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Mycorrhizal type regulates trade-offs between plant and soil carbon in forests

Nature Climate Change (2023)Cite this article

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Abstract

Forest ecosystems store ~80% of the carbon in terrestrial ecosystems, but their long-term carbon sequestration depends partly on how plant biomass and soil carbon stocks will respond to global changes. Although the stimulation of plant growth by global change drivers has been widely observed, the response of soil carbon stock to global changes remains uncertain. Here we conducted a meta-analysis on experimental observations of plant and soil carbon-related data worldwide. We found that plant biomass and soil carbon stock increased more under elevated CO2 than under nitrogen deposition and warming. Under nitrogen deposition and warming, soil carbon stock depended on mycorrhizal associations, decreasing in forests dominated by arbuscular mycorrhizal tree species while increasing in forests dominated by ectomycorrhizal tree species. These results suggest a mycorrhizae-mediated trade-off between plant biomass and soil carbon sequestration in forest ecosystems under nitrogen deposition and warming conditions.

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Fig. 1: Global distribution of N deposition, eCO2 and warming experiments included in this meta-analysis.
Fig. 2: Effects of global change drivers on carbon-related variables.
Fig. 3: Effects of global change drivers on carbon-related variables associated with mycorrhizal types.
Fig. 4: Overall effects of global change drivers on plant biomass and soil C stocks.
Fig. 5: Relationships between response ratio of total biomass, RR of soil C stocks to the magnitude of global change drivers.

Data availability

All relevant data presented in this meta-analysis are available at Figshare (https://doi.org/10.6084/m9.figshare.23984409.v1)55.

Code availability

All code used can be obtained from Figshare (https://doi.org/10.6084/m9.figshare.23937600.v2)55.

References

  1. Dixon, R. K. et al. Carbon pools and flux of global forest ecosystems. Science 263, 185–190 (1994).

    Article  CAS  Google Scholar 

  2. Pan, Y. D. et al. A large and persistent carbon sink in the world’s forests. Science 333, 988–993 (2011).

    Article  CAS  Google Scholar 

  3. Lal, R. Forest soils and carbon sequestration. For. Ecol. Manage 220, 242–258 (2005).

    Article  Google Scholar 

  4. Terrer, C. et al. Mycorrhizal association as a primary control of the CO2 fertilization effect. Science 353, 72–74 (2016).

    Article  CAS  Google Scholar 

  5. Schulte-Uebbing, L. & de Vries, W. Global-scale impacts of nitrogen deposition on tree carbon sequestration in tropical, temperate, and boreal forests: a meta-analysis. Glob. Change Biol. 24, e416–e431 (2017).

    Google Scholar 

  6. Lin, D. L., Xia, J. Y. & Wan, S. Q. Climate warming and biomass accumulation of terrestrial plants: a meta-analysis. N. Phytol. 188, 187–198 (2010).

    Article  Google Scholar 

  7. Liu, L. L. & Greaver, T. L. A global perspective on belowground carbon dynamics under nitrogen enrichment. Ecol. Lett. 13, 819–828 (2010).

    Article  Google Scholar 

  8. Crowther, T. W. et al. Quantifying global soil carbon losses in response to warming. Nature 540, 104–108 (2016).

    Article  CAS  Google Scholar 

  9. Zhou, L. Y. et al. Different responses of soil respiration and its components to nitrogen addition among biomes: a meta-analysis. Glob. Change Biol. 20, 2332–2343 (2014).

    Article  Google Scholar 

  10. Schlesinger, W. H. & Lichter, J. Limited carbon storage in soil and litter of experimental forest plots under increased atmospheric CO2. Nature 411, 466–469 (2001).

    Article  CAS  Google Scholar 

  11. 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).

    Article  CAS  Google Scholar 

  12. Gundale, M. J. et al. Anthropogenic nitrogen deposition in boreal forests has a minor impact on the global carbon cycle. Glob. Change Biol. 20, 276–286 (2014).

    Article  Google Scholar 

  13. Nadelhoffer, K. J. et al. Nitrogen deposition makes a minor contribution to carbon sequestration in temperate forests. Nature 398, 145–148 (1999).

    Article  CAS  Google Scholar 

  14. Terrer, C. et al. A tradeoff between plant and soil carbon storage under elevated CO2. Nature 591, 599–603 (2021).

    Article  CAS  Google Scholar 

  15. Ma, X. M. et al. Root and mycorrhizal strategies for nutrient acquisition in forests under nitrogen deposition: a meta-analysis. Soil Biol. Biochem. 163, 108418 (2021).

    Article  CAS  Google Scholar 

  16. Jastrow, J. D. et al. Elevated atmospheric carbon dioxide increases soil carbon. Glob. Change Biol. 11, 2057–2064 (2005).

    Article  Google Scholar 

  17. Soong, J. L. et al. Five years of whole-soil warming led to loss of subsoil carbon stocks and increased CO2 efflux. Sci. Adv. 7, eabd1343 (2021).

  18. Cheng, L. et al. Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2. Science 337, 1084–1087 (2012).

    Article  CAS  Google Scholar 

  19. Pellitier, P. T. & Zak, D. R. Ectomycorrhizal fungi and the enzymatic liberation of nitrogen from soil organic matter: why evolutionary history matters. N. Phytol. 217, 68–73 (2018).

    Article  CAS  Google Scholar 

  20. Phillips, R. P., Brzostek, E. & Midgley, M. G. The mycorrhizal‐associated nutrient economy: a new framework for predicting carbon nutrient couplings in temperate forests. N. Phytol. 222, 556–564 (2019).

    Google Scholar 

  21. Keller, A. B. & Phillips, R. P. Leaf litter decay rates differ between mycorrhizal groups in temperate, but not tropical, forests. N. Phytol. 199, 41–51 (2013).

    Google Scholar 

  22. Midgley, M. G., Brzostek, E. & Phillips, R. P. Decay rates of leaf litters from arbuscular mycorrhizal trees are more sensitive to soil effects than litters from ectomycorrhizal trees. J. Ecol. 103, 1454–1463 (2015).

    Article  Google Scholar 

  23. Treseder, K. K. & Allen, M. F. Mycorrhizal fungi have a potential role in soil carbon storage under elevated CO2 and nitrogen deposition. N. Phytol. 147, 189–200 (2000).

    Article  CAS  Google Scholar 

  24. van Groenigen, K. J. et al. Faster decomposition under increased atmospheric CO2 limits soil carbon storage. Science 344, 508–509 (2014).

    Article  Google Scholar 

  25. Zhou, L. Y. et al. Global systematic review with meta-analysis shows that warming effects on terrestrial plant biomass allocation are influenced by precipitation and mycorrhizal association. Nat. Commun. 13, 4914 (2022).

    Article  CAS  Google Scholar 

  26. Chen, J. et al. Differential responses of carbon-degrading enzyme activities to warming: implications for soil respiration. Glob. Change Biol. 24, 4816–4826 (2018).

    Article  Google Scholar 

  27. Liang, X. Y. et al. Global response patterns of plant photosynthesis to nitrogen addition: a meta-analysis. Glob. Change Biol. 26, 3585–3600 (2020).

    Article  Google Scholar 

  28. Peng, Y. F., Guo, D. L. & Yang, Y. H. Global patterns of root dynamics under nitrogen enrichment. Glob. Ecol. Biogeogr. 26, 102–114 (2017).

    Article  Google Scholar 

  29. Li, W. B. et al. Effects of nitrogen enrichment on tree carbon allocation: a global synthesis. Glob. Ecol. Biogeogr. 29, 573–589 (2020).

    Article  Google Scholar 

  30. Peng, Y. F. & Yang, Y. H. Allometric biomass partitioning under nitrogen enrichment: evidence from manipulative experiments around the world. Sci. Rep. 6, 28918 (2016).

    Article  CAS  Google Scholar 

  31. Zhao, X. X. et al. Fine-root functional trait response to nitrogen decomposition across forest ecosystems: a meta-analysis. Sci. Total Environ. 844, 157111 (2022).

    Article  CAS  Google Scholar 

  32. Lu, X. F. et al. Decrease in soil pH has greater effects than increase in aboveground carbon inputs on soil organic carbon in terrestrial ecosystems of China under nitrogen enrichment. J. Appl. Ecol. 59, 768–778 (2022).

    Article  CAS  Google Scholar 

  33. Averill, C., Dietze, M. C. & Bhatnagar, J. M. Continental-scale nitrogen pollution is shifting forest mycorrhizal associations and soil carbon stocks. Glob. Change Biol. 24, 4544–4553 (2018).

    Article  Google Scholar 

  34. Kjøller, R. et al. Dramatic changes in ectomycorrhizal community composition, root tip abundance and mycelial production along a stand-scale nitrogen deposition gradient. N. Phytol. 194, 278–286 (2012).

    Article  Google Scholar 

  35. Carrara, J. E. et al. Differences in microbial community response to nitrogen fertilization result in unique enzyme shifts between arbuscular and ectomycorrhizal-dominated soils. Glob. Change Biol. 27, 2049–2060 (2021).

    Article  CAS  Google Scholar 

  36. Deng, Q. et al. Responses of terrestrial ecosystem phosphorus cycling to nitrogen addition: a meta-analysis. Glob. Ecol. Biogeogr. 26, 713–728 (2017).

    Article  Google Scholar 

  37. Högberg, P. et al. Tree growth and soil acidification in response to 30 years of experimental nitrogen loading on boreal forest. Glob. Change Biol. 12, 489–499 (2006).

    Article  Google Scholar 

  38. Bae, K. et al. Soil nitrogen availability affects belowground carbon allocation and soil respiration in northern hardwood forests of New Hampshire. Ecosystems 18, 1179–1191 (2015).

    Article  CAS  Google Scholar 

  39. Xing, A. J. et al. High-level nitrogen additions accelerate soil respiration reduction over time in a boreal forest. Ecol. Lett. 25, 1869–1878 (2022).

    Article  Google Scholar 

  40. Sulman, B. N. et al. Microbe-driven turnover offsets mineral-mediated storage of soil carbon under elevated CO2. Nat. Clim. Change 4, 1099–1102 (2014).

    Article  CAS  Google Scholar 

  41. Phillips, R. P., Finzi, A. C. & Bernhardt, E. S. Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol. Lett. 14, 187–194 (2011).

    Article  Google Scholar 

  42. Pierson, D. et al. Mineral stabilization of soil carbon is suppressed by live roots, outweighing influences from litter quality or quantity. Biogeochemistry 154, 433–449 (2021).

    Article  CAS  Google Scholar 

  43. Reich, P. B. & Hobbie, S. E. Decade-long soil nitrogen constraint on the CO2 fertilization of plant biomass. Nat. Clim. Change 3, 278–282 (2013).

    Article  CAS  Google Scholar 

  44. Terrer, C. et al. Nitrogen and phosphorus constrain the CO2 fertilization of global plant biomass. Nat. Clim. Change 9, 684–689 (2019).

    Article  CAS  Google Scholar 

  45. Mao, Z. K. et al. Tree mycorrhizal associations mediate soil fertility effects on forest community structure in a temperate forest. N. Phytol. 223, 475–486 (2019).

    Article  CAS  Google Scholar 

  46. Luo, Y. Q. et al. Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. BioScience 54, 731–739 (2004).

    Article  Google Scholar 

  47. Song, J. et al. A meta-analysis of 1119 manipulative experiments on terrestrial carbon-cycling responses to global change. Nat. Ecol. Evol. 3, 1309–1320 (2019).

    Article  Google Scholar 

  48. Bueno, C. G. et al. Plant mycorrhizal status, but not type, shifts with latitude and elevation in Europe. Glob. Ecol. Biogeogr. 26, 690–699 (2017).

    Article  Google Scholar 

  49. Wang, B. & Qiu, Y. L. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16, 299–363 (2006).

    Article  CAS  Google Scholar 

  50. Brundrett, M. C. & Tedersoo, L. Evolutionary history of mycorrhizal symbioses and global host plant diversity. N. Phytol. 220, 1108–1115 (2018).

    Article  Google Scholar 

  51. Viechtbauer, W. Conducting meta-analyses in R with the metafor package. J. Stat. Softw. 36, 185–190 (2010).

    Article  Google Scholar 

  52. Jonathan, J. A. C. & Egger, M. Funnel plots for detecting bias in meta-analysis: guidelines on choice of axis. J. Clin. Epidemiol. 54, 1046–1055 (2001).

    Article  Google Scholar 

  53. Egger, M. et al. Bias in meta-analysis detected by a simple, graphical test. Br. Med. J. 315, 629–634 (1997).

    Article  CAS  Google Scholar 

  54. Duval, S. & Tweedie, R. A nonparametric ‘trim and fill’ method of accounting for publication bias in meta-analysis. J. Am. Stat. Assoc. 95, 89–98 (2000).

    Google Scholar 

  55. Yang, K. et al. Supporting data for ‘Mycorrhizal type regulates tradeoffs between plant and soil carbon in forests’. Figshare https://doi.org/10.6084/m9.figshare.23984409.v1 and https://doi.org/10.6084/m9.figshare.23937600.v2 (2023).

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Acknowledgements

This study was financially supported by CAS Project for Young Scientists in Basic Research grant YSBR-037 (K.Y.), the National Natural Science Foundation of China grants 32192435 (J.Z.) and 31922059 (K.Y.), the National Key Research and Development Program of China grants 2020YFA0608103 (J.Z.) and 2022YFF1300500 (K.Y.).

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Author notes

  1. These authors contributed equally: Kai Yang, Qian Zhang.

Authors and Affiliations

  1. Qingyuan Forest CERN, National Observation and Research Station, Liaoning Province, Chinese Academy of Sciences, Shenyang, China

    Kai Yang, Qian Zhang, Jiaojun Zhu, Qiqi Wang & Tian Gao

  2. Key Laboratory of Forest Ecology and Management, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, China

    Kai Yang, Qian Zhang, Jiaojun Zhu, Qiqi Wang & Tian Gao

  3. Key Laboratory of Terrestrial Ecosystem Carbon Neutrality, Liaoning Province, Chinese Academy of Sciences, Shenyang, China

    Kai Yang, Jiaojun Zhu & Tian Gao

  4. Department of Forestry and Environmental Conservation, Clemson University, Clemson, SC, USA

    G. Geoff Wang

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Contributions

K.Y. and J.Z. designed the study. Q.Z. collected data. K.Y. and Q.Z. performed the meta-analysis. K.Y. wrote the article, with significant contributions provided by J.Z., G.G.W., Q.Z., Q.W. and T.G. All the authors contributed to the discussions and paper revision.

Corresponding author

Correspondence to Jiaojun Zhu.

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Peer review information

Nature Climate Change thanks Shuijin Hu and Ashley Lang for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–5, Tables 1–3 and database references.

Supplementary Table 1

The systematic review reports are a checklist of details that include type of review, authors’ contacts, the contents of manuscript and other items.

Supplementary Data 1

The database of carbon-related variables under nitrogen deposition, elevated CO2 and warming effects.

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Yang, K., Zhang, Q., Zhu, J. et al. Mycorrhizal type regulates trade-offs between plant and soil carbon in forests. Nat. Clim. Chang. (2023). https://doi.org/10.1038/s41558-023-01864-5

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