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The blind men and the elephant: the impact of context and scale in evaluating conflicts between plant hydraulic safety and efficiency

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Abstract

Given the fundamental importance of xylem safety and efficiency for plant survival and fitness, it is not surprising that these are among the most commonly studied features of hydraulic architecture. However, much remains to be learned about the nature and universality of conflicts between hydraulic safety and efficiency. Although selection for suites of hydraulic traits that confer adequate plant fitness under given conditions is likely to occur at the organismal level, most studies of hydraulic architecture have been confined to scales smaller than the whole plant, such as small-diameter branches and roots. Here we discuss the impact of the spatial and temporal contexts in which hydraulic traits are studied on the interpretation of their role in maintaining plant hydraulic function. We argue that further advances in understanding the ecological implications of different suites of plant hydraulic traits will be enhanced by adopting an integrated approach that considers variation in hydraulic traits throughout the entire plant, dynamic behavior of water transport, xylem tension and water transport efficiency in intact plants, alternate mechanisms that modulate hydraulic safety and efficiency, and alternate measures of hydraulic safety and safety margins.

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References

  • Ackerly D (2004) Functional strategies of chaparral shrubs in relation to seasonal water deficit and disturbance. Ecol Monogr 74:25–44

    Article  Google Scholar 

  • Addington RN, Donovan LA, Mitchell RJ, Vose JM, Pecot SD, Jack SB, Hacke UG, Sperry JS, Oren R (2006) Adjustments in hydraulic architecture of Pinus palustris maintain similar stomatal conductance in xeric and mesic habitats. Plant Cell Environ 29:535–545

    Article  CAS  PubMed  Google Scholar 

  • Ambrose AR, Sillett SC, Dawson TE (2009) Effects of tree height on branch hydraulics, leaf structure and gas exchange in California redwoods. Plant Cell Environ 32:743–757

    Article  PubMed  Google Scholar 

  • Andrade JL, Meinzer FC, Goldstein G, Holbrook NM, Cavelier J, Jackson P, Silvera K (1998) Regulation of water flux through trunks, branches and leaves in trees of a lowland tropical forest. Oecologia 115:463–471

    Article  Google Scholar 

  • Beikircher B, Mayr S (2008) The hydraulic architecture of Juniperus communis L. ssp. communis: shrubs and trees compared. Plant Cell Environ 31:1545–1556

    Article  PubMed  Google Scholar 

  • Brodribb TJ, Holbrook NM (2004a) Stomatal protection against hydraulic failure: a comparison of coexisting ferns and angiosperms. New Phytol 162:663–670

    Article  Google Scholar 

  • Brodribb TJ, Holbrook NM (2004b) Diurnal depression of leaf hydraulic conductance in a tropical tree species. Plant Cell Environ 27:820–827

    Article  Google Scholar 

  • Brodribb TJ, Holbrook NM, Edwards EJ, Gutiérrez MV (2003) Relations between stomatal closure, leaf turgor and xylem vulnerability in eight tropical dry forest trees. Plant Cell Environ 26:443–450

    Article  Google Scholar 

  • Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Sternberg LDL (2003) Dynamic changes in hydraulic conductivity in petioles of two savanna tree species: factors and mechanisms contributing to the refilling of embolized vessels. Plant Cell Environ 26:1633–1645

    Article  Google Scholar 

  • Bucci SJ, Goldstein G, Meinzer FC, Scholz FG, Franco AC, Bustamante M (2004) Functional convergence in hydraulic architecture and water relations of savanna trees: from leaf to whole plant. Tree Physiol 24:891–899

    CAS  PubMed  Google Scholar 

  • Bucci SJ, Goldstein G, Meinzer FC, Franco AC, Campanello P, Scholz FG (2005) Mechanisms contributing to seasonal homeostasis of minimum leaf water potential and predawn disequilibrium between soil and plant water potential in neotropical savanna trees. Trees 19:296–304

    Article  Google Scholar 

  • Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Franco AC, Campanello PI, Villalobos-Vega R, Bustamante M, Miralles-Wilhelm F (2006) Nutrient availability constrains the hydraulic architecture and water relations of savannah trees. Plant Cell Environ 29:2153–2167

    Article  CAS  PubMed  Google Scholar 

  • Burgess SSO, Pittermann J, Dawson TE (2006) Hydraulic efficiency and safety of branch xylem increases with height in Sequoia sempervirens (D. Don) crowns. Plant Cell Environ 29:229–239

    Article  PubMed  Google Scholar 

  • Cochard H, Lemoine D, Dreyer E (1999) The effects of acclimation to sunlight on the xylem vulnerability to embolism in Fagus sylvatica L. Plant Cell Environ 22:101–108

    Article  Google Scholar 

  • Cowan IR (1972) An electrical analogue of evaporation from, and flow of water in plants. Planta 106:221–226

    Article  Google Scholar 

  • Domec J-C, Gartner BL (2002a) Age- and position-related changes in hydraulic versus mechanical dysfunction of xylem: inferring the design criteria for Douglas-fir wood structure. Tree Physiol 22:91–104

    CAS  PubMed  Google Scholar 

  • Domec J-C, Gartner BL (2002b) How do water transport and storage differ in coniferous earlywood and latewood? J Exp Bot 53:2369–2379

    Article  CAS  PubMed  Google Scholar 

  • Domec J-C, Gartner BL (2003) Relationship between growth rates and xylem hydraulic characteristics in young, mature and old-growth ponderosa pine trees. Plant Cell Environ 26:471–483

    Article  Google Scholar 

  • Domec J-C, Warren JM, Meinzer FC, Brooks JR, Coulombe R (2004) Native root xylem embolism and stomatal closure in stands of Douglas-fir and ponderosa pine: mitigation by hydraulic redistribution. Oecologia 141:7–16

    Article  PubMed  Google Scholar 

  • Domec J-C, Pruyn ML, Gartner BL (2005) Axial and radial profiles in conductivities, water storage and native embolism in trunks of young and old-growth ponderosa pine trees. Plant Cell Environ 28:1103–1113

    Article  Google Scholar 

  • Domec J-C, Lachenbruch B, Meinzer FC (2006) Bordered pit structure and function determine spatial patterns of air-seeding thresholds in xylem of Douglas-fir (Pseudotsuga menziesii; Pinaceae) trees. Am J Bot 93:1588–1600

    Article  Google Scholar 

  • Domec J-C, Meinzer FC, Lachenbruch B, Housset J (2007) Dynamic variation in sapwood specific conductivity in six woody species. Tree Physiol 27:1389–1400

    PubMed  Google Scholar 

  • Domec J-C, Lachenbruch B, Meinzer FC, Woodruff DR, Warren JM, McCulloh KA (2008) Maximum height in a conifer is associated with conflicting requirements for xylem design. Proc Natl Acad Sci USA 105:12069–12074

    Article  CAS  PubMed  Google Scholar 

  • Dunham SM, Lachenbruch B, Ganio LM (2007) Bayesian analysis of Douglas-fir hydraulic architecture at multiple scales. Trees 21:65–78

    Article  Google Scholar 

  • Dunham SM, Ganio LM, Gitelman AI, Lachenbruch B (2008) Partitioning variation in Douglas-fir xylem properties among multiple scales via a Bayesian hierarchical model. Tree Physiol 28:1017–1024

    PubMed  Google Scholar 

  • Goldstein G, Andrade JL, Meinzer FC, Holbrook NM, Cavelier J, Jackson P, Celis A (1998) Stem water storage and diurnal patterns of water use in tropical forest canopy trees. Plant Cell Environ 21:397–406

    Article  Google Scholar 

  • Hacke UG, Jansen S (2009) Embolism resistance of three boreal conifer species varies with pit structure. New Phytol 182:675–686

    Article  PubMed  Google Scholar 

  • Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloh KA (2001) Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126:457–461

    Article  Google Scholar 

  • Hölttä T, Cochard H, Eero N, Mencuccini M (2009) Capacitive effect of cavitation in xylem conduits: results from a dynamic model. Plant Cell Environ 32:10–21

    Article  PubMed  Google Scholar 

  • Huber B (1928) Weitere quantitative Untersuchungen über das Wasserleitungssystem der Pflanzen. Jb Wiss Bot 67:877–959

    Google Scholar 

  • Huber B, Schmidt e (1936) Weitere thermo-elektrische Untersuchungen über den Transpirationsstrom der Bäume. Tharandt Forst Jb 87:369–412

    Google Scholar 

  • Jacobsen AL, Pratt RB, Davis SD, Ewers FW (2007) Cavitation resistance and seasonal hydraulics differ among three arid Californian plant communities. Plant Cell Environ 30:1599–1609

    Article  PubMed  Google Scholar 

  • Jacobsen AL, Pratt RB, Davis SD, Ewers FW (2008) Comparative community physiology: nonconvergence in water relations among three semi-arid shrub communities. New Phytol 180:100–113

    Article  PubMed  Google Scholar 

  • Johnson DM, Meinzer FC, Woodruff DR, McCulloh KA (2009a) Leaf xylem embolism, detected acoustically and by cryo-SEM, corresponds to decreases in leaf hydraulic conductance in four evergreen species. Plant Cell Environ 32:828–836

    Article  PubMed  Google Scholar 

  • Johnson DM, Woodruff DR, McCulloh KA, Meinzer FC (2009b) Leaf hydraulic conductance, measured in situ, declines and recovers daily: leaf hydraulics, water potential and stomatal conductance in four temperate and three tropical tree species. Tree Physiol 29:879–887

    Article  CAS  PubMed  Google Scholar 

  • Kavanagh KL, Bond BJ, Aitken SN, Gartner BL, Knowe S (1999) Shoot and root vulnerability to xylem cavitation in four populations of Douglas-fir seedlings. Tree Physiol 19:31–37

    PubMed  Google Scholar 

  • Koch GW, Sillett SC, Jennings GM, Davis SD (2004) The limits to tree height. Nature 428:851–854

    Article  CAS  PubMed  Google Scholar 

  • Maherali H, DeLucia EH (2001) Influence of climate-driven shifts in biomass allocation on water transport and storage in ponderosa pine. Oecologia 129:481–491

    Google Scholar 

  • Maherali H, Pockman WT, Jackson RB (2004) Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology 85:2184–2199

    Article  Google Scholar 

  • Maherali H, Moura CF, Caldeira MC, Willson CJ, Jackson RB (2006) Functional coordination between leaf gas exchange and vulnerability to xylem cavitation in temperate forest trees. Plant Cell Environ 29:571–583

    Article  PubMed  Google Scholar 

  • Martinez-Vilalta J, Prat E, Oliveras I, Piñol J (2002) Xylem hydraulic properties of roots and stems of nine Mediterranean woody species. Oecologia 133:19–29

    Article  Google Scholar 

  • McCulloh KA, Sperry JS (2005) Patterns in hydraulic architecture and their implications for transport efficiency. Tree Physiol 25:257–267

    PubMed  Google Scholar 

  • McCulloh KA, Sperry JS, Adler FR (2003) Water transport in plants obeys Murray’s law. Nature 421:939–942

    Article  CAS  PubMed  Google Scholar 

  • McCulloh KA, Sperry JS, Adler FR (2004) Murray’s law and the hydraulic vs mechanical functioning of wood. Funct Ecol 18:931–938

    Article  Google Scholar 

  • McCulloh KA, Sperry JS, Lachenbruch B, Meinzer FC, Reich PB, Voelker S (2010) Moving water well: comparing hydraulic efficiency in twigs and trunks of coniferous, ring-porous and diffuse-porous saplings from temperate and tropical forests. New Phytol 186:439–450

    Article  PubMed  Google Scholar 

  • McDowell N, Barnard H, Bond BJ, Hinckley T, Hubbard RM, Ishii H, Köstner B, Magnani F, Marshall JD, Meinzer FC, Phillips N, Ryan MG, Whitehead D (2002) The relationship between tree height and leaf area: sapwood area ratio. Oecologia 132:12–20

    Article  Google Scholar 

  • McElrone AJ, Bichler J, Pockman WT, Addington RN, Linder CR, Jackson RB (2007) Aquaporin-mediated changes in hydraulic conductivity of deep tree roots accessed via caves. Plant Cell Environ 30:1411–1421

    Article  CAS  PubMed  Google Scholar 

  • Meinzer FC, Goldstein G, Franco AC, Bustamante M, Igler E, Jackson P, Caldas L, Rundel PW (1999) Atmospheric and hydraulic limitations on transpiration in Brazilian cerrado woody species. Funct Ecol 13:273–282

    Article  Google Scholar 

  • Meinzer FC, Campanello PI, Domec J-C, Gatti MG, Goldstein G, Villalobos-Vega R, Woodruff DR (2008a) Constraints on physiological function associated with branch architecture and wood density in tropical forest trees. Tree Physiol 28:1609–1617

    PubMed  Google Scholar 

  • Meinzer FC, Woodruff DR, Domec J-C, Goldstein G, Campanello PI, Gatti MG, Villalobos-Vega R (2008b) Coordination of leaf and stem water transport properties in tropical forest trees. Oecologia 156:31–41

    Article  PubMed  Google Scholar 

  • Meinzer FC, Johnson DM, Lachenbruch B, McCulloh KA, Woodruff DR (2009) Xylem hydraulic safety margins in woody plants: coordination of stomatal control of xylem tension with hydraulic capacitance. Funct Ecol 23:922–930

    Article  Google Scholar 

  • Mencuccini M, Grace J, Fioravanti M (1997) Biomechanical and hydraulic determinants of tree structure in Scots pine: anatomical characteristics. Tree Physiol 17:105–113

    PubMed  Google Scholar 

  • Nardini A, Salleo S (2000) Limitation of stomatal conductance by hydraulic traits: sensing or preventing xylem cavitation? Trees 15:239–245

    Article  Google Scholar 

  • Oliveras I, Martinez-Vilalta J, Jimenez-Ortiz T, Lledo MJ, Escarre A, Piñol J (2003) Hydraulic properties of Pinus halepensis, Pinus pinea and Tetraclinis articulata in a dune ecosystem of Eastern Spain. Plant Ecol 169:131–141

    Article  Google Scholar 

  • Pataki DE, Oren R, Phillips N (1998) Responses of sap flux and stomatal conductance of Pinus taeda L. trees to stepwise reductions in leaf area. J Exp Bot 49:871–878

    Article  CAS  Google Scholar 

  • Perämäki M, Vesala T, Nikinmaa E (2005) Modeling the dynamics of pressure propagation and diameter variation in tree sapwood. Tree Physiol 25:1091–1099

    PubMed  Google Scholar 

  • Phillips N, Nagchaudhuri A, Oren R, Katul G (1997) Time constant for water transport in loblolly pine trees estimated from time series of evaporative demand and stem sap flow. Trees 11:412–419

    Article  Google Scholar 

  • Piñol J, Sala A (2000) Ecological implications of xylem cavitation for several Pinaceae in the Pacific Northern USA. Funct Ecol 14:538–545

    Article  Google Scholar 

  • Pittermann J, Sperry JS, Hacke UG, Wheeler JK, Sikkema EH (2005) Torus-margo pits help conifers compete with angiosperms. Science 310:1924–1925

    Article  CAS  PubMed  Google Scholar 

  • Pittermann J, Sperry JS, Hacke UG, Wheeler JK, Sikkema EH (2006) Inter-tracheid pitting and the hydraulic efficiency of conifer wood: the role of tracheid allometry and cavitation protection. Am J Bot 93:1265–1273

    Article  Google Scholar 

  • Pockman WT, Sperry JS (2000) Vulnerability to xylem cavitation and the distribution of Sonoran desert vegetation. Am J Bot 87:1287–1299

    Article  PubMed  Google Scholar 

  • Pratt RB, Jacobsen AL, Ewers FW, Davis SD (2007) Relationships among xylem transport, biomechanics and storage in stems and roots of nine Rhamnaceae species of the California chaparral. New Phytol 174:787–798

    Article  CAS  PubMed  Google Scholar 

  • Rosner S, Klein A, Wimmer R, Karlsson B (2006) Extraction of features from ultrasound acoustic emissions: a tool to assess the hydraulic vulnerability of Norway spruce trunkwood? New Phytol 171:105–116

    Article  PubMed  Google Scholar 

  • Rosner S, Klein A, Müller U, Karlsson B (2007) Hydraulic and mechanical properties of young Norway spruce clones related to growth and wood structure. Tree Physiol 27:1165–1178

    PubMed  Google Scholar 

  • Ryan MG, Phillips N, Bond BJ (2006) The hydraulic limitation hypothesis revisited. Plant Cell Environ 29:367–381

    Article  PubMed  Google Scholar 

  • Sack L, Cowan PD, Jaikumar N, Holbrook NM (2003) The ‘hydrology’of leaves: co-ordination of structure and function in temperate woody species. Plant Cell Environ 26:1343–1356

    Article  Google Scholar 

  • Scholz FG, Bucci SJ, Goldstein G, Meinzer FC, Franco AC, Miralles-Wilhelm F (2007) Biophysical properties and functional significance of stem water storage tissues in neotropical savanna trees. Plant Cell Environ 30:236–248

    Article  PubMed  Google Scholar 

  • Scholz FG, Bucci SJ, Goldstein G, Meinzer FC, Franco AC, Miralles-Wilhelm F (2008) Temporal dynamics of stem expansion and contraction in savanna trees: withdrawal and recharge of stored water. Tree Physiol 28:469–480

    PubMed  Google Scholar 

  • Sparks JP, Black RA (1999) Regulation of water loss in populations of Populus trichocarpa: the role of stomatal control in preventing xylem cavitation. Tree Physiol 19:453–459

    PubMed  Google Scholar 

  • Sperry JS, Hacke UG (2004) Analysis of circular bordered pit function—I. Angiosperm vessels with homogenous pit membranes. Am J Bot 91:369–385

    Article  Google Scholar 

  • Sperry JS, Saliendra NZ (1994) Intra- and inter-plant variation in xylem cavitation in Betula occidentalis. Plant Cell Environ 17:1233–1241

    Article  Google Scholar 

  • Sperry JS, Alder NN, Eastlack SE (1993) The effect of reduced hydraulic conductance on stomatal conductance and xylem cavitation. J Exp Bot 44:1075–1082

    Article  Google Scholar 

  • Sperry JS, Adler FR, Campbell GS, Comstock JP (1998) Limitation of plant water use by rhizosphere and xylem conductance: results from a model. Plant Cell Environ 21:347–359

    Article  Google Scholar 

  • Sperry JS, Meinzer FC, McCulloh KA (2008) Safety and efficiency conflicts in hydraulic architecture: scaling from tissues to trees. Plant Cell Environ 31:632–645

    Article  PubMed  Google Scholar 

  • Spicer R, Gartner BL (2001) The effects of cambial age and position within the stem on specific conductivity in Douglas-fir (Pseudotsuga menziesii) sapwood. Trees 15:222–229

    Article  Google Scholar 

  • Taneda H, Sperry JS (2008) A case-study of water transport in co-occurring ring- versus diffuse-porous trees: contrasts in water-status, conducting capacity, cavitation and vessel refilling. Tree Physiol 28:1641–1651

    PubMed  Google Scholar 

  • Tyree MT, Snyderman DA, Wilmot TR, Machado J-L (1991) Water relations and hydraulic architecture of a tropical tree (Schefflera morototoni). Plant Physiol 96:1105–1113

    Article  CAS  PubMed  Google Scholar 

  • Tyree MT, Davis SD, Cochard H (1994) Biophysical perspectives of xylem evolution–is there a tradeoff of hydraulic efficiency for vulnerability to dysfunction? IAWA 15:335–360

    Google Scholar 

  • Vogt UK (2001) Hydraulic vulnerability, vessel refilling, and seasonal courses of stem water potential of Sorbus aucuparia L. and Sambucus nigra L. J Exp Bot 52:1527–1536

    Article  CAS  PubMed  Google Scholar 

  • West GB, Brown JH, Enquist BJ (1999) A general model for the structure and allometry of plant vascular systems. Nature 400:664–667

    Article  CAS  Google Scholar 

  • Wheeler JK, Sperry JS, Hacke UG, Hoang N (2005) Inter-vessel pitting and cavitation in woody Rosaceae and other vesselled plants: a basis for a safety versus efficiency trade-off in xylem transport. Plant Cell Environ 28:800–812

    Article  Google Scholar 

  • Whitehead D, Livingston NJ, Kelliher FM, Hogan KP, Pepin S, McSeveny TM, Byers JN (1996) Response of transpiration and photosynthesis to a transient change in illuminated foliage area for a Pinus radiata D. Don tree. Plant Cell Environ 19:949–957

    Article  Google Scholar 

  • Willson CJ, Manos PS, Jackson RB (2008) Hydraulic traits are influenced by phylogenetic history in the drought-resistant, invasive genus Juniperus (Cupressaceae). Am J Bot 95:299–314

    Article  CAS  Google Scholar 

  • Woodruff DR, Bond BJ, Meinzer FC (2004) Does turgor limit growth in tall trees? Plant Cell Environ 27:229–236

    Article  Google Scholar 

  • Woodruff DR, McCulloh KA, Warren JM, Meinzer FC, Lachenbruch B (2007) Impacts of tree height on leaf hydraulic architecture and stomatal control in Douglas-fir. Plant Cell Environ 30:559–569

    Article  PubMed  Google Scholar 

  • Woodruff DR, Meinzer FC, Lachenbruch B (2008) Height-related trends in leaf xylem anatomy and shoot hydraulic characteristics in a tall conifer: safety versus efficiency in water transport. New Phytol 180:90–99

    Article  CAS  PubMed  Google Scholar 

  • Wright IJ, Falster DS, Pickup M, Westoby M (2006) Cross-species patterns in the coordination between leaf and stem traits. Physiol Plant 127:445–456

    Article  CAS  Google Scholar 

  • Zimmermann MH (1978) Hydraulic architecture of some diffuse-porous trees. Can J Bot 56:2286–2295

    Article  Google Scholar 

  • Zotz G, Tyree MT, Patiño S, Carlton MR (1998) Hydraulic architecture and water use of selected species from a lower montane forest in Panama. Trees 12:302–309

    Article  Google Scholar 

  • Zwieniecki MA, Holbrook NM (1998) Diurnal variation in xylem hydraulic conductivity in white ash (Fraxinus americana L.), red maple (Acer rubrum L.) and red spruce (Picea rubens Sarg.). Plant Cell Environ 21:1173–1180

    Article  Google Scholar 

  • Zwieniecki MA, Hutyra L, Thompson MV, Holbrook NM (2000) Dynamic changes in petiole specific conductivity in red maple (Acer rubrum L.), tulip tree (Liriodendron tulipifera L.) and northern fox grape (Vitis labrusca L.). Plant Cell Environ 23:407–414

    Article  Google Scholar 

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Acknowledgments

This work was supported by National Science Foundation Grants 99-05012, 05-44470 and 09-19871.

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Correspondence to Frederick C. Meinzer.

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Communicated by Ram Oren.

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Meinzer, F.C., McCulloh, K.A., Lachenbruch, B. et al. The blind men and the elephant: the impact of context and scale in evaluating conflicts between plant hydraulic safety and efficiency. Oecologia 164, 287–296 (2010). https://doi.org/10.1007/s00442-010-1734-x

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