The identity of the dominant root-associated microbial symbionts in a forest determines the ability of trees to access limiting nutrients from atmospheric or soil pools1,2, sequester carbon3,4 and withstand the effects of climate change5,6. Characterizing the global distribution of these symbioses and identifying the factors that control this distribution are thus integral to understanding the present and future functioning of forest ecosystems. Here we generate a spatially explicit global map of the symbiotic status of forests, using a database of over 1.1 million forest inventory plots that collectively contain over 28,000 tree species. Our analyses indicate that climate variables—in particular, climatically controlled variation in the rate of decomposition—are the primary drivers of the global distribution of major symbioses. We estimate that ectomycorrhizal trees, which represent only 2% of all plant species7, constitute approximately 60% of tree stems on Earth. Ectomycorrhizal symbiosis dominates forests in which seasonally cold and dry climates inhibit decomposition, and is the predominant form of symbiosis at high latitudes and elevation. By contrast, arbuscular mycorrhizal trees dominate in aseasonal, warm tropical forests, and occur with ectomycorrhizal trees in temperate biomes in which seasonally warm-and-wet climates enhance decomposition. Continental transitions between forests dominated by ectomycorrhizal or arbuscular mycorrhizal trees occur relatively abruptly along climate-driven decomposition gradients; these transitions are probably caused by positive feedback effects between plants and microorganisms. Symbiotic nitrogen fixers—which are insensitive to climatic controls on decomposition (compared with mycorrhizal fungi)—are most abundant in arid biomes with alkaline soils and high maximum temperatures. The climatically driven global symbiosis gradient that we document provides a spatially explicit quantitative understanding of microbial symbioses at the global scale, and demonstrates the critical role of microbial mutualisms in shaping the distribution of plant species.
This is a preview of subscription content, access via your institution
Open Access articles citing this article.
Global systematic review with meta-analysis shows that warming effects on terrestrial plant biomass allocation are influenced by precipitation and mycorrhizal association
Nature Communications Open Access 20 August 2022
Nature Communications Open Access 10 January 2022
Subscribe to Nature+
Get immediate online access to the entire Nature family of 50+ journals
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
Information regarding symbiotic guild assignments, model selection (including global rasters of our model projections for ectomycorrhizal, arbuscular mycorrhizal and N-fixer proportion of tree basal area) and analyses is available as Supplementary Data. The GFBi database is available upon written request at https://www.gfbinitiative.org/datarequest. Any other relevant data are available from the corresponding authors upon reasonable request.
Batterman, S. A. et al. Key role of symbiotic dinitrogen fixation in tropical forest secondary succession. Nature 502, 224–227 (2013).
Shah, F. et al. Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors. New Phytol. 209, 1705–1719 (2016).
Averill, C., Turner, B. L. & Finzi, A. C. Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505, 543–545 (2014).
Clemmensen, K. E. et al. Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339, 1615–1618 (2013).
Cheeke, T. E. et al. Dominant mycorrhizal association of trees alters carbon and nutrient cycling by selecting for microbial groups with distinct enzyme function. New Phytol. 214, 432–442 (2017).
Terrer, C., Vicca, S., Hungate, B. A., Phillips, R. P. & Prentice, I. C. Mycorrhizal association as a primary control of the CO2 fertilization effect. Science 353, 72–74 (2016).
Brundrett, M. C. & Tedersoo, L. Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol. 220, 1108–1115 (2018).
Averill, C. & Hawkes, C. V. Ectomycorrhizal fungi slow soil carbon cycling. Ecol. Lett. 19, 937–947 (2016).
Bennett, J. A. et al. Plant–soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science 355, 181–184 (2017).
Phillips, R. P., Brzostek, E. & Midgley, M. G. The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests. New Phytol. 199, 41–51 (2013).
Crowther, T. W. et al. Mapping tree density at a global scale. Nature 525, 201–205 (2015).
van der Heijden, M. G., Martin, F. M., Selosse, M. A. & Sanders, I. R. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol. 205, 1406–1423 (2015).
Binkley, D., Sollins, P., Bell, R., Sachs, D. & Myrold, D. Biogeochemistry of adjacent conifer and alder-conifer stands. Ecology 73, 2022–2033 (1992).
Leake, J. et al. Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can. J. Bot. 82, 1016–1045 (2004).
Hedin, L. O., Brookshire, E. N. J., Menge, D. N. L. & Barron, A. R. The nitrogen paradox in tropical rainforest ecosystems. Annu. Rev. Ecol. Evol. Syst. 40, 613–635 (2009).
Read, D. J. Mycorrhizas in ecosystems. Experientia 47, 376–391 (1991).
Houlton, B. Z., Wang, Y.-P., Vitousek, P. M. & Field, C. B. A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454, 327–330 (2008).
Peay, K. G. The mutualistic niche: mycorrhizal symbiosis and community dynamics. Annu. Rev. Ecol. Evol. Syst. 47, 143–164 (2016).
Pellegrini, A. F. A., Staver, A. C., Hedin, L. O., Charles-Dominique, T. & Tourgee, A. Aridity, not fire, favors nitrogen-fixing plants across tropical savanna and forest biomes. Ecology 97, 2177–2183 (2016).
Tuomi, M. et al. Leaf litter decomposition—estimates of global variability based on Yasso07 model. Ecol. Modell. 220, 3362–3371 (2009).
Ma, Z. et al. Evolutionary history resolves global organization of root functional traits. Nature 555, 94–97 (2018).
Lu, M. & Hedin, L. O. Global plant–symbiont organization and emergence of biogeochemical cycles resolved by evolution-based trait modelling. Nat. Ecol. Evol. 3, 239–250 (2019).
Scheffer, M., Carpenter, S., Foley, J. A., Folke, C. & Walker, B. Catastrophic shifts in ecosystems. Nature 413, 591–596 (2001).
Reich, P. B. et al. Geographic range predicts photosynthetic and growth response to warming in co-occurring tree species. Nat. Clim. Change 5, 148 (2015).
McGroddy, M. E., Daufresne, T. & Hedin, L. O. Scaling of C:N:P stoichiometry in forests worldwide: implications of terrestrial redfield-type ratios. Ecology 85, 2390–2401 (2004).
Reich, P. B. & Oleksyn, J. Global patterns of plant leaf N and P in relation to temperature and latitude. Proc. Natl Acad. Sci. USA 101, 11001–11006 (2004).
Corrales, A., Mangan, S. A., Turner, B. L. & Dalling, J. W. An ectomycorrhizal nitrogen economy facilitates monodominance in a neotropical forest. Ecol. Lett. 19, 383–392 (2016).
Menge, D. N., Lichstein, J. W. & Angeles-Pérez, G. Nitrogen fixation strategies can explain the latitudinal shift in nitrogen-fixing tree abundance. Ecology 95, 2236–2245 (2014).
Liao, W., Menge, D. N. L., Lichstein, J. W. & Ángeles-Pérez, G. Global climate change will increase the abundance of symbiotic nitrogen-fixing trees in much of North America. Glob. Change Biol. 23, 4777–4787 (2017).
Gei, M. et al. Legume abundance along successional and rainfall gradients in neotropical forests. Nat. Ecol. Evol. 2, 1104–1111 (2018).
Liang, J. et al. Positive biodiversity–productivity relationship predominant in global forests. Science 354, aaf8957 (2016).
Chamberlain, S. A. & Szöcs, E. taxize: taxonomic search and retrieval in R. F1000Res. 2, 191 (2013).
Brundrett, M. C. Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320, 37–77 (2009).
Werner, G. D., Cornwell, W. K., Sprent, J. I., Kattge, J. & Kiers, E. T. A single evolutionary innovation drives the deep evolution of symbiotic N2-fixation in angiosperms. Nat. Commun. 5, 4087 (2014).
Werner, G. D., Cornwell, W. K., Cornelissen, J. H. & Kiers, E. T. Evolutionary signals of symbiotic persistence in the legume–rhizobia mutualism. Proc. Natl Acad. Sci. USA 112, 10262–10269 (2015).
Afkhami, M. E. et al. Symbioses with nitrogen-fixing bacteria: nodulation and phylogenetic data across legume genera. Ecology 99, 502 (2018).
Tedersoo, L. et al. Global database of plants with root-symbiotic nitrogen fixation: Nod DB. J. Veg. Sci. 29, 560–568 (2018).
Hayward, J. & Hynson, N. A. New evidence of ectomycorrhizal fungi in the Hawaiian Islands associated with the endemic host Pisonia sandwicensis (Nyctaginaceae). Fungal Ecol. 12, 62–69 (2014).
Lambers, H., Martinoia, E. & Renton, M. Plant adaptations to severely phosphorus-impoverished soils. Curr. Opin. Plant Biol. 25, 23–31 (2015).
Wang, B. & Qiu, Y.-L. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16, 299–363 (2006).
Soltis, D. E. et al. Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proc. Natl Acad. Sci. USA 92, 2647–2651 (1995).
Palosuo, T., Liski, J., Trofymow, J. & Titus, B. Litter decomposition affected by climate and litter quality—testing the Yasso model with litterbag data from the Canadian intersite decomposition experiment. Ecol. Modell. 189, 183–198 (2005).
Bradford, M. A. et al. Climate fails to predict wood decomposition at regional scales. Nat. Clim. Change 4, 625 (2014).
Evans, J. S. & Murphy, M. A. rfUtilities: random forests model selection and performance evaluation. R package version 2.1-3 https://cran.r-project.org/web/packages/rfUtilities/ (2018).
Core Writing Team et al. (eds) Climate Change 2014 Synthesis Report (IPCC, Geneva, 2014).
Schepaschenko, D. et al. A dataset of forest biomass structure for Eurasia. Sci. Data 4, 170070 (2017).
This work was made possible by the Global Forest Biodiversity Database, which represents the work of over 200 independent investigators and their public and private funding agencies (see Supplementary Acknowledgements).
Nature thanks Martin Bidartondo, David Bohan and the other anonymous reviewer(s) for their contribution to the peer review of this work.
The authors declare no competing interests.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This file contains Supplementary Tables 1–8 and Supplementary Figures 1–26.
This file contains Supplementary Acknowledgments.
This zip folder contains Supplementary Data files and a guide showing the climatic controls of decomposition drive the global biogeography of forest tree symbioses.
About this article
Cite this article
Steidinger, B.S., Crowther, T.W., Liang, J. et al. Climatic controls of decomposition drive the global biogeography of forest-tree symbioses. Nature 569, 404–408 (2019). https://doi.org/10.1038/s41586-019-1128-0
This article is cited by
Nature Ecology & Evolution (2022)
Nature Microbiology (2022)
Nature Plants (2022)
Nature Ecology & Evolution (2022)
The ISME Journal (2022)