Hydraulic traits that buffer deep‐rooted plants from changes in hydrology and climate

Groundwater‐dependent ecosystems are often defined by the presence of deeply rooted phreatophytic plants. When connected to groundwater, phreatophytes in arid regions decouple ecosystem net primary productivity from precipitation, underscoring a disproportionately high biodiversity and exchange of resources relative to surrounding areas. However, groundwater‐dependent ecosystems are widely threatened due to the effects of water diversions, groundwater abstraction, and higher frequencies of episodic drought and heat waves. The resilience of these ecosystems to shifting ecohydrological–climatological conditions will depend largely on the capacity of dominant, phreatophytic plants to cope with dramatic reductions in water availability and increases in atmospheric water demand. This paper disentangles the broad range of hydraulic traits expressed by phreatophytic vegetation to better understand their capacity to survive or even thrive under shifting ecohydrological conditions. We focus on three elements of plant water relations: (a) hydraulic architecture (including root area to leaf area ratios and rooting depth), (b) xylem structure and function, and (c) stomatal regulation. We place the expression of these traits across a continuum of phreatophytic habits from obligate to semi‐obligate to semi‐facultative to facultative. Although many species occupy multiple phreatophytic niches depending on access to groundwater, we anticipate that populations are largely locally adapted to a narrow range of ecohydrological conditions regardless of gene flow across ecohydrological gradients. Consequently, we hypothesize that reductions in available groundwater and increases in atmospheric water demand will result in either (a) stand replacement of obligate phreatophytic species with more facultative species as a function of widespread mortality in highly groundwater‐dependent populations or (b) directional selection in semi‐obligate and semi‐facultative phreatophytes towards the expression of traits associated with highly facultative phreatophytes in the absence of species replacement. Anticipated shifts in the expression of hydraulic traits may have profound impacts on water cycling processes, species assemblages, and habitat structure of groundwater‐dependent woodlands and riparian forests.

[1]  L. Flanagan,et al.  Using stable isotopes to quantify water sources for trees and shrubs in a riparian cottonwood ecosystem in flood and drought years , 2019, Hydrological Processes.

[2]  J. Olden,et al.  Prepare river ecosystems for an uncertain future , 2019, Nature.

[3]  R. Scott,et al.  Critical Zone Water Balance Over 13 Years in a Semiarid Savanna , 2019, Water Resources Research.

[4]  K. Grady,et al.  Genotypic variation in phenological plasticity: Reciprocal common gardens reveal adaptive responses to warmer springs but not to fall frost , 2018, Global change biology.

[5]  D. Mackay,et al.  Distributed Plant Hydraulic and Hydrological Modeling to Understand the Susceptibility of Riparian Woodland Trees to Drought‐Induced Mortality , 2018, Water Resources Research.

[6]  B. Choat,et al.  Triggers of tree mortality under drought , 2018, Nature.

[7]  A. L. Muler,et al.  Can hydraulically redistributed water assist surrounding seedlings during summer drought? , 2018, Oecologia.

[8]  Yeong-Seok Jo,et al.  Population genomic analysis suggests strong influence of river network on spatial distribution of genetic variation in invasive saltcedar across the southwestern United States , 2018, Molecular ecology.

[9]  James Cleverly,et al.  Divergence in plant water-use strategies in semiarid woody species. , 2017, Functional plant biology : FPB.

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

[11]  Michael Dorman,et al.  A synthesis of radial growth patterns preceding tree mortality , 2017, Global change biology.

[12]  E. Glenn,et al.  Can local adaptation explain varying patterns of herbivory tolerance in a recently introduced woody plant in North America? , 2017, Conservation physiology.

[13]  G. Asner,et al.  Airborne laser-guided imaging spectroscopy to map forest trait diversity and guide conservation , 2017, Science.

[14]  Dana H. Ikeda,et al.  Genetically informed ecological niche models improve climate change predictions , 2017, Global change biology.

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

[16]  P. Bellingham,et al.  Root traits are multidimensional: specific root length is independent from root tissue density and the plant economic spectrum , 2016 .

[17]  R. Guy,et al.  Comparative physiology of allopatric Populus species: geographic clines in photosynthesis, height growth, and carbon isotope discrimination in common gardens , 2015, Front. Plant Sci..

[18]  T. Delworth,et al.  Regional rainfall decline in Australia attributed to anthropogenic greenhouse gases and ozone levels , 2014 .

[19]  Rafael Poyatos,et al.  A new look at water transport regulation in plants. , 2014, The New phytologist.

[20]  R. Froend,et al.  Phreatophytic vegetation responses to groundwater depth in a drying mediterranean-type landscape , 2014 .

[21]  P. Reich.  The world‐wide ‘fast–slow’ plant economics spectrum: a traits manifesto , 2014 .

[22]  A. Norton,et al.  Hybridization of an invasive shrub affects tolerance and resistance to defoliation by a biological control agent , 2014, Evolutionary applications.

[23]  T. Kolb,et al.  Species variation in water relations and xylem vulnerability to cavitation at a forest-woodland ecotone , 2013 .

[24]  J. Stromberg.  Root patterns and hydrogeomorphic niches of riparian plants in the American Southwest , 2013 .

[25]  O. Körner,et al.  High temperature stress monitoring and detection using chlorophyll a fluorescence and infrared thermography in chrysanthemum (Dendranthema grandiflora). , 2013, Plant physiology and biochemistry : PPB.

[26]  T. Kolb,et al.  Conservative leaf economic traits correlate with fast growth of genotypes of a foundation riparian species near the thermal maximum extent of its geographic range , 2013 .

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

[28]  W. Bond,et al.  Diverse functional responses to drought in a Mediterranean-type shrubland in South Africa. , 2012, The New phytologist.

[29]  T. Whitham,et al.  Relative importance of genetic, ontogenetic, induction, and seasonal variation in producing a multivariate defense phenotype in a foundation tree species , 2012, Oecologia.

[30]  L. Reynolds,et al.  Vulnerability of riparian ecosystems to elevated CO2 and climate change in arid and semiarid western North America , 2012 .

[31]  T. Kolb,et al.  Genetic variation in productivity of foundation riparian species at the edge of their distribution: implications for restoration and assisted migration in a warming climate , 2011 .

[32]  J. E. Roelle,et al.  Genetic and environmental influences on leaf phenology and cold hardiness of native and introduced riparian trees , 2011, International journal of biometeorology.

[33]  K. Hultine,et al.  Ecohydrological consequences of non‐native riparian vegetation in the southwestern United States: A review from an ecophysiological perspective , 2011 .

[34]  S. Rood,et al.  Root architecture of riparian trees: river cut-banks provide natural hydraulic excavation, revealing that cottonwoods are facultative phreatophytes , 2011, Trees.

[35]  R. Froend,et al.  Resilience of phreatophytic vegetation to groundwater drawdown: is recovery possible under a drying climate? , 2011 .

[36]  J. Stromberg,et al.  Effects of stream flow patterns on riparian vegetation of a semiarid river: Implications for a changing climate , 2010 .

[37]  J. Ehleringer,et al.  Ecophysiology of riparian cottonwood and willow before, during, and after two years of soil water removal. , 2010, Ecological applications : a publication of the Ecological Society of America.

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

[39]  D. White,et al.  Plasticity in the Huber value contributes to homeostasis in leaf water relations of a mallee Eucalypt with variation to groundwater depth. , 2009, Tree physiology.

[40]  O. W. Van Auken,et al.  Causes and consequences of woody plant encroachment into western North American grasslands. , 2009, Journal of environmental management.

[41]  I. Rodríguez‐Iturbe,et al.  Ecohydrology of groundwater‐dependent ecosystems: 1. Stochastic water table dynamics , 2009 .

[42]  J. Chave,et al.  Towards a worldwide wood economics spectrum. , 2009, Ecology letters.

[43]  R. Scott,et al.  Sensitivity of mesquite shrubland CO2 exchange to precipitation in contrasting landscape settings. , 2008, Ecology.

[44]  G. Bonan.  Forests and Climate Change: Forcings, Feedbacks, and the Climate Benefits of Forests , 2008, Science.

[45]  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.

[46]  R. Scott,et al.  The ecohydrologic significance of hydraulic redistribution in a semiarid savanna , 2008 .

[47]  J. Gornall,et al.  Geographic variation in ecophysiological traits of black cottonwood (Populus trichocarpa)This article is one of a selection of papers published in the Special Issue on Poplar Research in Canada. , 2007 .

[48]  M. Gribskov,et al.  The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray) , 2006, Science.

[49]  D. Stannard,et al.  Effects of long-term water table drawdown on evapotranspiration and vegetation in an arid region phreatophyte community , 2006 .

[50]  S. Running,et al.  Impacts of climate change on natural forest productivity – evidence since the middle of the 20th century , 2006 .

[51]  R. Froend,et al.  Defining phreatophyte response to reduced water availability: preliminary investigations on the use of xylem cavitation vulnerability in Banksia woodland species , 2006 .

[52]  J. Sperry,et al.  Influence of soil texture on hydraulic properties and water relations of a dominant warm-desert phreatophyte. , 2006, Tree physiology.

[53]  David C. Goodrich,et al.  Controls on transpiration in a semiarid riparian cottonwood forest , 2006 .

[54]  P. Reich,et al.  Assessing the generality of global leaf trait relationships. , 2005, The New phytologist.

[55]  David G. Williams,et al.  Precipitation pulse use by an invasive woody legume: the role of soil texture and pulse size , 2005, Oecologia.

[56]  T. Kawecki,et al.  Conceptual issues in local adaptation , 2004 .

[57]  D. Goodrich,et al.  Hydraulic redistribution by a dominant, warm‐desert phreatophyte: seasonal patterns and response to precipitation pulses , 2004 .

[58]  Stephen M. Schrader,et al.  Electron transport is the functional limitation of photosynthesis in field-grown Pima cotton plants at high temperature , 2004 .

[59]  Sean C. Thomas,et al.  The worldwide leaf economics spectrum , 2004, Nature.

[60]  W. J. Shuttleworth,et al.  Interannual and seasonal variation in fluxes of water and carbon dioxide from a riparian woodland ecosystem , 2004 .

[61]  B. Lamont,et al.  Long‐distance seed dispersal in a metapopulation of Banksia hookeriana inferred from a population allocation analysis of amplified fragment length polymorphism data , 2004, Molecular ecology.

[62]  T. Keefer,et al.  Contrasting patterns of hydraulic redistribution in three desert phreatophytes , 2003, Oecologia.

[63]  K. Snyder,et al.  Night-time conductance in C3 and C4 species: do plants lose water at night? , 2003, Journal of experimental botany.

[64]  J. Sperry,et al.  Desert shrub water relations with respect to soil characteristics and plant functional type , 2002 .

[65]  J. Turner,et al.  Influence of groundwater depth on the seasonal sources of water accessed by Banksia tree species on a shallow, sandy coastal aquifer , 2002, Oecologia.

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

[67]  David G. Williams,et al.  Water sources used by riparian trees varies among stream types on the San Pedro River, Arizona. , 2000 .

[68]  R. B. Jackson,et al.  Root water uptake and transport: using physiological processes in global predictions. , 2000, Trends in plant science.

[69]  Philip K. Groom,et al.  Impact of groundwater abstraction on a Banksia woodland, Swan Coastal Plain, Western Australia , 2000 .

[70]  P. Hanson,et al.  Effects of altered water regimes on forest root systems , 2000 .

[71]  P. Shafroth,et al.  Responses of Riparian Cottonwoods to Alluvial Water Table Declines , 1999, Environmental management.

[72]  H. Jones.  Stomatal control of photosynthesis and transpiration , 1998 .

[73]  P. Reich,et al.  From tropics to tundra: global convergence in plant functioning. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[74]  T. Kolb,et al.  Boxelder water sources and physiology at perennial and ephemeral stream sites in Arizona. , 1997, Tree physiology.

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

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

[77]  J. Stromberg,et al.  Effects of Groundwater Decline on Riparian Vegetation of Semiarid Regions: The San Pedro, Arizona , 1996 .

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

[79]  J. Ehleringer,et al.  Gender‐Specific Physiology, Carbon Isotope Discrimination, and Habitat Distribution in Boxelder, Acer Negundo , 1993 .

[80]  D. E. Busch,et al.  Water Uptake in Woody Riparian Phreatophytes of the Southwestern United States: A Stable Isotope Study. , 1992, Ecological applications : a publication of the Ecological Society of America.

[81]  B. Lamont,et al.  Seed Bank and Population Dynamics of Banksia cuneata: The Role of Time, Fire, and Moisture , 1991, Botanical Gazette.

[82]  S. Rood,et al.  Collapse of riparian poplar forests downstream from dams in western prairies: Probable causes and prospects for mitigation , 1990 .

[83]  S. Archer,et al.  Have Southern Texas Savannas Been Converted to Woodlands in Recent History? , 1989, The American Naturalist.

[84]  J. Araus,et al.  Field high-throughput phenotyping: the new crop breeding frontier. , 2014, Trends in plant science.

[85]  F. Thomas.  Ecology of Phreatophytes , 2014 .

[86]  R. Froend,et al.  Water stress vulnerability of four Banksia species in contrasting ecohydrological habitats on the Gnangara Mound, Western Australia. , 2009, Plant, cell & environment.

[87]  D. E. Busch,et al.  Water relations of riparian plants from warm desert regions , 2009, Wetlands.

[88]  J. Gornall,et al.  Geographic variation in ecophysiological traits of black cottonwood (Populus trichocarpa)1 , 2008 .

[89]  David P. Braun,et al.  Effects of Groundwater Decline on Riparian Vegetation of Semiarid Regions : The San Pedro , Arizona , 2007 .

[90]  Acer Negundo.  Gender-Specific Physiology , Carbon Isotope Discrimination , and Habitat Distribution in Boxelder , , 2007 .

[91]  J. R. Brown,et al.  Woody plant seed dispersal and gap formation in a North American subtropical savanna woodland: the role of domestic herbivores , 2004, Vegetatio.

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

[93]  Mitchel P. McClaran,et al.  A century of vegetation change on the Santa Rita Experimental Range , 2003 .

[94]  James R. Ehleringer,et al.  Streamside trees that do not use stream water , 1991, Nature.

[95]  O. E. Meinzer.  Outline of ground-water hydrology, with definitions , 1923 .