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.
This is a preview of subscription content, access via your institution
Subscribe to Nature+
Get immediate online access to the entire Nature family of 50+ journals
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
Data that support the findings of this study have been deposited in NERC Environmental Information Data Centre at https://doi.org/10.5285/b3a55011-bf46-40f5-8850-86dc8bc4c85d for root biomass, https://doi.org/10.5285/c2587e20-ba4a-4444-8ce9-ccdec15b0aa3 for tree census, https://doi.org/10.5285/c0294ec9-45d6-464c-b543-ce9ece9fd968 for litterfall production and https://doi.org/10.5285/6e70665f-b558-4949-b42a-49fbaec7e7cc for LAI. The Global Wood Density Database can be requested from https://doi.org/10.5061/dryad.234. Plot mean datasets for all response variables and AFEX plot treatment identifications are available at https://github.com/kmander7/Paper-AFEX-NPP.
Vitousek, P. M. Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology 65, 285–298 (1984).
Wright, S. J. et al. Plant responses to fertilization experiments in lowland, species rich, tropical forests. Ecology 99, 1129–1138 (2018).
Turner, B. L. et al. Pervasive phosphorus limitation of tree species but not communities in tropical forests. Nature 555, 367–370 (2018).
Fleischer, K. et al. Amazon forest response to CO2 fertilization depend on plant phosphorus acquisition. Nat. Geosci. 12, 736–741 (2019).
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).
Sun, Y. et al. Diagnosing phosphorus limitation in natural terrestrial ecosystems in carbon cycle models. Earths Future 5, 730–749 (2017).
Zhang, Q. et al. Nitrogen and phosphorus limitations significantly reduce allowable CO2 emissions. Geophys. Lett. 41, 632–637 (2014).
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).
Jordan, C. F. The nutrient balance of an Amazonian rainforest. Ecology 63, 647–654 (1982).
Walker, T. W. & Syers, J. K. The fate of phosphorus during pedogenesis. Geoderma 15, 1–19 (1976).
Crews, T. E. et al. Changes in soil phosphorus fractions and ecosystem dynamics across a long chronosequence in Hawaii. Ecology 76, 1408–1424 (1995).
Hedin, L. O. et al. Nutrient losses over four million years of tropical forest development. Ecology 84, 2231–2255 (2003).
Dalling, J. W. et al. in Tropical Tree Physiology (Springer, 2016).
Herrera, R. R. & Medina, E. Amazon ecosystems, their structure and functioning with particular emphasis on nutrients. Interciencia 3, 223–231 (1978).
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).
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).
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).
Wright, S. J. Plant responses to nutrient addition experiments conducted in tropical forests. Ecol. Monogr. 89, e01382 (2019).
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).
Sollins, P. Factors influencing species composition in tropical lowland rain forest: does soil matter? Ecology 79, 23–30 (1998).
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).
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).
Sayer, E. J. et al. Variable responses of lowland tropical forest nutrient status to fertilization and litter manipulation. Ecosystems 15, 387–400 (2012).
Ganade, G. & Brown, V. Succession in old pastures of central Amazonia: role of soil fertility and plant litter. Ecology 83, 743–754 (2002).
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).
Davidson, E. et al. Nitrogen and phosphorus limitation of biomass growth in a tropical secondary forest. Ecol. Appl. 14, 150–163 (2004).
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).
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).
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).
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).
Quesada, C. A. et al. Soils of Amazonia with particular reference to the rainfor sites. Biogeosciences 8, 1415–1440 (2011).
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).
Rowland, L. et al. Scaling leaf respiration with nitrogen and phosphorus in tropical forests across two continents. New Phytol. 214, 1064–1077 (2017).
Vicca, S. et al. Fertile forests produce biomass more efficiently. Ecol. Lett. 15, 520–526 (2012).
Wright, I. J. et al. The worldwide leaf economics spectrum. Nature 428, 821–826 (2004).
Hinsinger, P. How do plant roots acquire mineral nutrients? Chemical processes involved in the rhizosphere. Adv. Agron. 64, 225–265 (1998).
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).
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).
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).
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).
Wurzburger, N. & Wright, S. J. Fine root responses to fertilization reveal multiple nutrient limitation in a lowland tropical forest. Ecology 96, 2137–2146 (2015).
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).
Jansens, I. A. et al. Reductions of forest soil respiration in response to nitrogen deposition. Nat. Geosci. 3, 315–322 (2010).
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).
Bouma, T. in Advances in Photosynthesis and Respiration Vol. 18 (eds Lambers, H. & Ribas-Carbo, M.) 177–194 (Springer, 2005).
Malhi, Y. et al. Comprehensive assessment of carbon productivity, allocation and storage in three Amazonian forests. Glob. Change Biol. 15, 1255–1274 (2009).
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).
Cox, P. M. et al. Sensitivity of tropical carbon to climate change constrained by carbon dioxide variability. Nature 494, 341–344 (2013).
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).
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).
Laurance, W. F. et al. An Amazonian rainforest and its fragments as a laboratory of global change. Biol. Rev. 93, 223–247 (2018).
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).
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).
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).
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).
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).
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).
Chave, J. et al. Improved allometric to estimate the above ground biomass of tropical trees. Glob. Change Biol. 20, 3177–3190 (2014).
Chave, J. et al. Towards a worldwide wood economics spectrum. Ecol. Lett. 12, 351–366 (2009).
Zanne, A. E. et al. Global Wood Density Database https://doi.org/10.5061/dryad.234 (2009).
Higuchi, N. & Carvalho, J. A. in Anais do Seminário: Emissão e Sequestro de CO2—Uma Nova Oportunidade de Negócios para o Brasil (CVRD, 1994).
Brienen, R. J. W., Philips, O. L. & Zagt, R. J. Long term decline of the Amazon carbon sink. Nature 519, 344–348 (2015).
Malhado, A. C. M. et al. Seasonal leaf dynamics in an Amazonian tropical forest. Forest Ecol. Manag. 258, 1161–1165 (2009).
Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest Package: tests in linear mixed effects models. J. Stat. Softw. 82, 1–26 (2017).
Bates, D., Marcher, M., Bolker, B. M. & Walker, S. C. Fitting linear mixed effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
Moraes, A. C. M. et al. Fine Litterfall Production and Nutrient Composition Data from a Fertilized Site in Central Amazon, Brazil (NERC, 2020).
Cunha, H. F. V. et al. Fine Root Biomass in Fertilised Plots in the Central Amazon, 2017–2019 (NERC Environmental Information Data Centre, 2021).
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).
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).
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).
The authors declare no competing interests.
Peer review information
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.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Extended data figures and tables
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.
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 (d–f). 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.
About this article
Cite this article
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). https://doi.org/10.1038/s41586-022-05085-2