Climatic controls of decomposition drive the global biogeography of forest-tree symbioses

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.A spatially explicit global map of tree symbioses with nitrogen-fixing bacteria and mycorrhizal fungi reveals that climate variables are the primary drivers of the distribution of different types of symbiosis.

N. Picard | C. Zhang | M. Herold | N. Picard | F. Rovero | A. Marshall | Jean‐François Bastin | D. Routh | T. Crowther | F. Kraxner | P. Reich | B. Enquist | O. Phillips | E. Broadbent | P. Brancalion | A. A. Almeyda Zambrano | M. Schelhaas | G. Nabuurs | A. Shvidenko | T. Killeen | D. Gianelle | Y. Malhi | D. Coomes | S. Lewis | T. Feldpausch | J. Barroso | M. Bastian | F. Bongers | C. Clark | D. Harris | Emanuel H. Martin | A. Araujo-Murakami | Alexander Parada-Gutierrez | L. Poorter | J. Poulsen | D. Sheil | J. Silva-Espejo | M. Silveira | H. Steege | R. Condit | T. Baker | Yude Pan | Mait Lang | E. Cienciala | M. Köhl | R. Chazdon | S. Vieira | H. Verbeeck | J. Herbohn | D. Neill | N. Pitman | L. Arroyo | G. Aymard | O. Bánki | C. Mendoza | F. Valladares | C. Hui | G. D. Werner | G. Alberti | F. Wittmann | P. Boeckx | L. Finér | D. Kennard | T. Eyre | N. Imai | K. Kitayama | V. Avitabile | T. Zawila-Niedzwiecki | V. Johannsen | C. Antón-Fernández | V. Šebeň | K. von Gadow | B. Schmid | F. Brearley | A. Hemp | B. Sonké | P. Mundhenk | S. Wiser | K. Peay | E. Kearsley | B. DeVries | J. Oleksyn | J. Svenning | A. Paquette | D. Schepaschenko | Zhi-Xin Zhu | M. Piedade | J. Schöngart | N. Targhetta | M. Rodeghiero | P. Schall | C. Ammer | K. Stereńczak | H. Pretzsch | P. Saikia | M. L. Khan | H. Bruelheide | M. Scherer‐Lorenzen | T. Jucker | L. Frizzera | J. Fridman | D. Piotto | R. Bałazy | F. Bussotti | S. de-Miguel | M. Huber | J. Gamarra | C. Merow | D. Kenfack | E. H. Honorio Coronado | B. Marimon | R. Brienen | R. Zagt | B. Jaroszewicz | F. van der Plas | P. Niklaus | B. Westerlund | O. Bouriaud | P. Sist | Eric B. Searle | B. Hérault | H. Glick | G. Hengeveld | S. Pfautsch | H. Viana | Nadja Tchebakova | James Watson | Huicui Lu | E. Parfenova | H. S. Kim | Susanne Brandl | V. Neldner | M. Ngugi | A. Jagodziński | P. Peri | P. Álvarez-Loayza | V. Wortel | J. Meave | E. Rutishauser | P. Birnbaum | M. Svoboda | R. Cazzolla Gatti | A. Roopsind | Raquel S. Thomas | Mathieu Decuyper | Eric Marcon | N. Parthasarathy | B. H. Marimon‐Junior | T. Ibanez | R. Vásquez Martínez | C. Fletcher | R. César | A. L. de Gasper | Fernando Cornejo Valverde | K. Kartawinata | A. Poulsen | P. Umunay | S. Dayanandan | M. G. Nava-Miranda | G. Derroire | James Singh | G. Keppel | E. Tikhonova | P. Saner | L. Alves | V. Usoltsev | F. Slik | Aurélie Dourdain | M. Parren | S. Rolim | H. Korjus | Abel Monteagudo Mendoza | S. A. Mukul | T. Fayle | D. Laarmann | P. Ontikov | O. Martynenko | A. Hillers | A. F. Souza | David B. Clark | G. Colletta | V. Karminov | M. Zhou | P. B. Reich | Christian Salas‐Eljatib | M. Abegg | B. S. Steidinger | T. W. Crowther | J. Liang | M. E. Nuland | G. D. A. Werner | G. Nabuurs | S. de-Miguel | M. Zhou | B. Herault | X. Zhao | D. Routh | K. G. Peay | GFBI consortium | L. Birigazzi | J. Cumming | I. C. Zo-Bi | A. Hector | A. B. Fandohan | Hyunkook Cho | Chelsea Chisholm | Minjee Park | N. Obiang | C. Y. Adou Yao | B. Steidinger | R. Nevenić | N. Picard | Hua‐Feng Wang | V. Moreno | Tran Van Do | Goran Češljar | P. Crim | Esteban Alvarez-Davila | Freddy Ramirez Arevalo | I. Djordjevic | C. A. Joly | Omar Melo-Cruz | R. Bitariho | J. Serra-Diaz | J. Corral-Rivas | Z. Zhu | Han Y. H. Chen | Brian Salvin Maitner | M. Fischer | S. Kepfer-Rojas | I. Polo | Edgar Ortiz-Malavasi | J. Liang | X. Zhao | C. Zhang | M. E. Van Nuland | N. Lukina | Ilbin Jung | Meinrad C. Yves Giorgio Angelica Esteban Patricia Luciana Abegg Adou Yao Alberti Almeyda Zambrano A | Amaral Iêda | Zorayda Restrepo-Correa | S. Kepfer‐Rojas | M. Zhou

[1]  Sandra Carberry,et al.  The Past, the Present, and the Future , 2016, UMAP.

[2]  José Luis Hernández-Stefanoni,et al.  Legume abundance along successional and rainfall gradients in Neotropical forests , 2018, Nature Ecology & Evolution.

[3]  S. Vicca,et al.  Mycorrhizal association as a primary control of the CO2 fertilization effect , 2016, Science.

[4]  J. Liski,et al.  Litter decomposition affected by climate and litter quality—Testing the Yasso model with litterbag data from the Canadian intersite decomposition experiment , 2005 .

[5]  Eduard Szöcs,et al.  taxize: taxonomic search and retrieval in R , 2013, F1000Research.

[6]  Meelis Pärtel,et al.  Global database of plants with root‐symbiotic nitrogen fixation: NodDB , 2018 .

[7]  A. Staver,et al.  Aridity, not fire, favors nitrogen-fixing plants across tropical savanna and forest biomes. , 2016, Ecology.

[8]  Richard P Phillips,et al.  The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests. , 2013, The New phytologist.

[9]  J. Cornelissen,et al.  Evolutionary signals of symbiotic persistence in the legume–rhizobia mutualism , 2015, Proceedings of the National Academy of Sciences.

[10]  Nicole A. Hynson,et al.  New evidence of ectomycorrhizal fungi in the Hawaiian Islands associated with the endemic host Pisonia sandwicensis (Nyctaginaceae) , 2014 .

[11]  C. Bettigole,et al.  Mapping tree density at a global scale , 2015, Nature.

[12]  J. Bever,et al.  Dominant mycorrhizal association of trees alters carbon and nutrient cycling by selecting for microbial groups with distinct enzyme function. , 2017, The New phytologist.

[13]  Dali Guo,et al.  Evolutionary history resolves global organization of root functional traits , 2018, Nature.

[14]  J. H. Burns,et al.  Symbioses with nitrogen-fixing bacteria: nodulation and phylogenetic data across legume genera. , 2017, Ecology.

[15]  D. Menge,et al.  Global climate change will increase the abundance of symbiotic nitrogen‐fixing trees in much of North America , 2017, Global change biology.

[16]  Jefferson S. Hall,et al.  Key role of symbiotic dinitrogen fixation in tropical forest secondary succession , 2013, Nature.

[17]  D. Hibbett,et al.  Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors , 2015, The New phytologist.

[18]  Jens Kattge,et al.  A single evolutionary innovation drives the deep evolution of symbiotic N2-fixation in angiosperms , 2014, Nature Communications.

[19]  L. Hedin,et al.  Global plant–symbiont organization and emergence of biogeochemical cycles resolved by evolution-based trait modelling , 2019, Nature Ecology & Evolution.

[20]  K. Peay The Mutualistic Niche: Mycorrhizal Symbiosis and Community Dynamics , 2016 .

[21]  B. Wang,et al.  Phylogenetic distribution and evolution of mycorrhizas in land plants , 2006, Mycorrhiza.

[22]  D. Binkley,et al.  Biogeochemistry of adjacent conifer and alder-conifer stands , 1992 .

[23]  C. Field,et al.  A unifying framework for dinitrogen fixation in the terrestrial biosphere , 2008, Nature.

[24]  D. Soltis,et al.  Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Eduard Szöcs,et al.  taxize: taxonomic search and retrieval in R , 2013, F1000Research.

[26]  P. Reich,et al.  Global patterns of plant leaf N and P in relation to temperature and latitude. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[27]  P. Reich,et al.  Geographic range predicts photosynthetic and growth response to warming in co-occurring tree species , 2015 .

[28]  Mark C. Brundrett 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 , 2009, Plant and Soil.

[29]  D. Menge,et al.  Nitrogen fixation strategies can explain the latitudinal shift in nitrogen-fixing tree abundance. , 2014, Ecology.

[30]  Filippo Bussotti,et al.  Positive biodiversity-productivity relationship predominant in global forests , 2016, Science.

[31]  Damian P. Donnelly,et al.  Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning , 2004 .

[32]  M. V. D. van der Heijden,et al.  Mycorrhizal ecology and evolution : the past , the present , and the future , 2015 .

[33]  O. Ovaskainen,et al.  Roots and Associated Fungi Drive Long-Term Carbon Sequestration in Boreal Forest , 2013, Science.

[34]  D. Read,et al.  Mycorrhizas in ecosystems , 1991, Experientia.

[35]  Steffen Fritz,et al.  A dataset of forest biomass structure for Eurasia , 2017, Scientific Data.

[36]  Benjamin L Turner,et al.  Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage , 2014, Nature.

[37]  J. Liski,et al.  Leaf litter decomposition-Estimates of global variability based on Yasso07 model , 2009, 0906.0886.

[38]  Alexander R. Barron,et al.  The Nitrogen Paradox in Tropical Forest Ecosystems , 2009 .

[39]  S. Carpenter,et al.  Catastrophic shifts in ecosystems , 2001, Nature.

[40]  L. Tedersoo,et al.  Evolutionary history of mycorrhizal symbioses and global host plant diversity. , 2018, The New phytologist.

[41]  J. A. Bennett,et al.  Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics , 2017, Science.

[42]  Jeffrey S. Evans Random Forests Model Selection and Performance Evaluation , 2015 .

[43]  C. Hawkes,et al.  Ectomycorrhizal fungi slow soil carbon cycling. , 2016, Ecology letters.

[44]  H. Lambers,et al.  Plant adaptations to severely phosphorus-impoverished soils. , 2015, Current opinion in plant biology.

[45]  J. R. King,et al.  Climate fails to predict wood decomposition at regional scales , 2014 .

[46]  T. Daufresne,et al.  SCALING OF C:N:P STOICHIOMETRY IN FORESTS WORLDWIDE: IMPLICATIONS OF TERRESTRIAL REDFIELD‐TYPE RATIOS , 2004 .

[47]  Benjamin L Turner,et al.  An ectomycorrhizal nitrogen economy facilitates monodominance in a neotropical forest. , 2016, Ecology letters.