
Austrian Science Fund
Research Council of Finland	THAW-N 349503, 359248, 347188, N-PERM 341348, ACCC 337550
Research Council of Finland
Fonds Wetenschappelijk Onderzoek	12ZZV21N
Fonds Wetenschappelijk Onderzoek
National Science Foundation	1331083, 1931333
National Science Foundation
National Research Foundation of Korea	KOPRI-PN22012, NRF-2021M1A5A1075508
National Research Foundation of Korea
Marie Skłodowska-Curie agreement	657627
European Research Council	77102, 819202
European Research Council
Biological and Environmental Research	DE-SC0014085, DE-SC0020227, DE-SC0006982
Biological and Environmental Research
Norges Teknisk-Naturvitenskapelige Universitet	250740
Norges Teknisk-Naturvitenskapelige Universitet
Svalbard Environmental Protection Fund	15/128, 16/113
Emerald Publishing	269957, 294948
Emerald Publishing
European Commission Directorate-General for Research	EVK2-2001-00235, 771012
Knut och Alice Wallenbergs Stiftelse	KAW 2020.0126
Knut och Alice Wallenbergs Stiftelse
Norges forskningsråd	276080, 274712, 343398, SFF-III 223257
Norges forskningsråd
Svenska Forskningsrådet Formas	2021-02449, 2013-655
Svenska Forskningsrådet Formas
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung	PZ00P2_174047
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
Miljøstyrelsen	MUFFIN 332196
Miljøstyrelsen
Swedish Research Council VR	2018-04004
Australian Research Council	DP220100915
Australian Research Council
National Science Foundation of United States	PLR 1417763, PLR 1418010, ANS-2113641

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Maes, S. L., Dietrich, J., Midolo, G., Schwieger, S., Kummu, M., Vandvik, V., Aerts, R., Althuizen, I. H. J., Biasi, C., Björk, R. G., Böhner, H., Carbognani, M., Chiari, G., Christiansen, C. T., Clemmensen, K. E., Cooper, E. J., Cornelissen, J. H. C., Elberling, B., Faubert, P., ... Dorrepaal, E. (2024). Environmental drivers of increased ecosystem respiration in a warming tundra. Nature, 629(8010), 105-113. https://doi.org/10.1038/s41586-024-07274-7

@article{bd85e6672a124ffeb92f493dae4d654e,

title = "Environmental drivers of increased ecosystem respiration in a warming tundra",

abstract = "Arctic and alpine tundra ecosystems are large reservoirs of organic carbon1,2. Climate warming may stimulate ecosystem respiration and release carbon into the atmosphere3,4. The magnitude and persistency of this stimulation and the environmental mechanisms that drive its variation remain uncertain5–7. This hampers the accuracy of global land carbon–climate feedback projections7,8. Here we synthesize 136 datasets from 56 open-top chamber in situ warming experiments located at 28 arctic and alpine tundra sites which have been running for less than 1 year up to 25 years. We show that a mean rise of 1.4 °C [confidence interval (CI) 0.9–2.0 °C] in air and 0.4 °C [CI 0.2–0.7 °C] in soil temperature results in an increase in growing season ecosystem respiration by 30% [CI 22–38%] (n = 136). Our findings indicate that the stimulation of ecosystem respiration was due to increases in both plant-related and microbial respiration (n = 9) and continued for at least 25 years (n = 136). The magnitude of the warming effects on respiration was driven by variation in warming-induced changes in local soil conditions, that is, changes in total nitrogen concentration and pH and by context-dependent spatial variation in these conditions, in particular total nitrogen concentration and the carbon:nitrogen ratio. Tundra sites with stronger nitrogen limitations and sites in which warming had stimulated plant and microbial nutrient turnover seemed particularly sensitive in their respiration response to warming. The results highlight the importance of local soil conditions and warming-induced changes therein for future climatic impacts on respiration.",

author = "S.L. Maes and J. Dietrich and G. Midolo and S. Schwieger and M. Kummu and V. Vandvik and R. Aerts and I.H.J. Althuizen and C. Biasi and R.G. Bj{\"o}rk and H. B{\"o}hner and M. Carbognani and G. Chiari and C.T. Christiansen and K.E. Clemmensen and E.J. Cooper and J.H.C. Cornelissen and B. Elberling and P. Faubert and N. Fetcher and T.G.W. Forte and J. Gaudard and K. Gavazov and Z. Guan and J. Gu{\dh}mundsson and R. Gya and S. Hallin and B.B. Hansen and S.V. Haugum and J.-S. He and {Hicks Pries}, C. and M.J. Hovenden and M. Jalava and I.S. J{\'o}nsd{\'o}ttir and J. Juhanson and J.Y. Jung and E. Kaarlej{\"a}rvi and M.J. Kwon and R.E. Lamprecht and {Le Moullec}, M. and H. Lee and M.E. Marushchak and A. Michelsen and T.M. Munir and E.M. Myrsky and C.S. Nielsen and M. Nyberg and J. Olofsson and H. {\'O}skarsson and T.C. Parker and E.P. Pedersen and {Petit Bon}, M. and A. Petraglia and K. Raundrup and N.M.R. Ravn and R. Rinnan and H. Rodenhizer and I. Ryde and N.M. Schmidt and E.A.G. Schuur and S. Sj{\"o}gersten and S. Stark and M. Strack and J. Tang and A. Tolvanen and J.P. T{\"o}pper and M.K. V{\"a}is{\"a}nen and {van Logtestijn}, R.S.P. and C. Voigt and J. Walz and J.T. Weedon and Y. Yang and H. Yl{\"a}nne and M.P. Bj{\"o}rkman and J.M. Sarneel and E. Dorrepaal",

year = "2024",

month = may,

day = "2",

doi = "10.1038/s41586-024-07274-7",

language = "English",

volume = "629",

pages = "105--113",

journal = "Nature",

issn = "0028-0836",

publisher = "Nature Publishing Group",

number = "8010",

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Maes, SL, Dietrich, J, Midolo, G, Schwieger, S, Kummu, M, Vandvik, V, Aerts, R, Althuizen, IHJ, Biasi, C, Björk, RG, Böhner, H, Carbognani, M, Chiari, G, Christiansen, CT, Clemmensen, KE, Cooper, EJ, Cornelissen, JHC, Elberling, B, Faubert, P, Fetcher, N, Forte, TGW, Gaudard, J, Gavazov, K, Guan, Z, Guðmundsson, J, Gya, R, Hallin, S, Hansen, BB, Haugum, SV, He, J-S, Hicks Pries, C, Hovenden, MJ, Jalava, M, Jónsdóttir, IS, Juhanson, J, Jung, JY, Kaarlejärvi, E, Kwon, MJ, Lamprecht, RE, Le Moullec, M, Lee, H, Marushchak, ME, Michelsen, A, Munir, TM, Myrsky, EM, Nielsen, CS, Nyberg, M, Olofsson, J, Óskarsson, H, Parker, TC, Pedersen, EP, Petit Bon, M, Petraglia, A, Raundrup, K, Ravn, NMR, Rinnan, R, Rodenhizer, H, Ryde, I, Schmidt, NM, Schuur, EAG, Sjögersten, S, Stark, S, Strack, M, Tang, J, Tolvanen, A, Töpper, JP, Väisänen, MK, van Logtestijn, RSP, Voigt, C, Walz, J, Weedon, JT, Yang, Y, Ylänne, H, Björkman, MP, Sarneel, JM & Dorrepaal, E 2024, 'Environmental drivers of increased ecosystem respiration in a warming tundra', Nature, vol. 629, no. 8010, pp. 105-113. https://doi.org/10.1038/s41586-024-07274-7

TY - JOUR

T1 - Environmental drivers of increased ecosystem respiration in a warming tundra

AU - Maes, S.L.

AU - Dietrich, J.

AU - Midolo, G.

AU - Schwieger, S.

AU - Kummu, M.

AU - Vandvik, V.

AU - Aerts, R.

AU - Althuizen, I.H.J.

AU - Biasi, C.

AU - Björk, R.G.

AU - Böhner, H.

AU - Carbognani, M.

AU - Chiari, G.

AU - Christiansen, C.T.

AU - Clemmensen, K.E.

AU - Cooper, E.J.

AU - Cornelissen, J.H.C.

AU - Elberling, B.

AU - Faubert, P.

AU - Fetcher, N.

AU - Forte, T.G.W.

AU - Gaudard, J.

AU - Gavazov, K.

AU - Guan, Z.

AU - Guðmundsson, J.

AU - Gya, R.

AU - Hallin, S.

AU - Hansen, B.B.

AU - Haugum, S.V.

AU - He, J.-S.

AU - Hicks Pries, C.

AU - Hovenden, M.J.

AU - Jalava, M.

AU - Jónsdóttir, I.S.

AU - Juhanson, J.

AU - Jung, J.Y.

AU - Kaarlejärvi, E.

AU - Kwon, M.J.

AU - Lamprecht, R.E.

AU - Le Moullec, M.

AU - Lee, H.

AU - Marushchak, M.E.

AU - Michelsen, A.

AU - Munir, T.M.

AU - Myrsky, E.M.

AU - Nielsen, C.S.

AU - Nyberg, M.

AU - Olofsson, J.

AU - Óskarsson, H.

AU - Parker, T.C.

AU - Pedersen, E.P.

AU - Petit Bon, M.

AU - Petraglia, A.

AU - Raundrup, K.

AU - Ravn, N.M.R.

AU - Rinnan, R.

AU - Rodenhizer, H.

AU - Ryde, I.

AU - Schmidt, N.M.

AU - Schuur, E.A.G.

AU - Sjögersten, S.

AU - Stark, S.

AU - Strack, M.

AU - Tang, J.

AU - Tolvanen, A.

AU - Töpper, J.P.

AU - Väisänen, M.K.

AU - van Logtestijn, R.S.P.

AU - Voigt, C.

AU - Walz, J.

AU - Weedon, J.T.

AU - Yang, Y.

AU - Ylänne, H.

AU - Björkman, M.P.

AU - Sarneel, J.M.

AU - Dorrepaal, E.

PY - 2024/5/2

Y1 - 2024/5/2

N2 - Arctic and alpine tundra ecosystems are large reservoirs of organic carbon1,2. Climate warming may stimulate ecosystem respiration and release carbon into the atmosphere3,4. The magnitude and persistency of this stimulation and the environmental mechanisms that drive its variation remain uncertain5–7. This hampers the accuracy of global land carbon–climate feedback projections7,8. Here we synthesize 136 datasets from 56 open-top chamber in situ warming experiments located at 28 arctic and alpine tundra sites which have been running for less than 1 year up to 25 years. We show that a mean rise of 1.4 °C [confidence interval (CI) 0.9–2.0 °C] in air and 0.4 °C [CI 0.2–0.7 °C] in soil temperature results in an increase in growing season ecosystem respiration by 30% [CI 22–38%] (n = 136). Our findings indicate that the stimulation of ecosystem respiration was due to increases in both plant-related and microbial respiration (n = 9) and continued for at least 25 years (n = 136). The magnitude of the warming effects on respiration was driven by variation in warming-induced changes in local soil conditions, that is, changes in total nitrogen concentration and pH and by context-dependent spatial variation in these conditions, in particular total nitrogen concentration and the carbon:nitrogen ratio. Tundra sites with stronger nitrogen limitations and sites in which warming had stimulated plant and microbial nutrient turnover seemed particularly sensitive in their respiration response to warming. The results highlight the importance of local soil conditions and warming-induced changes therein for future climatic impacts on respiration.

AB - Arctic and alpine tundra ecosystems are large reservoirs of organic carbon1,2. Climate warming may stimulate ecosystem respiration and release carbon into the atmosphere3,4. The magnitude and persistency of this stimulation and the environmental mechanisms that drive its variation remain uncertain5–7. This hampers the accuracy of global land carbon–climate feedback projections7,8. Here we synthesize 136 datasets from 56 open-top chamber in situ warming experiments located at 28 arctic and alpine tundra sites which have been running for less than 1 year up to 25 years. We show that a mean rise of 1.4 °C [confidence interval (CI) 0.9–2.0 °C] in air and 0.4 °C [CI 0.2–0.7 °C] in soil temperature results in an increase in growing season ecosystem respiration by 30% [CI 22–38%] (n = 136). Our findings indicate that the stimulation of ecosystem respiration was due to increases in both plant-related and microbial respiration (n = 9) and continued for at least 25 years (n = 136). The magnitude of the warming effects on respiration was driven by variation in warming-induced changes in local soil conditions, that is, changes in total nitrogen concentration and pH and by context-dependent spatial variation in these conditions, in particular total nitrogen concentration and the carbon:nitrogen ratio. Tundra sites with stronger nitrogen limitations and sites in which warming had stimulated plant and microbial nutrient turnover seemed particularly sensitive in their respiration response to warming. The results highlight the importance of local soil conditions and warming-induced changes therein for future climatic impacts on respiration.

UR - http://www.scopus.com/inward/record.url?scp=85190691054&partnerID=8YFLogxK

U2 - 10.1038/s41586-024-07274-7

DO - 10.1038/s41586-024-07274-7

M3 - Article

SN - 0028-0836

VL - 629

SP - 105

EP - 113

JO - Nature

JF - Nature

IS - 8010

ER -

Environmental drivers of increased ecosystem respiration in a warming tundra

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