Co-occurring woody species have diverse hydraulic strategies and mortality rates during an extreme drought.

From 2011 to 2013, Texas experienced its worst drought in recorded history. This event provided a unique natural experiment to assess species-specific responses to extreme drought and mortality of four co-occurring woody species: Quercus fusiformis, Diospyros texana, Prosopis glandulosa, and Juniperus ashei. We examined hypothesized mechanisms that could promote these species' diverse mortality patterns using postdrought measurements on surviving trees coupled to retrospective process modelling. The species exhibited a wide range of gas exchange responses, hydraulic strategies, and mortality rates. Multiple proposed indices of mortality mechanisms were inconsistent with the observed mortality patterns across species, including measures of the degree of iso/anisohydry, photosynthesis, carbohydrate depletion, and hydraulic safety margins. Large losses of spring and summer whole-tree conductance (driven by belowground losses of conductance) and shallower rooting depths were associated with species that exhibited greater mortality. Based on this retrospective analysis, we suggest that species more vulnerable to drought were more likely to have succumbed to hydraulic failure belowground.

[1]  Daniel M. Johnson,et al.  Leaf hydraulic parameters are more plastic in species that experience a wider range of leaf water potentials , 2018 .

[2]  Jordi Martínez-Vilalta,et al.  A multi-species synthesis of physiological mechanisms in drought-induced tree mortality , 2017, Nature Ecology & Evolution.

[3]  Daniel M. Johnson,et al.  Measuring canopy loss and climatic thresholds from an extreme drought along a fivefold precipitation gradient across Texas , 2017, Global change biology.

[4]  Jordi Martínez-Vilalta,et al.  Water potential regulation, stomatal behaviour and hydraulic transport under drought: deconstructing the iso/anisohydric concept. , 2017, Plant, cell & environment.

[5]  D. Mackay,et al.  Plant hydraulics improves and topography mediates prediction of aspen mortality in southwestern USA. , 2017, The New phytologist.

[6]  M. G. Ryan,et al.  A belowground perspective on the drought sensitivity of forests: Towards improved understanding and simulation , 2016 .

[7]  Danielle E. Marias,et al.  Mapping 'hydroscapes' along the iso- to anisohydric continuum of stomatal regulation of plant water status. , 2016, Ecology letters.

[8]  A. McElrone,et al.  Mechanical Failure of Fine Root Cortical Cells Initiates Plant Hydraulic Decline during Drought1[OPEN] , 2016, Plant Physiology.

[9]  Sari Palmroth,et al.  A test of the hydraulic vulnerability segmentation hypothesis in angiosperm and conifer tree species. , 2016, Tree physiology.

[10]  Amanda M. Schwantes,et al.  Quantifying drought-induced tree mortality in the open canopy woodlands of central Texas , 2016 .

[11]  Canopy foliation and area as predictors of mortality risk from episodic drought for individual trees of Ashe juniper , 2016, Plant Ecology.

[12]  Brendan Choat,et al.  Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe , 2016, Proceedings of the National Academy of Sciences.

[13]  Leaf Morphological Traits of then Shrub Species at the Tamaulipan Thorn Scrub , 2016 .

[14]  G. Nowacki,et al.  An interdisciplinary approach to better assess global change impacts and drought vulnerability on forest dynamics. , 2016, Tree physiology.

[15]  R. Washington-Allen,et al.  Tree mortality from an exceptional drought spanning mesic to semiarid ecoregions. , 2016, Ecological applications : a publication of the Ecological Society of America.

[16]  D. Murray,et al.  Tree species influence woodland canopy characteristics and crown fire potential , 2016 .

[17]  N. McDowell,et al.  Responses of two semiarid conifer tree species to reduced precipitation and warming reveal new perspectives for stomatal regulation. , 2016, Plant, cell & environment.

[18]  Andrew A. Bishop,et al.  Predictions of future ephemeral springtime waterbird stopover habitat availability under global change , 2015 .

[19]  Joseph R. Stinziano,et al.  Non-structural carbohydrates in woody plants compared among laboratories. , 2015, Tree physiology.

[20]  Jordi Martínez-Vilalta,et al.  Coordination of physiological traits involved in drought-induced mortality of woody plants. , 2015, The New phytologist.

[21]  N. McDowell,et al.  Interdependence of chronic hydraulic dysfunction and canopy processes can improve integrated models of tree response to drought , 2015 .

[22]  Nate G. McDowell,et al.  On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene , 2015 .

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

[24]  J. Sperry,et al.  What plant hydraulics can tell us about responses to climate-change droughts. , 2015, The New phytologist.

[25]  T. Dawson,et al.  Predicting plant vulnerability to drought in biodiverse regions using functional traits , 2015, Proceedings of the National Academy of Sciences.

[26]  N. McDowell,et al.  Carbohydrate dynamics and mortality in a piñon-juniper woodland under three future precipitation scenarios. , 2015, Plant, cell & environment.

[27]  N. Diffenbaugh,et al.  Anthropogenic warming has increased drought risk in California , 2015, Proceedings of the National Academy of Sciences.

[28]  J. Sperry,et al.  The standard centrifuge method accurately measures vulnerability curves of long-vesselled olive stems. , 2015, The New phytologist.

[29]  Daniel Griffin,et al.  How unusual is the 2012–2014 California drought? , 2014 .

[30]  A. Hector,et al.  Drought survival of tropical tree seedlings enhanced by non-structural carbohydrate levels , 2014 .

[31]  Role of aquaporin activity in regulating deep and shallow root hydraulic conductance during extreme drought , 2014, Trees.

[32]  N. McDowell,et al.  How do trees die? A test of the hydraulic failure and carbon starvation hypotheses , 2013, Plant, cell & environment.

[33]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[34]  P. Jones,et al.  Global warming and changes in drought , 2014 .

[35]  D. Woodruff The impacts of water stress on phloem transport in Douglas-fir trees. , 2014, Tree physiology.

[36]  M. G. Ryan,et al.  Evaluating theories of drought-induced vegetation mortality using a multimodel-experiment framework. , 2013, The New phytologist.

[37]  A. Nardini,et al.  Shoot desiccation and hydraulic failure in temperate woody angiosperms during an extreme summer drought. , 2013, The New phytologist.

[38]  David T. Taylor,et al.  Climate Change and North American Rangelands: Trends, Projections, and Implications , 2013 .

[39]  H. Cochard,et al.  Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees. , 2013, Tree physiology.

[40]  M. Germino,et al.  Nonstructural leaf carbohydrate dynamics of Pinus edulis during drought-induced tree mortality reveal role for carbon metabolism in mortality mechanism. , 2013, The New phytologist.

[41]  D. White,et al.  Drought response strategies define the relative contributions of hydraulic dysfunction and carbohydrate depletion during tree mortality. , 2013, The New phytologist.

[42]  D. Twidwell,et al.  Long-Term Effects of Fire, Livestock Herbivory Removal, and Weather Variability in Texas Semiarid Savanna , 2018 .

[43]  S. Schwinning,et al.  Hydraulic responses to extreme drought conditions in three co-dominant tree species in shallow soil over bedrock , 2013, Oecologia.

[44]  A. Nardini,et al.  Global convergence in the vulnerability of forests to drought , 2012, Nature.

[45]  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.

[46]  Hervé Cochard,et al.  How reliable is the double-ended pressure sleeve technique for assessing xylem vulnerability to cavitation in woody angiosperms? , 2011, Physiologia plantarum.

[47]  N. Holbrook,et al.  Effects of the hydraulic coupling between xylem and phloem on diurnal phloem diameter variation. , 2011, Plant, cell & environment.

[48]  Nathan G. McDowell,et al.  Update on Mechanisms of Vegetation Mortality Mechanisms Linking Drought , Hydraulics , Carbon Metabolism , and Vegetation Mortality 1 [ W ] , 2011 .

[49]  R. B. Jackson,et al.  Water uptake and hydraulic redistribution across large woody root systems to 20 m depth. , 2010, Plant, cell & environment.

[50]  Brendan Choat,et al.  Measurement of vulnerability to water stress-induced cavitation in grapevine: a comparison of four techniques applied to a long-vesseled species. , 2010, Plant, cell & environment.

[51]  W. Landman Climate change 2007: the physical science basis , 2010 .

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

[53]  E. Nikinmaa,et al.  Linking phloem function to structure: analysis with a coupled xylem-phloem transport model. , 2009, Journal of theoretical biology.

[54]  Joel D. McMillin,et al.  Bark beetle-caused mortality in a drought-affected ponderosa pine landscape in Arizona, USA , 2009 .

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

[56]  J. Hicke,et al.  Cross-scale Drivers of Natural Disturbances Prone to Anthropogenic Amplification: The Dynamics of Bark Beetle Eruptions , 2008 .

[57]  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.

[58]  P. Gensel,et al.  :The Emerald Planet: How Plants Changed Earth's History , 2008 .

[59]  Robert B Jackson,et al.  Hydraulic traits are influenced by phylogenetic history in the drought-resistant, invasive genus Juniperus (Cupressaceae). , 2008, American journal of botany.

[60]  F. Pugnaire,et al.  Rooting depth and soil moisture control Mediterranean woody seedling survival during drought , 2007 .

[61]  G. Goldstein,et al.  Diurnal and seasonal variation in root xylem embolism in neotropical savanna woody species: impact on stomatal control of plant water status. , 2006, Plant, cell & environment.

[62]  M. Loureiro,et al.  Drought tolerance is associated with rooting depth and stomatal control of water use in clones of Coffea canephora. , 2005, Annals of botany.

[63]  G. Goldstein,et al.  Processes preventing nocturnal equilibration between leaf and soil water potential in tropical savanna woody species. , 2004, Tree physiology.

[64]  R. B. Jackson,et al.  Variation in Xylem Structure and Function in Stems and Roots of Trees to 20 M Depth , 2004 .

[65]  P. Barnes,et al.  Leaf demography and growth responses to altered resource availability in woody plants of contrasting leaf habit in a subtropical savanna , 2002, Plant Ecology.

[66]  H. A. Mooney,et al.  Maximum rooting depth of vegetation types at the global scale , 1996, Oecologia.

[67]  N. Buchmann,et al.  Rooting depth, water availability, and vegetation cover along an aridity gradient in Patagonia , 1996, Oecologia.

[68]  R. B. Jackson,et al.  Rooting depths, lateral root spreads and below‐ground/above‐ground allometries of plants in water‐limited ecosystems , 2002 .

[69]  A. Lugo,et al.  Climate Change and Forest Disturbances , 2001 .

[70]  Nathan Phillips,et al.  Survey and synthesis of intra‐ and interspecific variation in stomatal sensitivity to vapour pressure deficit , 1999 .

[71]  R. B. Jackson,et al.  Ecosystem rooting depth determined with caves and DNA. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

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

[73]  W. Dugas,et al.  ESTIMATING ASHE JUNIPER LEAF AREA FROM TREE AND STEM CHARACTERISTICS , 1998 .

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

[75]  François Tardieu,et al.  Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modelling isohydric and anisohydric behaviours , 1998 .

[76]  William T. Pockman,et al.  Use of centrifugal force in the study of xylem cavitation , 1997 .

[77]  John S. Sperry,et al.  Intra‐ and inter‐plant variation in xylem cavitation in Betula occidentalis , 1994 .

[78]  S. Davis,et al.  Drought tolerance and xylem embolism in co-occurring species of coastal sage and chaparral , 1994 .

[79]  R. Ansley,et al.  Seasonal trends in leaf area of honey mesquite trees: determination using image analysis. , 1992 .

[80]  Frank W. Ewers,et al.  TECHNIQUES FOR MEASURING VESSEL LENGTHS AND DIAMETERS IN STEMS OF WOODY PLANTS , 1989 .

[81]  V. Young The Effect of the 1949-54 Drought on the Ranges of Texas. , 1956 .