Amazon forest response to CO2 fertilization dependent on plant phosphorus acquisition

Global terrestrial models currently predict that the Amazon rainforest will continue to act as a carbon sink in the future, primarily owing to the rising atmospheric carbon dioxide (CO2) concentration. Soil phosphorus impoverishment in parts of the Amazon basin largely controls its functioning, but the role of phosphorus availability has not been considered in global model ensembles—for example, during the Fifth Climate Model Intercomparison Project. Here we simulate the planned free-air CO2 enrichment experiment AmazonFACE with an ensemble of 14 terrestrial ecosystem models. We show that phosphorus availability reduces the projected CO2-induced biomass carbon growth by about 50% to 79 ± 63 g C m−2 yr−1 over 15 years compared to estimates from carbon and carbon–nitrogen models. Our results suggest that the resilience of the region to climate change may be much less than previously assumed. Variation in the biomass carbon response among the phosphorus-enabled models is considerable, ranging from 5 to 140 g C m−2 yr−1, owing to the contrasting plant phosphorus use and acquisition strategies considered among the models. The Amazon forest response thus depends on the interactions and relative contributions of the phosphorus acquisition and use strategies across individuals, and to what extent these processes can be upregulated under elevated CO2.Phosphorus limitation can significantly reduce the response of the Amazon forest to CO2 fertilization, according to ecosystem-model ensemble simulations of a free-air CO2 enrichment experiment.

[1]  Mingzhu He,et al.  Drought effect on plant nitrogen and phosphorus: a meta-analysis. , 2014, The New phytologist.

[2]  Atul K. Jain,et al.  Where does the carbon go? A model–data intercomparison of vegetation carbon allocation and turnover processes at two temperate forest free-air CO2 enrichment sites , 2014, The New phytologist.

[3]  R. E. Dickson,et al.  Elevated carbon dioxide and ozone alter productivity and ecosystem carbon content in northern temperate forests , 2014, Global change biology.

[4]  Atul K. Jain,et al.  Using ecosystem experiments to improve vegetation models , 2015 .

[5]  Atul K. Jain,et al.  Comprehensive ecosystem model‐data synthesis using multiple data sets at two temperate forest free‐air CO2 enrichment experiments: Model performance at ambient CO2 concentration , 2014 .

[6]  Paul Steele,et al.  Law Dome CO2, CH4 and N2O ice core records extended to 2000 years BP , 2006 .

[7]  L. Anderson,et al.  Soils of Amazonia with particular reference to the RAINFOR sites , 2009 .

[8]  G. P. Kyle,et al.  Global and regional evolution of short-lived radiatively-active gases and aerosols in the Representative Concentration Pathways , 2011 .

[9]  Michael T. Coe,et al.  Testing the performance of a dynamic global ecosystem model: Water balance, carbon balance, and vegetation structure , 2000 .

[10]  Yadvinder Malhi,et al.  Basin-wide variations in foliar properties of Amazonian forest: phylogeny, soils and climate. , 2009 .

[11]  William R. Wieder,et al.  Future productivity and carbon storage limited by terrestrial nutrient availability , 2015 .

[12]  Anja Rammig,et al.  Model-data synthesis for the next generation of forest free-air CO2 enrichment (FACE) experiments. , 2016, The New phytologist.

[13]  Yadvinder Malhi,et al.  Confronting model predictions of carbon fluxes with measurements of Amazon forests subjected to experimental drought. , 2013, The New phytologist.

[14]  Susan E. Trumbore,et al.  Respiration from a tropical forest ecosystem: partitioning of sources and low carbon use efficiency , 2004 .

[15]  Benjamin L Turner,et al.  Plant responses to fertilization experiments in lowland, species-rich, tropical forests. , 2018, Ecology.

[16]  G. Collatz,et al.  Physiological and environmental regulation of stomatal conductance, photosynthesis and transpiration: a model that includes a laminar boundary layer , 1991 .

[17]  O. Phillips,et al.  Carbon uptake by mature Amazon forests has mitigated Amazon nations’ carbon emissions , 2017, Carbon Balance and Management.

[18]  W. Post,et al.  The role of phosphorus dynamics in tropical forests – a modeling study using CLM-CNP , 2013 .

[19]  J. Chambers,et al.  Comprehensive assessment of carbon productivity, allocation and storage in three Amazonian forests , 2009 .

[20]  J. Tomasella,et al.  Pedotransfer functions for tropical soils , 2004 .

[21]  David S. Lee,et al.  Historical (1850–2000) gridded anthropogenic and biomass burning emissions of reactive gases and aerosols: methodology and application , 2010 .

[22]  F. Hoffman,et al.  Phosphorus feedbacks constraining tropical ecosystem responses to changes in atmospheric CO2 and climate , 2016 .

[23]  P. Cox,et al.  Sensitivity of tropical carbon to climate change constrained by carbon dioxide variability , 2013, Nature.

[24]  B. Kruijt,et al.  Should phosphorus availability be constraining moist tropical forest responses to increasing CO2 concentrations , 2001 .

[25]  Benjamin Smith,et al.  Using models to guide field experiments: a priori predictions for the CO2 response of a nutrient‐ and water‐limited native Eucalypt woodland , 2016, Global change biology.

[26]  P. Ciais,et al.  Fertile forests produce biomass more efficiently. , 2012, Ecology letters.

[27]  Benjamin L Turner,et al.  Pervasive phosphorus limitation of tree species but not communities in tropical forests , 2018, Nature.

[28]  P. Reich,et al.  Elevated CO2 does not increase eucalypt forest productivity on a low-phosphorus soil , 2017 .

[29]  Jeffrey M. Warren,et al.  CO2 enhancement of forest productivity constrained by limited nitrogen availability , 2010, Proceedings of the National Academy of Sciences.

[30]  J. Berry,et al.  A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species , 1980, Planta.

[31]  B. Kruijt,et al.  Leaf photosynthetic light response : a mechanistic model for scaling photosynthesis to leaves and canopies , 1998 .

[32]  M. Hoosbeek Elevated CO2 increased phosphorous loss from decomposing litter and soil organic matter at two FACE experiments with trees , 2015, Biogeochemistry.

[33]  D. Etheridge,et al.  Natural and anthropogenic changes in atmospheric CO2 over the last 1000 years from air in Antarctic ice and firn , 1996 .

[34]  Benjamin Smith,et al.  A new version of the CABLE land surface model (Subversion revision r4601) incorporating land use and land cover change, woody vegetation demography, and a novel optimisation-based approach to plant coordination of photosynthesis , 2018, Geoscientific Model Development.

[35]  Corinne Le Quéré,et al.  Climate Change 2013: The Physical Science Basis , 2013 .

[36]  A. Arneth,et al.  Variations in chemical and physical properties of Amazon forest soils in relation to their genesis , 2010 .

[37]  J. Terborgh,et al.  Basin-wide variations in Amazon forest structure and function are mediated by both soils and climate , 2012 .

[38]  S. Reed,et al.  Incorporating phosphorus cycling into global modeling efforts: a worthwhile, tractable endeavor. , 2015, The New phytologist.

[39]  J. Terborgh,et al.  Long-term decline of the Amazon carbon sink , 2015, Nature.

[40]  F. Woodward,et al.  Carbon residence time dominates uncertainty in terrestrial vegetation responses to future climate and atmospheric CO2 , 2013, Proceedings of the National Academy of Sciences.

[41]  Jitendra Kumar,et al.  Root structural and functional dynamics in terrestrial biosphere models--evaluation and recommendations. , 2015, The New phytologist.

[42]  Yadvinder Malhi,et al.  High-resolution hydraulic parameter maps for surface soils in tropical South America , 2013 .

[43]  Andrew D. Friend,et al.  Carbon and nitrogen cycle dynamics in the O‐CN land surface model: 1. Model description, site‐scale evaluation, and sensitivity to parameter estimates , 2010 .

[44]  S. Wofsy,et al.  Mechanistic scaling of ecosystem function and dynamics in space and time: Ecosystem Demography model version 2 , 2009 .

[45]  D. Etheridge,et al.  Law Dome CO 2 , CH 4 and N 2 O ice core records extended to 2000 years , 2006 .

[46]  R. McMurtrie,et al.  Long-Term Response of Nutrient-Limited Forests to CO"2 Enrichment; Equilibrium Behavior of Plant-Soil Models. , 1993, Ecological applications : a publication of the Ecological Society of America.

[47]  Nate G. McDowell,et al.  Taking off the training wheels: the properties of a dynamic vegetation model without climate envelopes, CLM4.5(ED) , 2015 .

[48]  Peter M. Vitousek,et al.  Litterfall, Nutrient Cycling, and Nutrient Limitation in Tropical Forests , 1984 .

[49]  P. Ciais,et al.  A representation of the phosphorus cycle for ORCHIDEE (revision 4520) , 2017 .

[50]  C. Koven,et al.  Multiple soil nutrient competition between plants, microbes, and mineral surfaces: model development, parameterization, and example applications in several tropical forests , 2015 .

[51]  P. Cox,et al.  The Joint UK Land Environment Simulator (JULES), model description – Part 1: Energy and water fluxes , 2011 .

[52]  Silvia Caldararu,et al.  Towards a more physiological representation of vegetation phosphorus processes in land surface models. , 2019, The New phytologist.

[53]  Luana S. Basso,et al.  Drought sensitivity of Amazonian carbon balance revealed by atmospheric measurements , 2014, Nature.

[54]  A. Rammig,et al.  Amazon Forest Ecosystem Responses to Elevated Atmospheric CO2 and Alterations in Nutrient Availability: Filling the Gaps with Model-Experiment Integration , 2016, Front. Earth Sci..

[55]  Jeffrey Q. Chambers,et al.  Recognizing Amazonian tree species in the field using bark tissues spectra , 2018, Forest Ecology and Management.

[56]  Atul K. Jain,et al.  Evaluation of 11 terrestrial carbon–nitrogen cycle models against observations from two temperate Free-Air CO2 Enrichment studies , 2014, The New phytologist.

[57]  Daniel M. Ricciuto,et al.  Predicting long‐term carbon sequestration in response to CO2 enrichment: How and why do current ecosystem models differ? , 2015 .

[58]  O. Phillips,et al.  Basin-wide variations in Amazon forest nitrogen-cycling characteristics as inferred from plant and soil 15N:14N measurements , 2014 .

[59]  Peter M. Vitousek,et al.  Nutrient Cycling and Limitation: Hawai'i as a Model System , 2004 .

[60]  H. Lambers,et al.  Plant nutrient-acquisition strategies change with soil age. , 2008, Trends in ecology & evolution.

[61]  Stephen Sitch,et al.  Simulated resilience of tropical rainforests to CO2-induced climate change , 2013 .

[62]  Benjamin L Turner,et al.  Tropical forest responses to increasing atmospheric CO2: current knowledge and opportunities for future research. , 2013, Functional plant biology : FPB.

[63]  P. Ciais,et al.  Global forest carbon uptake due to nitrogen and phosphorus deposition from 1850 to 2100 , 2017, Global change biology.

[64]  Benjamin Smith,et al.  Implications of incorporating N cycling and N limitations on primary production in an individual-based dynamic vegetation model , 2013 .

[65]  William D. Collins,et al.  Forest response to increased disturbance in the central Amazon and comparison to western Amazonian forests , 2014 .

[66]  Rachel M. Law,et al.  A global model of carbon, nitrogen and phosphorus cycles for the terrestrial biosphere , 2009 .

[67]  Pavel Kabat,et al.  Comparative measurements of carbon dioxide fluxes from two nearby towers in a central Amazonian rainforest: the Manaus LBA site , 2002 .

[68]  H. Lambers,et al.  Root-released organic anions in response to low phosphorus availability: recent progress, challenges and future perspectives , 2019, Plant and Soil.

[69]  O. Phillips,et al.  Above- and below-ground net primary productivity across ten Amazonian forests on contrasting soils , 2009 .