Multiple mechanisms of Amazonian forest biomass losses in three dynamic global vegetation models under climate change.

*The large-scale loss of Amazonian rainforest under some future climate scenarios has generally been considered to be driven by increased drying over Amazonia predicted by some general circulation models (GCMs). However, the importance of rainfall relative to other drivers has never been formally examined. *Here, we conducted factorial simulations to ascertain the contributions of four environmental drivers (precipitation, temperature, humidity and CO(2)) to simulated changes in Amazonian vegetation carbon (C(veg)), in three dynamic global vegetation models (DGVMs) forced with climate data based on HadCM3 for four SRES scenarios. *Increased temperature was found to be more important than precipitation reduction in causing losses of Amazonian C(veg) in two DGVMs (Hyland and TRIFFID), and as important as precipitation reduction in a third DGVM (LPJ). Increases in plant respiration, direct declines in photosynthesis and increases in vapour pressure deficit (VPD) all contributed to reduce C(veg) under high temperature, but the contribution of each mechanism varied greatly across models. Rising CO(2) mitigated much of the climate-driven biomass losses in the models. *Additional work is required to constrain model behaviour with experimental data under conditions of high temperature and drought. Current models may be overly sensitive to long-term elevated temperatures as they do not account for physiological acclimation.

[1]  A. Taylor,et al.  Widespread Increase of Tree Mortality Rates in the Western United States , 2009, Science.

[2]  P. Kasemsap,et al.  Photosynthetic capacity and temperature responses of photosynthesis of rubber trees (Hevea brasiliensis Müll. Arg.) acclimate to changes in ambient temperatures , 2009, Trees.

[3]  Stefano Tarantola,et al.  Variance‐Based Methods , 2008 .

[4]  Sandy P. Harrison,et al.  The influence of vegetation, fire spread and fire behaviour on biomass burning and trace gas emissions: results from a process-based model , 2010 .

[5]  Andrew D. Friend,et al.  A process-based, terrestrial biosphere model of ecosystem dynamics (Hybrid v3.0) , 1997 .

[6]  Robert K. Colwell,et al.  Species Loss and Aboveground Carbon Storage in a Tropical Forest , 2005, Science.

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

[8]  Gene Stevens,et al.  Analysis of deterministic simulation model performance using non-replicated factorial two-level experiments , 1996 .

[9]  T. Lenton,et al.  A factorial analysis of the marine carbon cycle and ocean circulation controls on atmospheric CO2 , 2005 .

[10]  A. Leakey,et al.  High-temperature inhibition of photosynthesis is greater under sunflecks than uniform irradiance in a tropical rain forest tree seedling , 2003 .

[11]  R. Sutton,et al.  Exploring multi-model atmospheric GCM ensembles with ANOVA , 2008 .

[12]  F. Woodward,et al.  Assessing uncertainties in a second-generation dynamic vegetation model caused by ecological scale limitations. , 2010, The New phytologist.

[13]  A. Rogers,et al.  Rising atmospheric carbon dioxide: plants FACE the future. , 2004, Annual review of plant biology.

[14]  R. Betts,et al.  Using a GCM analogue model to investigate the potential for Amazonian forest dieback , 2004 .

[15]  R. Sage,et al.  Thermal acclimation of photosynthesis in black spruce [Picea mariana (Mill.) B.S.P.]. , 2008, Plant, cell & environment.

[16]  Eric A Davidson,et al.  Drought effects on litterfall, wood production and belowground carbon cycling in an Amazon forest: results of a throughfall reduction experiment , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

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

[18]  G. Collatz,et al.  Coupled Photosynthesis-Stomatal Conductance Model for Leaves of C4 Plants , 1992 .

[19]  J. Terborgh,et al.  The regional variation of aboveground live biomass in old‐growth Amazonian forests , 2006 .

[20]  William F. Laurance,et al.  Amazonian Tree Mortality during the 1997 El Niño Drought , 2000 .

[21]  M. Goulden,et al.  Diurnal patterns of leaf photosynthesis, conductance and water potential at the top of a lowland rain forest canopy in Cameroon: measurements from the Radeau des Cimes. , 1994, Tree physiology.

[22]  W. Post,et al.  Plant Respiration in a Warmer World , 2006, Science.

[23]  D. Nepstad,et al.  Interactions among Amazon land use, forests and climate: prospects for a near-term forest tipping point , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[24]  C. Nobre,et al.  Climate change consequences on the biome distribution in tropical South America , 2007 .

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

[26]  M. Williams,et al.  Net primary production of forests: a constant fraction of gross primary production? , 1998, Tree physiology.

[27]  A. Rogers,et al.  Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. , 2009, Journal of experimental botany.

[28]  Roger M. Gifford,et al.  Whole plant respiration and photosynthesis of wheat under increased CO2 concentration and temperature: long‐term vs. short‐term distinctions for modelling , 1995 .

[29]  R. Betts,et al.  Detection of a direct carbon dioxide effect in continental river runoff records , 2006, Nature.

[30]  Mark G Tjoelker,et al.  The hot and the cold: unravelling the variable response of plant respiration to temperature. , 2005, Functional plant biology : FPB.

[31]  Andrew D. Friend,et al.  Modelling the impact of future changes in climate, CO2 concentration and land use on natural ecosystems and the terrestrial carbon sink , 2004 .

[32]  R. Betts,et al.  The role of ecosystem-atmosphere interactions in simulated Amazonian precipitation decrease and forest dieback under global climate warming , 2004 .

[33]  D. Metcalfe,et al.  The fate of assimilated carbon during drought: impacts on respiration in Amazon rainforests , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[34]  A. Friend PGEN: an integrated model of leaf photosynthesis, transpiration, and conductance , 1995 .

[35]  Hisashi Sato,et al.  SEIB–DGVM: A new Dynamic Global Vegetation Model using a spatially explicit individual-based approach , 2007 .

[36]  O. Phillips,et al.  The changing Amazon forest , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[37]  C. Nobre,et al.  Exploring the range of climate biome projections for tropical South America: The role of CO2 fertilization and seasonality , 2009 .

[38]  Scott D. Miller,et al.  Seasonal drought stress in the Amazon: Reconciling models and observations , 2008 .

[39]  D. Macherel,et al.  The crucial role of plant mitochondria in orchestrating drought tolerance. , 2009, Annals of botany.

[40]  L. Aragão,et al.  Exploring the likelihood and mechanism of a climate-change-induced dieback of the Amazon rainforest , 2009, Proceedings of the National Academy of Sciences.

[41]  J. Shuman,et al.  Evaluating the sensitivity of Eurasian forest biomass to climate change using a dynamic vegetation model , 2009 .

[42]  J. Lloyd,et al.  On the temperature dependence of soil respiration , 1994 .

[43]  P. Jarvis The Interpretation of the Variations in Leaf Water Potential and Stomatal Conductance Found in Canopies in the Field , 1976 .

[44]  Peter M. Cox,et al.  Description of the "TRIFFID" Dynamic Global Vegetation Model , 2001 .

[45]  S L Lewis,et al.  Pattern and process in Amazon tree turnover, 1976-2001. , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[46]  S. Sitch,et al.  The role of fire disturbance for global vegetation dynamics: coupling fire into a Dynamic Global Vegetation Model , 2008 .

[47]  I. Fung,et al.  Root functioning modifies seasonal climate. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[48]  R. Oren,et al.  Water deficits and hydraulic limits to leaf water supply. , 2002, Plant, cell & environment.

[49]  Benjamin Poulter,et al.  Modeling the Sensitivity of the Seasonal Cycle of GPP to Dynamic LAI and Soil Depths in Tropical Rainforests , 2009, Ecosystems.

[50]  Denis Loustau,et al.  Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data , 2002 .

[51]  P. P. Harris,et al.  Amazonian climate: results and future research , 2004 .

[52]  M. H. Costa,et al.  Vegetation‐atmosphere‐soil nutrient feedbacks in the Amazon for different deforestation scenarios , 2009 .

[53]  C. D. Keeling,et al.  Tropical rain forest tree growth and atmospheric carbon dynamics linked to interannual temperature variation during 1984–2000 , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[54]  E. Rastetter,et al.  Seasonal variation in net carbon exchange and evapotranspiration in a Brazilian rain forest: a modelling analysis , 1998 .

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

[56]  M. Keller,et al.  Isoprene emission from tropical forest canopy leaves , 1999 .

[57]  R. Dickinson,et al.  Rainfall and its seasonality over the Amazon in the 21st century as assessed by the coupled models for the IPCC AR4 , 2006 .

[58]  Tim E. Jupp,et al.  Increasing risk of Amazonian drought due to decreasing aerosol pollution , 2008 .

[59]  Kenneth J Feeley,et al.  Decelerating growth in tropical forest trees. , 2007, Ecology letters.

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

[61]  Sandy P. Harrison,et al.  Global Biogeochemical Cycles in the Climate System , 2001 .

[62]  Stephen S. O. Burgess,et al.  Hydraulic redistribution in three Amazonian trees , 2005, Oecologia.

[63]  Roderick C. Dewar,et al.  Acclimation of the respiration/photosynthesis ratio to temperature: insights from a model , 1999 .

[64]  Kaoru Kitajima,et al.  Cloud cover limits net CO2 uptake and growth of a rainforest tree during tropical rainy seasons , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[65]  F. Woodward,et al.  Using temperature‐dependent changes in leaf scaling relationships to quantitatively account for thermal acclimation of respiration in a coupled global climate–vegetation model , 2008 .

[66]  I. C. Prentice,et al.  Evaluation of ecosystem dynamics, plant geography and terrestrial carbon cycling in the LPJ dynamic global vegetation model , 2003 .

[67]  I. C. Prentice,et al.  BIOME3: An equilibrium terrestrial biosphere model based on ecophysiological constraints, resource availability, and competition among plant functional types , 1996 .

[68]  Jens Kattge,et al.  Temperature acclimation in a biochemical model of photosynthesis: a reanalysis of data from 36 species. , 2007, Plant, cell & environment.

[69]  Stephen Sitch,et al.  Simulating fire regimes in human‐dominated ecosystems: Iberian Peninsula case study , 2002 .

[70]  Michael L. Goulden,et al.  Are tropical forests near a high temperature threshold , 2008 .

[71]  C. Hopkinson,et al.  Effects of global change on carbon storage in tropical forests of South America , 1995 .

[72]  K. Hikosaka,et al.  Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate. , 2006, Journal of experimental botany.

[73]  C. Körner Through enhanced tree dynamics carbon dioxide enrichment may cause tropical forests to lose carbon. , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[74]  N. McDowell,et al.  Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? , 2008, The New phytologist.

[75]  Stephen Sitch,et al.  Towards quantifying uncertainty in predictions of Amazon ‘dieback’ , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[76]  M. Hulme,et al.  A high-resolution data set of surface climate over global land areas , 2002 .

[77]  F. Woodward,et al.  The global distribution of ecosystems in a world without fire. , 2004, The New phytologist.

[78]  I. C. Prentice,et al.  Evaluation of the terrestrial carbon cycle, future plant geography and climate‐carbon cycle feedbacks using five Dynamic Global Vegetation Models (DGVMs) , 2008 .

[79]  Y. Shimabukuro,et al.  Interactions between rainfall, deforestation and fires during recent years in the Brazilian Amazonia , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[80]  A. Raschi,et al.  Photosynthetic Characteristics of Sun and Shade Leaves in the Canopy of Arbutus unedo L. Trees Exposed to In Situ Long-Term Elevated CO2 , 1999, Photosynthetica.

[81]  T. Pons,et al.  Respiration as a percentage of daily photosynthesis in whole plants is homeostatic at moderate, but not high, growth temperatures. , 2007, The New phytologist.

[82]  Richard Essery,et al.  Explicit representation of subgrid heterogeneity in a GCM land surface scheme , 2003 .

[83]  Pete Smith,et al.  Integrating plant–soil interactions into global carbon cycle models , 2009 .

[84]  Mark G Tjoelker,et al.  Thermal acclimation and the dynamic response of plant respiration to temperature. , 2003, Trends in plant science.

[85]  Benjamin Smith,et al.  CO2 fertilization in temperate FACE experiments not representative of boreal and tropical forests , 2008 .

[86]  S. Idso,et al.  Seventeen years of carbon dioxide enrichment of sour orange trees: final results , 2007 .

[87]  A. Di Fiore,et al.  Increasing biomass in Amazonian forest plots. , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[88]  Alexei G. Sankovski,et al.  Special report on emissions scenarios , 2000 .

[89]  P. Meir,et al.  Evaluating climatic and soil water controls on evapotranspiration at two Amazonian rainforest sites , 2008 .

[90]  Andrew D. Friend,et al.  Climate change impacts on ecosystems and the terrestrial carbon sink: a new assessment , 1999 .

[91]  E. S. Tribuzy Variações da temperatura foliar do dossel e o seu efeito na taxa assimilatória de CO2 na Amazônia Central. , 2005 .

[92]  D. Nepstad,et al.  Mortality of large trees and lianas following experimental drought in an Amazon forest. , 2007, Ecology.

[93]  R. Betts,et al.  Amazonian forest dieback under climate-carbon cycle projections for the 21st century , 2004 .

[94]  G. Farquhar,et al.  Effects of rising temperatures and [CO2] on the physiology of tropical forest trees , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[95]  Wolfgang Lucht,et al.  Tipping elements in the Earth's climate system , 2008, Proceedings of the National Academy of Sciences.

[96]  R. Betts,et al.  Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model , 2000, Nature.

[97]  Evan H. DeLucia,et al.  Forest carbon use efficiency: is respiration a constant fraction of gross primary production? , 2007 .

[98]  I. Prentice,et al.  Terrestrial nitrogen cycle simulation with a dynamic global vegetation model , 2008 .

[99]  J. Flexas,et al.  Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress , 2006 .

[100]  O. Phillips,et al.  Effect of 7 yr of experimental drought on vegetation dynamics and biomass storage of an eastern Amazonian rainforest. , 2010, The New phytologist.

[101]  Peter M. Cox,et al.  An analogue model to derive additional climate change scenarios from existing GCM simulations , 2000 .

[102]  R Fisher,et al.  Design of Experiments , 1936 .

[103]  Richard Harding,et al.  A canopy conductance and photosynthesis model for use in a GCM land surface scheme , 1998 .

[104]  Benjamin Z. Houlton,et al.  Nitrogen constraints on terrestrial carbon uptake: Implications for the global carbon‐climate feedback , 2009 .

[105]  Mauricio da Costa,et al.  Impacts of experimentally imposed drought on leaf respiration and morphology in an Amazon rain forest , 2010 .

[106]  J. Stewart Modelling surface conductance of pine forest , 1988 .

[107]  P. Cox,et al.  Calibration of a land-surface model using data from primary forest sites in Amazonia , 2004 .

[108]  J. V. Soares,et al.  Distribution of aboveground live biomass in the Amazon basin , 2007 .

[109]  S. Lewis,et al.  Changing Ecology of Tropical Forests: Evidence and Drivers , 2009 .

[110]  Andrew White,et al.  Evaluation and analysis of a dynamic terrestrial ecosystem model under preindustrial conditions at the global scale , 2000 .

[111]  J. Terborgh,et al.  Drought Sensitivity of the Amazon Rainforest , 2009, Science.

[112]  Mark G. Tjoelker,et al.  Foliar respiration acclimation to temperature and temperature variable Q10 alter ecosystem carbon balance , 2005 .

[113]  A. McGuire,et al.  Global climate change and terrestrial net primary production , 1993, Nature.