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Coordination of leaf and stem water transport properties in tropical forest trees

  • Physiological Ecology - Original Paper
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Abstract

Stomatal regulation of transpiration constrains leaf water potential (ΨL) within species-specific ranges that presumably avoid excessive tension and embolism in the stem xylem upstream. However, the hydraulic resistance of leaves can be highly variable over short time scales, uncoupling tension in the xylem of leaves from that in the stems to which they are attached. We evaluated a suite of leaf and stem functional traits governing water relations in individuals of 11 lowland tropical forest tree species to determine the manner in which the traits were coordinated with stem xylem vulnerability to embolism. Stomatal regulation of ΨL was associated with minimum values of water potential in branches (Ψbr) whose functional significance was similar across species. Minimum values of Ψbr coincided with the bulk sapwood tissue osmotic potential at zero turgor derived from pressure–volume curves and with the transition from a linear to exponential increase in xylem embolism with increasing sapwood water deficits. Branch xylem pressure corresponding to 50% loss of hydraulic conductivity (P 50) declined linearly with daily minimum Ψbr in a manner that caused the difference between Ψbr and P 50 to increase from 0.4 MPa in the species with the least negative Ψbr to 1.2 MPa in the species with the most negative Ψbr. Both branch P 50 and minimum Ψbr increased linearly with sapwood capacitance (C) such that the difference between Ψbr and P 50, an estimate of the safety margin for avoiding runaway embolism, decreased with increasing sapwood C. The results implied a trade-off between maximizing water transport and minimizing the risk of xylem embolism, suggesting a prominent role for the buffering effect of C in preserving the integrity of xylem water transport. At the whole-tree level, discharge and recharge of internal C appeared to generate variations in apparent leaf-specific conductance to which stomata respond dynamically.

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References

  • 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 

  • Begg JE, Turner NC (1970) Water potential gradients in field tobacco. Plant Physiol 46:343–346

    PubMed  Google Scholar 

  • Bowman WD, Roberts SW (1985) Seasonal changes in tissue elasticity in chaparral shrubs. Physiol Plant 65:233–236

    Article  Google Scholar 

  • Brodribb TJ, Holbrook NM (2003) Stomatal closure during leaf dehydration, correlation with other leaf physiological traits. Plant Physiol 132:2166–2173

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Brodribb TJ, Holbrook NM, Gutiérrez MV (2002) Hydraulic and photosynthetic co-ordination in seasonally dry tropical forest trees. Plant Cell Environ 25:1435–1444

    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 LDSL (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, Scholz FG, Goldstein G, Meinzer FC, Hinojosa JA, Hoffmann WA, Franco AC (2004a) Processes preventing nocturnal equilibration between leaf and soil water potential in tropical savanna woody species. Tree Physiol 24:1119–1127

    PubMed  Google Scholar 

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

    PubMed  CAS  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 

  • Buckley TN (2005) The control of stomata by water balance. New Phytol 168:275–291

    Article  PubMed  CAS  Google Scholar 

  • Chapotin SM, Razanameharizaka JH, Nolbrook NM (2006) A biomechanical perspective on the role of large stem volume and high water content in baobab trees (Adansonia spp.; Bombacaceae). Am J Bot 93:1251–1264

    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 

  • Dye PJ, Olbrich BW (1993) Estimating transpiration from 6-year-old Eucalyptus grandis trees: development of a canopy conductance model and comparison with independent sap flux measurements. Plant Cell Environ 16:45–53

    Article  Google Scholar 

  • Evans RD, Black RA, Link SO (1990) Rehydration-induced changes in pressure–volume relationships of Artemisia tridentata Nutt. ssp. tridentata. Plant Cell Environ 13:455–461

    Article  Google Scholar 

  • Fisher RA, Williams M, Lobo do Vale R, Lola Da Costa A, Meir P (2006) Evidence from Amazonian forests is consistent with isohydric control of leaf water potential. Plant Cell Environ 29:151–165

    Article  PubMed  Google Scholar 

  • Franks PJ (2004) Stomatal control and hydraulic conductance, with special reference to tall trees. Tree Physiol 24:865–878

    PubMed  Google Scholar 

  • Franks PJ, Drake PL, Froend RH (2007) Anisohydric but isohydrodynamic: seasonally constant plant water potential gradient explained by a stomatal control mechanism incorporating variable plant hydraulic conductance. Plant Cell Environ 30:19–30

    Article  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, 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 

  • Holbrook NM, Sinclair TR (1992) Water balance in the arborescent palm, Sabal palmetto. II. Transpiration and water storage. Plant Cell Environ 15:401–409

    Article  Google Scholar 

  • James SA, Clearwater MJ, Meinzer FC, Goldstein G (2002) Variable length heat dissipation sensors for the measurement of sap flow in trees with deep sapwood. Tree Physiol 22:277–283

    PubMed  Google Scholar 

  • Kobayashi Y, Tanaka T (2001) Water flow, hydraulic characteristics of Japanese red pine and oak trees. Hydrol Proc 15:1731–1750

    Article  Google Scholar 

  • Loustau D, Berbigier P, Roumagnae P, Arruda-Pacheco C, David JS, Ferreira MI, Pereira JS, Tavares R (1996) Transpiration of a 64-year-old maritime pine stand in Portugal. 1. Seasonal course of water flux through maritime pine. Oecologia 107:33–42

    Article  Google Scholar 

  • McDowell NG, Licata J, Bond BJ (2005) Environmental senstivity of gas exchange in different-sized trees. Oecologia 145:9–20

    Article  PubMed  Google Scholar 

  • Meinzer FC (2002) Co-ordination of liquid and vapor phase water transport properties in plants. Plant Cell Environ 25:265–274

    Article  PubMed  Google Scholar 

  • Meinzer FC (2003) Functional convergence in plant responses to the environment. Oecologia 134:1–11

    Article  PubMed  Google Scholar 

  • Meinzer FC, Rundel PW, Sharifi MR, Nilsen ET (1986) Turgor and osmotic relations of the desert shrub Larrea tridentata. Plant Cell Environ 9:467–475

    Article  Google Scholar 

  • Meinzer FC, Goldstein G, Jackson PJ, Holbrook NM, Gutierrez MV (1995) Environmental and physiological regulation of transpiration in tropical forest gap species: the influence of boundary layer and hydraulic properties. Oecologia 101:514–522

    Article  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, James SA, Goldstein G, Woodruff D (2003) Whole-tree water transport scales with sapwood capacitance in tropical forest canopy trees. Plant Cell Environ 26:1147–1155

    Article  Google Scholar 

  • Meinzer FC, James SA, Goldstein G (2004) Dynamics of transpiration, sap flow and use of stored water in tropical forest canopy trees. Tree Physiol 24:901–909

    PubMed  Google Scholar 

  • Meinzer FC, Brooks JR, Domec JC, Gartner BL, Warren JM, Woodruff DR, Bible K (2006) Dynamics of water transport and storage in conifers studied with deuterium and heat tracing techniques. Plant Cell Environ 29:105–114

    Article  PubMed  CAS  Google Scholar 

  • Mencuccini M (2003) The ecological significance of long-distance water transport: short-term regulation, long-term acclimation and the hydraulic costs of stature across plant life forms. Plant Cell Environ 26:163–182

    Article  Google Scholar 

  • Panshin AJ, de Zeeuw C (1980) Textbook of wood technology. McGraw-Hill, New York

    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

    Google Scholar 

  • Phillips NG, Ryan MG, Bond BJ, McDowell NG, Hinckley TM, Cermák J (2003) Reliance of stored water increases with tree size in three species in the Pacific Northwest. Tree Physiol 23:237–245

    PubMed  CAS  Google Scholar 

  • Phillips NG, Oren R, Licata J, Linder S (2004) Time series diagnosis of tree hydraulic characteristics. Tree Physiol 24:879–890

    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  PubMed  CAS  Google Scholar 

  • Reich PB, Walters MB, Ellsworth DS (1997) From tropics to tundra: global convergence in plant functioning. Proc Natl Acad Sci USA 94:13730–13734

    Article  PubMed  CAS  Google Scholar 

  • Roberts JM, Cabral OMR, Ferreira de Aguiar L (1990) Stomatal and boundary layer conductances in an Amazonian terra firme rain forest. J Appl Ecol 27:336–353

    Article  Google Scholar 

  • Sack L, Holbrook NM (2006) Leaf hydraulics. Annu Rev Plant Biol 57:361–381

    Article  PubMed  CAS  Google Scholar 

  • Santiago LS, Goldstein G, Meinzer FC, Fisher JB, Machado K, Woodruff D, Jones T (2004) Leaf photosynthetic traits scale with hydraulic conductivity and wood density in Panamanian forest canopy trees. Oecologia 140:543–550

    Article  PubMed  CAS  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 

  • 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 

  • Stratton L, Goldstein G, Meinzer FC (2000) Stem water storage capacity and efficiency of water transport: their functional significance in a Hawaiian dry forest. Plant Cell Environ 23:99–106

    Article  Google Scholar 

  • Tardieu F, Simonneau T (1998) Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modelling isohydric and anisohydric behaviours. J Exp Bot 49:419–432

    Article  Google Scholar 

  • Turner NC, Schulze E-D, Gollan T (1984) The response of stomata and leaf gas exchange to vapour pressure deficits and soil water content I. Species comparisons at high soil water contents. Oecologia 63:338–342

    Article  Google Scholar 

  • Tyree MT, Hammel HT (1972) The measurement of the turgor pressure and water relations of plants by the pressure bomb technique. J Exp Bot 23:267–282

    Article  Google Scholar 

  • Tyree MT, Sperry JS (1988) Do woody plants operate near the point of catastrophic xylem dysfunction caused by dynamic water stress? Plant Physiol 88:574–580

    Article  PubMed  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 

  • Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gullas J, Hikosaka K, Lamont BB, Lee T, Lusk C, Midgley J, Navas M-L, Niinemets U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This research was supported by National Science Foundation grant IBN 99-05012 to F. Meinzer and G. Goldstein. The authors thank the Smithsonian Tropical Research Institute for providing facilities and logistical support, and the expertise of the canopy crane operators. The authors are grateful to Kate McCulloh for providing data on xylem vessel diameter and frequency. This research complied with the laws of the Republic of Panama.

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Authors and Affiliations

  1. USDA Forest Service, Forestry Sciences Laboratory, 3200 SW Jefferson Way, Corvallis, OR, 97331, USA

    Frederick C. Meinzer & David R. Woodruff

  2. Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC, 27695, USA

    Jean-Christophe Domec

  3. Department of Biology, University of Miami, PO Box 249118, Coral Gables, FL, 33124, USA

    Guillermo Goldstein & Randol Villalobos-Vega

  4. Laboratorio de Ecología Funcional, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pab. II, 4 piso, Buenos Aires, C1428EHA, Argentina

    Paula I. Campanello & M. Genoveva Gatti

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  1. Frederick C. Meinzer
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  2. David R. Woodruff
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  3. Jean-Christophe Domec
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  4. Guillermo Goldstein
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  5. Paula I. Campanello
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  6. M. Genoveva Gatti
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  7. Randol Villalobos-Vega
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Correspondence to Frederick C. Meinzer.

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Communicated by Manuel Lerdau.

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Meinzer, F.C., Woodruff, D.R., Domec, JC. et al. Coordination of leaf and stem water transport properties in tropical forest trees. Oecologia 156, 31–41 (2008). https://doi.org/10.1007/s00442-008-0974-5

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  • DOI: https://doi.org/10.1007/s00442-008-0974-5

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