Compositional response of Amazon forests to climate change

Most of the planet's diversity is concentrated in the tropics, which includes many regions undergoing rapid climate change. Yet, while climate‐induced biodiversity changes are widely documented elsewhere, few studies have addressed this issue for lowland tropical ecosystems. Here we investigate whether the floristic and functional composition of intact lowland Amazonian forests have been changing by evaluating records from 106 long‐term inventory plots spanning 30 years. We analyse three traits that have been hypothesized to respond to different environmental drivers (increase in moisture stress and atmospheric CO2 concentrations): maximum tree size, biogeographic water‐deficit affiliation and wood density. Tree communities have become increasingly dominated by large‐statured taxa, but to date there has been no detectable change in mean wood density or water deficit affiliation at the community level, despite most forest plots having experienced an intensification of the dry season. However, among newly recruited trees, dry‐affiliated genera have become more abundant, while the mortality of wet‐affiliated genera has increased in those plots where the dry season has intensified most. Thus, a slow shift to a more dry‐affiliated Amazonia is underway, with changes in compositional dynamics (recruits and mortality) consistent with climate‐change drivers, but yet to significantly impact whole‐community composition. The Amazon observational record suggests that the increase in atmospheric CO2 is driving a shift within tree communities to large‐statured species and that climate changes to date will impact forest composition, but long generation times of tropical trees mean that biodiversity change is lagging behind climate change.

J. Terborgh | A. Di Fiore | O. Phillips | L. Aragão | J. Barlow | Y. Malhi | E. Gloor | J. Chave | S. Lewis | M. Réjou‐Méchain | S. Fauset | T. Feldpausch | G. V. D. van der Heijden | J. Barroso | F. Bongers | A. Araujo-Murakami | L. Poorter | H. Ramírez-Angulo | M. Silveira | E. Vilanova | V. Vos | T. Baker | A. Prieto | C. Quesada | A. Rudas | T. Lovejoy | S. Vieira | T. Erwin | W. Laurance | J. Lloyd | N. Higuchi | S. Laurance | D. Neill | N. Pitman | R. Salomão | D. Galbraith | G. Lopez-Gonzalez | J. Peacock | L. Arroyo | D. Bonal | J. Stropp | A. Andrade | N. Silva | A. Torres-Lezama | E. Arets | J. Comiskey | G. Pickavance | L. Qie | H. ter Steege | E. H. Honorio Coronado | J. Camargo | B. Marimon | I. Vieira | R. Brienen | G. Aymard C. | M. Toledo | C. Baraloto | J. Engel | P. Pétronelli | C. Vela | P. Camargo | B. Hérault | R. Boot | M. Peña-Claros | Víctor Chama Moscoso | Zorayda Restrepo Correa | A. Roopsind | Raquel S. Thomas | P. Zuidema | A. Monteagudo-Mendoza | B. H. Marimon‐Junior | R. Umetsu | Esteban Álvarez-Dávila | R. Vásquez Martínez | P. Núñez Vargas | Fernando Cornejo Valverde | Luis VALENZUELA GAMARRA | K. Dexter | W. Castro | N. P. Pallqui Camacho | Martin J. P. Sullivan | W. Hubau | P. Morandi | G. Pardo | Adriane Esquivel‐Muelbert | Nallaret Davila Cardozo | C. Stahl | Everton C Almeida | Edmar Almeida de Oliveira | A. C. Lola da Costa | Jhon del Aguila Pasquel | Luisa Fernanda Duque | F. Elias | Gerardo Flores Llampazo | Rafael Herrera Fernández | Eliana Jimenez-Rojas | A. Lima | Omar Aurelio Melo Cruz | Alexander Parada Gutierrez | M. C. Peñuela-Mora | J. S. Silva Espejo | James Singh | Peter J van de Meer | Peter van der Hout | A. Torres‐Lezama | Esteban Alvarez-Davila | J. Del Aguila Pasquel | Everton Almeida | J. del Aguila Pasquel | Luis Valenzuela Gamarra | Percy Núñez Vargas | E. Almeida | Adriane Esquível-Muelbert

[1]  Pierre Gentine,et al.  Tall Amazonian forests are less sensitive to precipitation variability , 2018, Nature Geoscience.

[2]  Jaap Schaveling,et al.  The Evolutionary Heritage , 2018 .

[3]  R. Primack,et al.  Long-term carbon sink in Borneo’s forests halted by drought and vulnerable to edge effects , 2017, Nature Communications.

[4]  H. Muller‐Landau,et al.  Drought-induced mortality patterns and rapid biomass recovery in a terra firme forest in the Colombian Amazon. , 2017, Ecology.

[5]  W. D. Stevens,et al.  Amazon plant diversity revealed by a taxonomically verified species list , 2017, Proceedings of the National Academy of Sciences.

[6]  O. Phillips,et al.  Biogeographic distributions of neotropical trees reflect their directly measured drought tolerances , 2017, Scientific Reports.

[7]  Unprecedented drought over tropical South America in 2016: significantly under-predicted by tropical SST , 2017, Scientific Reports.

[8]  Kyle G. Dexter,et al.  Seasonal drought limits tree species across the Neotropics , 2017 .

[9]  A Alonso,et al.  Persistent effects of pre-Columbian plant domestication on Amazonian forest composition , 2017, Science.

[10]  R. O’Hara,et al.  Cross-realm assessment of climate change impacts on species’ abundance trends , 2017, Nature Ecology &Evolution.

[11]  B. Enquist,et al.  Predictability in community dynamics. , 2017, Ecology letters.

[12]  William Farfan-Rios,et al.  Ancient human disturbances may be skewing our understanding of Amazonian forests , 2017, Proceedings of the National Academy of Sciences.

[13]  A. Di Fiore,et al.  Evolutionary heritage influences Amazon tree ecology , 2016, Proceedings of the Royal Society B: Biological Sciences.

[14]  Alice Boit,et al.  Resilience of Amazon forests emerges from plant trait diversity , 2016 .

[15]  José A. Sobrino,et al.  Record-breaking warming and extreme drought in the Amazon rainforest during the course of El Niño 2015–2016 , 2016, Scientific Reports.

[16]  J. Terborgh,et al.  Amazon forest response to repeated droughts , 2016 .

[17]  L. Poorter,et al.  Old‐growth Neotropical forests are shifting in species and trait composition , 2016 .

[18]  David Kenfack,et al.  Contrasting effects of defaunation on aboveground carbon storage across the global tropics , 2016, Nature Communications.

[19]  J. Canadell,et al.  Greening of the Earth and its drivers , 2016 .

[20]  Juliana Schietti,et al.  Dispersal limitation induces long-term biomass collapse in overhunted Amazonian forests , 2016, Proceedings of the National Academy of Sciences.

[21]  J. Terborgh,et al.  Consistent, small effects of treefall disturbances on the composition and diversity of four Amazonian forests , 2016, The Journal of ecology.

[22]  Nathan J B Kraft,et al.  Megafauna extinction, tree species range reduction, and carbon storage in Amazonian forests , 2016 .

[23]  Ke Zhang,et al.  Ecosystem heterogeneity determines the ecological resilience of the Amazon to climate change , 2015, Proceedings of the National Academy of Sciences.

[24]  Y. Malhi,et al.  Death from drought in tropical forests is triggered by hydraulics not carbon starvation , 2015, Nature.

[25]  O. Ovaskainen,et al.  Defaunation affects carbon storage in tropical forests , 2015, Science Advances.

[26]  C. Field,et al.  Projections of future meteorological drought and wet periods in the Amazon , 2015, Proceedings of the National Academy of Sciences.

[27]  D. Bates,et al.  Linear Mixed-Effects Models using 'Eigen' and S4 , 2015 .

[28]  N. McDowell,et al.  Larger trees suffer most during drought in forests worldwide , 2015, Nature Plants.

[29]  O. Phillips,et al.  Recent Amazon climate as background for possible ongoing and future changes of Amazon humid forests , 2015 .

[30]  P. Stevenson,et al.  Thermophilization of adult and juvenile tree communities in the northern tropical Andes , 2015, Proceedings of the National Academy of Sciences.

[31]  D. Tao,et al.  A Comparison of Tree Species Diversity in Two Subtropical Forests, Guangxi, Southwest China , 2015 .

[32]  J. Marengo,et al.  Extreme seasonal droughts and floods in Amazonia: causes, trends and impacts , 2015 .

[33]  Philippe Ciais,et al.  Projected strengthening of Amazonian dry season by constrained climate model simulations , 2015 .

[34]  N. McDowell,et al.  Darcy's law predicts widespread forest mortality under climate warming , 2015 .

[35]  Kalle Ruokolainen,et al.  Hyperdominance in Amazonian forest carbon cycling , 2015, Nature Communications.

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

[37]  Maggi Kelly,et al.  Twentieth-century shifts in forest structure in California: Denser forests, smaller trees, and increased dominance of oaks , 2015, Proceedings of the National Academy of Sciences.

[38]  F. Bongers,et al.  No growth stimulation of tropical trees by 150 years of CO2 fertilization but water-use efficiency increased , 2015 .

[39]  Josyane Ronchail,et al.  The extreme 2014 flood in south-western Amazon basin: the role of tropical-subtropical South Atlantic SST gradient , 2014 .

[40]  C. Tucker,et al.  Vegetation dynamics and rainfall sensitivity of the Amazon , 2014, Proceedings of the National Academy of Sciences.

[41]  B. Nelson,et al.  Improved allometric models to estimate the aboveground biomass of tropical trees , 2014, Global change biology.

[42]  Jens Kattge,et al.  The emergence and promise of functional biogeography , 2014, Proceedings of the National Academy of Sciences.

[43]  B. Young,et al.  Imputation of missing data in life‐history trait datasets: which approach performs the best? , 2014 .

[44]  G. Miguez-Macho,et al.  Potential hydrologic changes in the Amazon by the end of the 21st century and the groundwater buffer , 2014 .

[45]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[46]  O. Phillips,et al.  Shifting dynamics of climate-functional groups in old-growth Amazonian forests , 2014 .

[47]  P. Jones,et al.  Updated high‐resolution grids of monthly climatic observations – the CRU TS3.10 Dataset , 2014 .

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

[49]  Y. Knyazikhin,et al.  Potential hydrologic changes in the Amazon by the end of the 21st century and the groundwater buffer , 2014 .

[50]  J. Terborgh,et al.  Hyperdominance in the Amazonian Tree Flora , 2013, Science.

[51]  Depth of soil water uptake by tropical rainforest trees during dry periods: does tree dimension matter? , 2013, Oecologia.

[52]  J. Svenning,et al.  Disequilibrium vegetation dynamics under future climate change. , 2013, American journal of botany.

[53]  José A. Sobrino,et al.  Spatial and temporal patterns of the recent warming of the Amazon forest , 2013 .

[54]  D. Roberts,et al.  The steady-state mosaic of disturbance and succession across an old-growth Central Amazon forest landscape , 2013, Proceedings of the National Academy of Sciences.

[55]  H. Douville,et al.  Present-day and future Amazonian precipitation in global climate models: CMIP5 versus CMIP3 , 2013, Climate Dynamics.

[56]  Simon L Lewis,et al.  Drought-induced shifts in the floristic and functional composition of tropical forests in Ghana. , 2012, Ecology letters.

[57]  J. Terborgh,et al.  Tree height integrated into pantropical forest biomass estimates , 2012 .

[58]  P. Stevenson,et al.  The Genus Cecropia: A Biological Clock to Estimate the Age of Recently Disturbed Areas in the Neotropics , 2012, PloS one.

[59]  C. Quesada,et al.  Deriving Plant Functional Types for Amazonian forests for use in vegetation dynamics models , 2012 .

[60]  F. Jiguet,et al.  Differences in the climatic debts of birds and butterflies at a continental scale , 2012 .

[61]  R. B. Jackson,et al.  A Large and Persistent Carbon Sink in the World’s Forests , 2011, Science.

[62]  O. Phillips,et al.  ForestPlots.net: a web application and research tool to manage and analyse tropical forest plot data , 2011 .

[63]  J. Marengo,et al.  The drought of 2010 in the context of historical droughts in the Amazon region , 2011 .

[64]  D. Coomes,et al.  Moving on from Metabolic Scaling Theory: hierarchical models of tree growth and asymmetric competition for light , 2011 .

[65]  D. Coomes,et al.  Estimating the wood density of species for carbon stock assessments , 2011 .

[66]  Y. Malhi,et al.  Upslope migration of Andean trees , 2011 .

[67]  S. Hubbell,et al.  Directional changes in the species composition of a tropical forest. , 2011, Ecology.

[68]  Brian J. Enquist,et al.  Long‐term change within a Neotropical forest: assessing differential functional and floristic responses to disturbance and drought , 2011 .

[69]  O. Phillips,et al.  The 2010 Amazon Drought , 2011, Science.

[70]  James Rosindell,et al.  Unified neutral theory of biodiversity and biogeography , 2010, Scholarpedia.

[71]  S. Andelman,et al.  Drought-mortality relationships for tropical forests. , 2010, The New phytologist.

[72]  Christopher Baraloto,et al.  Functional trait variation and sampling strategies in species-rich plant communities , 2010 .

[73]  Daniel S Falster,et al.  Angiosperm wood structure: Global patterns in vessel anatomy and their relation to wood density and potential conductivity. , 2010, American journal of botany.

[74]  G. Huffman,et al.  The TRMM Multi-Satellite Precipitation Analysis (TMPA) , 2010 .

[75]  L. Poorter,et al.  The importance of wood traits and hydraulic conductance for the performance and life history strategies of 42 rainforest tree species. , 2010, The New phytologist.

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

[77]  James H Brown,et al.  Extensions and evaluations of a general quantitative theory of forest structure and dynamics , 2009, Proceedings of the National Academy of Sciences.

[78]  O. Phillips,et al.  Branch xylem density variations across the Amazon Basin , 2009 .

[79]  J. Chave,et al.  Towards a Worldwide Wood Economics Spectrum 2 . L E a D I N G D I M E N S I O N S I N W O O D F U N C T I O N , 2022 .

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

[81]  Sean C. Thomas,et al.  Increasing carbon storage in intact African tropical forests , 2009, Nature.

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

[83]  H. Barlow,et al.  Elevation increases in moth assemblages over 42 years on a tropical mountain , 2009, Proceedings of the National Academy of Sciences.

[84]  P. Marquet,et al.  A Significant Upward Shift in Plant Species Optimum Elevation During the 20th Century , 2008, Science.

[85]  R. Q. Thomas,et al.  Clustered disturbances lead to bias in large-scale estimates based on forest sample plots. , 2008, Ecology letters.

[86]  Nigel,et al.  Tree recruitment in an empty forest. , 2008, Ecology.

[87]  Richard Condit,et al.  Assessing Evidence for a Pervasive Alteration in Tropical Tree Communities , 2008, PLoS biology.

[88]  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.

[89]  C. Nobre,et al.  The Drought of Amazonia in 2005 , 2008 .

[90]  S. Lavorel,et al.  Incorporating plant functional diversity effects in ecosystem service assessments , 2007, Proceedings of the National Academy of Sciences.

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

[92]  Stephen P. Hubbell,et al.  Drought sensitivity shapes species distribution patterns in tropical forests , 2007, Nature.

[93]  C. Peres,et al.  Basin‐Wide Effects of Game Harvest on Vertebrate Population Densities in Amazonian Forests: Implications for Animal‐Mediated Seed Dispersal , 2007 .

[94]  Y. Shimabukuro,et al.  Spatial patterns and fire response of recent Amazonian droughts , 2007 .

[95]  Y. Hong,et al.  The TRMM Multisatellite Precipitation Analysis (TMPA): Quasi-Global, Multiyear, Combined-Sensor Precipitation Estimates at Fine Scales , 2007 .

[96]  B. Enquist,et al.  Rebuilding community ecology from functional traits. , 2006, Trends in ecology & evolution.

[97]  R. Condit,et al.  Demographic and life-history correlates for Amazonian trees , 2005 .

[98]  S. Wright,et al.  Tropical forests in a changing environment. , 2005, Trends in ecology & evolution.

[99]  M. Westoby,et al.  Alternative height strategies among 45 dicot rain forest species from tropical Queensland, Australia , 2005 .

[100]  F. Bongers,et al.  Beyond the regeneration phase: differentiation of height–light trajectories among tropical tree species , 2005 .

[101]  A. Di Fiore,et al.  Variation in wood density determines spatial patterns inAmazonian forest biomass , 2004 .

[102]  W. Laurance Forest-climate interactions in fragmented tropical landscapes. , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[103]  R. Condit,et al.  Pervasive alteration of tree communities in undisturbed Amazonian forests , 2004, Nature.

[104]  H. Muller‐Landau Interspecific and Inter‐site Variation in Wood Specific Gravity of Tropical Trees , 2004 .

[105]  Mark D. Bertness,et al.  Structure and organization of a northern New England salt marsh plant community , 2004 .

[106]  O. Phillips,et al.  Extinction risk from climate change , 2004, Nature.

[107]  O. Phillips,et al.  The changing ecology of tropical forests , 1997, Biodiversity & Conservation.

[108]  M. Westoby,et al.  Plant height and evolutionary games , 2003 .

[109]  Iain R. Lake,et al.  Extent of Nontimber Resource Extraction in Tropical Forests: Accessibility to Game Vertebrates by Hunters in the Amazon Basin , 2003 .

[110]  David J. Currie,et al.  A Globally Consistent Richness‐Climate Relationship for Angiosperms , 2003, The American Naturalist.

[111]  O. Phillips,et al.  An international network to monitor the structure, composition and dynamics of Amazonian forests (RAINFOR) , 2002 .

[112]  R. Busing,et al.  The Unified Neutral Theory of Biodiversity and Biogeography , 2002 .

[113]  O. Phillips,et al.  Field Manual for plot establishment and remeasurement , 2002 .

[114]  James H. Brown,et al.  Allometric scaling of production and life-history variation in vascular plants , 1999, Nature.

[115]  Phillips,et al.  Changes in the carbon balance of tropical forests: evidence from long-term plots , 1998, Science.

[116]  S. Hubbell,et al.  Changes in tree species abundance in a Neotropical forest: impact of climate change , 1996, Journal of Tropical Ecology.

[117]  G. Farquhar,et al.  The CO 2 Dependence of Photosynthesis, Plant Growth Responses to Elevated Atmospheric CO 2 Concentrations and Their Interaction with Soil Nutrient Status. I. General Principles and Forest Ecosystems , 1996 .

[118]  C. Chapman,et al.  Survival without Dispersers: Seedling Recruitment under Parents , 1995 .

[119]  O. Phillips,et al.  Increasing Turnover Through Time in Tropical Forests , 1994, Science.

[120]  S J Wright,et al.  Seasonal drought, soil fertility and the species density of tropical forest plant communities. , 1992, Trends in ecology & evolution.

[121]  M. B. Davis,et al.  Lags in vegetation response to greenhouse warming , 1989 .

[122]  A. Gentry,et al.  Changes in Plant Community Diversity and Floristic Composition on Environmental and Geographical Gradients , 1988 .

[123]  Stephen P. Hubbell,et al.  Tree Dispersion, Abundance, and Diversity in a Tropical Dry Forest , 1979, Science.

[124]  J. Connell,et al.  Mechanisms of Succession in Natural Communities and Their Role in Community Stability and Organization , 1977, The American Naturalist.