Climatic controls of decomposition drive the global biogeography of forest-tree symbioses
Abstract
The identity of the dominant microbial symbionts in a forest determines the ability of trees to access limiting nutrients from atmospheric or soil pools, sequester carbon and withstand the impacts of climate change. Characterizing the global distribution of symbioses, and identifying the factors that control it, are thus integral to understanding present and future forest ecosystem functioning. In this work we generate the first spatially explicit global map of forest symbiotic status using a database of over 1.1 million forest inventory plots with over 28,000 tree species. Our analyses indicate that climatic variables, and in particular climatically-controlled variation in decomposition rate, are the primary drivers of the global distribution of major symbioses. We estimate that ectomycorrhizal (EM) trees, which represent only 2% of all plant species, constitute approximately 60% of tree stems on Earth. EM symbiosis dominates forests where seasonally cold and dry climates inhibit decomposition, and are the predominant symbiosis at high latitudes and elevation. On the other hand, arbuscular mycorrhizal (AM) trees dominate aseasonally warm tropical forests and occur with EM trees in temperate biomes where seasonally warm-and-wet climates enhance decomposition. Continental transitions between AM and EM dominated forests occur relatively abruptly along climate driven decomposition gradients, whichmore »
- Authors:
-
- Stanford Univ., CA (United States)
- Swiss Federal Institute of Technology (ETH), Zürich (Switzerland)
- Purdue Univ., West Lafayette, IN (United States); Beijing Forestry Univ. (China)
- Univ. of Oxford (United Kingdom)
- Univ. of Minnesota, Minneapolis, MN (United States); Univ. of Western Sydney, NSW (Australia). Hawkesbury Inst. for the Environment
- Wageningen Univ. (Netherlands)
- Univ. of Lleida (Spain); Forest Science and Technology Centre of Catalonia (CTFC), Solsona (Spain)
- Purdue Univ., West Lafayette, IN (United States)
- Food and Agriculture Organization of the United Nations, Rome (Italy)
- Univ. of Montpellier (France); Institut National Polytechnique Félix Houphouët-Boigny (INP-HB), Yamoussoukro (Côte d’Ivoire)
- Beijing Forestry Univ. (China)
- Publication Date:
- Research Org.:
- Stanford Univ., CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- Contributing Org.:
- GFBI consortium
- OSTI Identifier:
- 1524787
- Grant/Contract Number:
- SC0016097
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature (London)
- Additional Journal Information:
- Journal Name: Nature (London); Journal Volume: 569; Journal Issue: 7756; Journal ID: ISSN 0028-0836
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Steidinger, B. S., Crowther, T. W., Liang, J., Van Nuland, M. E., Werner, G. D. A., Reich, P. B., Nabuurs, G., de-Miguel, S., Zhou, M., Picard, N., Herault, B., Zhao, X., Zhang, C., Routh, D., and Peay, K. G. Climatic controls of decomposition drive the global biogeography of forest-tree symbioses. United States: N. p., 2019.
Web. doi:10.1038/s41586-019-1128-0.
Steidinger, B. S., Crowther, T. W., Liang, J., Van Nuland, M. E., Werner, G. D. A., Reich, P. B., Nabuurs, G., de-Miguel, S., Zhou, M., Picard, N., Herault, B., Zhao, X., Zhang, C., Routh, D., & Peay, K. G. Climatic controls of decomposition drive the global biogeography of forest-tree symbioses. United States. https://doi.org/10.1038/s41586-019-1128-0
Steidinger, B. S., Crowther, T. W., Liang, J., Van Nuland, M. E., Werner, G. D. A., Reich, P. B., Nabuurs, G., de-Miguel, S., Zhou, M., Picard, N., Herault, B., Zhao, X., Zhang, C., Routh, D., and Peay, K. G. Wed .
"Climatic controls of decomposition drive the global biogeography of forest-tree symbioses". United States. https://doi.org/10.1038/s41586-019-1128-0. https://www.osti.gov/servlets/purl/1524787.
@article{osti_1524787,
title = {Climatic controls of decomposition drive the global biogeography of forest-tree symbioses},
author = {Steidinger, B. S. and Crowther, T. W. and Liang, J. and Van Nuland, M. E. and Werner, G. D. A. and Reich, P. B. and Nabuurs, G. and de-Miguel, S. and Zhou, M. and Picard, N. and Herault, B. and Zhao, X. and Zhang, C. and Routh, D. and Peay, K. G.},
abstractNote = {The identity of the dominant microbial symbionts in a forest determines the ability of trees to access limiting nutrients from atmospheric or soil pools, sequester carbon and withstand the impacts of climate change. Characterizing the global distribution of symbioses, and identifying the factors that control it, are thus integral to understanding present and future forest ecosystem functioning. In this work we generate the first spatially explicit global map of forest symbiotic status using a database of over 1.1 million forest inventory plots with over 28,000 tree species. Our analyses indicate that climatic variables, and in particular climatically-controlled variation in decomposition rate, are the primary drivers of the global distribution of major symbioses. We estimate that ectomycorrhizal (EM) trees, which represent only 2% of all plant species, constitute approximately 60% of tree stems on Earth. EM symbiosis dominates forests where seasonally cold and dry climates inhibit decomposition, and are the predominant symbiosis at high latitudes and elevation. On the other hand, arbuscular mycorrhizal (AM) trees dominate aseasonally warm tropical forests and occur with EM trees in temperate biomes where seasonally warm-and-wet climates enhance decomposition. Continental transitions between AM and EM dominated forests occur relatively abruptly along climate driven decomposition gradients, which is likely caused by positive plant-microbe feedbacks. Symbiotic N-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 we document represents the first 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.},
doi = {10.1038/s41586-019-1128-0},
journal = {Nature (London)},
number = 7756,
volume = 569,
place = {United States},
year = {Wed May 15 00:00:00 EDT 2019},
month = {Wed May 15 00:00:00 EDT 2019}
}
Web of Science
Works referenced in this record:
Key role of symbiotic dinitrogen fixation in tropical forest secondary succession
journal, September 2013
- Batterman, Sarah A.; Hedin, Lars O.; van Breugel, Michiel
- Nature, Vol. 502, Issue 7470
Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors
journal, November 2015
- Shah, Firoz; Nicolás, César; Bentzer, Johan
- New Phytologist, Vol. 209, Issue 4
Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage
journal, January 2014
- Averill, Colin; Turner, Benjamin L.; Finzi, Adrien C.
- Nature, Vol. 505, Issue 7484
Roots and Associated Fungi Drive Long-Term Carbon Sequestration in Boreal Forest
journal, March 2013
- Clemmensen, K. E.; Bahr, A.; Ovaskainen, O.
- Science, Vol. 339, Issue 6127
Dominant mycorrhizal association of trees alters carbon and nutrient cycling by selecting for microbial groups with distinct enzyme function
journal, December 2016
- Cheeke, Tanya E.; Phillips, Richard P.; Brzostek, Edward R.
- New Phytologist, Vol. 214, Issue 1
Mycorrhizal association as a primary control of the CO 2 fertilization effect
journal, June 2016
- Terrer, César; Vicca, Sara; Hungate, Bruce A.
- Science, Vol. 353, Issue 6294
Evolutionary history of mycorrhizal symbioses and global host plant diversity
journal, January 2018
- Brundrett, Mark C.; Tedersoo, Leho
- New Phytologist, Vol. 220, Issue 4
Ectomycorrhizal fungi slow soil carbon cycling
journal, June 2016
- Averill, Colin; Hawkes, Christine V.
- Ecology Letters, Vol. 19, Issue 8
Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics
journal, January 2017
- Bennett, Jonathan A.; Maherali, Hafiz; Reinhart, Kurt O.
- Science, Vol. 355, Issue 6321
The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests
journal, April 2013
- Phillips, Richard P.; Brzostek, Edward; Midgley, Meghan G.
- New Phytologist, Vol. 199, Issue 1
Mapping tree density at a global scale
journal, September 2015
- Crowther, T. W.; Glick, H. B.; Covey, K. R.
- Nature, Vol. 525, Issue 7568
Mycorrhizal ecology and evolution: the past, the present, and the future
journal, February 2015
- van der Heijden, Marcel G. A.; Martin, Francis M.; Selosse, Marc-André
- New Phytologist, Vol. 205, Issue 4
Biogeochemistry of Adjacent Conifer and Alder-Conifer Stands
journal, December 1992
- Binkley, Dan; Sollins, Phillip; Bell, Randy
- Ecology, Vol. 73, Issue 6
Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning
journal, August 2004
- Leake, Jonathan; Johnson, David; Donnelly, Damian
- Canadian Journal of Botany, Vol. 82, Issue 8
The Nitrogen Paradox in Tropical Forest Ecosystems
journal, December 2009
- Hedin, Lars O.; Brookshire, E. N. Jack; Menge, Duncan N. L.
- Annual Review of Ecology, Evolution, and Systematics, Vol. 40, Issue 1
A unifying framework for dinitrogen fixation in the terrestrial biosphere
journal, June 2008
- Houlton, Benjamin Z.; Wang, Ying-Ping; Vitousek, Peter M.
- Nature, Vol. 454, Issue 7202
The Mutualistic Niche: Mycorrhizal Symbiosis and Community Dynamics
journal, November 2016
- Peay, Kabir G.
- Annual Review of Ecology, Evolution, and Systematics, Vol. 47, Issue 1
Aridity, not fire, favors nitrogen-fixing plants across tropical savanna and forest biomes
journal, September 2016
- Pellegrini, Adam F. A.; Staver, A. Carla; Hedin, Lars O.
- Ecology, Vol. 97, Issue 9
Leaf litter decomposition—Estimates of global variability based on Yasso07 model
journal, December 2009
- Tuomi, M.; Thum, T.; Järvinen, H.
- Ecological Modelling, Vol. 220, Issue 23
Evolutionary history resolves global organization of root functional traits
journal, February 2018
- Ma, Zeqing; Guo, Dali; Xu, Xingliang
- Nature, Vol. 555, Issue 7694
Global plant–symbiont organization and emergence of biogeochemical cycles resolved by evolution-based trait modelling
journal, January 2019
- Lu, Mingzhen; Hedin, Lars O.
- Nature Ecology & Evolution, Vol. 3, Issue 2
Catastrophic shifts in ecosystems
journal, October 2001
- Scheffer, Marten; Carpenter, Steve; Foley, Jonathan A.
- Nature, Vol. 413, Issue 6856
Geographic range predicts photosynthetic and growth response to warming in co-occurring tree species
journal, January 2015
- Reich, Peter B.; Sendall, Kerrie M.; Rice, Karen
- Nature Climate Change, Vol. 5, Issue 2
Scaling of C:N:P Stoichiometry in Forests Worldwide: Implications of Terrestrial Redfield-Type Ratios
journal, September 2004
- McGroddy, Megan E.; Daufresne, Tanguy; Hedin, Lars O.
- Ecology, Vol. 85, Issue 9
Global patterns of plant leaf N and P in relation to temperature and latitude
journal, June 2004
- Reich, P. B.; Oleksyn, J.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 30
An ectomycorrhizal nitrogen economy facilitates monodominance in a neotropical forest
journal, February 2016
- Corrales, Adriana; Mangan, Scott A.; Turner, Benjamin L.
- Ecology Letters, Vol. 19, Issue 4
Nitrogen fixation strategies can explain the latitudinal shift in nitrogen-fixing tree abundance
journal, August 2014
- Menge, Duncan N. L.; Lichstein, Jeremy W.; Ángeles-Pérez, Gregorio
- Ecology, Vol. 95, Issue 8
Global climate change will increase the abundance of symbiotic nitrogen-fixing trees in much of North America
journal, May 2017
- Liao, Wenying; Menge, Duncan N. L.; Lichstein, Jeremy W.
- Global Change Biology, Vol. 23, Issue 11
Legume abundance along successional and rainfall gradients in Neotropical forests
journal, May 2018
- Gei, Maga; Rozendaal, Danaë M. A.; Poorter, Lourens
- Nature Ecology & Evolution, Vol. 2, Issue 7
Positive biodiversity-productivity relationship predominant in global forests
journal, October 2016
- Liang, J.; Crowther, T. W.; Picard, N.
- Science, Vol. 354, Issue 6309
taxize: taxonomic search and retrieval in R
journal, January 2013
- Chamberlain, Scott A.; Szöcs, Eduard
- F1000Research, Vol. 2
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
journal, February 2009
- Brundrett, Mark C.
- Plant and Soil, Vol. 320, Issue 1-2
A single evolutionary innovation drives the deep evolution of symbiotic N2-fixation in angiosperms
journal, June 2014
- Werner, Gijsbert D. A.; Cornwell, William K.; Sprent, Janet I.
- Nature Communications, Vol. 5, Issue 1
Evolutionary signals of symbiotic persistence in the legume–rhizobia mutualism
journal, June 2015
- Werner, Gijsbert D. A.; Cornwell, William K.; Cornelissen, Johannes H. C.
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 33
Symbioses with nitrogen-fixing bacteria: nodulation and phylogenetic data across legume genera
journal, January 2018
- Afkhami, Michelle E.; Luke Mahler, D.; Burns, Jean H.
- Ecology, Vol. 99, Issue 2
Global database of plants with root-symbiotic nitrogen fixation: NodDB
journal, May 2018
- Tedersoo, Leho; Laanisto, Lauri; Rahimlou, Saleh
- Journal of Vegetation Science, Vol. 29, Issue 3
New evidence of ectomycorrhizal fungi in the Hawaiian Islands associated with the endemic host Pisonia sandwicensis (Nyctaginaceae)
journal, December 2014
- Hayward, Jeremy; Hynson, Nicole A.
- Fungal Ecology, Vol. 12
Plant adaptations to severely phosphorus-impoverished soils
journal, June 2015
- Lambers, Hans; Martinoia, Enrico; Renton, Michael
- Current Opinion in Plant Biology, Vol. 25
Phylogenetic distribution and evolution of mycorrhizas in land plants
journal, May 2006
- Wang, B.; Qiu, Y. -L.
- Mycorrhiza, Vol. 16, Issue 5
Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms.
journal, March 1995
- Soltis, D. E.; Soltis, P. S.; Morgan, D. R.
- Proceedings of the National Academy of Sciences, Vol. 92, Issue 7
Litter decomposition affected by climate and litter quality—Testing the Yasso model with litterbag data from the Canadian intersite decomposition experiment
journal, November 2005
- Palosuo, T.; Liski, J.; Trofymow, J. A.
- Ecological Modelling, Vol. 189, Issue 1-2
Climate fails to predict wood decomposition at regional scales
journal, June 2014
- Bradford, Mark A.; Warren II, Robert J.; Baldrian, Petr
- Nature Climate Change, Vol. 4, Issue 7
A dataset of forest biomass structure for Eurasia
journal, May 2017
- Schepaschenko, Dmitry; Shvidenko, Anatoly; Usoltsev, Vladimir
- Scientific Data, Vol. 4, Issue 1
Aridity, Not Fire, Favors Nitrogen-Fixing Plants Across Tropical Savanna and Forest Biomes
journal, October 2016
- Pellegrini, Adam F. A.; Staver, Ann Carla; Hedin, Lars O.
- The Bulletin of the Ecological Society of America, Vol. 97, Issue 4
Mycorrhizas in Ecosystems
journal, January 1994
- Pedersen, Christian T.
- Soil Science, Vol. 157, Issue 2
taxize: taxonomic search and retrieval in R
journal, January 2013
- Chamberlain, Scott A.; Szöcs, Eduard
- F1000Research, Vol. 2
Plant adaptations to severely phosphorus-impoverished soils
text, January 2015
- Lambers, Hans; Martinoia, Enrico; Renton, Michael
- Elsevier
Positive biodiversity-productivity relationship predominant in global forests
text, January 2016
- Fischer, Markus; Ba Azy, R.; Neldner, V. J.
- American Association for the Advancement of Science
Positive biodiversity-productivity relationship predominant in global forests
text, January 2016
- Liang, J.; Crowther, T. W.; Picard, N.
- American Association for the Advancement of Science
Works referencing / citing this record:
Facultative mycorrhizal associations promote plant naturalization worldwide
journal, November 2019
- Pyšek, Petr; Guo, Wen‐Yong; Štajerová, Kateřina
- Ecosphere, Vol. 10, Issue 11
Global mycorrhizal plant distribution linked to terrestrial carbon stocks
journal, November 2019
- Soudzilovskaia, Nadejda A.; van Bodegom, Peter M.; Terrer, César
- Nature Communications, Vol. 10, Issue 1
Global imprint of mycorrhizal fungi on whole-plant nutrient economics
journal, October 2019
- Averill, Colin; Bhatnagar, Jennifer M.; Dietze, Michael C.
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 46
Climate drives the spatial distribution of mycorrhizal host plants in terrestrial ecosystems
journal, May 2019
- Barceló, Milagros; Bodegom, Peter M.; Soudzilovskaia, Nadejda A.
- Journal of Ecology, Vol. 107, Issue 6
Fungal functional ecology: bringing a trait‐based approach to plant‐associated fungi
journal, November 2019
- Zanne, Amy E.; Abarenkov, Kessy; Afkhami, Michelle E.
- Biological Reviews, Vol. 95, Issue 2
Tree communities and soil properties influence fungal community assembly in neotropical forests
journal, February 2020
- Schimann, Heidy; Vleminckx, Jason; Baraloto, Christopher
- Biotropica, Vol. 52, Issue 3
Imaging spectroscopy reveals the effects of topography and logging on the leaf chemistry of tropical forest canopy trees
journal, December 2019
- Swinfield, Tom; Both, Sabine; Riutta, Terhi
- Global Change Biology, Vol. 26, Issue 2
Asymmetric patterns of global diversity among plants and mycorrhizal fungi
journal, November 2019
- Toussaint, Aurele; Bueno, Guillermo; Davison, John
- Journal of Vegetation Science, Vol. 31, Issue 2
Dual‐mycorrhizal plants: their ecology and relevance
journal, October 2019
- Teste, François P.; Jones, Melanie D.; Dickie, Ian A.
- New Phytologist, Vol. 225, Issue 5
Climate change effects on plant-soil feedbacks and consequences for biodiversity and functioning of terrestrial ecosystems
journal, November 2019
- Pugnaire, Francisco I.; Morillo, José A.; Peñuelas, Josep
- Science Advances, Vol. 5, Issue 11
The global soil community and its influence on biogeochemistry
journal, August 2019
- Crowther, T. W.; van den Hoogen, J.; Wan, J.
- Science, Vol. 365, Issue 6455
Constraining carbon and nutrient flows in soil with ecological stoichiometry
text, January 2019
- Buchkowski, Robert; Shaw, Alanna; Sihi, Debjani
- Zenodo
Decelerated carbon cycling by ectomycorrhizal fungi is controlled by substrate quality and community composition
journal, November 2019
- Fernandez, Christopher W.; See, Craig R.; Kennedy, Peter G.
- New Phytologist, Vol. 226, Issue 2
Imaging spectroscopy reveals the effects of topography and logging on the leaf chemistry of tropical forest canopy trees.
text, January 2020
- Swinfield, Thomas; Both, Sabine; Riutta, Terhi
- Apollo - University of Cambridge Repository
Constraining carbon and nutrient flows in soil with ecological stoichiometry
text, January 2019
- Buchkowski, Robert; Shaw, Alanna; Sihi, Debjani
- Zenodo
Global mycorrhizal plant distribution linked to terrestrial carbon stocks
journal, November 2019
- Soudzilovskaia, Nadejda A.; van Bodegom, Peter M.; Terrer, César
- Nature Communications, Vol. 10, Issue 1
Community composition of arctic root-associated fungi mirrors host plant phylogeny
journal, September 2020
- Botnen, S. S.; Thoen, E.; Eidesen, P. B.
- FEMS Microbiology Ecology, Vol. 96, Issue 11
Imaging spectroscopy reveals the effects of topography and logging on the leaf chemistry of tropical forest canopy trees
journal, December 2019
- Swinfield, Tom; Both, Sabine; Riutta, Terhi
- Global Change Biology, Vol. 26, Issue 2
Climate change effects on plant-soil feedbacks and consequences for biodiversity and functioning of terrestrial ecosystems
journal, November 2019
- Pugnaire, Francisco I.; Morillo, José A.; Peñuelas, Josep
- Science Advances, Vol. 5, Issue 11