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

Walker, Tom W. N.; Janssens, Ivan A.; Weedon, James T.; Sigurdsson, Bjarni D.; Richter, Andreas; Peñuelas, Josep; Leblans, Niki I. W.; Bahn, Michael; Bartrons, Mireia; De Jonge, Cindy; Fuchslueger, Lucia; Gargallo-Garriga, Albert; Gunnarsdóttir, Gunnhildur E.; Marañón-Jiménez, Sara; Oddsdóttir, Edda S.; Ostonen, Ivika; Poeplau, Christopher; Prommer, Judith; Radujković, Dajana; Sardans, Jordi; Sigurðsson, Páll; Soong, Jennifer L.; Vicca, Sara; Wallander, Håkan; Ilieva-Makulec, Krassimira; Verbruggen, Erik

doi:10.1038/s41559-019-1055-3

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

Abstract

Temperature governs most biotic processes, yet we know little about how warming affects whole ecosystems. In this research, 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.

Authors:

^[1];

^[2];

^[3];

^[4];

^[5];

^[6]; Leblans, Niki I. W. ^[7]; Bahn, Michael ^[8];

^[9];

^[2];

^[10]; Gargallo-Garriga, Albert ^[11]; Gunnarsdóttir, Gunnhildur E. ^[12];

^[13];

^[14];

^[15];

^[16];

^[17];

^[2]; Sardans, Jordi ^[6] more »

Eidgenoessische Technische Hochschule, Zurich (Switzerland). Inst. for Integrative Biology; Univ. de Lausanne (Switzerland). Dept. of Ecology & Evolution
Univ. of Antwerp, Wilrijk (Belgium). Dept. of Biology
Vrije Univ., Amsterdam (Netherlands). Dept. of Ecological Sciences
Agricultural Univ. of Iceland, Borgarnes (Iceland)
Univ. of Vienna (Austria). Dept. of Microbiology and Ecosystem Science; International Inst. for Applied Systems Analysis, Laxenberg (Austria). Ecosystems Services and Management Program
CREAF-CSIC-UAB, Bellaterra (Spain). CSIC Global Ecology Unit; CREAF, Cerdanoyla del Valles (Spain)
Univ. of Antwerp, Wilrijk (Belgium). Dept. of Biology; Agricultural Univ. of Iceland, Borgarnes (Iceland)
Univ. of Innsbruck (Austria). Dept. of Ecology
CREAF-CSIC-UAB, Bellaterra (Spain). CSIC Global Ecology Unit; Univ. of Vic-Central Univ. of Catalonia, Vic (Spain). Aquatic Ecology Group
Univ. of Antwerp, Wilrijk (Belgium). Dept. of Biology; Univ. of Vienna (Austria). Dept. of Microbiology and Ecosystem Science
CREAF-CSIC-UAB, Bellaterra (Spain). CSIC Global Ecology Unit; CREAF, Cerdanoyla del Valles (Spain); Global Change Research Inst., Brno (Czech Republic)
Agricultural Univ. of Iceland, Borgarnes (Iceland); Soil Conservation Service of Iceland, Hella (Iceland)
Univ. of Antwerp, Wilrijk (Belgium). Dept. of Biology; CREAF-CSIC-UAB, Bellaterra (Spain). CSIC Global Ecology Unit; CREAF, Cerdanoyla del Valles (Spain)
Icelandic Forest Research, Reykjavík (Iceland)
Univ. of Tartu (Estonia). Inst. of Ecology and Earth Sciences
Thünen Inst. of Climate-Smart Agriculture, Braunschweig (Germany)
Univ. of Vienna (Austria). Dept. of Microbiology and Ecosystem Science
Univ. of Antwerp, Wilrijk (Belgium). Dept. of Biology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Climate and Ecosystem Science Division
Lund Univ. (Sweden). Dept. of Biology
Cardinal St. Wyszynski Univ., Warsaw (Poland). Inst. of Ecology & Bioethics

Publication Date:: Mon Dec 09 00:00:00 EST 2019

Research Org.:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Biological and Environmental Research (BER); Swiss National Science Foundation (SNSF); European Research Council (ERC); Research Foundation - Flanders (FWO); Austrian Science Fund (FWF); European Union (EU); Flanders Research Foundation Aspiration Grant; Spanish Government; Catalan Government; Icelandic Research Fund; JPI Climate Project

OSTI Identifier:: 1631625

Grant/Contract Number:: AC02-05CH11231; 31003A-176044; ERC-2013-SyG-610028-IMBALANCE-P; FWO-G0F2217N; FWF-I-3237; COFUND-291780; 676108; 11G1613N; CGL2016-79835-P; SGR-2017-1005; PRO2008-SO2-PENUELAS; 163272-053-FORHOT-FOREST; BMWFW-6.020/0008

Resource Type:: Accepted Manuscript

Journal Name:: Nature Ecology and Evolution

Additional Journal Information:: Journal Volume: 4; Journal Issue: 1; Journal ID: ISSN 2397-334X

Publisher:: Nature Publishing Group

Country of Publication:: United States

Language:: English

Subject:: 54 ENVIRONMENTAL SCIENCES; climate-change ecology; ecology; ecosystem ecology

Citation Formats


                    Walker, Tom W. N., Janssens, Ivan A., Weedon, James T., Sigurdsson, Bjarni D., Richter, Andreas, Peñuelas, Josep, Leblans, Niki I. W., Bahn, Michael, Bartrons, Mireia, De Jonge, Cindy, Fuchslueger, Lucia, Gargallo-Garriga, Albert, Gunnarsdóttir, Gunnhildur E., Marañón-Jiménez, Sara, Oddsdóttir, Edda S., Ostonen, Ivika, Poeplau, Christopher, Prommer, Judith, Radujković, Dajana, Sardans, Jordi, Sigurðsson, Páll, Soong, Jennifer L., Vicca, Sara, Wallander, Håkan, Ilieva-Makulec, Krassimira, and Verbruggen, Erik. A systemic overreaction to years versus decades of warming in a subarctic grassland ecosystem.  United States: N. p., 2019. 
Web.  doi:10.1038/s41559-019-1055-3.

Copy to clipboard


                    Walker, Tom W. N., Janssens, Ivan A., Weedon, James T., Sigurdsson, Bjarni D., Richter, Andreas, Peñuelas, Josep, Leblans, Niki I. W., Bahn, Michael, Bartrons, Mireia, De Jonge, Cindy, Fuchslueger, Lucia, Gargallo-Garriga, Albert, Gunnarsdóttir, Gunnhildur E., Marañón-Jiménez, Sara, Oddsdóttir, Edda S., Ostonen, Ivika, Poeplau, Christopher, Prommer, Judith, Radujković, Dajana, Sardans, Jordi, Sigurðsson, Páll, Soong, Jennifer L., Vicca, Sara, Wallander, Håkan, Ilieva-Makulec, Krassimira, & Verbruggen, Erik. A systemic overreaction to years versus decades of warming in a subarctic grassland ecosystem.  United States.  https://doi.org/10.1038/s41559-019-1055-3

Copy to clipboard


                    Walker, Tom W. N., Janssens, Ivan A., Weedon, James T., Sigurdsson, Bjarni D., Richter, Andreas, Peñuelas, Josep, Leblans, Niki I. W., Bahn, Michael, Bartrons, Mireia, De Jonge, Cindy, Fuchslueger, Lucia, Gargallo-Garriga, Albert, Gunnarsdóttir, Gunnhildur E., Marañón-Jiménez, Sara, Oddsdóttir, Edda S., Ostonen, Ivika, Poeplau, Christopher, Prommer, Judith, Radujković, Dajana, Sardans, Jordi, Sigurðsson, Páll, Soong, Jennifer L., Vicca, Sara, Wallander, Håkan, Ilieva-Makulec, Krassimira, and Verbruggen, Erik. Mon .  
"A systemic overreaction to years versus decades of warming in a subarctic grassland ecosystem".  United States.  https://doi.org/10.1038/s41559-019-1055-3.  https://www.osti.gov/servlets/purl/1631625.

Copy to clipboard


                    
@article{osti_1631625,

  title        = {A systemic overreaction to years versus decades of warming in a subarctic grassland ecosystem},

  author       = {Walker, Tom W. N. and Janssens, Ivan A. and Weedon, James T. and Sigurdsson, Bjarni D. and Richter, Andreas and Peñuelas, Josep and Leblans, Niki I. W. and Bahn, Michael and Bartrons, Mireia and De Jonge, Cindy and Fuchslueger, Lucia and Gargallo-Garriga, Albert and Gunnarsdóttir, Gunnhildur E. and Marañón-Jiménez, Sara and Oddsdóttir, Edda S. and Ostonen, Ivika and Poeplau, Christopher and Prommer, Judith and Radujković, Dajana and Sardans, Jordi and Sigurðsson, Páll and Soong, Jennifer L. and Vicca, Sara and Wallander, Håkan and Ilieva-Makulec, Krassimira and Verbruggen, Erik},

  abstractNote = {Temperature governs most biotic processes, yet we know little about how warming affects whole ecosystems. In this research, 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.},

  doi          = {10.1038/s41559-019-1055-3},

  journal      = {Nature Ecology and Evolution},

  number       = 1,

  volume       = 4,

  place        = {United States},

  year         = {Mon Dec 09 00:00:00 EST 2019},

  month        = {Mon Dec 09 00:00:00 EST 2019}

}

Copy to clipboard

Journal Article:

Free Publicly Available Full Text

Accepted Manuscript (DOE)

Publisher's Version of Record

https://doi.org/10.1038/s41559-019-1055-3

Other availability

Search WorldCat to find libraries that may hold this journal

Citation Metrics:

Cited by: 25 works

Citation information provided by
Web of Science

Save / Share:

Export Metadata

Save to My Library

Works referenced in this record:

Ambient changes exceed treatment effects on plant species abundance in global change experiments
journal, October 2018

Langley, J. Adam; Chapman, Samantha K.; La Pierre, Kimberly J.
Global Change Biology, Vol. 24, Issue 12
DOI: 10.1111/gcb.14442

Microbial temperature sensitivity and biomass change explain soil carbon loss with warming
journal, September 2018

Walker, Tom W. N.; Kaiser, Christina; Strasser, Florian
Nature Climate Change, Vol. 8, Issue 10
DOI: 10.1038/s41558-018-0259-x

A 3,000-year lag between the geological and ecological shutdown of Florida's coral reefs
journal, August 2018

Toth, Lauren T.; Kuffner, Ilsa B.; Stathakopoulos, Anastasios
Global Change Biology, Vol. 24, Issue 11
DOI: 10.1111/gcb.14389

Warming-related increases in soil CO2 efflux are explained by increased below-ground carbon flux
journal, July 2014

Giardina, Christian P.; Litton, Creighton M.; Crow, Susan E.
Nature Climate Change, Vol. 4, Issue 9
DOI: 10.1038/nclimate2322

Biodiversity increases and decreases ecosystem stability
journal, October 2018

Pennekamp, Frank; Pontarp, Mikael; Tabi, Andrea
Nature, Vol. 563, Issue 7729
DOI: 10.1038/s41586-018-0627-8

Novel competitors shape species’ responses to climate change
journal, September 2015

Alexander, Jake M.; Diez, Jeffrey M.; Levine, Jonathan M.
Nature, Vol. 525, Issue 7570
DOI: 10.1038/nature14952

Plant Species Richness and Ecosystem Multifunctionality in Global Drylands
journal, January 2012

Maestre, F. T.; Quero, J. L.; Gotelli, N. J.
Science, Vol. 335, Issue 6065
DOI: 10.1126/science.1215442

Sensitivity of soil carbon fractions and their specific stabilization mechanisms to extreme soil warming in a subarctic grassland
journal, September 2016

Poeplau, Christopher; Kätterer, Thomas; Leblans, Niki I. W.
Global Change Biology, Vol. 23, Issue 3
DOI: 10.1111/gcb.13491

A meta-analysis of responses of soil biota to global change
journal, January 2011

Blankinship, Joseph C.; Niklaus, Pascal A.; Hungate, Bruce A.
Oecologia, Vol. 165, Issue 3
DOI: 10.1007/s00442-011-1909-0

The whole-soil carbon flux in response to warming
journal, March 2017

Hicks Pries, Caitlin E.; Castanha, C.; Porras, R. C.
Science, Vol. 355, Issue 6332
DOI: 10.1126/science.aal1319

Impact of Soil Warming on the Plant Metabolome of Icelandic Grasslands
journal, August 2017

Gargallo-Garriga, Albert; Ayala-Roque, Marta; Sardans, Jordi
Metabolites, Vol. 7, Issue 3
DOI: 10.3390/metabo7030044

Catastrophic shifts in ecosystems
journal, October 2001

Scheffer, Marten; Carpenter, Steve; Foley, Jonathan A.
Nature, Vol. 413, Issue 6856
DOI: 10.1038/35098000

Geothermal ecosystems as natural climate change experiments: The ForHot research site in Iceland as a case study
journal, January 2016

Sigurdsson, Bjarni D.; Leblans, Niki I. W.; Dauwe, Steven
Icelandic Agricultural Sciences, Vol. 29
DOI: 10.16886/IAS.2016.05

Plastic and genetic responses of a common sedge to warming have contrasting effects on carbon cycle processes
journal, November 2018

Walker, Tom W. N.; Weckwerth, Wolfram; Bragazza, Luca
Ecology Letters, Vol. 22, Issue 1
DOI: 10.1111/ele.13178

Extinction risk from climate change
journal, January 2004

Thomas, Chris D.; Cameron, Alison; Green, Rhys E.
Nature, Vol. 427, Issue 6970
DOI: 10.1038/nature02121

Shifts in Arctic vegetation and associated feedbacks under climate change
journal, March 2013

Pearson, Richard G.; Phillips, Steven J.; Loranty, Michael M.
Nature Climate Change, Vol. 3, Issue 7
DOI: 10.1038/nclimate1858

Phenological responses of Icelandic subarctic grasslands to short-term and long-term natural soil warming
journal, June 2017

Leblans, Niki I. W.; Sigurdsson, Bjarni D.; Vicca, Sara
Global Change Biology, Vol. 23, Issue 11
DOI: 10.1111/gcb.13749

Biodiversity and ecosystem stability in a decade-long grassland experiment
journal, June 2006

Tilman, David; Reich, Peter B.; Knops, Johannes M. H.
Nature, Vol. 441, Issue 7093
DOI: 10.1038/nature04742

Land use alters the resistance and resilience of soil food webs to drought
journal, January 2012

de Vries, Franciska T.; Liiri, Mira E.; Bjørnlund, Lisa
Nature Climate Change, Vol. 2, Issue 4
DOI: 10.1038/nclimate1368

Quantifying global soil carbon losses in response to warming
journal, November 2016

Crowther, T. W.; Todd-Brown, K. E. O.; Rowe, C. W.
Nature, Vol. 540, Issue 7631
DOI: 10.1038/nature20150

Hierarchical responses of plant-soil interactions to climate change: consequences for the global carbon cycle
journal, February 2013

Bardgett, Richard D.; Manning, Pete; Morriën, Elly
Journal of Ecology, Vol. 101, Issue 2
DOI: 10.1111/1365-2745.12043

Changes in plant community composition lag behind climate warming in lowland forests
journal, October 2011

Bertrand, Romain; Lenoir, Jonathan; Piedallu, Christian
Nature, Vol. 479, Issue 7374
DOI: 10.1038/nature10548

Temperature response of soil respiration largely unaltered with experimental warming
journal, November 2016

Carey, Joanna C.; Tang, Jianwu; Templer, Pamela H.
Proceedings of the National Academy of Sciences, Vol. 113, Issue 48
DOI: 10.1073/pnas.1605365113

Biogeochemical plant–soil microbe feedback in response to climate warming in peatlands
journal, December 2012

Bragazza, Luca; Parisod, Julien; Buttler, Alexandre
Nature Climate Change, Vol. 3, Issue 3
DOI: 10.1038/nclimate1781

On the Sensitivity of Field Reconstruction and Prediction Using Empirical Orthogonal Functions Derived from Gappy Data
journal, October 2013

Taylor, Marc H.; Losch, Martin; Wenzel, Manfred
Journal of Climate, Vol. 26, Issue 22
DOI: 10.1175/JCLI-D-13-00089.1

A framework for assessing ecosystem dynamics in response to chronic resource alterations induced by global change
journal, December 2009

Smith, Melinda D.; Knapp, Alan K.; Collins, Scott L.
Ecology, Vol. 90, Issue 12
DOI: 10.1890/08-1815.1

Phenology Feedbacks on Climate Change
journal, May 2009

Penuelas, J.; Rutishauser, T.; Filella, I.
Science, Vol. 324, Issue 5929
DOI: 10.1126/science.1173004

Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world
journal, October 2017

Melillo, J. M.; Frey, S. D.; DeAngelis, K. M.
Science, Vol. 358, Issue 6359
DOI: 10.1126/science.aan2874

Shifts in the dynamics of productivity signal ecosystem state transitions at the biome-scale
journal, July 2018

Hu, Zhongmin; Guo, Qun; Li, Shenggong
Ecology Letters, Vol. 21, Issue 10
DOI: 10.1111/ele.13126

Geothermally warmed soils reveal persistent increases in the respiratory costs of soil microbes contributing to substantial C losses
journal, April 2018

Marañón-Jiménez, S.; Soong, J. L.; Leblans, N. I. W.
Biogeochemistry, Vol. 138, Issue 3
DOI: 10.1007/s10533-018-0443-0

On the sensitivity of field reconstruction and prediction using Empirical Orthogonal Functions derived from gappy data
text, January 2013

Taylor, Marc; Losch, Martin; Wenzel, Manfred
figshare
DOI: 10.6084/m9.figshare.732650.v3

Plastic and genetic responses of a common sedge to warming have contrasting effects on carbon cycle processes
text, January 2019

Walker, Tom W. N.; Weckwerth, Wolfram; Bragazza, Luca
ETH Zurich
DOI: 10.3929/ethz-b-000389378

Biodiversity increases and decreases ecosystem stability
text, January 2018

Pennekamp, Frank; Pontarp, Mikael; Tabi, Andrea
Nature Publishing Group
DOI: 10.5167/uzh-164959

On the sensitivity of field reconstruction and prediction using Empirical Orthogonal Functions derived from gappy data
text, January 2013

Taylor, Marc; Losch, Martin; Wenzel, Manfred
figshare
DOI: 10.6084/m9.figshare.732650

Phenology Feedbacks on Climate Change
text, January 2009

Peñuelas, Josep; Rutishauser, This; Filella, Iollanda
American Association for the Advancement of Science
DOI: 10.7892/boris.36392

Extinction risk from climate change
journal, January 2004

Thomas, Chris D.; Cameron, Alison; Green, Rhys E.
Nature, Vol. 427, Issue 6970
DOI: 10.1038/nature02121

Microbial temperature sensitivity and biomass change explain soil carbon loss with warming
journal, September 2018

Walker, Tom W. N.; Kaiser, Christina; Strasser, Florian
Nature Climate Change, Vol. 8, Issue 10
DOI: 10.1038/s41558-018-0259-x

Prolonged exposure does not increase soil microbial community compositional response to warming along geothermal gradients
journal, December 2017

Radujković, Dajana; Verbruggen, Erik; Sigurdsson, Bjarni D.
FEMS Microbiology Ecology, Vol. 94, Issue 2
DOI: 10.1093/femsec/fix174

Hierarchical responses of plant-soil interactions to climate change: consequences for the global carbon cycle
journal, February 2013

Bardgett, Richard D.; Manning, Pete; Morriën, Elly
Journal of Ecology, Vol. 101, Issue 2
DOI: 10.1111/1365-2745.12043

Plastic and genetic responses of a common sedge to warming have contrasting effects on carbon cycle processes
journal, November 2018

Walker, Tom W. N.; Weckwerth, Wolfram; Bragazza, Luca
Ecology Letters, Vol. 22, Issue 1
DOI: 10.1111/ele.13178

Sensitivity of soil carbon fractions and their specific stabilization mechanisms to extreme soil warming in a subarctic grassland
journal, September 2016

Poeplau, Christopher; Kätterer, Thomas; Leblans, Niki I. W.
Global Change Biology, Vol. 23, Issue 3
DOI: 10.1111/gcb.13491

Phenological responses of Icelandic subarctic grasslands to short-term and long-term natural soil warming
journal, June 2017

Leblans, Niki I. W.; Sigurdsson, Bjarni D.; Vicca, Sara
Global Change Biology, Vol. 23, Issue 11
DOI: 10.1111/gcb.13749

Impact of Soil Warming on the Plant Metabolome of Icelandic Grasslands
journal, August 2017

Gargallo-Garriga, Albert; Ayala-Roque, Marta; Sardans, Jordi
Metabolites, Vol. 7, Issue 3
DOI: 10.3390/metabo7030044