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Global plant–symbiont organization and emergence of biogeochemical cycles resolved by evolution-based trait modelling

Nature Ecology & Evolution volume 3, pages 239–250 (2019)Cite this article

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A Publisher Correction to this article was published on 26 May 2020

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Abstract

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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Fig. 1: Timeline of the plant–symbiont relationship on land.
Fig. 2: Global geographical distribution of AMF, EMF and NFB trees.
Fig. 3: Prediction of community composition and nutrient limitation across biomes.
Fig. 4: AMF–EMF bistable states in low-fertility tropical forest, and divergence of communities into alternative stable states.
Fig. 5: Observed and predicted EMF relative abundances across the US FIA plots, and bistable dynamics in the temperate region.

Code availability

The R scripts used in Fig. 2 and MATLAB scripts used in Figs. 3–5 and Table 1 are available from the corresponding author upon reasonable request.

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Change history

  • 26 May 2020

    An amendment to this paper has been published and can be accessed via a link at the top of the paper.

References

  1. 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).

  2. Smith, S. E. & Read, D. J. Mycorrhizal Symbiosis 3rd edn (Elsevier Science, Academic press, 2008).

  3. 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).

    PubMed  Google Scholar 

  4. Bennett, J. A. et al. Plant–soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science 355, 181–184 (2017).

    CAS  Google Scholar 

  5. 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).

    CAS  PubMed  Google Scholar 

  6. 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).

    CAS  PubMed  Google Scholar 

  7. Batterman, S. A. et al. Key role of symbiotic dinitrogen fixation in tropical forest secondary succession. Nature 502, 224–227 (2013).

    CAS  PubMed  Google Scholar 

  8. Averill, C., Turner, B. L. & Finzi, A. C. Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505, 543–545 (2014).

    CAS  PubMed  Google Scholar 

  9. 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).

    CAS  PubMed  Google Scholar 

  10. 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).

    Google Scholar 

  11. 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).

    CAS  PubMed  Google Scholar 

  12. 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).

    Google Scholar 

  13. 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).

    PubMed  Google Scholar 

  14. Sprent, J. Legume Nodulation: a Global Perspective (John Wiley & Sons, Wiley-Blackwell, 2009).

  15. Ma, Z. et al. Evolutionary history resolves global organization of root functional traits. Nature 555, 94–97 (2018).

    CAS  PubMed  Google Scholar 

  16. Cairney, J. W. G. Evolution of mycorrhiza systems. Naturwissenschaften 87, 467–475 (2000).

    CAS  PubMed  Google Scholar 

  17. Brundrett, M. C. Coevolution of roots and mycorrhizas of land plants. New Phytol. 154, 275–304 (2002).

    Google Scholar 

  18. 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).

    PubMed  Google Scholar 

  19. 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).

    CAS  PubMed  Google Scholar 

  20. Jenny, H. Causes of the high nitrogen and organic matter content of certain tropical forest soils. Soil Sci. 69, 63–69 (1950).

    CAS  Google Scholar 

  21. Peh, K. S. H., Lewis, S. L. & Lloyd, J. Mechanisms of monodominance in diverse tropical tree-dominated systems. J. Ecol. 99, 891–898 (2011).

    Google Scholar 

  22. 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).

    CAS  PubMed  Google Scholar 

  23. 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).

    PubMed  Google Scholar 

  24. 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).

    Google Scholar 

  25. 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).

    PubMed  Google Scholar 

  26. Stephenson, N. L. & van Mantgem, P. J. Forest turnover rates follow global and regional patterns of productivity. Ecol. Lett. 8, 524–531 (2005).

    PubMed  Google Scholar 

  27. Fay, P. A. et al. Grassland productivity limited by multiple nutrients. Nat. Plants 1, 15080 (2015).

    CAS  PubMed  Google Scholar 

  28. Davidson, E. A. et al. Nitrogen and phosphorus limitation of biomass growth in a tropical secondary forest. Ecol. Appl. 14, 150–163 (2004).

    Google Scholar 

  29. 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).

    CAS  Google Scholar 

  30. 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).

    Google Scholar 

  31. Uliassi, D. D. & Ruess, R. W. Limitations to symbiotic nitrogen fixation in primary succession on the Tanana River floodplain. Ecology 83, 88–103 (2002).

    Google Scholar 

  32. Vitousek, P. M. & Farrington, H. Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry 37, 63–75 (1997).

    CAS  Google Scholar 

  33. Connell, J. H. & Lowman, M. D. Low-diversity tropical rain forests: some possible mechanisms for their existence. Am. Nat. 134, 88–119 (1989).

    Google Scholar 

  34. 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).

    CAS  PubMed  Google Scholar 

  35. Scheffer, M. et al. Early-warning signals for critical transitions. Nature 461, 53–59 (2009).

    CAS  PubMed  Google Scholar 

  36. Phillips, O. & Miller, J. S. Global Patterns of Plant Diversity: Alwyn H. Gentry’s Forest Transect Data Set (Missouri Botanical Press, St. Louis, 2002).

  37. Read, D. J. Mycorrhizas in ecosystems. Experientia 47, 376–391 (1991).

    Google Scholar 

  38. Read, D. J. & Perez‐Moreno, J. Mycorrhizas and nutrient cycling in ecosystems—a journey towards relevance? New Phytol. 157, 475–492 (2003).

    Google Scholar 

  39. HussDanell, K. Tansley Review No. 93. Actinorhizal symbioses and their N2 fixation. New Phytol. 136, 375–405 (1997).

    CAS  Google Scholar 

  40. 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).

  41. Racette, S. & Torrey, J. G. The isolation, culture and infectivity of a Frankia strain from Gymnostoma papuanum (Casuarinaceae). Plant Soil 118, 165–170 (1989).

    Google Scholar 

  42. Pawlowski, K. & Newton, W. E. Nitrogen-Fixing Actinorhizal Symbioses (Springer, Dordrecht, 2008).

  43. Wang, B. & Qiu, Y. L. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16, 299–363 (2006).

    CAS  PubMed  Google Scholar 

  44. Brundrett, M. Mycorrhizas in natural ecosystems. Adv. Ecol. Res. 21, 171–313 (1991).

    Google Scholar 

  45. Beer, C. et al. Terrestrial gross carbon dioxide uptake: global distribution and covariation with climate. Science 329, 834–838 (2010).

    CAS  PubMed  Google Scholar 

  46. 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).

    Google Scholar 

  47. 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).

    CAS  PubMed  Google Scholar 

  48. Barron, A. R. et al. Molybdenum limitation of asymbiotic nitrogen fixation in tropical forest soils. Nat. Geosci. 2, 42–45 (2009).

    CAS  Google Scholar 

  49. Binkley, D., Sollins, P., Bell, R., Sachs, D. & Myrold, D. Biogeochemistry of adjacent conifer and alder-conifer stands. Ecology 73, 2022–2033 (1992).

    CAS  Google Scholar 

  50. 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).

    Google Scholar 

  51. Fischer, G. et al. Global Agro-ecological Zones Assessment for Agriculture (GAEZ 2008) (IIASA & FAO, 2008).

  52. Smithson, M. & Verkuilen, J. A better lemon squeezer? Maximum-likelihood regression with beta-distributed dependent variables. Psychol. Methods 11, 54–71 (2006).

    PubMed  Google Scholar 

  53. Bayer, F. M. & Cribari-Neto, F. Model selection criteria in beta regression with varying dispersion. Commun. Stat. Simul. Comput. 46, 729–746 (2017).

    Google Scholar 

  54. Cribari-Neto, F. & Zeileis, A. Beta regression in R. J. Appl. Stat. 34, 1–24 (2010).

    Google Scholar 

  55. 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).

    Google Scholar 

  56. Vitousek, P. & Sanford, R. Nutrient cycling in moist tropical forest. Annu. Rev. Ecol. Syst. 17, 137–167 (1986).

    Google Scholar 

  57. 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).

    PubMed  Google Scholar 

  58. Ter Steege, H. et al. Continental-scale patterns of canopy tree composition and function across Amazonia. Nature 443, 444–447 (2006).

    CAS  PubMed  Google Scholar 

  59. 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).

    Google Scholar 

  60. Cleveland, C. C. et al. Global patterns of terrestrial biological nitrogen (N2) fixation in natural ecosystems. Glob. Biogeochem. Cycles 13, 623–645 (1999).

    CAS  Google Scholar 

  61. 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).

    CAS  PubMed  Google Scholar 

  62. 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).

    Google Scholar 

  63. 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).

    CAS  Google Scholar 

  64. Bai, E., Houlton, B. Z. & Wang, Y. P. Isotopic identification of nitrogen hotspots across natural terrestrial ecosystems. Biogeosciences 9, 3287–3304 (2012).

    CAS  Google Scholar 

  65. Fang, Y. T. et al. Microbial denitrification dominates nitrate losses from forest ecosystems. Proc. Natl Acad. Sci. USA 112, 1470–1474 (2015).

    CAS  PubMed  Google Scholar 

  66. 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).

    CAS  PubMed  Google Scholar 

  67. Hedin, L. O., Vitousek, P. M. & Matson, P. A. Nutrient losses over four million years of tropical forest development. Ecology 84, 2231–2255 (2003).

    Google Scholar 

  68. 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).

    CAS  Google Scholar 

  69. 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).

    PubMed  Google Scholar 

  70. 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).

    PubMed  Google Scholar 

  71. Bonfante, P. & Genre, A. Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nat. Commun. 1, 48 (2010).

    PubMed  Google Scholar 

  72. Henkel, T. W. Monodominance in the ectomycorrhizal Dicymbe corymbosa (Caesalpiniaceae) from Guyana. J. Trop. Ecol. 19, 417–437 (2003).

    Google Scholar 

  73. 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).

    Google Scholar 

  74. Hayman, D. Mycorrhizae of nitrogen-fixing legumes. MIRCEN J. Appl. Microbiol. Biotechnol. 2, 121–145 (1986).

    Google Scholar 

  75. 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).

    Google Scholar 

  76. Güsewell, S. N. P ratios in terrestrial plants: variation and functional significance. New Phytol. 164, 243–266 (2004).

    Google Scholar 

  77. 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).

    Google Scholar 

  78. Manzoni, S., Jackson, R. B., Trofymow, J. A. & Porporato, A. The global stoichiometry of litter nitrogen mineralization. Science 321, 684–686 (2008).

    CAS  PubMed  Google Scholar 

  79. Overpeck, J. T., Rind, D. & Goldberg, R. Climate-induced changes in forest disturbance and vegetation. Nature 343, 51–53 (1990).

    Google Scholar 

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Acknowledgements

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.

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  1. Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, USA

    Mingzhen Lu & Lars O. Hedin

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M.L. and L.O.H. designed the research. M.L. compiled and analysed the belowground strategies database, performed the modelling work and analysed the output data. M.L. and L.O.H. wrote the paper.

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Correspondence to Mingzhen Lu.

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Supplementary Figures 1–7, Supplementary Tables 1–3, Supplementary Notes 1–10 and Supplementary References

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Supplementary Video

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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