Environmental drivers of increased ecosystem respiration in a warming tundra.

Item request has been placed! ×
Item request cannot be made. ×
loading   Processing Request
  • Additional Information
    • Source:
      Publisher: Nature Publishing Group Country of Publication: England NLM ID: 0410462 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1476-4687 (Electronic) Linking ISSN: 00280836 NLM ISO Abbreviation: Nature Subsets: MEDLINE
    • Publication Information:
      Publication: Basingstoke : Nature Publishing Group
      Original Publication: London, Macmillan Journals ltd.
    • Subject Terms:
    • Abstract:
      Arctic and alpine tundra ecosystems are large reservoirs of organic carbon 1,2 . Climate warming may stimulate ecosystem respiration and release carbon into the atmosphere 3,4 . The magnitude and persistency of this stimulation and the environmental mechanisms that drive its variation remain uncertain 5-7 . This hampers the accuracy of global land carbon-climate feedback projections 7,8 . 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.
      (© 2024. The Author(s).)
    • References:
      Schuur, E. A. G. et al. Permafrost and climate change: carbon cycle feedbacks from the warming arctic. Annu. Rev. Environ. Resour. 47, 343–371 (2022). (PMID: 10.1146/annurev-environ-012220-011847)
      Tarnocai, C. et al. Soil organic carbon pools in the northern circumpolar permafrost region. Glob. Biogeochem. Cycles https://doi.org/10.1029/2008GB003327 (2009).
      Virkkala, A.-M. et al. Statistical upscaling of ecosystem CO 2 fluxes across the terrestrial tundra and boreal domain: regional patterns and uncertainties. Glob. Change Biol. 27, 4040–4059 (2021). (PMID: 10.1111/gcb.15659)
      Karhu, K. Temperature sensitivity of soil respiration rates enhanced by microbial community response. Nature 513, 81–83 (2014). (PMID: 2518690210.1038/nature13604)
      Rustad, L. E. et al. A meta-analysis of the response of soil respiration, net nitrogen mineralization and aboveground plant growth to experimental ecosystem warming. Oecologia 126, 543–562 (2001). (PMID: 2854724010.1007/s004420000544)
      Carey, J. C. et al. Temperature response of soil respiration largely unaltered with experimental warming. Proc. Natl Acad. Sci. USA 113, 13797–13802 (2016). (PMID: 27849609513776310.1073/pnas.1605365113)
      Bouskill, N. J., Riley, W. J. & Grant, R. F. Alaskan carbon–climate feedbacks will be weaker than inferred from short-term experiments. Nat. Commun. 11, 5798 (2020).
      Schadel, C. et al. Divergent patterns of experimental and model-derived permafrost ecosystem carbon dynamics in response to Arctic warming. Environ. Res. Lett. 13, 105002 (2018). (PMID: 10.1088/1748-9326/aae0ff)
      Lu, M. et al. Responses of ecosystem carbon cycle to experimental warming: a meta-analysis. Ecology 94, 726–738 (2013). (PMID: 2368789810.1890/12-0279.1)
      Natali, S. M. et al. Large loss of CO 2 in winter observed across the northern permafrost region. Nat. Clim. Change 9, 852–857 (2019). (PMID: 10.1038/s41558-019-0592-8)
      Oberbauer, S. F. et al. Tundra CO 2 fluxes in response to experimental warming across latitudinal and moisture gradients. Ecol. Monogr. 77, 221–238 (2007). (PMID: 10.1890/06-0649)
      Schuur, E. A. G. et al. Vulnerability of permafrost carbon to climate change: Implications for the global carbon cycle. Bioscience 58, 701–714 (2008). (PMID: 10.1641/B580807)
      Bond-Lamberty, B., Wang, C. & Gower, S. T. A global relationship between the heterotrophic and autotrophic components of soil respiration? Glob. Change Biol. 10, 1756–1766 (2004). (PMID: 10.1111/j.1365-2486.2004.00816.x)
      Arctic Climate Change Update 2021: Key Trends and Impacts. Summary for Policy-makers (AMAP, 2021).
      Rantanen, M. et al. The Arctic has warmed nearly four times faster than the globe since 1979. Commun. Earth Environ. 3, 168 (2022). (PMID: 10.1038/s43247-022-00498-3)
      Bouskill, N. J., Riley, W. J. & Tang, J. Y. Meta-analysis of high-latitude nitrogen-addition and warming studies implies ecological mechanisms overlooked by land models. Biogeosciences 11, 6969–6983 (2014). (PMID: 10.5194/bg-11-6969-2014)
      van Gestel, N. et al. Predicting soil carbon loss with warming. Nature 554, E4–E5 (2018). (PMID: 2946909810.1038/nature25745)
      Hicks Pries, C. E. et al. Decadal warming causes a consistent and persistent shift from heterotrophic to autotrophic respiration in contrasting permafrost ecosystems. Glob. Change Biol. 21, 4508–4519 (2015). (PMID: 10.1111/gcb.13032)
      Dorrepaal, E. et al. Carbon respiration from subsurface peat accelerated by climate warming in the subarctic. Nature 460, 616–619 (2009). (PMID: 10.1038/nature08216)
      Natali, S. M. et al. Effects of experimental warming of air, soil and permafrost on carbon balance in Alaskan tundra. Glob. Change Biol. 17, 1394–1407 (2011). (PMID: 10.1111/j.1365-2486.2010.02303.x)
      Romero-Olivares, A. L., Allison, S. D. & Treseder, K. K. Soil microbes and their response to experimental warming over time: a meta-analysis of field studies. Soil Biol. Biochem. 107, 32–40 (2017). (PMID: 10.1016/j.soilbio.2016.12.026)
      Wang, X. et al. Soil respiration under climate warming: differential response of heterotrophic and autotrophic respiration. Glob. Change Biol. 20, 3229–3237 (2014). (PMID: 10.1111/gcb.12620)
      Shaver, G. R. et al. Global warming and terrestrial ecosystems: a conceptual framework for analysis: ecosystem responses to global warming will be complex and varied. Bioscience 50, 871–882 (2000). (PMID: 10.1641/0006-3568(2000)050[0871:GWATEA]2.0.CO;2)
      Christiansen, C. T. et al. Enhanced summer warming reduces fungal decomposer diversity and litter mass loss more strongly in dry than in wet tundra. Glob. Change Biol. 23, 406–420 (2017). (PMID: 10.1111/gcb.13362)
      Scharn, R., Little, C. J., Bacon, C. D., Alatalo, J. M. & Antonelli, A. Decreased soil moisture due to warming drives phylogenetic diversity and community transitions in the tundra. Environ. Res. Lett. 16, 064031 (2021).
      Schuur, E. A. G. et al. Climate change and the permafrost carbon feedback. Nature 520, 171–179 (2015). (PMID: 2585545410.1038/nature14338)
      Pold, G., Baillargeon, N., Lepe, A., Rastetter, E. B. & Sistla, S. A. Warming effects on arctic tundra biogeochemistry are limited but habitat-dependent: a meta-analysis. Ecosphere 12, e03777 (2021).
      Elmendorf, S. C. et al. Plot-scale evidence of tundra vegetation change and links to recent summer warming. Nat. Clim. Change 2, 453–457 (2012). (PMID: 10.1038/nclimate1465)
      Jeanbille, M. et al. Site-specific responses of fungal and bacterial abundances to experimental warming in litter and soil across Arctic and alpine tundra. Arct. Sci. https://doi.org/10.1139/as-2020-0053 (2021).
      Bjorkman, A. D. et al. Plant functional trait change across a warming tundra biome. Nature 562, 57–62 (2018). (PMID: 3025822910.1038/s41586-018-0563-7)
      Nyberg, M. & Hovenden, M. J. Warming increases soil respiration in a carbon-rich soil without changing microbial respiratory potential. Biogeosciences 17, 4405–4420 (2020). (PMID: 10.5194/bg-17-4405-2020)
      Keuper, F. et al. Carbon loss from northern circumpolar permafrost soils amplified by rhizosphere priming. Nat. Geosci. 13, 560–565 (2020). (PMID: 10.1038/s41561-020-0607-0)
      Shaver, A. G. R., Street, L. E., Rastetter, E. B., Van Wijk, M. T. & Williams, M. Functional convergence in regulation of net CO 2 flux in heterogeneous tundra landscapes in Alaska and Sweden. J. Ecol. 95, 802–817 (2007). (PMID: 10.1111/j.1365-2745.2007.01259.x)
      Conant, R. T. et al. Sensitivity of organic matter decomposition to warming varies with its quality. Glob. Change Biol. 14, 868–877 (2008). (PMID: 10.1111/j.1365-2486.2008.01541.x)
      Bao, T., Zhu, R., Li, X., Ye, W. & Cheng, X. Effects of multiple environmental variables on tundra ecosystem respiration in maritime Antarctica. Sci Rep. 8, 12336 (2018).
      Stuart Chapin, F. III et al. The changing global carbon cycle: linking plant–soil carbon dynamics to global consequences. J. Ecol. 97, 840–850 (2009). (PMID: 10.1111/j.1365-2745.2009.01529.x)
      Allison, S. D., Romero-Olivares, A. L., Lu, Y., Taylor, J. W. & Treseder, K. K. Temperature sensitivities of extracellular enzyme V max and K m across thermal environments. Glob. Change Biol. 24, 2884–2897 (2018). (PMID: 10.1111/gcb.14045)
      Davidson, E. A. & Janssens, I. A. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440, 165–173 (2006). (PMID: 1652546310.1038/nature04514)
      Bao, T., Jia, G. & Xu, X. Weakening greenhouse gas sink of pristine wetlands under warming. Nat. Clim. Change https://doi.org/10.1038/s41558-023-01637-0 (2023).
      Giesler, R., Esberg, C., Lagerström, A. & Graae, B. J. Phosphorus availability and microbial respiration across different tundra vegetation types. Biogeochemistry 108, 429–445 (2012). (PMID: 10.1007/s10533-011-9609-8)
      Mekonnen, Z. A., Riley, W. J. & Grant, R. F. 21st century tundra shrubification could enhance net carbon uptake of North America Arctic tundra under an RCP8.5 climate trajectory. Environ. Res. Lett. 13, 054029 (2018).
      Parker, T. C. et al. Rhizosphere allocation by canopy-forming species dominates soil CO 2 efflux in a subarctic landscape. New Phytol. 227, 1818–1830 (2020). (PMID: 3224852410.1111/nph.16573)
      Sistla, S. A. et al. Long-term warming restructures Arctic tundra without changing net soil carbon storage. Nature 497, 615–617 (2013). (PMID: 2367666910.1038/nature12129)
      Marion, G. M. et al. Open-top designs for manipulating field temperature in high-latitude ecosystems. Glob. Change Biol. 3, 20–32 (1997). (PMID: 10.1111/j.1365-2486.1997.gcb136.x)
      Wu, Z., Dijkstra, P., Koch, G. W., Peñuelas, J. & Hungate, B. A. Responses of terrestrial ecosystems to temperature and precipitation change: a meta-analysis of experimental manipulation. Glob. Change Biol. 17, 927–942 (2011). (PMID: 10.1111/j.1365-2486.2010.02302.x)
      Hedges, L. V. Distribution theory for Glass’s estimator of effect size and related estimators. J. Educ. Stat. 6, 107–128 (1981). (PMID: 10.3102/10769986006002107)
      Dijkstra, F. A., Carrillo, Y., Pendall, E. & Morgan, J. A. Rhizosphere priming: a nutrient perspective. Front. Microbiol. 4, 216 (2013).
      Feng, J. & Zhu, B. Global patterns and associated drivers of priming effect in response to nutrient addition. Soil Biol. Biochem. 153, 108118 (2021). (PMID: 10.1016/j.soilbio.2020.108118)
      Yin, H. et al. Enhanced root exudation stimulates soil nitrogen transformations in a subalpine coniferous forest under experimental warming. Glob. Change Biol. 19, 2158–2167 (2013). (PMID: 10.1111/gcb.12161)
      Jiang, Z., Liu, Y., Yang, J., Zhou, Z. & Gunina, A. Effects of nitrogen fertilization on the rhizosphere priming. Plant Soil 462, 489–503 (2021). (PMID: 10.1007/s11104-021-04872-6)
      Terrer, C. et al. Ecosystem responses to elevated CO 2 governed by plant–soil interactions and the cost of nitrogen acquisition. New Phytol. 217, 507–522 (2018). (PMID: 2910576510.1111/nph.14872)
      IPCC: Summary for Policymakers. In Climate Change 2022: Impacts, Adaptation and Vulnerability (eds Pörtner, H.-O. et al.) (Cambridge Univ. Press, 2022).
      Blume-Werry, G., Milbau, A., Teuber, L. M., Johansson, M. & Dorrepaal, E. Dwelling in the deep—strongly increased root growth and rooting depth enhance plant interactions with thawing permafrost soil. New Phytol. 223, 1328–1339 (2019). (PMID: 3107486710.1111/nph.15903)
      Voigt, C. et al. Warming of subarctic tundra increases emissions of all three important greenhouse gases—carbon dioxide, methane and nitrous oxide. Glob. Change Biol. 23, 3121–3138 (2017). (PMID: 10.1111/gcb.13563)
      Li, F. et al. Warming effects on methane fluxes differ between two alpine grasslands with contrasting soil water status. Agric. For. Meteorol. 290, 107988 (2020). (PMID: 10.1016/j.agrformet.2020.107988)
      Björk, R. G. et al. Linkages between N turnover and plant community structure in a tundra landscape. Plant Soil 294, 247–261 (2007). (PMID: 10.1007/s11104-007-9250-4)
      Sullivan, B. W. & Hart, S. C. Evaluation of mechanisms controlling the priming of soil carbon along a substrate age gradient. Soil Biol. Biochem. 58, 293–301 (2013). (PMID: 10.1016/j.soilbio.2012.12.007)
      Milcu, A., Heim, A., Ellis, R. J., Scheu, S. & Manning, P. Identification of general patterns of nutrient and labile carbon control on soil carbon dynamics across a successional gradient. Ecosystems 14, 710–719 (2011). (PMID: 10.1007/s10021-011-9440-z)
      Metcalfe, D. B. et al. Patchy field sampling biases understanding of climate change impacts across the Arctic. Nat. Ecol. Evol. 2, 1443–1448 (2018). (PMID: 3001313310.1038/s41559-018-0612-5)
      Björkman, M. P. et al. Winter carbon dioxide effluxes from arctic ecosystems: an overview and comparison of methodologies. Global Biogeochem. Cycles https://doi.org/10.1029/2009GB003667 (2010).
      Blok, D., Elberling, B. & Michelsen, A. Initial stages of tundra shrub litter decomposition maybe accelerated by deeper winter snow but slowed down by spring warming. Ecosystems 19, 155–169 (2016). (PMID: 10.1007/s10021-015-9924-3)
      Morgner, E., Elberling, B., Strebel, D. & Cooper, E. J. The importance of winter in annual ecosystem respiration in the High Arctic: effects of snow depth in two vegetation types. Polar Res. 29, 58–74 (2010). (PMID: 10.1111/j.1751-8369.2010.00151.x)
      Qian, H., Joseph, R. & Zeng, N. Enhanced terrestrial carbon uptake in the northern high latitudes in the 21st century from the Coupled Carbon Cycle Climate Model Intercomparison Project model projections. Glob. Change Biol. 16, 641–656 (2010). (PMID: 10.1111/j.1365-2486.2009.01989.x)
      Melillo, J. M. et al. Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world. Science 358, 101–105 (2017). (PMID: 2898305010.1126/science.aan2874)
      Hicks Pries, C. E., Schuur, E. A. G., Natali, S. M. & Crummer, K. G. Old soil carbon losses increase with ecosystem respiration in experimentally thawed tundra. Nat. Clim. Change 6, 214–218 (2016). (PMID: 10.1038/nclimate2830)
      Hicks Pries, C. E., Schuur, E. A. G. & Crummer, K. G. Thawing permafrost increases old soil and autotrophic respiration in tundra: partitioning ecosystem respiration using δ 13 C and {increment} 14 C. Glob. Change Biol. 19, 649–661 (2013). (PMID: 10.1111/gcb.12058)
      Wei, D. et al. Plant uptake of CO 2 outpaces losses from permafrost and plant respiration on the Tibetan Plateau. Proc. Natl Acad. Sci. USA 118, e2015283118 (2021).
      Henry, G. H. R. & Molau, U. Tundra plants and climate change: the international tundra experiment (ITEX). Glob. Change Biol. 3, 1–9 (1997). (PMID: 10.1111/j.1365-2486.1997.gcb132.x)
      Rousseeuw, P. J. & Hubert, M. Robust statistics for outlier detection. WIREs Data Mining Knowl. Discov. 1, 73–79 (2011).
      Borenstein, M., Hedges, L. V., Higgins, J. P. T. & Rothstein, H. R. Introduction to Meta-analysis (Wiley, 2009).
      Walker, D. A. et al. The Circumpolar Arctic vegetation map. J. Veg. Sci. 16, 267–282 (2005). (PMID: 10.1111/j.1654-1103.2005.tb02365.x)
      R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2021) .
      Viechtbauer, W. Conducting meta-analyses in R with the metafor. J. Stat. Softw. 36, 1–48 (2010). (PMID: 10.18637/jss.v036.i03)
      Hedges, L. V., Gurevitch, J. & Curtis, P. S. The meta-analysis of response ratios in experimental ecology. Ecology 80, 1150–1156 (1999). (PMID: 10.1890/0012-9658(1999)080[1150:TMAORR]2.0.CO;2)
      Konstantopoulos, S. Fixed effects and variance components estimation in three‐level meta‐analysis. Res. Synth. Methods 2, 61–76 (2011). (PMID: 2606160010.1002/jrsm.35)
      Nakagawa, S. & Santos, E. S. A. Methodological issues and advances in biological meta-analysis. Evol. Ecol. 26, 1253–1274 (2012). (PMID: 10.1007/s10682-012-9555-5)
      I shak, K. J., Platt, R. W., Joseph, L., Hanley, J. A. & Caro, J. J. Meta-analysis of longitudinal studies. Clin. Trials 4, 525–539 (2007). (PMID: 10.1177/1740774507083567)
      Trikalinos, T. A. & Olkin, I. Meta-analysis of effect sizes reported at multiple time points: a multivariate approach. Clin. Trials 9, 610–620 (2012). (PMID: 2287254610.1177/1740774512453218)
      Signorini, M., Midolo, G., Cesco, S., Mimmo, T. & Borruso, L. A Matter of metals: copper but not cadmium affects the microbial alpha-diversity of soils and sediments—a meta-analysis. Microb. Ecol. https://doi.org/10.1007/s00248-022-02115-4 (2022).
      Jenkins, D. G. et al. A meta-analysis of isolation by distance: relic or reference standard for landscape genetics? Ecography 33, 315–320 (2010). (PMID: 10.1111/j.1600-0587.2010.06285.x)
      Vaessen, T. et al. The association between self-reported stress and cardiovascular measures in daily life: a systematic review. PLoS ONE https://doi.org/10.1371/journal.pone.0259557 (2021).
      Raue, A. et al. Structural and practical identifiability analysis of partially observed dynamical models by exploiting the profile likelihood. Bioinformatics 25, 1923–1929 (2009). (PMID: 1950594410.1093/bioinformatics/btp358)
      Jennions, M. D. & Møller, A. P. Publication bias in ecology and evolution: an empirical assessment using the ‘trim and fill’ method. Biol. Rev. 77, 211–222 (2002). (PMID: 1205674710.1017/S1464793101005875)
      Testolin, R., Attorre, F. & Jiménez-Alfaro, B. Global distribution and bioclimatic characterization of alpine biomes. Ecography 43, 779–788 (2020). (PMID: 10.1111/ecog.05012)
      Poggio, L. et al. SoilGrids 2.0: producing soil information for the globe with quantified spatial uncertainty. SOIL 7, 217–240 (2021). (PMID: 10.5194/soil-7-217-2021)
      Warner, D. L., Bond-Lamberty, B. P., Jian, J., Stell, E. & Vargas, R. Global Gridded 1-km Annual Soil Respiration and Uncertainty Derived from SRDB V3 (ORNL DAAC, 2019); https://doi.org/10.3334/ORNLDAAC/1736 .
      Huntingford, C. et al. Implications of improved representations of plant respiration in a changing climate. Nat. Commun. 8, 1602 (2017).
      Dataset for “Environmental drivers of increased ecosystem respiration in a warming tundra”. Zenodo https://doi.org/10.5281/zenodo.10572479 (2024).
      Scripts for “Environmental drivers of increasd ecosystem respiration in a warming tundra”. GitHub https://github.com/mjalava/tundraflux (2024).
    • Accession Number:
      7440-44-0 (Carbon)
      N762921K75 (Nitrogen)
      0 (Soil)
    • Publication Date:
      Date Created: 20240417 Date Completed: 20240501 Latest Revision: 20240504
    • Publication Date:
      20240504
    • Accession Number:
      PMC11062900
    • Accession Number:
      10.1038/s41586-024-07274-7
    • Accession Number:
      38632407