Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe

Y Pan, , A large and persistent carbon sink in the world’s forests. Science 333, 988–993 (2011).

GB Bonan, Forests and climate change: Forcings, feedbacks, and the climate benefits of forests. Science 320, 1444–1449 (2008).

PM Cox, , Amazonian forest dieback under climate-carbon cycle projections for the 21st century. Theor Appl Climatol 78, 137–156 (2004).

CD Allen, , A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manage 259, 660–648 (2010).

WRL Anderegg, JM Kane, LDL Anderegg, Consequences of widespread tree mortality triggered by drought and temperature stress. Nat Clim Chang 3, 30–36 (2013).

A Dai, Increasing drought under global warming in observations and models. Nat Clim Chang 3, 52–58 (2013).

WRL Anderegg, , Tree mortality predicted from drought-induced vascular damage. Nat Geosci 8, 367–371 (2015).

CD Allen, DD Breshears, NG McDowell, On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene. Ecosphere 6, 129 (2015).

NA Soudzilovskaia, , Functional traits predict relationship between plant abundance dynamic and long-term climate warming. Proc Natl Acad Sci USA 110, 18180–18184 (2013).

TL Powell, , Confronting model predictions of carbon fluxes with measurements of Amazon forests subjected to experimental drought. New Phytol 200, 350–365 (2013).

NG McDowell, , The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends Ecol Evol 26, 523–532 (2011).

WRL Anderegg, JA Berry, CB Field, Linking definitions, mechanisms, and modeling of drought-induced tree death. Trends Plant Sci 17, 693–700 (2012).

H Hartmann, HD Adams, WR Anderegg, S Jansen, MJ Zeppel, Research frontiers in drought-induced tree mortality: Crossing scales and disciplines. New Phytol 205, 965–969 (2015).

WRL Anderegg, , The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off. Proc Natl Acad Sci USA 109, 233–237 (2012).

WA Hoffmann, RM Marchin, P Abit, OL Lau, Hydraulic failure and tree dieback are associated with high wood density in a temperate forest under extreme drought. Glob Chang Biol 17, 2731–2742 (2011).

A Nardini, M Battistuzzo, T Savi, Shoot desiccation and hydraulic failure in temperate woody angiosperms during an extreme summer drought. New Phytol 200, 322–329 (2013).

PJ Mitchell, , Drought response strategies define the relative contributions of hydraulic dysfunction and carbohydrate depletion during tree mortality. New Phytol 197, 862–872 (2013).

B Choat, , Global convergence in the vulnerability of forests to drought. Nature 491, 752–755 (2012).

MK Bartlett, C Scoffoni, L Sack, The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: A global meta-analysis. Ecol Lett 15, 393–405 (2012).

RA Duursma, , Rooting depth explains [CO2] x drought interaction in Eucalyptus saligna. Tree Physiol 31, 922–931 (2011).

NG McDowell, CD Allen, Darcy’s law predicts widespread forest mortality under climate warming. Nat Clim Chang 5, 669–672 (2015).

WR Anderegg, Spatial and temporal variation in plant hydraulic traits and their relevance for climate change impacts on vegetation. New Phytol 205, 1008–1014 (2015).

DM Johnson, KA McCulloh, DR Woodruff, FC Meinzer, Hydraulic safety margins and embolism reversal in stems and leaves: Why are conifers and angiosperms so different? Plant Sci 195, 48–53 (2012).

NJB Kraft, MR Metz, RS Condit, J Chave, The relationship between wood density and mortality in a global tropical forest data set. New Phytol 188, 1124–1136 (2010).

J Chave, , Towards a worldwide wood economics spectrum. Ecol Lett 12, 351–366 (2009).

TJ Brodribb, H Cochard, Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiol 149, 575–584 (2009).

B Choat, CR Brodersen, AJ McElrone, Synchrotron X-ray microtomography of xylem embolism in Sequoia sempervirens saplings during cycles of drought and recovery. New Phytol 205, 1095–1105 (2015).

MJ O’Brien, S Leuzinger, CD Philipson, J Tay, A Hector, Drought survival of tropical tree seedlings enhanced by non-structural carbohydrate levels. Nat Clim Chang 4, 710–714 (2014).

HD Adams, , Nonstructural leaf carbohydrate dynamics of Pinus edulis during drought-induced tree mortality reveal role for carbon metabolism in mortality mechanism. New Phytol 197, 1142–1151 (2013).

T Klein, G Hoch, D Yakir, C Körner, Drought stress, growth and nonstructural carbohydrate dynamics of pine trees in a semi-arid forest. Tree Physiol 34, 981–992 (2014).

AG Quentin, , Non-structural carbohydrates in woody plants compared among laboratories. Tree Physiol 35, 1146–1165 (2015).

JM Kane, TE Kolb, Importance of resin ducts in reducing ponderosa pine mortality from bark beetle attack. Oecologia 164, 601–609 (2010).

ML Suarez, T Kitzberger, Recruitment patterns following a severe drought: Long-term compositional shifts in Patagonian forests. Can J For Res 38, 3002–3010 (2008).

R Condit, SP Hubbell, RB Foster, Mortality rates of 205 neotropical tree and shrub species and the impact of a severe drought. Ecol Monogr 65, 419–439 (1995).

D Faber-Langendoen, JR Tester, Oak mortality in sand savannas following drought in east-central Minnesota. Bull Torrey Bot Club 120, 248–256 (1993).

AR Gitlin, , Mortality gradients within and among dominant plant populations as barometers of ecosystem change during extreme drought. Conserv Biol 20, 1477–1486 (2006).

JM Olano, MW Palmer, Stand dynamics of an Appalachian old-growth forest during a severe drought episode. For Ecol Manage 174, 139–148 (2003).

JW Stringer, TW Kimmerer, JC Overstreet, JP Dunn, Oak mortality in eastern Kentucky. South J Appl For 13, 86–91 (1989).

KR Kukowski, S Schwinning, BF Schwartz, Hydraulic responses to extreme drought conditions in three co-dominant tree species in shallow soil over bedrock. Oecologia 171, 819–830 (2013).

ML Floyd, , Relationship of stand characteristics to drought-induced mortality in three southwestern piñion-juniper woodlands. Ecol Appl 19, 1223–1230 (2009).

RJ Klos, GG Wang, WL Bauerle, JR Rieck, Drought impact on forest growth and mortality in the southeast USA: An analysis using Forest Health and Monitoring data. Ecol Appl 19, 699–708 (2009).

AJ Viljoen, The influence of the 1991/92 drought on the woody vegetation of the Kruger National Park. Koedoe 38, 85–97 (1995).

TG O’connor, Impact of sustained drought on a semi-arid Colophospermum mopane savanna. Afr J Range Forage Sci 15, 83–91 (1998).

JS Lwanga, Localized tree mortality following the drought of 1999 at Ngogo, Kibale National Park, Uganda. Afr J Ecol 41, 194–196 (2003).

MG Van Nieuwstadt, D Sheil, Drought, fire and tree survival in a Borneo rain forest, East Kalimantan, Indonesia. J Ecol 93, 191–201 (2005).

MD Potts, Drought in a Bornean everwet rain forest. J Ecol 91, 467–474 (2003).

M Nakagawa, , Impact of severe drought associated with the 1997–1998 El Nino in a tropical forest in Sarawak. J Trop Ecol 16, 355–367 (2000).

DM Newbery, M Lingenfelder, Plurality of tree species responses to drought perturbation in Bornean tropical rain forest. Plant Ecol 201, 147–167 (2009).

RJ Fensham, The influence of cattle grazing on tree mortality after drought in savanna woodland in north Queensland. Aust J Ecol 23, 405–407 (1998).

RJ Fensham, JE Holman, Temporal and spatial patterns in drought-related tree dieback in Australian savanna. J Appl Ecol 36, 1035–1050 (1999).

KJ Rice, SL Matzner, W Byer, JR Brown, Patterns of tree dieback in Queensland, Australia: The importance of drought stress and the role of resistance to cavitation. Oecologia 139, 190–198 (2004).

RJ Fensham, RJ Fairfax, DW Butler, D Bowman, Effects of fire and drought in a tropical eucalypt savanna colonized by rain forest. J Biogeogr 30, 1405–1414 (2003).

J Martínez-Vilalta, J Piñol, Drought-induced mortality and hydraulic architecture in pine populations of the NE Iberian Peninsula. For Ecol Manage 161, 247–256 (2002).

L Gu, SG Pallardy, KP Hosman, Y Sun, Drought-influenced mortality of tree species with different predawn leaf water dynamics in a decade-long study of a central US forest. Biogeosciences 12, 2831–2845 (2015).

JL Ganey, SC Vojta, Tree mortality in drought-stressed mixed-conifer and ponderosa pine forests, Arizona, USA. For Ecol Manage 261, 162–168 (2011).

RJ Fensham, J Fraser, HJ MacDermott, J Firn, Dominant tree species are at risk from exaggerated drought under climate change. Glob Chang Biol 21, 3777–3785 (2015).

JJ Camarero, A Gazol, G Sangüesa-Barreda, J Oliva, SM Vicente-Serrano, To die or not to die: Early warnings of tree dieback in response to a severe drought. J Ecol 103, 44–57 (2015).

L Cavin, EP Mountford, GF Peterken, AS Jump, Extreme drought alters competitive dominance within and between tree species in a mixed forest stand. Funct Ecol 27, 1424–1435 (2013).

M Coll, J Peñuelas, M Ninyerola, X Pons, J Carnicer, Multivariate effect gradients driving forest demographic responses in the Iberian Peninsula. For Ecol Manage 303, 195–209 (2013).

WR Anderegg, , Tree mortality from drought, insects, and their interactions in a changing climate. New Phytol 208, 674–683 (2015).

RL Chazdon, A Redondo Brenes, B Vilchez Alvarado, Effects of climate and stand age on annual tree dynamics in tropical second-growth rain forests. Ecology 86, 1808–1815 (2005).

RJ Fensham, RJ Fairfax, JM Dwyer, Potential aboveground biomass in drought-prone forest used for rangeland pastoralism. Ecol Appl 22, 894–908 (2012).

C Peng, , A drought-induced pervasive increase in tree mortality across Canada’s boreal forests. Nat Clim Chang 1, 467–471 (2011).

T Klein, The variability of stomatal sensitivity to leaf water potential across tree species indicates a continuum between isohydric and anisohydric behaviours. Funct Ecol 28, 1313–1320 (2014).

SM Gleason Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world’s woody plant species. New Phytol 209 123–136 (2015).

AE Zanne Data from: Towards a worldwide wood economics spectrum. Available at dx.doi.org/10.5061/dryad.234. Accessed March 17 2016. (2009).

J Kattge, , TRY – a global database of plant traits. Glob Chang Biol 17, 2905–2935 (2011).

SJ Wright, , Functional traits and the growth-mortality trade-off in tropical trees. Ecology 91, 3664–3674 (2010).

I Harris, P Jones, T Osborn, D Lister, Updated high‐resolution grids of monthly climatic observations–the CRU TS3. 10 Dataset. Int J Climatol 34, 623–642 (2014).

D Bates Package “lme4.” R Founda Stat Comput Vienna. Available at https://cran.r-project.org/web/packages/lme4/index.html. Accessed March 16 2015. (2014).

; Team RC R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing). Available at www.R-project.org. Accessed January 1 2013. (2012).

A Liaw M Wiener L Breiman A Cutler Package “randomForest.” Available at https://cran.r-project.org/web/packages/randomForest/index.html. Accessed December 12 2009. (2009).

J Settele, , Terrestrial and inland water systems. Climate change 2014: Impacts, adaptation, and vulnerability. Part A: Global and sectoral aspects. Proceedings of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, eds CB Field, (Cambridge Univ Press, Cambridge, United Kingdom), pp. 271–359 (2014).