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Direct evidence for phosphorus limitation on Amazon forest productivity

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Abstract

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.

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Data availability

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.

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 https://github.com/kmander7/Paper-AFEX-NPP.

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Acknowledgements

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

  1. Coordination of Environmental Dynamics, National Institute for Amazonian Research, Manaus, Brazil

    Hellen Fernanda Viana Cunha, Laynara Figueiredo Lugli, Flavia Delgado Santana, Izabela Fonseca Aleixo, Anna Martins Moraes, Sabrina Garcia, Erick Oblitas Mendoza, Bárbara Brum, Jéssica Schmeisk Rosa, Bruno Takeshi Tanaka Portela, Gyovanni Ribeiro, Sara Deambrozi Coelho, Sheila Trierveiler de Souza, Lara Siebert Silva, Felipe Antonieto, Maria Pires, Ana Caroline Miron, Rafael L. de Assis, Antonio Ocimar Manzi & Carlos Alberto Quesada

  2. Asian School of the Environment, Nanyang Technological University, Singapore, Singapore

    Kelly M. Andersen

  3. Geography, College of Life and Environmental Sciences, University of Exeter, Exeter, UK

    Kelly M. Andersen, Luiz E. O. C. Aragão, Lina M. Mercado & Iain P. Hartley

  4. TUM School of Life Sciences, Technical University of Munich, Freising, Germany

    Laynara Figueiredo Lugli

  5. Biological Dynamics of Forest Fragment Project, National Institute for Amazonian Research, Manaus, Brazil

    Raffaello Di Ponzio, Ana Cláudia Salomão & José Luis Camargo

  6. Colorado State University, Fort Collins, CO, USA

    Amanda L. Cordeiro

  7. Department of Biology, University of Hamburg, Hamburg, Germany

    Ana Caroline Miron

  8. Natural History Museum, University of Oslo, Oslo, Norway

    Rafael L. de Assis

  9. Faculdade de Filosofia, Ciência e Letras de Ribeirão Preto, Universidade de São Paulo, São Paulo, Brazil

    Tomas F. Domingues

  10. National Institute for Space Research, São Jose dos Campos, São Paulo, Brazil

    Luiz E. O. C. Aragão & Antonio Ocimar Manzi

  11. School of Geosciences, University of Edinburgh, Edinburgh, UK

    Patrick Meir

  12. Research School of Biology, Australian National University, Canberra, Australian Capital Territory, Australia

    Patrick Meir

  13. University of Campinas, São Paulo, Brazil

    Laszlo Nagy

  14. UK Centre for Ecology and Hydrology, Wallingford, UK

    Lina M. Mercado

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  1. Hellen Fernanda Viana Cunha
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Contributions

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.

Corresponding author

Correspondence to Hellen Fernanda Viana Cunha.

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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 (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.

Extended Data Table 1 NPP comparisons along the Basin
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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.

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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). https://doi.org/10.1038/s41586-022-05085-2

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