Global mycorrhizal plant distribution linked to terrestrial carbon stocks

Soudzilovskaia, Nadejda A.; van Bodegom, Peter M.; Terrer, César; van’t Zelfde, Maarten; McCallum, Ian; Luke McCormack, M.; Fisher, Joshua B.; Brundrett, Mark C.; de Sá, Nuno César; Tedersoo, Leho

doi:10.1038/s41467-019-13019-2

Global mycorrhizal plant distribution linked to terrestrial carbon stocks

Journal Article · Thu Nov 07 00:00:00 EST 2019 · Nature Communications

DOI:https://doi.org/10.1038/s41467-019-13019-2· OSTI ID:1615894

^[1]; ^[1]; ^[2]; van’t Zelfde, Maarten ^[1]; McCallum, Ian ^[3]; ^[4]; Fisher, Joshua B. ^[5]; ^[6]; ^[1]; Tedersoo, Leho ^[7]

Leiden Univ. (Netherlands)
Univ. Autonoma de Barcelona (Spain); Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
International Inst. for Applied Systems, Laxenburg (Austria)
The Morton Arboretum, Lisle, IL (United States)
California Institute of Technology (CalTech), Pasadena, CA (United States). Jet Propulsion Lab. (JPL); Univ. of California, Los Angeles, CA (United States)
Univ. of Western Australia, Perth, WA (Australia)
Univ. of Tartu (Estonia)

Vegetation impacts on ecosystem functioning are mediated by mycorrhizas, plant–fungal associations formed by most plant species. Ecosystems dominated by distinct mycorrhizal types differ strongly in their biogeochemistry. Quantitative analyses of mycorrhizal impacts on ecosystem functioning are hindered by the scarcity of information on mycorrhizal distributions. Here we present global, high-resolution maps of vegetation biomass distribution by dominant mycorrhizal associations. Arbuscular, ectomycorrhizal, and ericoid mycorrhizal vegetation store, respectively, 241 ± 15, 100 ± 17, and 7 ± 1.8 GT carbon in aboveground biomass, whereas non-mycorrhizal vegetation stores 29 ± 5.5 GT carbon. Soil carbon stocks in both topsoil and subsoil are positively related to the community-level biomass fraction of ectomycorrhizal plants, though the strength of this relationship varies across biomes. We show that human-induced transformations of Earth’s ecosystems have reduced ectomycorrhizal vegetation, with potential ramifications to terrestrial carbon stocks. Our work provides a benchmark for spatially explicit and globally quantitative assessments of mycorrhizal impacts on ecosystem functioning and biogeochemical cycling.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA)

Grant/Contract Number:: AC52-07NA27344

OSTI ID:: 1615894

Report Number(s):: LLNL-JRNL--795542; 996752

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 10; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (62)

Distribution and Evolution of Mycorrhizal Types and Other Specialised Roots in Australia Brundrett, Mark C. Biogeography of Mycorrhizal Symbiosis https://doi.org/10.1007/978-3-319-56363-3_17	book	January 2017
Evolution of Ectomycorrhizal Symbiosis in Plants Tedersoo, Leho; Brundrett, Mark C. Biogeography of Mycorrhizal Symbiosis https://doi.org/10.1007/978-3-319-56363-3_19	book	June 2017
Mycorrhizas and dark septate root endophytes in polar regions Newsham, K. K.; Upson, R.; Read, D. J. Fungal Ecology, Vol. 2, Issue 1 https://doi.org/10.1016/j.funeco.2008.10.005	journal	February 2009
Harmonized soil property values for broad-scale modelling (WISE30sec) with estimates of global soil carbon stocks Batjes, N. H. Geoderma, Vol. 269 https://doi.org/10.1016/j.geoderma.2016.01.034	journal	May 2016
Distribution patterns of arbuscular mycorrhizal and non-mycorrhizal plant species in Germany Menzel, Andreas; Hempel, Stefan; Manceur, Ameur M. Perspectives in Plant Ecology, Evolution and Systematics, Vol. 21 https://doi.org/10.1016/j.ppees.2016.06.002	journal	August 2016
Uncertainty in plant functional type distributions and its impact on land surface models Hartley, A. J.; MacBean, N.; Georgievski, G. Remote Sensing of Environment, Vol. 203 https://doi.org/10.1016/j.rse.2017.07.037	journal	December 2017
The root of the matter: Linking root traits and soil organic matter stabilization processes Poirier, Vincent; Roumet, Catherine; Munson, Alison D. Soil Biology and Biochemistry, Vol. 120 https://doi.org/10.1016/j.soilbio.2018.02.016	journal	May 2018
Recent reversal in loss of global terrestrial biomass Liu, Yi Y.; van Dijk, Albert I. J. M.; de Jeu, Richard A. M. Nature Climate Change, Vol. 5, Issue 5 https://doi.org/10.1038/nclimate2581	journal	March 2015
Formation of soil organic matter via biochemical and physical pathways of litter mass loss Cotrufo, M. Francesca; Soong, Jennifer L.; Horton, Andrew J. Nature Geoscience, Vol. 8, Issue 10 https://doi.org/10.1038/ngeo2520	journal	September 2015
Nitrogen and phosphorus constrain the CO2 fertilization of global plant biomass Terrer, César; Jackson, Robert B.; Prentice, I. Colin Nature Climate Change, Vol. 9, Issue 9 https://doi.org/10.1038/s41558-019-0545-2	journal	August 2019
Climatic controls of decomposition drive the global biogeography of forest-tree symbioses Steidinger, B. S.; Crowther, T. W.; Liang, J. Nature, Vol. 569, Issue 7756 https://doi.org/10.1038/s41586-019-1128-0	journal	May 2019
A dataset of forest biomass structure for Eurasia Schepaschenko, Dmitry; Shvidenko, Anatoly; Usoltsev, Vladimir Scientific Data, Vol. 4, Issue 1 https://doi.org/10.1038/sdata.2017.70	journal	May 2017
Ectomycorrhizal fungi slow soil carbon cycling Averill, Colin; Hawkes, Christine V. Ecology Letters, Vol. 19, Issue 8 https://doi.org/10.1111/ele.12631	journal	June 2016
The Microbial Efficiency-Matrix Stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Cotrufo, M. Francesca; Wallenstein, Matthew D.; Boot, Claudia M. Global Change Biology, Vol. 19, Issue 4 https://doi.org/10.1111/gcb.12113	journal	February 2013
Tree-mycorrhizal associations detected remotely from canopy spectral properties Fisher, Joshua B.; Sweeney, Sean; Brzostek, Edward R. Global Change Biology, Vol. 22, Issue 7 https://doi.org/10.1111/gcb.13264	journal	April 2016
Tree mycorrhizal type predicts within-site variability in the storage and distribution of soil organic matter Craig, Matthew E.; Turner, Benjamin L.; Liang, Chao Global Change Biology, Vol. 24, Issue 8 https://doi.org/10.1111/gcb.14132	journal	April 2018
Effects of incorporating spatial autocorrelation into the analysis of species distribution data Dormann, Carsten F. Global Ecology and Biogeography, Vol. 16, Issue 2 https://doi.org/10.1111/j.1466-8238.2006.00279.x	journal	March 2007
The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests Phillips, Richard P.; Brzostek, Edward; Midgley, Meghan G. New Phytologist, Vol. 199, Issue 1 https://doi.org/10.1111/nph.12221	journal	April 2013
Quantitative assessment of the differential impacts of arbuscular and ectomycorrhiza on soil carbon cycling Soudzilovskaia, Nadejda A.; Heijden, Marcel G. A.; Cornelissen, Johannes H. C. New Phytologist, Vol. 208, Issue 1 https://doi.org/10.1111/nph.13447	journal	May 2015
Revisiting the ‘Gadgil effect’: do interguild fungal interactions control carbon cycling in forest soils? Fernandez, Christopher W.; Kennedy, Peter G. New Phytologist, Vol. 209, Issue 4 https://doi.org/10.1111/nph.13648	journal	September 2015
Production and turnover of ectomycorrhizal extramatrical mycelial biomass and necromass under elevated CO ₂ and nitrogen fertilization Ekblad, Alf; Mikusinska, Anna; Ågren, Göran I. New Phytologist, Vol. 211, Issue 3 https://doi.org/10.1111/nph.13961	journal	April 2016
Mycorrhizal fungi as drivers and modulators of terrestrial ecosystem processes Wurzburger, Nina; Brookshire, E. N. Jack; McCormack, M. Luke New Phytologist, Vol. 213, Issue 3 https://doi.org/10.1111/nph.14409	journal	January 2017
Ecosystem responses to elevated CO ₂ governed by plant-soil interactions and the cost of nitrogen acquisition Terrer, César; Vicca, Sara; Stocker, Benjamin D. New Phytologist, Vol. 217, Issue 2 https://doi.org/10.1111/nph.14872	journal	November 2017
Global diversity and geography of soil fungi Tedersoo, Leho; Bahram, Mohammad; Põlme, Sergei Science, Vol. 346, Issue 6213 https://doi.org/10.1126/science.1256688	journal	November 2014
Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism Davison, J.; Moora, M.; Opik, M. Science, Vol. 349, Issue 6251 https://doi.org/10.1126/science.aab1161	journal	August 2015
Mycorrhizal association as a primary control of the CO ₂ fertilization effect Terrer, César; Vicca, Sara; Hungate, Bruce A. Science, Vol. 353, Issue 6294 https://doi.org/10.1126/science.aaf4610	journal	June 2016
Plant-soil feedback and the maintenance of diversity in Mediterranean-climate shrublands Teste, François P.; Kardol, Paul; Turner, Benjamin L. Science, Vol. 355, Issue 6321 https://doi.org/10.1126/science.aai8291	journal	January 2017
Modeling the Terrestrial Biosphere Fisher, Joshua B.; Huntzinger, Deborah N.; Schwalm, Christopher R. Annual Review of Environment and Resources, Vol. 39, Issue 1 https://doi.org/10.1146/annurev-environ-012913-093456	journal	October 2014
The Abuse of Power: The Pervasive Fallacy of Power Calculations for Data Analysis Hoenig, John M.; Heisey, Dennis M. The American Statistician, Vol. 55, Issue 1 https://doi.org/10.1198/000313001300339897	journal	February 2001
SoilGrids250m: Global gridded soil information based on machine learning Hengl, Tomislav; Mendes de Jesus, Jorge; Heuvelink, Gerard B. M. PLOS ONE, Vol. 12, Issue 2 https://doi.org/10.1371/journal.pone.0169748	journal	February 2017
The Mutualism–Parasitism Continuum in Ectomycorrhizas: a Quantitative Assessment Using Meta-Analysis Karst, Justine; Marczak, Laurie; Jones, Melanie D. Ecology, Vol. 89, Issue 4 https://doi.org/10.1890/07-0823.1	journal	April 2008
Spatial Data Access Tool (SDAT) Daac, Ornl ORNL Distributed Active Archive Center https://doi.org/10.3334/ornldaac/1388	collection	January 2017
Neglecting plant–microbe symbioses leads to underestimation of modeled climate impacts Shi, Mingjie; Fisher, Joshua B.; Phillips, Richard P. Biogeosciences, Vol. 16, Issue 2 https://doi.org/10.5194/bg-16-457-2019	journal	January 2019
Plant functional type classification for earth system models: results from the European Space Agency's Land Cover Climate Change Initiative Poulter, B.; MacBean, N.; Hartley, A. Geoscientific Model Development, Vol. 8, Issue 7 https://doi.org/10.5194/gmd-8-2315-2015	journal	January 2015
Modeling the carbon cost of plant nitrogen acquisition: Mycorrhizal trade-offs and multipath resistance uptake improve predictions of retranslocation: Carbon cost of mycorrhizae Brzostek, Edward R.; Fisher, Joshua B.; Phillips, Richard P. Journal of Geophysical Research: Biogeosciences, Vol. 119, Issue 8 https://doi.org/10.1002/2014JG002660	journal	August 2014
Mixed effects models and extensions in ecology with R Zuur, Alain F.; Ieno, Elena N.; Walker, Neil Statistics for Biology and Health https://doi.org/10.1007/978-0-387-87458-6	book	January 2009
Mycorrhizas in ecosystems Read, D. J. Experientia, Vol. 47, Issue 4 https://doi.org/10.1007/BF01972080	journal	April 1991
Phylogenetic distribution and evolution of mycorrhizas in land plants Wang, B.; Qiu, Y. -L. Mycorrhiza, Vol. 16, Issue 5 https://doi.org/10.1007/s00572-005-0033-6	journal	May 2006
Stand Structure and Recent Climate Change Constrain Stand Basal Area Change in European Forests: A Comparison Across Boreal, Temperate, and Mediterranean Biomes Ruiz-Benito, P.; Madrigal-González, J.; Ratcliffe, S. Ecosystems, Vol. 17, Issue 8 https://doi.org/10.1007/s10021-014-9806-0	journal	August 2014
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 Brundrett, Mark C. Plant and Soil, Vol. 320, Issue 1-2 https://doi.org/10.1007/s11104-008-9877-9	journal	February 2009
Mapping the potential mycorrhizal associations of the conterminous United States of America Swaty, Randy; Michael, Haley M.; Deckert, Ron Fungal Ecology, Vol. 24 https://doi.org/10.1016/j.funeco.2016.05.005	journal	December 2016
Long term tillage, cover crop, and fertilization effects on microbial community structure, activity: Implications for soil quality Mbuthia, Lilian Wanjiru; Acosta-Martínez, Veronica; DeBruyn, Jennifer Soil Biology and Biochemistry, Vol. 89 https://doi.org/10.1016/j.soilbio.2015.06.016	journal	October 2015
Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage Averill, Colin; Turner, Benjamin L.; Finzi, Adrien C. Nature, Vol. 505, Issue 7484 https://doi.org/10.1038/nature12901	journal	January 2014
Engineering Meteorological Features to Select Stress Tolerant Hybrids in Maize Mimić, Gordan; Brdar, Sanja; Brkić, Milica Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-60366-y	journal	February 2020
Decline of vesicular-arbuscular mycorrhizae in long fallow disorder of field crops and its expression in phosphorus deficiency of sunflower Thompson, Jp Australian Journal of Agricultural Research, Vol. 38, Issue 5 https://doi.org/10.1071/AR9870847	journal	January 1987
Soil carbon debt of 12,000 years of human land use Sanderman, Jonathan; Hengl, Tomislav; Fiske, Gregory J. Proceedings of the National Academy of Sciences, Vol. 114, Issue 36 https://doi.org/10.1073/pnas.1706103114	journal	August 2017
Mycorrhizas in Ecosystems Pedersen, Christian T. Soil Science, Vol. 157, Issue 2 https://doi.org/10.1097/00010694-199402000-00010	journal	January 1994
Association of ectomycorrhizal trees with high carbon-to-nitrogen ratio soils across temperate forests is driven by smaller nitrogen not larger carbon stocks Zhu, Kai; McCormack, M. Luke; Lankau, Richard A. Journal of Ecology, Vol. 106, Issue 2 https://doi.org/10.1111/1365-2745.12918	journal	February 2018
Mycorrhizal types differ in ecophysiology and alter plant nutrition and soil processes Tedersoo, Leho; Bahram, Mohammad Biological Reviews, Vol. 94, Issue 5 https://doi.org/10.1111/brv.12538	journal	May 2019
Continental-scale nitrogen pollution is shifting forest mycorrhizal associations and soil carbon stocks Averill, Colin; Dietze, Michael C.; Bhatnagar, Jennifer M. Global Change Biology, Vol. 24, Issue 10 https://doi.org/10.1111/gcb.14368	journal	July 2018
Anthropogenic transformation of the biomes, 1700 to 2000: Anthropogenic transformation of the biomes Ellis, Erle C.; Klein Goldewijk, Kees; Siebert, Stefan Global Ecology and Biogeography https://doi.org/10.1111/j.1466-8238.2010.00540.x	journal	June 2010
Are ectomycorrhizal fungi alleviating or aggravating nitrogen limitation of tree growth in boreal forests? Näsholm, Torgny; Högberg, Peter; Franklin, Oskar New Phytologist, Vol. 198, Issue 1 https://doi.org/10.1111/nph.12139	journal	January 2013
Similar below-ground carbon cycling dynamics but contrasting modes of nitrogen cycling between arbuscular mycorrhizal and ectomycorrhizal forests Lin, Guigang; McCormack, M. Luke; Ma, Chengen New Phytologist, Vol. 213, Issue 3 https://doi.org/10.1111/nph.14206	journal	September 2016
Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics Bennett, Jonathan A.; Maherali, Hafiz; Reinhart, Kurt O. Science, Vol. 355, Issue 6321 https://doi.org/10.1126/science.aai8212	journal	January 2017
Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning Leake, Jonathan; Johnson, David; Donnelly, Damian Canadian Journal of Botany, Vol. 82, Issue 8 https://doi.org/10.1139/b04-060	journal	August 2004
Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes Read, David J.; Leake, Jonathan R.; Perez-Moreno, Jesus Canadian Journal of Botany, Vol. 82, Issue 8 https://doi.org/10.1139/b04-123	journal	August 2004
The Structure, Distribution, and Biomass of the World's Forests Pan, Yude; Birdsey, Richard A.; Phillips, Oliver L. Annual Review of Ecology, Evolution, and Systematics, Vol. 44, Issue 1 https://doi.org/10.1146/annurev-ecolsys-110512-135914	journal	November 2013
Terrestrial Ecoregions of the World: A New Map of Life on Earth Olson, David M.; Dinerstein, Eric; Wikramanayake, Eric D. BioScience, Vol. 51, Issue 11 https://doi.org/10.1641/0006-3568(2001)051[0933:TEOTWA]2.0.CO;2	journal	January 2001
Spatial Data Access Tool (SDAT) Daac, Ornl ORNL Distributed Active Archive Center https://doi.org/10.3334/ORNLDAAC/1388	collection	January 2017
Climatic controls of decomposition drive the global biogeography of forest-tree symbioses Steidinger, B. S.; Crowther, T. W.; Liang, J. Springer https://doi.org/10.5167/uzh-171436	text	January 2019
Plant functional type classification for Earth System Models: results from the European Space Agency's Land Cover Climate Change Initiative Poulter, B.; MacBean, N.; Hartley, A. Geoscientific Model Development Discussions, Vol. 8, Issue 1 https://doi.org/10.5194/gmdd-8-429-2015	journal	January 2015
The Mutualism–Parasitism Continuum in Ectomycorrhizas: a Quantitative Assessment Using Meta-Analysis Karst, Justine; Marczak, Laurie; Jones, Melanie D. Figshare https://doi.org/10.6084/m9.figshare.c.3300290	collection	January 2016

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Nitrogen and phosphorus constrain the CO2 fertilization of global plant biomass Terrer, César; Jackson, Robert B.; Prentice, I. Colin Nature Climate Change, Vol. 9, Issue 9 https://doi.org/10.1038/s41558-019-0545-2	journal	August 2019