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Direct evidence for phosphorus limitation on Amazon forest productivity


The productivity of rainforests growing on highly weathered tropical soils is expected to be limited by phosphorus availability1. Yet, controlled fertilization experiments have been unable to demonstrate a dominant role for phosphorus in controlling tropical forest net primary productivity. Recent syntheses have demonstrated that responses to nitrogen addition are as large as to phosphorus2, and adaptations to low phosphorus availability appear to enable net primary productivity to be maintained across major soil phosphorus gradients3. Thus, the extent to which phosphorus availability limits tropical forest productivity is highly uncertain. The majority of the Amazonia, however, is characterized by soils that are more depleted in phosphorus than those in which most tropical fertilization experiments have taken place2. Thus, we established a phosphorus, nitrogen and base cation addition experiment in an old growth Amazon rainforest, with a low soil phosphorus content that is representative of approximately 60% of the Amazon basin. Here we show that net primary productivity increased exclusively with phosphorus addition. After 2 years, strong responses were observed in fine root (+29%) and canopy productivity (+19%), but not stem growth. The direct evidence of phosphorus limitation of net primary productivity suggests that phosphorus availability may restrict Amazon forest responses to CO2 fertilization4, with major implications for future carbon sequestration and forest resilience to climate change.

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Fig. 1: Total soil phosphorus measured in primary forest plots across the Amazon basin, showing the low phosphorus concentration at our site and across central and eastern Amazonia.
Fig. 2: The effect of nitrogen, phosphorus and base cation availability on total NPP and its components.

Data availability

Data that support the findings of this study have been deposited in NERC Environmental Information Data Centre at for root biomass, for tree census, for litterfall production and for LAI. The Global Wood Density Database can be requested from Plot mean datasets for all response variables and AFEX plot treatment identifications are available at

Code availability

The R code used to find the best model for each variable is available in the Supplementary Material. R scripts used to generate the Supplementary Material are available at


  1. Vitousek, P. M. Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology 65, 285–298 (1984).

    CAS  Google Scholar 

  2. Wright, S. J. et al. Plant responses to fertilization experiments in lowland, species rich, tropical forests. Ecology 99, 1129–1138 (2018).

    PubMed  Google Scholar 

  3. Turner, B. L. et al. Pervasive phosphorus limitation of tree species but not communities in tropical forests. Nature 555, 367–370 (2018).

    ADS  CAS  PubMed  Google Scholar 

  4. Fleischer, K. et al. Amazon forest response to CO2 fertilization depend on plant phosphorus acquisition. Nat. Geosci. 12, 736–741 (2019).

    ADS  CAS  Google Scholar 

  5. Goll, D. S. et al. Nutrient limitation reduces land carbon uptake in simulations with a model of combined carbon, nitrogen and phosphorus cycling. Biogeosciences 9, 3547–3569 (2012).

    ADS  CAS  Google Scholar 

  6. Sun, Y. et al. Diagnosing phosphorus limitation in natural terrestrial ecosystems in carbon cycle models. Earths Future 5, 730–749 (2017).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  7. Zhang, Q. et al. Nitrogen and phosphorus limitations significantly reduce allowable CO2 emissions. Geophys. Lett. 41, 632–637 (2014).

    ADS  CAS  Google Scholar 

  8. Luo, Y., Hui, D. & Zhang, D. Elevated CO2 stimulates net accumulations of carbon and nitrogen in land ecosystem: a meta analysis. Ecology 87, 53–63 (2006).

    PubMed  Google Scholar 

  9. Jordan, C. F. The nutrient balance of an Amazonian rainforest. Ecology 63, 647–654 (1982).

    CAS  Google Scholar 

  10. Walker, T. W. & Syers, J. K. The fate of phosphorus during pedogenesis. Geoderma 15, 1–19 (1976).

    ADS  CAS  Google Scholar 

  11. Crews, T. E. et al. Changes in soil phosphorus fractions and ecosystem dynamics across a long chronosequence in Hawaii. Ecology 76, 1408–1424 (1995).

    Google Scholar 

  12. Hedin, L. O. et al. Nutrient losses over four million years of tropical forest development. Ecology 84, 2231–2255 (2003).

    Google Scholar 

  13. Dalling, J. W. et al. in Tropical Tree Physiology (Springer, 2016).

  14. Herrera, R. R. & Medina, E. Amazon ecosystems, their structure and functioning with particular emphasis on nutrients. Interciencia 3, 223–231 (1978).

    Google Scholar 

  15. Quesada, C. A. et al. Variations in chemical and physical properties of Amazon forest soils in relation to their genesis. Biogeosciences 7, 1515–1541 (2010).

    ADS  CAS  Google Scholar 

  16. Quesada, C. A. et al. Basin wide variations in Amazon forest structure and function are mediated by both soils and climate. Biogeosciences 9, 2203–2246 (2012).

    ADS  Google Scholar 

  17. Mercado, L. et al. Variations in Amazon forest productivity correlated with foliar nutrients and modelled rates of photosynthetic carbon supply. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366, 3316–3329 (2011).

    PubMed  PubMed Central  Google Scholar 

  18. Wright, S. J. Plant responses to nutrient addition experiments conducted in tropical forests. Ecol. Monogr. 89, e01382 (2019).

    Google Scholar 

  19. Yang, X. et al. The effects of phosphorus cycle dynamics carbon sources and sink in the Amazon region: a modelling study using ELM v1. J. Geophys. Res. Biogeosci. 124, 3686–3698 (2019).

    CAS  Google Scholar 

  20. Sollins, P. Factors influencing species composition in tropical lowland rain forest: does soil matter? Ecology 79, 23–30 (1998).

    Google Scholar 

  21. Alvarez-Clare, S. et al. A direct test of nitrogen and phosphorus limitation to net primary productivity in a lowland tropical wet forest. Ecology 94, 1540–1551 (2013).

    CAS  PubMed  Google Scholar 

  22. Wright, S. J. et al. Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest. Ecology 92, 1616–1625 (2011).

    PubMed  Google Scholar 

  23. Sayer, E. J. et al. Variable responses of lowland tropical forest nutrient status to fertilization and litter manipulation. Ecosystems 15, 387–400 (2012).

    CAS  Google Scholar 

  24. Ganade, G. & Brown, V. Succession in old pastures of central Amazonia: role of soil fertility and plant litter. Ecology 83, 743–754 (2002).

    Google Scholar 

  25. Markewitz, D. et al. Soil and tree response to P fertilization in a secondary tropical forest supported by an Oxisol. Biol. Fertil. Soils 48, 665–678 (2012).

    Google Scholar 

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

    Google Scholar 

  27. Massad, T. et al. Interactions between fire, nutrients, and insect herbivores affect the recovery of diversity in the southern Amazon. Oecologia 172, 219–229 (2013).

    ADS  PubMed  Google Scholar 

  28. Newbery, D. M. et al. Does low phosphorus supply limit seedling establishment and tree growth in groves of ectomycorrhizal trees in a central African rainforest? New Phytol. 156, 297–311 (2002).

    CAS  PubMed  Google Scholar 

  29. Mirmanto, E. et al. Effects of nitrogen and phosphorus fertilization in a lowland evergreen rainforest. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354, 1825–1829 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Lugli, L. F. et al. Rapid responses of root traits and productivity to phosphorus and cation additions in a tropical lowland forest in Amazonia. New Phytol. 230, 116–128 (2020).

    Google Scholar 

  31. Quesada, C. A. et al. Soils of Amazonia with particular reference to the rainfor sites. Biogeosciences 8, 1415–1440 (2011).

    ADS  CAS  Google Scholar 

  32. Giardina, C. et al. Primary production and carbon allocation in relation to nutrient supply in a tropical experiment forest. Glob. Change Biol. 9, 1438–1450 (2003).

    ADS  Google Scholar 

  33. Rowland, L. et al. Scaling leaf respiration with nitrogen and phosphorus in tropical forests across two continents. New Phytol. 214, 1064–1077 (2017).

    CAS  PubMed  Google Scholar 

  34. Vicca, S. et al. Fertile forests produce biomass more efficiently. Ecol. Lett. 15, 520–526 (2012).

    CAS  PubMed  Google Scholar 

  35. Wright, I. J. et al. The worldwide leaf economics spectrum. Nature 428, 821–826 (2004).

    ADS  CAS  PubMed  Google Scholar 

  36. Hinsinger, P. How do plant roots acquire mineral nutrients? Chemical processes involved in the rhizosphere. Adv. Agron. 64, 225–265 (1998).

    CAS  Google Scholar 

  37. Van Langehove, L. et al. Rapid root assimilation of added phosphorus in a lowland tropical rainforest of French Guiana. Soil Biol. Biochem. 140, 107646 (2019).

    Google Scholar 

  38. Martins, N. P. et al. Fine roots stimulate nutrient release during early stages of litter decomposition in a central Amazon rainforest. Plant Soil 469, 287–303 (2021).

    CAS  Google Scholar 

  39. Cordeiro, A. L. et al. Fine root dynamics vary with soil and precipitation in a low-nutrient tropical forest in the central Amazonia. Plant Environ. Interact. 220, 3–16 (2020).

    Google Scholar 

  40. Yavitt, J. Soil fertility and fine root dynamics in response to four years of nutrient (N,P, K) fertilization in a lowland tropical moist forest, Panamá. Austral. Ecol. 36, 433–445 (2011).

    Google Scholar 

  41. Wurzburger, N. & Wright, S. J. Fine root responses to fertilization reveal multiple nutrient limitation in a lowland tropical forest. Ecology 96, 2137–2146 (2015).

    PubMed  Google Scholar 

  42. Waring, B. G., Aviles, D. P., Murray, J. G. & Powers, J. S. Plant community responses to stand level nutrient fertilization in a secondary tropical dry forest. Ecology 100, e02691 (2019).

    PubMed  Google Scholar 

  43. Jansens, I. A. et al. Reductions of forest soil respiration in response to nitrogen deposition. Nat. Geosci. 3, 315–322 (2010).

    ADS  Google Scholar 

  44. Alvarez Claire, S. et al. Do foliar, litter, and root nitrogen and phosphorus concentration reflect nutrient limitation in a lowland tropical wet forest? PLoS ONE 10, e0123796 (2015).

    Google Scholar 

  45. Bouma, T. in Advances in Photosynthesis and Respiration Vol. 18 (eds Lambers, H. & Ribas-Carbo, M.) 177–194 (Springer, 2005).

  46. Malhi, Y. et al. Comprehensive assessment of carbon productivity, allocation and storage in three Amazonian forests. Glob. Change Biol. 15, 1255–1274 (2009).

    ADS  Google Scholar 

  47. Aragão, L. E. O. et al. Above and below ground net primary productivity across ten Amazonian forests on contrasting soils. Biogeosciences 6, 2759–2778 (2009).

    ADS  Google Scholar 

  48. Cox, P. M. et al. Sensitivity of tropical carbon to climate change constrained by carbon dioxide variability. Nature 494, 341–344 (2013).

    ADS  CAS  PubMed  Google Scholar 

  49. Quesada, C. A. & Lloyd, J. in Interactions Between Biosphere, Atmosphere and Human Land Use in the Amazon Basin (eds Nagy, L. et al.) 267–299 (Springer, 2016).

  50. Girardin, C. A. J. et al. Seasonal trends of Amazonian rainforest phenology, net primary production, and carbon allocation. Glob. Biogeochem. Cycles 30, 700–715 (2016).

    ADS  CAS  Google Scholar 

  51. Laurance, W. F. et al. An Amazonian rainforest and its fragments as a laboratory of global change. Biol. Rev. 93, 223–247 (2018).

    PubMed  Google Scholar 

  52. De Oliveira, A. & Mori, S. A. A central Amazonia terra firme forest. I. High tree species richness on poor soils. Biodivers. Conserv. 8, 1219–1244 (1999).

    Google Scholar 

  53. Ferreira, S. J. F., Luizão, F. J. & Dallarosa, R. L. G. Throughfall and rainfall interception by an upland forest submitted to selective logging in Central Amazonia [Portuguese]. Acta Amaz. 35, 55–62 (2005).

    Google Scholar 

  54. Tanaka, L. D. S., Satyamurty, P. & Machado, L. A. T. Diurnal variation of precipitation in central Amazon Basin. Int. J. Climatol. 34, 3574–3584 (2014).

    Google Scholar 

  55. Duque, A. et al. Insights into regional patterns of Amazonian forest structure and dominance from three large terra firme forest dynamics plots. Biodivers. Conserv. 26, 669–686 (2017).

    Google Scholar 

  56. Martins, D. L. et al. Soil induced impacts on forest structure drive coarse wood debris stocks across central Amazonia. Plant Ecol. Divers. 8, 229–241 (2014).

    Google Scholar 

  57. Metcalfe, D. B. et al. A method for extracting plant roots from soil which facilitates rapid sample processing without compromising measurent accuracy. New Phytol. 174, 697–703 (2007).

    CAS  PubMed  Google Scholar 

  58. Chave, J. et al. Improved allometric to estimate the above ground biomass of tropical trees. Glob. Change Biol. 20, 3177–3190 (2014).

    ADS  Google Scholar 

  59. Chave, J. et al. Towards a worldwide wood economics spectrum. Ecol. Lett. 12, 351–366 (2009).

    PubMed  Google Scholar 

  60. Zanne, A. E. et al. Global Wood Density Database (2009).

  61. Higuchi, N. & Carvalho, J. A. in Anais do Seminário: Emissão e Sequestro de CO2—Uma Nova Oportunidade de Negócios para o Brasil (CVRD, 1994).

  62. Brienen, R. J. W., Philips, O. L. & Zagt, R. J. Long term decline of the Amazon carbon sink. Nature 519, 344–348 (2015).

    ADS  CAS  PubMed  Google Scholar 

  63. Malhado, A. C. M. et al. Seasonal leaf dynamics in an Amazonian tropical forest. Forest Ecol. Manag. 258, 1161–1165 (2009).

    Google Scholar 

  64. Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest Package: tests in linear mixed effects models. J. Stat. Softw. 82, 1–26 (2017).

    Google Scholar 

  65. Bates, D., Marcher, M., Bolker, B. M. & Walker, S. C. Fitting linear mixed effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).

    Google Scholar 

  66. Moraes, A. C. M. et al. Fine Litterfall Production and Nutrient Composition Data from a Fertilized Site in Central Amazon, Brazil (NERC, 2020).

  67. Cunha, H. F. V. et al. Fine Root Biomass in Fertilised Plots in the Central Amazon, 2017–2019 (NERC Environmental Information Data Centre, 2021).

  68. Cunha, H. F. V. et al. Tree Census and Diameter Increment in Fertilised Plots in the Central Amazon, 2017–2020 (NERC Environmental Information Data Centre, 2021).

  69. Cunha, H. F. V. et al. Leaf Area Index (LAI) in Fertilised Plots in the Central Amazon, 2017–2018 (NERC Environmental Information Data Centre, 2021).

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We thank the late Paulo Apóstolo Assunção for the botanical identification of the trees and J. Cruz, A. dos Santos and B. S. da Silva for helping in field campaigns. The authors acknowledge funding from the UK Natural Environment Research Council (NERC), grant number NE/L007223/1. This is publication 850 in the technical series of the BDFFP. C.A.Q. acknowledges the grants from Brazilian National Council for Scientific and Technological Development (CNPq) CNPq/LBA 68/2013, CNPq/MCTI/FNDCT no. 18/2021 and his productivity grant. C.A.Q., H.F.V.C., F.D.S., I.A., L.F.L., E.O.M. and S.G. acknowledge the AmazonFACE programme for financial support in cooperation with Coordination for the Improvement of Higher Education Personnel (CAPES) and the National Institute of Amazonian Research as part of the grants CAPES-INPA/88887.154643/2017-00 and 88881.154644/2017-01. T.F.D. acknowledges funds from Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), grant 2015/50488-5, and the Partnership for Enhanced Engagement in Research (PEER) programme grant AID-OAA-A-11-00012. L.E.O.C.A. thanks CNPq (314416/2020-0).

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Authors and Affiliations



H.F.V.C., C.A.Q., I.P.H. and K.M.A. planned the study. H.F.V.C., R.D.P., A.M., M.P., J.S.R., B.B., A.L.C., S.D.C., S.T.d.S., F.A., L.S.S., G.R., R.L.d.A., A.C.S., B.T.T.P., A.C.M., L.F.L., E.O.M. and J.L.C. collected data and/or helped with project logistics. I.P.H., L.M.M., L.E.O.C.A., T.F.D., L.N., P.M. and C.A.Q. wrote the grants that funded this research. H.F.V.C., K.M.A. and I.A. organized the datasets. H.F.V.C., K.M.A., I.A. and A.M.M. conducted the statistical analyses. H.F.V.C., L.F.L., I.P.H., C.A.Q., L.M.M., S.G., I.A., K.M.A., F.D.S., T.F.D., A.L.C., P.M., R.D.P., R.L.d.A., L.E.O.C.A. and L.N. discussed the results and the structure of the paper and improved the manuscript.

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Correspondence to Hellen Fernanda Viana Cunha.

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Nature thanks Stuart Wright and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data figures and tables

Extended Data Fig. 1 Nutrient addition effects on Leaf area index.

LAI was measured over four field campaigns across treatments in a lowland forest in Central Amazon. Each panel represents mean ± 1SE LAI with (+) or without (−) the addition of specific nutrients (phosphorus addition (a); base cation addition (b); nitrogen addition (c)), based on the average LAI across the four field campaigns, n = 16 plots. No significant differences among the means were detected in linear mixed models for any of the nutrients. The dotted lines represent the mean values for the control plots (no nutrients added; n = 4 plots) for comparison purposes.

Extended Data Fig. 2 Nutrient addition effects on Leaf residence time (LRT).

Leaf residence time (yr) across treatments in a lowland forest in Central Amazon. Two separate measures of specific leaf area were used in the leaf residence time calculations based on: 1) fresh canopy leaves of common families represented across all plots sampled for a photosynthesis campaign (a-c); 2) composite leaf litter collected in the plots (df). Leaf residence time showed a decrease with P addition only (a, d) for both LRT estimates, with cations (b, e) and N (c, f) being shown for comparison. Means ± 1SE are presented, n = 16 plots. Linear mixed models were performed to evaluate responses in leaf residence time to added nutrients. The dotted lines represent the mean values for the control plots (no nutrients added; n = 4 plots) for comparison purposes.

Extended Data Table 1 NPP comparisons along the Basin

Supplementary information

Supplementary Material

Contains supplementary information on methods, descriptive statistics, and results of linear mixed models for all response variables. Supplementary Tables 1–33.

Reporting Summary

Peer Review File

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Cunha, H.F.V., Andersen, K.M., Lugli, L.F. et al. Direct evidence for phosphorus limitation on Amazon forest productivity. Nature 608, 558–562 (2022).

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