Advertisement

The relation between pressure–volume curve traits and stomatal regulation of water potential in five temperate broadleaf tree species

  • Christoph LeuschnerEmail author
  • Paul Wedde
  • Torben Lübbe
Research Paper

Abstract

Key message

In the five temperate tree species, leaf turgor loss point and the stringency of stomatal regulation are not related to each other and to the drought sensitivity of radial growth, suggesting that additional factors exert a large influence on the species’ drought tolerance.

Context

How trees are responding to drought will largely determine their fitness and survival in a warmer and drier world. Much of our understanding of the drought response strategies of woody plants has been based on the study of either plant hydraulics or leaf water status dynamics or stomatal behavior, while the interaction of these components is less often studied.

Aims

To examine the relatedness of leaf tissue osmotic and elastic properties to the isohydry–anisohydry syndrome in adult trees of five co-occurring broadleaf tree species (Acer pseudoplatanus L., Carpinus betulus L., Fagus sylvatica L., Fraxinus excelsior L., and Tilia cordata Mill.), which differ in the stringency of stomatal regulation.

Methods

Adult trees of the five species were accessed with a mobile canopy lift and pressure–volume (p-v) curves of sun leaf tissue analyzed for species differences and seasonal change in p-v curve parameters. The extent of seasonal fluctuation in daily leaf water potential (Ψl) minima served to position the species along the isohydry-anisohydry continuum.

Results

The five species differed greatly in the bulk modulus of elasticity (ε) (12 MPa to 33 MPa) and, to a lesser extent, in leaf water potential at turgor loss (πtlp) (− 2.3 MPa to − 2.9 MPa), exhibiting species-specific combinations of p-v parameters with the extent of Ψl fluctuation. However, πtlp and ε were only weakly, or not at all, related to the species’ position along the isohydry–anisohydry continuum. Anisohydric Fagus sylvatica with high ε and relatively low πtlp had a more drought-sensitive radial growth than the fairly isohydric Tilia cordata with low ε and relatively high πtlp.

Conclusion

The five coexisting tree species exhibit largely different drought response strategies, which are partly determined by species differences in leaf tissue elasticity and the stringency of stomatal regulation.

Keywords

Anisohydry Acer pseudoplatanus Carpinus betulus Fagus sylvatica Fraxinus excelsior Isohydry p-v curve analysis Tilia cordata 

Notes

Acknowledgments

The authors thank the Hainich National Park administration for the fruitful cooperation and the granting of research permits.

Author contribution

C.L. had the idea and developed together with P.W. the study design, P.W. conducted the measurements and the main data analysis, T.L. and C.L. conducted the additional statistical tests, and C.L. wrote the paper. All authors approved the final version of the manuscript.

Funding

This study received financial support from DFG (Deutsche Forschungsgemeinschaft) in the context of Graduiertenkolleg 1086 through a grant to C.L; this support is gratefully acknowledged.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interests.

References

  1. Aasamaa K, Söber A, Hartung W, Niinemets Ü (2004) Drought acclimation of two deciduous tree species of different layers in a temperate forest canopy. Trees 18:93–101CrossRefGoogle Scholar
  2. Abrams MD (1988) Genetic variation in leaf morphology and plant and tissue water relations during drought in Cercis canadensis L. For Sci 34:200–207Google Scholar
  3. Abrams MD (1991) Adaptations and responses to drought in Quercus species of North America. Tree Physiol 7:227–238CrossRefGoogle Scholar
  4. Abrams MD, Kubiske ME (1990) Photosynthesis and water relations during drought in Acer rubrum L. genotypes from contrasting sites in Central Pennsylvania. Funct Ecol 4:727–733CrossRefGoogle Scholar
  5. Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH(T), Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim JH, Allard G, Running SW, Semerci A, Cobb N (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684CrossRefGoogle Scholar
  6. Backes K, Leuschner C (2000) Leaf water relations of competitive F. sylvatica sylvatica L. and Quercus petraea (Matt.) Liebl. trees during four years differing in soil drought. Can J For Res 30:335–346CrossRefGoogle Scholar
  7. Baltzer JL, Davies SJ, Bunyavejchewin S, Noor SSM (2008) The role of desiccation tolerance in determining tree species distributions along the Malay-Thai Peninsula. Funct Ecol 22:221–231CrossRefGoogle Scholar
  8. Bartlett MK, Scoffoni C, Sack L (2012) The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta-analysis. Ecol Lett 15:393–405PubMedCrossRefPubMedCentralGoogle Scholar
  9. Blackman CJ, Brodribb TJ, Jordan GJ (2010) Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms. New Phytol 188:1113–1123PubMedCrossRefPubMedCentralGoogle Scholar
  10. Blum A (2016) Stress, strain, signaling, and adaptation—not just a matter of definition. J Exp Bot 67:563–566CrossRefGoogle Scholar
  11. Bréda N, Huc R, Granier A, Dreyer E (2006) Temperate forest trees and stands under severe drought: a review of ecophysiological responses, adaptation processes and long-term consequences. Ann For Sci 63:625–644CrossRefGoogle Scholar
  12. Brodribb TJ, McAdam SAM, Jordan GJ, Martins SCV (2014) Conifer species adapt to low-rainfall climates by following one of two divergent pathways. Proc Natl Acad Sci U S A 111:14489–14493PubMedPubMedCentralCrossRefGoogle Scholar
  13. Carlier G, Peltier JP, Gielly L (1992) Comportement hydrique du frêne (F. excelsior excelsior L.) dans une formation montagnarde mésoxérophile. Ann Sci For 49:207–223CrossRefGoogle Scholar
  14. Cavender-Bares J, Bazzaz FA (2000) Changes in drought response strategies with ontogeny in Quercus rubra: implications for scaling from seedlings to mature trees. Oecologia 124:8–18PubMedCrossRefGoogle Scholar
  15. Cheung YNS, Tyree MT, Dainty J (1975) Water relations parameters on single leaves obtained in a pressure bomb and some ecological interpretations. Can J Bot 53:1342–1346CrossRefGoogle Scholar
  16. Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Hacke UG, Jacobsen AL, Lens F, Maherali H, Martínez-Vilalta J, Mayr S, Mencuccini M, Mitchell PJ, Nardini A, Pittermann J, Pratt RB, Sperry JS, Westoby M, Wright IJ, Zanne AE (2012) Global convergence in the vulnerability of forests to drought. Nature 491:752–755PubMedCrossRefPubMedCentralGoogle Scholar
  17. Clifford SC, Arndt SK, Corlett JE, Joshi S, Sankhla M, Jones HG (1998) The role of solute accumulation, osmotic adjustment and changes in cell wall elasticity in drought tolerance of Ziziphus mauritiana (Lamk). J Exp Bot 49:967–977CrossRefGoogle Scholar
  18. Corcuera L, Camarero JJ, Gil-Pelegrin E (2002) Functional groups in Quercus species derived from the analysis of pressure-volume curves. Trees 16:465–472CrossRefGoogle Scholar
  19. Dreyer E, Bousquet F, Ducrey M (1990) Use of pressure volume curves in water relation analysis on woody shoots: influence of rehydration and comparison of four European oak species. Ann Sci For 47:285–297CrossRefGoogle Scholar
  20. Ellenberg H (1996) Vegetation Mitteleuropas mit den Alpen, 5th edn. Ulmer, StuttgartGoogle Scholar
  21. Fan S, Blake TJ, Blumwald E (1994) The relative contribution of elastic and osmotic adjustments to turgor maintenance of woody species. Physiol Plant 90:408–413CrossRefGoogle Scholar
  22. Gebauer T, Horna V, Leuschner C (2008) Variability in radial sap flux density patterns and sapwood area among seven co-occurring temperate broad-leaved tree species. Tree Physiol 28:1821–1830PubMedCrossRefGoogle Scholar
  23. Gebauer T, Horna V, Leuschner C (2012) Canopy transpiration of pure and mixed forest stands with variable abundance of European beech. J Hydrol 442-443:2–14CrossRefGoogle Scholar
  24. Gessler A, Keitel C, Kreuzwieser J, Matyssek R, Seiler W, Rennenberg H (2007) Potential risk for European beech (F. sylvatica sylvatica L.) in a changing climate. Trees 21:1–11CrossRefGoogle Scholar
  25. Guckland A, Jacob M, Flessa H, Thomas FM, Leuschner C (2009) Acidity, nutrient stocks and organic-matter content in soils of temperate deciduous forest with different abundance of European beech (F. sylvatica sylvatica L.). J Plant Nutr Soil Sci 172:500–511CrossRefGoogle Scholar
  26. Guicherd P, Peltier JP, Gout E, Bligny R, Marigo G (1997) Osmotic adjustment in F. excelsior excelsior L.: malate and mannitol accumulation in leaves under drought conditions. Trees 11:155–161Google Scholar
  27. Hiekel W, Fritzlar F, Nöllert A, Westhus W (2004) Die Naturräume Thüringens. Naturschutzreport (Jena) 21:6–381Google Scholar
  28. Hinckley TM, Teskey RO, Duhme F, Richter H (1981) Temperate hardwood forests. In: Kozlowski TT (ed) Water deficits and plant growth, Woody plant communities, vol VI. Academic, New York, pp 153–208Google Scholar
  29. Hsiao TC (1973) Plant responses to water stress. Ann Rev Plant Physiol Mol Biol 24:519–570CrossRefGoogle Scholar
  30. IPCC (2013) Climate change 2013: the physical science basis. In: Stocker TF et al (eds) Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, UK and New York, 1535 ppGoogle Scholar
  31. Jacob A, Hertel D, Leuschner C (2014) Diversity and species identity effects on fine root productivity and turnover in a species-rich temperate broad-leaved forest. Funct Plant Biol 41:678–789CrossRefGoogle Scholar
  32. Joly RJ, Zaerr JB (1987) Alteration of cell-wall water content and elasticity in Douglas-fir during periods of water deficit. Plant Physiol 83:418–422PubMedPubMedCentralCrossRefGoogle Scholar
  33. Khalil AAM, Grace J (1992) Acclimation to drought in A. pseudoplatanus pseudoplatanus L. (Sycamore) seedlings. J Exp Bot 43:1591–1602CrossRefGoogle Scholar
  34. Klein T (2014) The variability of stomatal sensitivity to leaf water potential across tree species indicates a continuum between isohydric and anisohydric behaviours. Funct Ecol 28:1313–1320CrossRefGoogle Scholar
  35. Knutzen F, Meier IC, Leuschner C (2015) Does reduced precipitation trigger physiological and morphological drought adaptations in European beech (F. sylvatica sylvatica L.)? Comparing provenances across a precipitation gradient. Tree Physiol 35:949–963PubMedCrossRefPubMedCentralGoogle Scholar
  36. Köcher P, Gebauer T, Horna V, Leuschner C (2009) Leaf water status and stem xylem flux in relation to soil drought in five temperate broad-leaved tree species with contrasting water use strategies. Ann For Sci 66:101–112CrossRefGoogle Scholar
  37. Köcher P, Horna V, Leuschner C (2012a) Environmental control of daily stem growth patterns in five temperate broad-leaved tree species. Tree Physiol 32:1021–1032PubMedCrossRefPubMedCentralGoogle Scholar
  38. Köcher P, Horna V, Beckmeyer I, Leuschner C (2012b) Hydraulic properties and embolism in small-diameter roots of five temperate broad-leaved tree species with contrasting drought tolerance. Ann For Sci 69:693–703CrossRefGoogle Scholar
  39. Koide RT, Robichaux RH, Morse RH, Smith CM (2000) Plant water status, hydraulic resistance and capacitance. In: Pearcy RW, Ehleringer JR, Mooney HA, Rundel PW (eds) Plant physiological ecology: field methods and instrumentation. Kluwer, Dordrecht, pp 161–183CrossRefGoogle Scholar
  40. Kozlowski TT, Pallardy SG (2002) Acclimation and adaptive responses of woody plants to environmental stresses. Biol Rev 68:270–334Google Scholar
  41. Kramer PJ, Boyer JS (1995) Water relations of plants and soils. Academic, San DiegoGoogle Scholar
  42. Kubiske ME, Abrams MD (1991) Rehydration effects on pressure-volume relationships in four temperate woody species: variability with site, time of season and drought conditions. Oecologia 85:537–542PubMedCrossRefPubMedCentralGoogle Scholar
  43. Kubiske ME, Abrams MD (1994) Ecophysiological analysis of woody species in contrasting temperate communities during wet and dry years. Oecologia 98:303–312PubMedCrossRefPubMedCentralGoogle Scholar
  44. Lakatos F, Molnar M (2009) Mass mortality of beech (Fagus sylvatica L.) in south-west Hungary. Acta Silv Lign Hung 5:75–82Google Scholar
  45. Lambers H, Chapin FS III, Pons TL (2008) Plant physiological ecology, 2nd edn. Springer, New YorkCrossRefGoogle Scholar
  46. Lenz TI, Wright IJ, Westoby M (2006) Interrelations among pressure-volume curve traits across species and water availability gradients. Physiol Plant 127:423–433CrossRefGoogle Scholar
  47. Leuschner C, Ellenberg H (2017) Ecology of Central European forests. Vegetation ecology of Central Europe, vol I. Springer Nature, Cham, 971pCrossRefGoogle Scholar
  48. Leuschner C, Meier IC (2018) The ecology of Central European tree species: trait spectra, functional trade-offs, and ecological classification of adult trees. Perspect Plant Ecol Evol Syst 33:89–103. doi.org/ https://doi.org/10.1016/j.ppees.2018.05.003 CrossRefGoogle Scholar
  49. Leuzinger S, Zotz G, Asshoff R, Körner C (2005) Responses of deciduous forest trees to severe drought. Tree Physiol 25:641–650PubMedCrossRefPubMedCentralGoogle Scholar
  50. Levitt J (1972) Responses of plants to environmental stresses. Academic, New YorkGoogle Scholar
  51. Lübbe T, Schuldt B, Leuschner C (2017) Acclimation of leaf water status and stem hydraulics to drought and tree neighbourhood: alternative strategies among the saplings of five temperate deciduous tree species. Tree Physiol 37:456–468PubMedCrossRefGoogle Scholar
  52. Martinez-Vilalta J, Garcia-Forner N (2017) Water potential regulation, stomatal behavior and hydraulic transport under drought: deconstructing the iso/anisohydric concept. Plant Cell Environ 40:962–976PubMedCrossRefGoogle Scholar
  53. McDowell NG, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while other succumb to drought? New Phytol 178:719–739PubMedCrossRefGoogle Scholar
  54. Meinzer FR (2002) Coordination of vapor and liquid phase water transport properties in plants. Plant Cell Environ 25:265–274PubMedCrossRefGoogle Scholar
  55. Meinzer FC, Woodruff DR, Marias DE, McCulloh KA, Sevanto S (2014) Dynamics of leaf water relations components in co-occurring iso- and anisohydric conifer species. Plant Cell Environ 37:2577–2586PubMedCrossRefGoogle Scholar
  56. Meinzer FC, Smith DD, Woodruff DR, Marias DE, McCulloh KA, Howard AR, Magedman AL (2017) Stomatal kinetics and photosynthetic gas exchange along a continuum of isohydric to anisohydric regulation of plant water status. Plant Cell Environ 40:1618–1628PubMedCrossRefGoogle Scholar
  57. Mencucchini 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 26:163–182CrossRefGoogle Scholar
  58. Merchant A (2014) The regulation of osmotic potential in trees. In: Tausz M, Grulke N (eds) Trees in a changing environment, Plant ecophysiology, vol 9. Springer, Dordrecht, pp 83–97Google Scholar
  59. Mitchell PJ, Veneklaas EJ, Lambers H, Burgess SO (2008) Leaf water relations during summer water deficit: differential repsonses in turgor maintenance and variation in leaf structure among different plant communities in South-Western Australia. Plant Cell Environ 31:1791–1802PubMedCrossRefGoogle Scholar
  60. Ngugi M, Doley D, Hunt M, Dart P, Ryan P (2003) Leaf water relations of Eucalyptus cloeziana and Eucalyptus argophloia in response to water deficit. Tree Physiol 23:335–343PubMedCrossRefGoogle Scholar
  61. Niinemets Ü (2001) Global-scale climate controls of leaf dry mass per area, density and thickness in trees and shrubs. Ecology 82:453–469CrossRefGoogle Scholar
  62. Niklas KJ (1991) Biomechanical attributes of the leaves of pine species. Ann Bot 68:253–262CrossRefGoogle Scholar
  63. Osonubi O, Davies WJ (1978) Solute accumulation in leaves and roots of woody plants subjected to water stress. Oecologia 32:323–332PubMedCrossRefGoogle Scholar
  64. Pallardy SG (2008) Physiology of woody plants, 3rd edn. Elsevier, AmsterdamGoogle Scholar
  65. Parker WC, Pallardy SG (1988) Leaf and root osmotic adjustment in drought-stressed Quercus alba, Q. macrocarpa, and Q. stellate seedlings. Can J For Res 18:1–5CrossRefGoogle Scholar
  66. Peltier J-P, Marigo G (1999) Drought adaptation in F. excelsior excelsior L.: physiological basis of the elastic adjustment. J Plant Physiol 154:529–535CrossRefGoogle Scholar
  67. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2018) nlme: linear and nonlinear mixed effects models. R Package Version 3:1–137 https://CRANGoogle Scholar
  68. Prometheuswiki (2018) Leaf pressure-volume curve parameters. http://prometheuswiki.org/tiki-index.php?page=Pressure-volume+curves. (accessed 2/2018)
  69. Saito T, Terashima I (2004) Reversible decreases in the bulk elastic modulus of mature leaves of deciduous Quercus species subjected to tow drought treatments. Plant Cell Environ 27:863–875CrossRefGoogle Scholar
  70. Sanders GJ, Arndt SK (2012) Osmotic adjustment under drought conditions. In: Aroca R (ed) Plant responses to drought stress. Springer, Berlin, Heidelberg, pp 199–229CrossRefGoogle Scholar
  71. Schaap MG, Leij FJ, van Genuchten MT (1998) Neural network analysis for hierarchical prediction of soil hydraulic properties. Soil Sci Soc Am J 62:847–855CrossRefGoogle Scholar
  72. Schuldt B, Knutzen F, Delzon S, Jansen S, Müller-Haubold H, Burlett R, Clough Y, Leuschner C (2016) How adaptable is the hydraulic system of European beech in the face of climate change-related precipitation reduction? New Phytol 210:443–458PubMedCrossRefPubMedCentralGoogle Scholar
  73. Schulte PJ (1992) The units of currency for plant water status. Plant Cell Environ 15:7–10CrossRefGoogle Scholar
  74. Sheffield J, Wood EF (2008) Global trends and variability in soil moisture and drought characteristics, 1950-2000, from observation-driven simulations of the terrestrial hydrological cycle. J Clim 21:432–458CrossRefGoogle Scholar
  75. Sokal RR, Rohlf FJ (1995) Biometry. The principles and practice of statistics in biological research, 3rd edn. W. H. Freeman and Co, New YorkGoogle Scholar
  76. Tardieu F, Simonneau T (1998) Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modelling isohydric and anisohydric bahaviours. J Exp Bot 49:419–432CrossRefGoogle Scholar
  77. Tschaplinski TJ, Blake TJ (1989) Water-stress tolerance and late-season organic solute accumulation in hybrid poplar. Can J Bot 67:1681–1688CrossRefGoogle Scholar
  78. Tyree MT, Jarvis PG (1982) Water in tissues and cells. Encyclopedia plant physiol. N.S., Vol. 12B. Springer, Berlin, pp 35–77Google Scholar
  79. Uemura A, Ishida A, Nakano T, Terashima I, Tanabe H, Matsumoto Y (2000) Acclimation of leaf characteristics of F. sylvatica species to previous-year and current year solar irradiances. Tree Physiol 20:945–951PubMedCrossRefPubMedCentralGoogle Scholar
  80. Van Mantgem PJ, Stephenson NL, Byrne JC, Daniels LD, Franklin JF, Fulé PZ, Harmon ME et al (2009) Widespread increase of tree mortality rates in the western United States. Science 323:521–524PubMedCrossRefPubMedCentralGoogle Scholar
  81. Williams CB, Naesborg RR, Dawson TE (2017) Coping with gravity: the foliar water relations of giant sequoia. Tree Physiol 37:1312–1326PubMedCrossRefPubMedCentralGoogle Scholar
  82. Wright IJ, Westoby M (2002) Leaves at low versus high rainfall: coordination of structure, lifespan and physiology. New Phytol 155:403–416CrossRefGoogle Scholar
  83. Zimmermann J, Hauck M, Dulamsuren C, Leuschner C (2015) Climate warming-related growth decline affects F. sylvatica sylvatica, but not other broad-leaved tree species in Central European mixed forests. Ecosystems 18:560–572CrossRefGoogle Scholar
  84. Zuur A, Ieno EN, Walker N, Savaliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer ScienceGoogle Scholar

Copyright information

© INRA and Springer-Verlag France SAS, part of Springer Nature 2019

Authors and Affiliations

  • Christoph Leuschner
    • 1
    Email author
  • Paul Wedde
    • 1
  • Torben Lübbe
    • 1
  1. 1.Department of Plant EcologyUniversity of GoettingenGoettingenGermany

Personalised recommendations