Hierarchical statistical modeling of xylem vulnerability to cavitation.

Cavitation of xylem elements diminishes the water transport capacity of plants, and quantifying xylem vulnerability to cavitation is important to understanding plant function. Current approaches to analyzing hydraulic conductivity (K) data to infer vulnerability to cavitation suffer from problems such as the use of potentially unrealistic vulnerability curves, difficulty interpreting parameters in these curves, a statistical framework that ignores sampling design, and an overly simplistic view of uncertainty. This study illustrates how two common curves (exponential-sigmoid and Weibull) can be reparameterized in terms of meaningful parameters: maximum conductivity (k(sat)), water potential (-P) at which percentage loss of conductivity (PLC) =X% (P(X)), and the slope of the PLC curve at P(X) (S(X)), a 'sensitivity' index. We provide a hierarchical Bayesian method for fitting the reparameterized curves to K(H) data. We illustrate the method using data for roots and stems of two populations of Juniperus scopulorum and test for differences in k(sat), P(X), and S(X) between different groups. Two important results emerge from this study. First, the Weibull model is preferred because it produces biologically realistic estimates of PLC near P = 0 MPa. Second, stochastic embolisms contribute an important source of uncertainty that should be included in such analyses.

[1]  P. Hietz,et al.  Vulnerability curves from conifer sapwood sections exposed over solutions with known water potentials. , 2003, Journal of experimental botany.

[2]  C. Osmond,et al.  Encyclopedia of plant physiology. New series. Volume 12B. Physiological plant ecology II. Water relations and carbon assimilation. , 2011 .

[3]  Hervé Cochard,et al.  Is xylem cavitation resistance a relevant criterion for screening drought resistance among Prunus species? , 2008, Journal of plant physiology.

[4]  J. Sperry,et al.  Xylem embolism in response to freeze-thaw cycles and water stress in ring-porous, diffuse-porous, and conifer species. , 1992, Plant physiology.

[5]  Barbara L. Gartner,et al.  Plant stems : physiology and functional morphology , 1995 .

[6]  James H. Torrie,et al.  Principles and procedures of statistics: a biometrical approach (2nd ed) , 1980 .

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

[8]  D. Bates,et al.  Mixed-Effects Models in S and S-PLUS , 2001 .

[9]  David B. Dunson,et al.  Bayesian Data Analysis , 2010 .

[10]  William T. Pockman,et al.  Limitation of transpiration by hydraulic conductance and xylem cavitation in Betula occidentalis , 1993 .

[11]  E. Russek-Cohen,et al.  Physiological response curve analysis using nonlinear mixed models , 2002, Oecologia.

[12]  E. DeLucia,et al.  Xylem conductivity and vulnerability to cavitation of ponderosa pine growing in contrasting climates. , 2000, Tree physiology.

[13]  Andrej Pázman,et al.  Nonlinear Regression , 2019, Handbook of Regression Analysis With Applications in R.

[14]  J. Piñol,et al.  Ecological implications of xylem cavitation for several Pinaceae in the Pacific Northern USA , 2000 .

[15]  N. Michele Holbrook,et al.  Stomatal Closure during Leaf Dehydration, Correlation with Other Leaf Physiological Traits1 , 2003, Plant Physiology.

[16]  F. Ewers,et al.  CAVITATION RESISTANCE AMONG 26 CHAPARRAL SPECIES OF SOUTHERN CALIFORNIA , 2007 .

[17]  J. Sperry,et al.  Do woody plants operate near the point of catastrophic xylem dysfunction caused by dynamic water stress? : answers from a model. , 1988, Plant physiology.

[18]  R. B. Jackson,et al.  Functional coordination between leaf gas exchange and vulnerability to xylem cavitation in temperate forest trees. , 2006, Plant, cell & environment.

[19]  Bradley P. Carlin,et al.  Bayesian measures of model complexity and fit , 2002 .

[20]  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.

[21]  I. Oliveras,et al.  Hydraulic properties of Pinus halepensis, Pinus pinea and Tetraclinis articulata in a dune ecosystem of Eastern Spain , 2003, Plant Ecology.

[22]  Michael H. Kutner Applied Linear Statistical Models , 1974 .

[23]  J. Sperry,et al.  Xylem cavitation in roots and stems of Douglas-fir and white fir. , 1997, Tree physiology.

[24]  R. P. Adams Juniperus maritima, the seaside juniper, a new species from Puget Sound, North America , 2007 .

[25]  James S. Clark,et al.  Why environmental scientists are becoming Bayesians , 2004 .

[26]  T. Brodribb,et al.  Stem hydraulic supply is linked to leaf photosynthetic capacity: evidence from New Caledonian and Tasmanian rainforests , 2000 .

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

[28]  Uwe G. Hacke,et al.  Xylem Hydraulics and the Soil-Plant-Atmosphere Continuum: Opportunities and Unresolved Issues , 2003 .

[29]  G. Goldstein,et al.  Genotypic variability in vulnerability of leaf xylem to cavitation in water-stressed and well-irrigated sugarcane. , 1992, Plant physiology.

[30]  Maurizio Mencuccini,et al.  Vulnerability to cavitation in populations of two desert species, Hymenoclea salsola and Ambrosia dumosa, from different climatic regions , 1997 .

[31]  Andrew Thomas,et al.  WinBUGS - A Bayesian modelling framework: Concepts, structure, and extensibility , 2000, Stat. Comput..

[32]  B. Choat,et al.  Pit Membrane Porosity and Water Stress-Induced Cavitation in Four Co-Existing Dry Rainforest Tree Species , 2003, Plant Physiology.

[33]  G. Seber,et al.  Nonlinear Regression: Seber/Nonlinear Regression , 2005 .

[34]  Kiona Ogle,et al.  Bayesian Data—Model Integration in Plant Physiological and Ecosystem Ecology , 2008 .

[35]  J. Piñol,et al.  Drought-induced mortality and hydraulic architecture in pine populations of the NE Iberian Peninsula , 2002 .

[36]  Catherine Potvin,et al.  THE STATISTICAL ANALYSIS OF ECOPHYSIOLOGICAL RESPONSE CURVES OBTAINED FROM EXPERIMENTS INVOLVING REPEATED MEASURES , 1990 .

[37]  J. O. Rawlings,et al.  The Weibull Function as a Dose‐Response Model to Describe Ozone Effects on Crop Yields 1 , 1985 .

[38]  C. Wikle Hierarchical Models in Environmental Science , 2003 .

[39]  Melvin T. Tyree,et al.  A method for measuring hydraulic conductivity and embolism in xylem , 1988 .

[40]  R. Hill,et al.  The importance of xylem constraints in the distribution of conifer species , 1999 .

[41]  John S. Sperry,et al.  DIFFERENCES IN DROUGHT ADAPTATION BETWEEN SUBSPECIES OF SAGEBRUSH (ARTEMISIA TRIDENTATA) , 1999 .

[42]  J. Sperry Hydraulic constraints on plant gas exchange , 2000 .

[43]  A. Gelman Prior distributions for variance parameters in hierarchical models (comment on article by Browne and Draper) , 2004 .

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

[45]  HighWire Press Philosophical Transactions of the Royal Society of London , 1781, The London Medical Journal.

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

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

[48]  Barbara L. Gartner,et al.  Cavitation and water storage capacity in bole xylem segments of mature and young Douglas-fir trees , 2001, Trees.

[49]  M. Zimmermann Xylem Structure and the Ascent of Sap , 1983, Springer Series in Wood Science.

[50]  J. Sperry,et al.  Cavitation fatigue and its reversal in sunflower (Helianthus annuus L.). , 2002, Journal of experimental botany.

[51]  S. Mayr,et al.  A new method for vulnerability analysis of small xylem areas reveals that compression wood of Norway spruce has lower hydraulic safety than opposite wood , 2003 .

[52]  J. Sperry,et al.  Evaluation of centrifugal methods for measuring xylem cavitation in conifers, diffuse- and ring-porous angiosperms. , 2007, The New phytologist.

[53]  B. Bond,et al.  Shoot and root vulnerability to xylem cavitation in four populations of Douglas-fir seedlings. , 1999, Tree physiology.

[54]  D. Eamus,et al.  Convergence in hydraulic architecture, water relations and primary productivity amongst habitats and across seasons in Sydney. , 2004, Functional plant biology : FPB.

[55]  I. Oliveras,et al.  Xylem hydraulic properties of roots and stems of nine Mediterranean woody species , 2002, Oecologia.

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

[57]  V. Barnett,et al.  Applied Linear Statistical Models , 1975 .

[58]  J. Sparks,et al.  Regulation of water loss in populations of Populus trichocarpa: the role of stomatal control in preventing xylem cavitation. , 1999, Tree physiology.

[59]  George Davey Smith,et al.  Meta-analysis: Principles and procedures , 1997, BMJ.

[60]  F. Ewers,et al.  The hydraulic architecture of trees and other woody plants , 1991 .

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

[62]  I. R. Cowan Regulation of Water Use in Relation to Carbon Gain in Higher Plants , 1982 .

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

[64]  Melvin T. Tyree,et al.  Water‐stress‐induced xylem embolism in three species of conifers , 1990 .

[65]  M. Lechowicz,et al.  The Relation of Foliar Phenology to Xylem Embolism in Trees , 1992 .

[66]  J. Sperry,et al.  Drought experience and cavitation resistance in six shrubs from the Great Basin, Utah , 2000 .

[67]  J. Sperry Limitations on Stem Water Transport and Their Consequences , 1995 .

[68]  J. Boyer Photosynthesis at low water potentials , 1976 .

[69]  Christian P. Robert,et al.  Monte Carlo Statistical Methods , 2005, Springer Texts in Statistics.

[70]  C. V. Willigen,et al.  A mathematical and statistical analysis of the curves illustrating vulnerability of xylem to cavitation. , 1998, Tree physiology.