One of the most distinct but unresolved global patterns is the apparent variation in plant–symbiont nutrient strategies across biomes. This pattern is central to our understanding of plant–soil–nutrient feedbacks in the land biosphere, which, in turn, are essential for our ability to predict the future dynamics of the Earth system. Here, we present an evolution-based trait-modelling approach for resolving (1) the organization of plant–symbiont relationships across biomes worldwide and (2) the emergent consequences for plant community composition and land biogeochemical cycles. Using game theory, we allow plants to use different belowground strategies to acquire nutrients and compete within local plant–soil–nutrient cycles in boreal, temperate and tropical biomes. The evolutionarily stable strategies that emerge from this analysis allow us to predict the distribution of belowground symbioses worldwide, the sequence and timing of plant succession, the bistability of ecto- versus arbuscular mycorrhizae in temperate and tropical forests, and major differences in the land carbon and nutrient cycles across biomes. Our findings imply that belowground symbioses have been central to the evolutionary assembly of plant communities and plant–nutrient feedbacks at the scale of land biomes. We conclude that complex global patterns emerge from local between-organism interactions in the context of Darwinian natural selection and evolution, and that the underlying dynamics can be mechanistically probed by our low-dimensional modelling approach.
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The data that support the findings of this study are available from the corresponding author upon reasonable request.
Read, D. J. in The Ecology and Physiology of the Fungal Mycelium (eds Jennings, D. H. & Yayner, A. M. D.) 215–240 (Cambridge Univ. Press, New York, 1984).
Smith, S. E. & Read, D. J. Mycorrhizal Symbiosis 3rd edn (Elsevier Science, Academic press, 2008).
Lambers, H., Raven, J. A., Shaver, G. R. & Smith, S. E. Plant nutrient-acquisition strategies change with soil age. Trends Ecol. Evol. 23, 95–103 (2008).
Bennett, J. A. et al. Plant–soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science 355, 181–184 (2017).
Sheffer, E., Batterman, S. A., Levin, S. A. & Hedin, L. O. Biome-scale nitrogen fixation strategies selected by climatic constraints on nitrogen cycle. Nat. Plants 1, 15182 (2015).
Houlton, B. Z., Wang, Y. P., Vitousek, P. M. & Field, C. B. A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454, 327–334 (2008).
Batterman, S. A. et al. Key role of symbiotic dinitrogen fixation in tropical forest secondary succession. Nature 502, 224–227 (2013).
Averill, C., Turner, B. L. & Finzi, A. C. Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505, 543–545 (2014).
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).
Hedin, L. O., Brookshire, E. N. J., Menge, D. N. L. & Barron, A. R. The nitrogen paradox in tropical forest ecosystems. Annu. Rev. Ecol. Evol. Syst. 40, 613–635 (2009).
Smith, S. E. & Smith, F. A. Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu. Rev. Plant Biol. 62, 227–250 (2011).
Talbot, J. M., Allison, S. D. & Treseder, K. K. Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct. Ecol. 22, 955–963 (2008).
McGuire, K. L., Zak, D. R., Edwards, I. P., Blackwood, C. B. & Upchurch, R. Slowed decomposition is biotically mediated in an ectomycorrhizal, tropical rain forest. Oecologia 164, 785–795 (2010).
Sprent, J. Legume Nodulation: a Global Perspective (John Wiley & Sons, Wiley-Blackwell, 2009).
Ma, Z. et al. Evolutionary history resolves global organization of root functional traits. Nature 555, 94–97 (2018).
Cairney, J. W. G. Evolution of mycorrhiza systems. Naturwissenschaften 87, 467–475 (2000).
Brundrett, M. C. Coevolution of roots and mycorrhizas of land plants. New Phytol. 154, 275–304 (2002).
Tedersoo, L., May, T. W. & Smith, M. E. Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20, 217–263 (2010).
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).
Jenny, H. Causes of the high nitrogen and organic matter content of certain tropical forest soils. Soil Sci. 69, 63–69 (1950).
Peh, K. S. H., Lewis, S. L. & Lloyd, J. Mechanisms of monodominance in diverse tropical tree-dominated systems. J. Ecol. 99, 891–898 (2011).
Peay, K. G., Kennedy, P. G., Davies, S. J., Tan, S. & Bruns, T. D. Potential link between plant and fungal distributions in a dipterocarp rainforest: community and phylogenetic structure of tropical ectomycorrhizal fungi across a plant and soil ecotone. New Phytol. 185, 529–542 (2010).
Barron, A. R., Purves, D. W. & Hedin, L. O. Facultative nitrogen fixation by canopy legumes in a lowland tropical forest. Oecologia 165, 511–520 (2011).
Bauters, M., Mapenzi, N., Kearsley, E., Vanlauwe, B. & Boeckx, P. Facultative nitrogen fixation by legumes in the central Congo basin is downregulated during late successional stages. Biotropica 48, 281–284 (2016).
Menge, D. N. L. & Hedin, L. O. Nitrogen fixation in different biogeochemical niches along a 120 000-year chronosequence in New Zealand. Ecology 90, 2190–2201 (2009).
Stephenson, N. L. & van Mantgem, P. J. Forest turnover rates follow global and regional patterns of productivity. Ecol. Lett. 8, 524–531 (2005).
Fay, P. A. et al. Grassland productivity limited by multiple nutrients. Nat. Plants 1, 15080 (2015).
Davidson, E. A. et al. Nitrogen and phosphorus limitation of biomass growth in a tropical secondary forest. Ecol. Appl. 14, 150–163 (2004).
Batterman, S. A., Wurzburger, N. & Hedin, L. O. Nitrogen and phosphorus interact to control tropical symbiotic N2 fixation: a test in Inga punctata. J. Ecol. 101, 1400–1408 (2013).
Gökkaya, K., Hurd, T. M. & Raynal, D. J. Symbiont nitrogenase, alder growth, and soil nitrate response to phosphorus addition in alder (Alnus incana ssp. rugosa) wetlands of the Adirondack Mountains, New York State, USA. Environ. Exp. Bot. 55, 97–109 (2006).
Uliassi, D. D. & Ruess, R. W. Limitations to symbiotic nitrogen fixation in primary succession on the Tanana River floodplain. Ecology 83, 88–103 (2002).
Vitousek, P. M. & Farrington, H. Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry 37, 63–75 (1997).
Connell, J. H. & Lowman, M. D. Low-diversity tropical rain forests: some possible mechanisms for their existence. Am. Nat. 134, 88–119 (1989).
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).
Scheffer, M. et al. Early-warning signals for critical transitions. Nature 461, 53–59 (2009).
Phillips, O. & Miller, J. S. Global Patterns of Plant Diversity: Alwyn H. Gentry’s Forest Transect Data Set (Missouri Botanical Press, St. Louis, 2002).
Read, D. J. Mycorrhizas in ecosystems. Experientia 47, 376–391 (1991).
Read, D. J. & Perez‐Moreno, J. Mycorrhizas and nutrient cycling in ecosystems—a journey towards relevance? New Phytol. 157, 475–492 (2003).
HussDanell, K. Tansley Review No. 93. Actinorhizal symbioses and their N2 fixation. New Phytol. 136, 375–405 (1997).
Bond, G. in Biological Nitrogen Fixation in Forest Ecosystems: Foundations and Applications (eds Gordon, J. C. & Wheeler, C. T.) 55–87 (Martinus Nijhoff Publishers, The Hague, 1983).
Racette, S. & Torrey, J. G. The isolation, culture and infectivity of a Frankia strain from Gymnostoma papuanum (Casuarinaceae). Plant Soil 118, 165–170 (1989).
Pawlowski, K. & Newton, W. E. Nitrogen-Fixing Actinorhizal Symbioses (Springer, Dordrecht, 2008).
Wang, B. & Qiu, Y. L. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16, 299–363 (2006).
Brundrett, M. Mycorrhizas in natural ecosystems. Adv. Ecol. Res. 21, 171–313 (1991).
Beer, C. et al. Terrestrial gross carbon dioxide uptake: global distribution and covariation with climate. Science 329, 834–838 (2010).
Manzoni, S., Trofymow, J. A., Jackson, R. B. & Porporato, A. Stoichiometric controls on carbon, nitrogen, and phosphorus dynamics in decomposing litter. Ecol. Monogr. 80, 89–106 (2010).
Lin, G. G., McCormack, M. L., Ma, C. E. & Guo, D. L. Similar below-ground carbon cycling dynamics but contrasting modes of nitrogen cycling between arbuscular mycorrhizal and ectomycorrhizal forests. New Phytol. 213, 1440–1451 (2017).
Barron, A. R. et al. Molybdenum limitation of asymbiotic nitrogen fixation in tropical forest soils. Nat. Geosci. 2, 42–45 (2009).
Binkley, D., Sollins, P., Bell, R., Sachs, D. & Myrold, D. Biogeochemistry of adjacent conifer and alder-conifer stands. Ecology 73, 2022–2033 (1992).
Fick, S. E. & Hijmans, R. J. WorldClim 2: new 1‐km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).
Fischer, G. et al. Global Agro-ecological Zones Assessment for Agriculture (GAEZ 2008) (IIASA & FAO, 2008).
Smithson, M. & Verkuilen, J. A better lemon squeezer? Maximum-likelihood regression with beta-distributed dependent variables. Psychol. Methods 11, 54–71 (2006).
Bayer, F. M. & Cribari-Neto, F. Model selection criteria in beta regression with varying dispersion. Commun. Stat. Simul. Comput. 46, 729–746 (2017).
Cribari-Neto, F. & Zeileis, A. Beta regression in R. J. Appl. Stat. 34, 1–24 (2010).
Pan, Y. D., Birdsey, R. A., Phillips, O. L. & Jackson, R. B. The structure, distribution, and biomass of the world’s forests. Annu. Rev. Ecol. Evol. Syst. 44, 593–622 (2013).
Vitousek, P. & Sanford, R. Nutrient cycling in moist tropical forest. Annu. Rev. Ecol. Syst. 17, 137–167 (1986).
Menge, D. N. L., Lichstein, J. W. & Angeles-Perez, G. Nitrogen fixation strategies can explain the latitudinal shift in nitrogen-fixing tree abundance. Ecology 95, 2236–2245 (2014).
Ter Steege, H. et al. Continental-scale patterns of canopy tree composition and function across Amazonia. Nature 443, 444–447 (2006).
Reich, P. B., Grigal, D. F., Aber, J. D. & Gower, S. T. Nitrogen mineralization and productivity in 50 hardwood and conifer stands on diverse soils. Ecology 78, 335–347 (1997).
Cleveland, C. C. et al. Global patterns of terrestrial biological nitrogen (N2) fixation in natural ecosystems. Glob. Biogeochem. Cycles 13, 623–645 (1999).
Sullivan, B. W. et al. Spatially robust estimates of biological nitrogen (N) fixation imply substantial human alteration of the tropical N cycle. Proc. Natl Acad. Sci. USA 111, 8101–8106 (2014).
Hedin, L. O., Armesto, J. J. & Johnson, A. H. Patterns of nutrient loss from unpolluted, old-growth temperate forests—evaluation of biogeochemical theory. Ecology 76, 493–509 (1995).
Brookshire, E. N. J., Hedin, L. O., Newbold, J. D., Sigman, D. M. & Jackson, J. K. Sustained losses of bioavailable nitrogen from montane tropical forests. Nat. Geosci. 5, 123–126 (2012).
Bai, E., Houlton, B. Z. & Wang, Y. P. Isotopic identification of nitrogen hotspots across natural terrestrial ecosystems. Biogeosciences 9, 3287–3304 (2012).
Fang, Y. T. et al. Microbial denitrification dominates nitrate losses from forest ecosystems. Proc. Natl Acad. Sci. USA 112, 1470–1474 (2015).
Houlton, B. Z., Sigman, D. M. & Hedin, L. O. Isotopic evidence for large gaseous nitrogen losses from tropical rainforests. Proc. Natl Acad. Sci. USA 103, 8745–8750 (2006).
Hedin, L. O., Vitousek, P. M. & Matson, P. A. Nutrient losses over four million years of tropical forest development. Ecology 84, 2231–2255 (2003).
Lewis, W. M., Melack, J. M., McDowell, W. H., McClain, M. & Richey, J. E. Nitrogen yields from undisturbed watersheds in the Americas. Biogeochemistry 46, 149–162 (1999).
Hao, S., Xue, J., Guo, D. & Wang, D. Earliest rooting system and root:shoot ratio from a new Zosterophyllum plant. New Phytol. 185, 217–225 (2010).
Strullu‐Derrien, C. et al. Fungal associations in Horneophyton ligneri from the Rhynie Chert (c. 407 million year old) closely resemble those in extant lower land plants: novel insights into ancestral plant–fungus symbioses. New Phytol. 203, 964–979 (2014).
Bonfante, P. & Genre, A. Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nat. Commun. 1, 48 (2010).
Henkel, T. W. Monodominance in the ectomycorrhizal Dicymbe corymbosa (Caesalpiniaceae) from Guyana. J. Trop. Ecol. 19, 417–437 (2003).
Makana, J. R. et al. Demography and biomass change in monodominant and mixed old-growth forest of the Congo. J. Trop. Ecol. 27, 447–461 (2011).
Hayman, D. Mycorrhizae of nitrogen-fixing legumes. MIRCEN J. Appl. Microbiol. Biotechnol. 2, 121–145 (1986).
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).
Güsewell, S. N. P ratios in terrestrial plants: variation and functional significance. New Phytol. 164, 243–266 (2004).
Vitousek, P. M., Matson, P. A. & Vancleve, K. Nitrogen availability and nitrification during succession—primary, secondary, and old-field seres. Plant Soil 115, 229–239 (1989).
Manzoni, S., Jackson, R. B., Trofymow, J. A. & Porporato, A. The global stoichiometry of litter nitrogen mineralization. Science 321, 684–686 (2008).
Overpeck, J. T., Rind, D. & Goldberg, R. Climate-induced changes in forest disturbance and vegetation. Nature 343, 51–53 (1990).
We thank S. Levin, D. Guo, N. Wurzburger, E. Sheffer and members of the Hedin laboratory for helpful comments, J. Sprent for sharing the nodulation database, Y. L. Qiu for sharing the mycorrhizal database, J. Lichstein and W. Liao for sharing the FIA database, Y. Sun for assisting with artwork and S. Wang for assisting with database compilation. We thank A. H. Gentry, the Missouri Botanical Garden and collectors who assisted A. H. Gentry or contributed data for specific A. H. Gentry sites. This work was supported by grants to L.O.H. from the Dean of Faculty Fund and the Carbon Mitigation Initiative at Princeton University.
The authors declare no competing interests.
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Supplementary Figures 1–7, Supplementary Tables 1–3, Supplementary Notes 1–10 and Supplementary References
Tropical forest community successional dynamics. Visual demonstration of successional dynamics (1,000 yrs) from a nutrient-poor tropical forest using a landscape of 15x15 patches. Each patch is represented by 3 trees, AMF in green, EMF in purple, and NFB in orange, with the tree height and crown radius proportional to the total biomass of each symbiotic group in each patch. The landscape recovered from 99% destruction of its equilibrium biomass, with NFB accounting for 10% of starting biomass and AMF and EMF each accounting for 45%. NFB dominated early succession, but the strategy was increasingly outcompeted by AMF as succession proceeded. In late succession, EMF became abundant and coexisted with AMF at the landscape scale as forest biomass again approached equilibrium. Throughout succession, stochastic disturbance occurred at the scale of individual patches, and contributed to the presence of NFB trees in the landscape.
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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). https://doi.org/10.1038/s41559-018-0759-0
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