Phosphorus scarcity contributes to nitrogen limitation in lowland tropical rainforests.
nitrogen
nutrient limitation
phosphorus
tropical ecology
Journal
Ecology
ISSN: 1939-9170
Titre abrégé: Ecology
Pays: United States
ID NLM: 0043541
Informations de publication
Date de publication:
06 2023
06 2023
Historique:
revised:
07
03
2023
received:
21
12
2022
accepted:
29
03
2023
medline:
5
6
2023
pubmed:
12
4
2023
entrez:
11
4
2023
Statut:
ppublish
Résumé
There is increasing evidence to suggest that soil nutrient availability can limit the carbon sink capacity of forests, a particularly relevant issue considering today's changing climate. This question is especially important in the tropics, where most part of the Earth's plant biomass is stored. To assess whether tropical forest growth is limited by soil nutrients and to explore N and P limitations, we analyzed stem growth and foliar elemental composition of the five stem widest trees per plot at two sites in French Guiana after 3 years of nitrogen (N), phosphorus (P), and N + P addition. We also compared the results between potential N-fixer and non-N-fixer species. We found a positive effect of N fertilization on stem growth and foliar N, as well as a positive effect of P fertilization on stem growth, foliar N, and foliar P. Potential N-fixing species had greater stem growth, greater foliar N, and greater foliar P concentrations than non-N-fixers. In terms of growth, there was a negative interaction between N-fixer status, N + P, and P fertilization, but no interaction with N fertilization. Because N-fixing plants do not show to be completely N saturated, we do not anticipate N providing from N-fixing plants would supply non-N-fixers. Although the soil-age hypothesis only anticipates P limitation in highly weathered systems, our results for stem growth and foliar elemental composition indicate the existence of considerable N and P co-limitation, which is alleviated in N-fixing plants. The evidence suggests that certain mechanisms invest in N to obtain the scarce P through soil phosphatases, which potentially contributes to the N limitation detected by this study.
Substances chimiques
Nitrogen
N762921K75
Phosphorus
27YLU75U4W
Soil
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e4049Informations de copyright
© 2023 The Authors. Ecology published by Wiley Periodicals LLC on behalf of The Ecological Society of America.
Références
Aguilos, M., B. Hérault, B. Burban, F. Wagner, and D. Bonal. 2018. “What Drives Long-Term Variations in Carbon Flux and Balance in a Tropical Rainforest in French Guiana?” Agricultural and Forest Meteorology 253-254: 114-23. https://doi.org/10.1016/j.agrformet.2018.02.009.
Aguilos, M., C. Stahl, B. Burban, B. Hérault, E. Courtois, S. Coste, F. Wagner, C. Ziegler, K. Takagi, and D. Bonal. 2019. “Interannual and Seasonal Variations in Ecosystem Transpiration and Water Use Efficiency in a Tropical Rainforest.” Forests 10(1): 14.
Alvarez-Clare, S., and M. C. Mack. 2015. “Do Foliar, Litter, and Root Nitrogen and Phosphorus Concentrations Reflect Nutrient Limitation in a Lowland Tropical Wet Forest?” PLoS One 10(4): e0123796.
Anjos, L., C. Gaistardo, J. Deckers, S. Dondeyne, E. Eberhardt, M. Gerasimova, B. Harms, et al. 2015. “World Reference Base for Soil Resources 2014. International Soil Classification System for Naming Soils and Creating Legends for Soil Maps.” In World Soil Resources Reports No. 106, edited by P. Schad, C. van Huyssteen, and E. Micheli. Rome, Italy: FAO. https://doi.org/10.1017/S0014479706394902.
Baribault, T. W., R. K. Kobe, and A. O. Finley. 2012. “Tropical Tree Growth is Correlated with Soil Phosphorus, Potassium, and Calcium, though Not for Legumes.” Ecological Monographs 82: 189-203. https://doi.org/10.1890/11-1013.1.
Bates, D., M. Maechler, B. Bolker, and S. Walker. 2015. “Fitting Linear Mixed-Effects Models Using lme4.” Journal of Statistical Software 67(1): 1-48. https://doi.org/10.18637/jss.v067.i01.
Batterman, S. A., J. S. Hall, B. L. Turner, L. O. Hedin, J. K. LaHaela Walter, P. Sheldon, and M. van Breugel. 2018. “Phosphatase Activity and Nitrogen Fixation Reflect Species Differences, Not Nutrient Trading or Nutrient Balance, across Tropical Rainforest Trees.” Ecology Letters 21: 1486-95. https://doi.org/10.1111/ele.13129.
Batterman, S. A., N. Wurzburger, and L. O. Hedin. 2013. “Nitrogen and Phosphorus Interact to Control Tropical Symbiotic N2 Fixation: A Test in Inga punctata.” Journal of Ecology 101: 1400-8. https://doi.org/10.1111/1365-2745.12138.
Bongers, F., P. Charles-Dominique, P. Forget, and M. Thèry. 2001. Nouragues Dynamics and Plant-Animal Interactions in a Neotropical Rainforest. Kluwer Academic Publishers. https://doi.org/10.1007/978-94-015-9821-7.
Brooks, M. E., K. Kristensen, K. J. van Benthem, A. Magnusson, C. W. Berg, A. Nielsen, H. J. Skaug, M. Maechler, and B. M. Bolker. 2017. “glmmTMB Balances Speed and Flexibility among Packages for Zero-inflated Generalized Linear Mixed Modeling.” The R Journal 9(2): 378-400. https://doi.org/10.32614/RJ-2017-066.
Brookshire, E. N. J., S. Gerber, D. N. L. Menge, and L. O. Hedin. 2012. “Large Losses of Inorganic Nitrogen from Tropical Rainforests Suggest a Lack of Nitrogen Limitation.” Ecology Letters 15: 9-16. https://doi.org/10.1111/j.1461-0248.2011.01701.x.
Chapin, F. S., P. M. Vitousek, and K. Van Cleve. 1986. “The Nature of Nutrient Limitation in Plant Communities.” The American Naturalist 127(1): 48-58. http://www.jstor.org/stable/2461646.
Chen, J., K. J. van Groenigen, B. A. Hungate, C. Terrer, J. W. Groenigen, F. T. Maestre, S. C. Ying, et al. 2020. “Long-Term Nitrogen Loading Alleviates Phosphorus Limitation in Terrestrial Ecosystems.” Global Change Biology 26: 5077-86. https://doi.org/10.1111/gcb.15218.
Cleveland, C. C., A. R. Townsend, D. S. Schimel, H. Fisher, R. W. Howarth, L. O. Hedin, S. S. Perakis, et al. 1999. “Global Patterns of Terrestrial Biological Nitrogen (N2) Fixation in Natural Ecosystems.” Global Biogeochemical Cycles 13: 623-45.
Courtois, E. A., C. Stahl, J. Van den Berge, L. Bréchet, L. Van Langenhove, A. Richter, I. Urbina, J. L. Soong, J. Peñuelas, and I. Janssens. 2018. “Spatial Variation of Soil CO2, CH4 and N2O Fluxes across Topographical Positions in Tropical Forests of the Guiana Shield.” Ecosystems 21: 1445-58. https://doi.org/10.1007/s10021-018-0232-6.
Cunha, H. F. V., K. M. Andersen, L. F. Lugli, F. D. Santana, I. F. Aleixo, A. M. Moraes, S. Garcia, et al. 2022. “Direct Evidence for Phosphorus Limitation on Amazon Forest Productivity.” Nature 608: 558-62. https://doi.org/10.1038/s41586-022-05085-2.
Du, E., C. Terrer, A. F. A. Pellegrini, A. Ahlström, C. J. van Lissa, X. Zhao, N. Xia, X. Wu, and R. B. Jackson. 2020. “Global Patterns of Terrestrial Nitrogen and Phosphorus Limitation.” Nature Geoscience 13: 221-6. https://doi.org/10.1038/s41561-019-0530-4.
Ellsworth, D. S., K. Y. Crous, M. G. de Kauwe, L. T. Verryckt, D. Goll, S. Zaehle, K. J. Bloomfield, et al. 2022. “Convergence in Phosphorus Constraints to Photosynthesis in Forests around the World.” Nature Communications 13: 5005. https://doi.org/10.1038/s41467-022-32545-0.
Elser, J. J., M. E. S. Bracken, D. S. Gruner, W. S. Harpole, N. Hillebrand, J. T. Ngai, E. W. Seabloom, J. B. Shurin, and J. E. Smith. 2007. “Global Analysis of Nitrogen and Phosphorus Limitation of Primary Producers in Freshwater, Marine and Terrestrial Ecosystems.” Ecology Letters 10: 1135-42.
Elser, J. J., W. F. Fagan, A. J. Kerkhoff, N. G. Swenson, and B. J. Enquist. 2010. “Biological Stoichiometry of Plant Production: Metabolism, Scaling and Ecological Response to Global Change.” The New Phytologist 186(3): 593-608.
Eviner, V. T., F. S. Chapin, III, and C. E. Vaughn. 2000. “Nutrient Manipulations in Terrestrial Ecosystems.” In Methods in Ecosystem Science, edited by O. E. Sala, R. B. Jackson, H. A. Mooney, and R. W. Howarth, 291-307. New York: Springer-Verlag.
Fernández-Martínez, M., S. Vicca, I. A. Janssens, J. Sardans, S. Luyssaert, M. Campioli, F. S. Chapin, III, et al. 2014. “Nutrient Availability as the Key Regulator of Global Forest Carbon Balance.” Nature Climate Change 4: 471-6.
Fleischer, K., A. Rammig, M. G. De Kauwe, A. P. Walker, T. F. Domingues, L. Fuchslueger, S. Garcia, et al. 2019. “Amazon Forest Response to CO2 Fertilization Dependent on Plant Phosphorus Acquisition.” Nature Geoscience 12: 736-41. https://doi.org/10.1038/s41561-019-0404-9.
Gourlet-Fleury, S., J. M. Guehl, and O. Laroussinie. 2004. “Ecology and Management of a Neotropical Rainforest.” In Lessons Drawn from Paracou, a Long-Term Experimental Research Site in French Guiana. Paris, France: Elsevier.
Grau, O., J. Peñuelas, B. Ferry, V. Freycon, L. Blanc, M. Desprez, C. Baraloto, et al. 2017. “Nutrient-Cycling Mechanisms Other than the Direct Absorption from Soil May Control Forest Structure and Dynamics in Poor Amazonian Soils.” Scientific Reports 7: 45017. https://doi.org/10.1038/srep45017.
Greenwood, D. J., T. V. Karpinets, K. Zhang, A. Bosh-Serra, A. Boldrini, and L. Karawulova. 2008. “A Unifying Concept for the Dependence of Whole-Crop N: P Ratio on Biomass: Theory and Experiment.” Annals of Botany 102(6): 967-77. https://doi.org/10.1093/aob/mcn188.
Güsewell, S. 2004. “N:P Ratios in Terrestrial Plants: Variation and Functional Significance.” New Phytologist 164: 243-66. https://doi.org/10.1111/j.1469-8137.2004.01192.x.
Ho Tong Minh, D., T. Le Toan, F. Rocca, S. Tebaldini, L. Villard, M. Réjou-Méchain, O. L. Phillips, et al. 2016. “SAR Tomography for the Retrieval of Forest Biomass and Height: Cross-Validation at Two Tropical Forest Sites in French Guiana.” Remote Sensing of Environment 175: 138-47. https://doi.org/10.1016/j.rse.2015.12.037.
Hou, E., Y. Luo, Y. Kuang, C. Chen, X. Lu, L. Jiang, X. Luo, and D. Wen. 2020. “Global Meta-Analysis Shows Pervasive Phosphorus Limitation of Aboveground Plant Production in Natural Terrestrial Ecosystems.” Nature Communications 11: 637. https://doi.org/10.1038/s41467-020-14492-w.
Houlton, B. Z., S. L. Morford, and R. A. Dahlgren. 2018. “Convergent Evidence for Widespread Rock Nitrogen Sources in Earth's Surface Environment.” Science 360: 58-62.
Hungate, B. A., J. S. Dukes, M. R. Shaw, Y. Luo, and C. B. Field. 2003. “Nitrogen and Climate Change.” Science 302: 1512-3.
Kassambara, A. 2020. “ggpubr: ‘ggplot2’ Based Publication Ready Plots.” R Package Version 0.4.0. https://CRAN.R-project.org/package=ggpubr.
Koch, A., W. Hubau, and S. L. Lewis. 2021. “Earth System Models Are Not Capturing Present-Day Tropical Forest Carbon Dynamics.” Earth's Future 9: 1-19.
Kuznetsova, A., P. B. Brockhoff, and R. H. B. Christensen. 2017. “lmerTest Package: Tests in Linear Mixed Effects Models.” Journal of Statistical Software 82(13): 1-26. https://doi.org/10.18637/jss.v082.i13.
Lai, H. R., J. S. Hall, S. A. Batterman, B. L. Turner, and M. van Breugel. 2018. “Nitrogen Fixer Abundance has No Effect on Biomass Recovery During Tropical Secondary Forest Succession.” Journal of Ecology 106: 1415-27. https://doi.org/10.1111/1365-2745.12979.
Lugli, L. F., J. S. Rosa, K. M. Andersen, R. Di Ponzio, R. V. Almeida, M. Pires, A. L. Cordeiro, et al. 2021. “Rapid Responses of Root Traits and Productivity to Phosphorus and Cation Additions in a Tropical Lowland Forest in Amazonia.” The New Phytologist 230: 116-28. https://doi.org/10.1111/nph.17154.
Manu, R., M. D. Corre, A. Aleeje, M. J. Mwanjalolo, F. Babweteera, E. Veldkamp, and O. van Straaten. 2022. “Responses of Tree Growth and Biomass Production to Nutrient Addition in a Semi-Deciduous Tropical Forest in Africa.” Ecology 103(6): e3659.
Mao, Q., H. Chen, C. Wang, Z. Pang, J. Mo, and X. Lu. 2021. “Effect of Long-Term Nitrogen and Phosphorus Additions on Understory Plant Nutrients in a Primary Tropical Forest.” Forests 12: 803. https://doi.org/10.3390/f12060803.
Margalef, O., J. Sardans, M. Fernández-Martínez, R. Molowny-Horas, I. A. Janssens, P. Ciais, D. Goll, et al. 2017. “Global Patterns of Phosphatase Activity in Natural Soils.” Scientific Reports 7: 1337. https://doi.org/10.1038/s41598-017-01418-8.
Mayor, J. R., S. J. Wright, and B. L. Turner. 2014. “Species-Specific Responses of Foliar Nutrients to Long-Term Nitrogen and Phosphorus Additions in a Lowland Tropical Forest.” Journal of Ecology 102(1): 36-44.
Morley, R. J. 2000. Origin and Evolution of Tropical Rain Forests. New York, NY: Wiley.
Nasto, M. K., B. B. Osborne, Y. Lekberg, G. P. Asner, C. S. Balzotti, S. Porder, P. G. Taylor, A. R. Townsend, and C. C. Cleveland. 2017. “Nutrient Acquisition, Soil Phosphorus Partitioning, and Competition among Trees in a Lowland Tropical Rain Forest.” New Phytologist 3: 4243-55.
Nasto, M. K., K. Winter, B. L. Turner, and C. C. Cleveland. 2019. “Nutrient Acquisition Strategies Augment Growth in Tropical N2-Fixing Trees in Nutrient-Poor Soil and under Elevated CO2.” Ecology 100(4): e02646. https://doi.org/10.1002/ecy.2646.
Ostertag, R., and N. M. DiManno. 2016. “Detecting Terrestrial Nutrient Limitation: A Global Meta-Analysis of Foliar Nutrient Concentrations after Fertilization.” Frontiers in Earth Science 4: 2296-6463.
Pan, Y., R. A. Birdsey, J. Fang, R. Houghton, P. E. Kauppi, W. A. Kurz, O. L. Phillips, et al. 2011. “A Large and Persistent Carbon Sink in the world's Forests.” Science 333: 988-93.
Penuelas, J., M. Fernández-Martínez, H. Vallicrosa, J. Maspons, P. Zuccarini, J. Carnicer, T. G. M. Sanders, et al. 2020. “Increasing Atmospheric CO2 Concentrations Correlate with Declining Nutritional Status of European Forests.” Commun Biol 3: 125. https://doi.org/10.1038/s42003-020-0839-y.
Perakis, S., and L. Hedin. 2002. “Nitrogen Loss from Unpolluted South American Forests Mainly Via Dissolved Organic Compounds.” Nature 415: 416-9.
Poorter, H. 1993. “Interspecific Variation in the Growth Response of Plants to an Elevated Ambient CO2 Concentration.” In CO2 and Biosphere. Advances in Vegetation Science, Vol 14, edited by J. Rozema, H. Lambers, S. C. van de Geijn, and M. L. Cambridge. Dordrecht: Springer. https://doi.org/10.1007/978-94-011-1797-5_6.
Prospero, J. M., A. E. Barkley, C. J. Gaston, A. Gatineau, A. Campos y Sansano, and K. Panechou. 2020. “Characterizing and Quantifying African Dust Transport and Deposition to South America: Implications for the Phosphorus Budget in the Amazon Basin.” Global Biogeochemical Cycles 34: e2020GB006536. https://doi.org/10.1029/2020GB006536.
Quesada, C. A., J. Lloyd, L. O. Anderson, N. M. Fyllas, M. Schwarz, and C. Czimczik. 2011. “Soils of Amazonia with Particular Reference to the RAINFOR Sites.” Biogeosciences 8: 1415-40. https://doi.org/10.5194/bg-8-1415-2011.
Raven, J. A. 2015. “Interactions between Nitrogen and Phosphorus Metabolism.” Annual Plant Reviews 48: 187-214. https://doi.org/10.1002/9781118958841.ch7.
Reichert, T., A. Rammig, L. Fuchslueger, L. F. Lugli, C. A. Quesada, and K. Fleischer. 2022. “Plant Phosphorus-Use and -Acquisition Strategies in Amazonia.” The New Phytologist 234: 1126-43. https://doi.org/10.1111/nph.17985.
Reis, C. R., F. S. Pacheco, S. C. Reed, G. Tejada, G. B. Nardoto, M. C. Forti, and J. P. Ometto. 2020. “Biological Nitrogen Fixation across Major Biomes in Latin America: Patterns and Global Change Effects.” Science of the Total Environment 746: 140998. https://doi.org/10.1016/j.scitotenv.2020.140998.
Schlesinger, W. H. 1997. Biogeochemistry: An Analysis of Global Change. San Diego, Calif: Academic Press.
Steidinger, B. S., T. W. Crowther, J. Liang, M. E. Van Nuland, G. D. Werner, P. B. Reich, G. J. Nabuurs, et al. 2019. “Climatic Controls of Decomposition Drive the Global Biogeography of Forest-Tree Symbioses.” Nature 569: 404-8. https://doi.org/10.1038/s41586-019-1128-0.
Sterner, R. W., and J. J. Elser. 2002. Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere. Woodstock, UK: Princeton University Press. http://www.jstor.org/stable/j.ctt1jktrp3.
Sullivan, B. W., S. Alvarez-Clare, S. C. Castle, S. Porder, S. C. Reed, L. Schreeg, A. R. Townsend, and C. C. Cleveland. 2014. “Assessing Nutrient Limitation in Complex Forested Ecosystems: Alternatives to Large-Scale Fertilization Experiments.” Ecology 95: 668-81. https://doi.org/10.1890/13-0825.1.
Tanner, E., V. Kapos, S. Freskos, J. Healey, and A. Theobald. 1990. “Nitrogen and Phosphorus Fertilization of Jamaican Montane Forest Trees.” Journal of Tropical Ecology 6(2): 231-8. https://doi.org/10.1017/S0266467400004375.
Tedersoo, L., L. Laanisto, S. Rahimlou, A. Toussaint, T. Hallikma, and M. Pärtel. 2018. “Global Database of Plants with Root-Symbiotic Nitrogen Fixation: NodDB.” Journal of Vegetation Science 29: 560-8. https://doi.org/10.1111/jvs.12627.
Terrer, C., R. B. Jackson, I. C. Prentice, T. F. Keenan, C. Kaiser, S. Vicca, J. B. Fisher, et al. 2019. “Nitrogen and Phosphorus Constrain the CO2 Fertilization of Global Plant Biomass.” Nature Climate Change 9: 684-9. https://doi.org/10.1038/s41558-019-0545-2.
Treseder, K. K., and P. M. Vitousek. 2001. “Effects of Soil Nutrient Availability on Investment in Acquisition of N and P in Hawaiian Rain Forests.” Ecology 82(4): 946-54.
Trumper, K., M. Bertzky, B. Dickson, G. van der Heijden, M. Jenkins, and P. Manning. 2009. The Natural Fix? The Role of Ecosystems in Climate Mitigation. A UNEP Rapid Response Assessment. Cambridge, UK: United Nations Environment Programme, UNEPWCMC.
Urbina, I., O. Grau, J. Sardans, O. Margalef, G. Peguero, D. Asensio, J. LLusià, et al. 2021. “High Foliar K and P Resorption Efficiencies in Old-Growth Tropical Forests Growing on Nutrient-Poor Soils.” Ecology and Evolution 11: 8969-82. https://doi.org/10.1002/ece3.7734.
Vallicrosa, H. 2023. “helenavallicrosa/FG_leaves: v1.0.0 (FG_N+P_fertilization_leaves+growth.v1).” Zenodo. https://doi.org/10.5281/zenodo.7781944.
Vallicrosa, H., J. Sardans, J. Maspons, and J. Peñuelas. 2022. “Global distribution and drivers of forest biome foliar nitrogen to phosphorus ratios (N:P).” Global Ecology and Biogeography 31: 861-71.
Van Langenhove, L., T. Depaepe, L. T. Verryckt, H. Vallicrosa, L. Fuchslueger, L. F. Lugli, L. Brechet, et al. 2021. “Impact of Nutrient Additions on Free-Living Nitrogen Fixation in Litter and Soil of Two French-Guianese Lowland Tropical Forests.” Journal of Geophysical Research Biogeosciences 126: e2020JG006023. https://doi.org/10.1029/2020JG006023.
Van Langenhove, L., T. Depaepe, S. Vicca, J. van den Berge, C. Stahl, E. Courtois, J. Weedon, et al. 2019. “Regulation of Nitrogen Fixation from Free-Living Organisms in Soil and Leaf Litter of Two Tropical Forests of the Guiana Shield.” Plant and Soil 450: 93-110. https://doi.org/10.1007/s11104-019-04012-1.
Van Langenhove, L., I. A. Janssens, L. Verryckt, L. Brechet, I. P. Hartley, C. Stahl, E. Courtois, et al. 2020. “Rapid root assimilation of added phosphorus in a lowland tropical rainforest of French Guiana.” Soil Biology and Biochemistry 140: 107646.
Van Langenhove, L., L. T. Verryckt, L. Bréchet, E. A. Courtois, C. Stahl, F. Hofhansl, M. Bauters, et al. 2020. “Atmospheric Deposition of Elements and its Relevance for Nutrient Budgets of Tropical Forests.” Biogeochemistry 149: 175-93. https://doi.org/10.1007/s10533-020-00673-8.
Vance, C. P., C. Uhde-Stone, and D. L. Allan. 2003. “Phosphorus Acquisition and Use: Critical Adaptations by Plants for Securing a Nonrenewable Resource.” New Phytologist 157: 423-47. https://doi.org/10.1046/j.1469-8137.2003.00695.x.
Verryckt, L. T., S. Vicca, L. van Langenhove, C. Stahl, D. Asensio, I. Urbina, R. Ogaya, et al. 2022. “Vertical Profiles of Leaf Photosynthesis and Leaf Traits and Soil Nutrients in Two Tropical Rainforests in French Guiana before and after a 3-Year Nitrogen and Phosphorus Addition Experiment.” Earth System Science Data 14(1): 5-18. https://doi.org/10.5194/essd-14-5-2022.
Vicca, S., S. Luyssaert, J. Peñuelas, M. Campioli, F. S. Chapin, III, P. Ciais, A. Heinemeyer, et al. 2012. “Fertile Forests Produce Biomass more Efficiently.” Ecology Letters 15: 520-6.
Vitousek, P. M. 1984. “Litterfall, Nutrient Cycling, and Nutrient Limitation in Tropical Forests.” Ecology 65: 285-98. https://doi.org/10.2307/1939481.
Vitousek, P. M., and H. Farrington. 1997. “Nutrient Limitation and Soil Development: Experimental Test of a Biogeochemical Theory.” Biogeochemistry 37: 63-75. https://doi.org/10.1023/A:1005757218475.
Vitousek, P. M., S. Porder, B. Z. Houlton, and O. A. Chadwick. 2010. “Terrestrial Phosphorus Limitation: Mechanisms, Implications and Nitrogen-Phosphorus Interactions.” Ecological Applications 20: 5-15.
Vitousek, P. M., and R. L. Sanford, Jr. 1986. “Nutrient Cycling in Moist Tropical Forest.” Annual Review of Ecology and Systematics 17(1): 137-67.
Walker, T. W., and J. K. Syers. 1976. “Fate of Phosphorus during Pedogenesis.” Geoderma 15: 1-19.
Wang, R., D. Goll, Y. Balkanski, D. Hauglustaine, O. Boucher, P. Ciais, I. Janssens, et al. 2017. “Global Forest Carbon Uptake Due to Nitrogen and Phosphorus Deposition from 1850 to 2100.” Global Change Biology 23: 4854-72.
Wickham, H. 2016. ggplot2: Elegant Graphics for Data Analysis. New York: Springer-Verlag.
Wieder, W. R., C. C. Cleveland, W. K. Smith, and K. Todd-Brown. 2015. “Future Productivity and Carbon Storage Limited by Terrestrial Nutrient Availability.” Nature Geoscience 8: 441-4. https://doi.org/10.1038/ngeo2413.
Wright, S. J. 2019. “Plant Responses to Nutrient Addition Experiments Conducted in Tropical Forests.” Ecological Monographs 89(4): e01382. https://doi.org/10.1002/ecm.1382.
Wright, S. J., B. L. Turner, J. B. Yavitt, K. E. Harms, M. Kaspari, E. V. J. Tanner, J. Bujan, et al. 2018. “Plant Responses to Fertilization Experiments in Lowland, Species-Rich, Tropical Forests.” Ecology 99: 1129-38. https://doi.org/10.1002/ecy.2193.
Wright, S. J., J. B. Yavitt, N. Wurzburger, B. L. Turner, E. V. J. Tanner, E. J. Sayer, L. S. Santiago, et al. 2011. “Potassium, Phosphorus, or Nitrogen Limit Root Allocation, Tree Growth, or Litter Production in a Lowland Tropical Forest.” Ecology 92: 1616-25. https://doi.org/10.1890/10-1558.1.