Global convergence in the vulnerability of forests to drought

Shifts in rainfall patterns and increasing temperatures associated with climate change are likely to cause widespread forest decline in regions where droughts are predicted to increase in duration and severity. One primary cause of productivity loss and plant mortality during drought is hydraulic failure. Drought stress creates trapped gas emboli in the water transport system, which reduces the ability of plants to supply water to leaves for photosynthetic gas exchange and can ultimately result in desiccation and mortality. At present we lack a clear picture of how thresholds to hydraulic failure vary across a broad range of species and environments, despite many individual experiments. Here we draw together published and unpublished data on the vulnerability of the transport system to drought-induced embolism for a large number of woody species, with a view to examining the likely consequences of climate change for forest biomes. We show that 70% of 226 forest species from 81 sites worldwide operate with narrow (<1 megapascal) hydraulic safety margins against injurious levels of drought stress and therefore potentially face long-term reductions in productivity and survival if temperature and aridity increase as predicted for many regions across the globe. Safety margins are largely independent of mean annual precipitation, showing that there is global convergence in the vulnerability of forests to drought, with all forest biomes equally vulnerable to hydraulic failure regardless of their current rainfall environment. These findings provide insight into why drought-induced forest decline is occurring not only in arid regions but also in wet forests not normally considered at drought risk.

[1]  Wendy Applequist,et al.  THE MISSOURI BOTANICAL GARDEN. , 1903, Science.

[2]  A. Tyree,et al.  Vulnerability of Xylem to Cavitation and Embolism , 1989 .

[3]  William T. Pockman,et al.  Sustained and significant negative water pressure in xylem , 1995, Nature.

[4]  J. Sperry,et al.  Limits to water transport in Juniperus osteosperma and Pinus edulis: implications for drought tolerance and regulation of transpiration , 1998 .

[5]  Frederick R. Adler,et al.  Limitation of plant water use by rhizosphere and xylem conductance: results from a model , 1998 .

[6]  J. Sperry,et al.  Vulnerability to xylem cavitation and the distribution of Sonoran Desert vegetation. , 1996, American journal of botany.

[7]  Robert B. Jackson,et al.  ADAPTIVE VARIATION IN THE VULNERABILITY OF WOODY PLANTS TO XYLEM CAVITATION , 2004 .

[8]  J. Piñol,et al.  The hydraulic architecture of Pinaceae – a review , 2004, Plant Ecology.

[9]  J. Sperry,et al.  Root and stem xylem embolism, stomatal conductance, and leaf turgor in Acer grandidentatum populations along a soil moisture gradient , 1996, Oecologia.

[10]  B. Choat,et al.  Hydraulic architecture of deciduous and evergreen dry rainforest tree species from north-eastern Australia , 2005, Trees.

[11]  Simon L Lewis,et al.  Tropical forests and the changing earth system , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[12]  M. Tyree,et al.  Interspecific variation in xylem vulnerability to cavitation among tropical tree and shrub species. , 2005, Tree physiology.

[13]  K. Price,et al.  Regional vegetation die-off in response to global-change-type drought. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[14]  J. Sperry,et al.  Size and function in conifer tracheids and angiosperm vessels. , 2006, American journal of botany.

[15]  G. Hegerl,et al.  Detection of human influence on twentieth-century precipitation trends , 2007, Nature.

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

[17]  T. Brodribb,et al.  Hydraulic Failure Defines the Recovery and Point of Death in Water-Stressed Conifers[OA] , 2008, Plant Physiology.

[18]  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.

[19]  Bettina M. J. Engelbrecht,et al.  Tolerance to low leaf water status of tropical tree seedlings is related to drought performance and distribution. , 2009 .

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

[21]  Daniel M. Johnson,et al.  Xylem hydraulic safety margins in woody plants: coordination of stomatal control of xylem tension with hydraulic capacitance , 2009 .

[22]  N. McDowell,et al.  A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests , 2010 .

[23]  Patrick Meir,et al.  Amazonian rain forests and drought: response and vulnerability. , 2010, The New phytologist.

[24]  D. Bowman,et al.  Xylem function and growth rate interact to determine recovery rates after exposure to extreme water deficit. , 2010, The New phytologist.

[25]  C. Douthe,et al.  Mechanism of water-stress induced cavitation in conifers: bordered pit structure and function support the hypothesis of seal capillary-seeding , 2010, Plant, cell & environment.

[26]  Maosheng Zhao,et al.  Drought-Induced Reduction in Global Terrestrial Net Primary Production from 2000 Through 2009 , 2010, Science.

[27]  Brendan Choat,et al.  The Dynamics of Embolism Repair in Xylem: In Vivo Visualizations Using High-Resolution Computed Tomography1[C][W][OA] , 2010, Plant Physiology.

[28]  G. Goldstein,et al.  Hydraulic Capacitance: Biophysics and Functional Significance of Internal Water Sources in Relation to Tree Size , 2011 .

[29]  Eric Rignot,et al.  The Copenhagen Diagnosis: Updating the World on the Latest Climate Science , 2011 .

[30]  F. Meinzer,et al.  Size- and age-related changes in tree structure and function , 2011 .

[31]  C. Field,et al.  The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off , 2011, Proceedings of the National Academy of Sciences.

[32]  H. Cochard,et al.  Uniform Selection as a Primary Force Reducing Population Genetic Differentiation of Cavitation Resistance across a Species Range , 2011, PloS one.

[33]  N. McDowell,et al.  The interdependence of mechanisms underlying climate-driven vegetation mortality. , 2011, Trends in ecology & evolution.

[34]  Hervé Cochard,et al.  Genotypic variability and phenotypic plasticity of cavitation resistance in Fagus sylvatica L. across Europe. , 2011, Tree physiology.