How adaptable is the hydraulic system of European beech in the face of climate change-related precipitation reduction?

New Phytologist

Volumn 210, Issue 2, 2016, Pages 443-458

  Schuldt, Bernhard ^a   Knutzen, Florian ^a   Delzon, Sylvain ^b   Jansen, Steven ^c   Müller Haubold, Hilmar ^a   Burlett, Régis ^b   Clough, Yann ^d   Leuschner, Christoph ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c UNIVERSITY OF ULM   (Germany)

^d LUND UNIVERSITY   (Sweden)

Author keywords

Drought stress; Functional trait; Hydraulic conductivity; Leaf morphology; Pit membrane; Precipitation gradient; Vulnerability to cavitation; Wood anatomy

Indexed keywords

FAGUS; FAGUS SYLVATICA;

RAIN;

ADAPTATION; ANALYSIS; ANATOMY AND HISTOLOGY; BEECH; CLIMATE CHANGE; EUROPE; GROWTH, DEVELOPMENT AND AGING; PHYSIOLOGY; PLANT LEAF; PLANT STEM; PRESSURE; PRINCIPAL COMPONENT ANALYSIS; STATISTICAL MODEL; WOOD; XYLEM;

ADAPTATION, PHYSIOLOGICAL; CLIMATE CHANGE; EUROPE; FAGUS; LINEAR MODELS; PLANT LEAVES; PLANT STEMS; PRESSURE; PRINCIPAL COMPONENT ANALYSIS; RAIN; WOOD; XYLEM;

EID: 84952836668     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13798     Document Type: Article

References (91)

1. Anderegg WRL. 2015. Spatial and temporal variation in plant hydraulic traits and their relevance for climate change impacts on vegetation. New Phytologist 205: 1008-1014.
2. Anderegg WRL, Flint A, Huang C, Flint L, Berry JA, Davis FW, Sperry JS, Field CB. 2015. Tree mortality predicted from drought-induced vascular damage. Nature Geoscience 8: 367-371.
3. Anderegg WRL, Meinzer FC. 2015. Wood anatomy and plant hydraulics in a changing climate. In: Hacke U, ed. Functional and ecological xylem anatomy. Cham, Switzerland: Springer International Publishing, 235-253.
4. Anfodillo T, Petit G, Crivellaro A. 2013. Axial conduit widening in woody species: a still neglected anatomical pattern. IAWA Journal 34: 352-364.
5. Aranda I, Cano FJ, Gasco A, Cochard H, Nardini A, Mancha JA, Lopez R, Sanchez-Gomez D. 2015. Variation in photosynthetic performance and hydraulic architecture across European beech (Fagus sylvatica L.) populations supports the case for local adaptation to water stress. Tree Physiology 35: 34-46.
6. Bohn U, Neuhäusl R, Mitarbeit U. 2003. Map of the natural vegetation of Europe. Scale 1:2500000. Bonn, Germany: Bundesamt für Naturschutz (BfN)/Federal Agency for Nature Conservation.
7. Bolte A, Czajkowski T, Kompa T. 2007. The north-eastern distribution range of European beech: a review. Forestry 80: 413-429.
8. Bouche PS, Larter M, Domec JC, Burlett R, Gasson P, Jansen S, Delzon S. 2014. A broad survey of hydraulic and mechanical safety in the xylem of conifers. Journal of Experimental Botany 65: 4419-4431.
9. 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. Annals of Forest Science 63: 625-644.
10. Bresson CC, Vitasse Y, Kremer A, Delzon S. 2011. To what extent is altitudinal variation of functional traits driven by genetic adaptation in European oak and beech? Tree Physiology 31: 1164-1174.
11. Brodribb TJ, Holbrook NM, Edwards EJ, Gutierrez MV. 2003. Relations between stomatal closure, leaf turgor and xylem vulnerability in eight tropical dry forest trees. Plant, Cell & Environment 26: 443-450.
12. Carlquist S. 1966. Wood anatomy of compositae: a summary, with comments on factors controlling wood evolution. Aliso 6: 25-44.
13. Carlquist S. 1977. Ecological factors in wood evolution - floristic approach. American Journal of Botany 64: 887-896.
14. Carlquist S. 2012. How wood evolves: a new synthesis. Botany-Botanique 90: 901-940.
15. Chenlemuge T, Schuldt B, Dulamsuren C, Hertel D, Leuschner C, Hauck M. 2015. Stem increment and hydraulic architecture of a boreal conifer (Larix sibirica) under contrasting macroclimates. Trees-Structure and Function 29: 623-636.
16. Christensen-Dalsgaard KK, Tyree MT. 2014. Frost fatigue and spring recovery of xylem vessels in three diffuse-porous trees in situ. Plant, Cell & Environment 37: 1074-1085.
17. Cochard H, Casella E, Mencuccini M. 2007. Xylem vulnerability to cavitation varies among poplar and willow clones and correlates with yield. Tree Physiology 27: 1761-1767.
18. Cochard H, Coll L, Le Roux X, Ameglio T. 2002. Unraveling the effects of plant hydraulics on stomatal closure during water stress in walnut. Plant Physiology 128: 282-290.
19. Cochard H, Damour G, Bodet C, Tharwat I, Poirier M, Ameglio T. 2005. Evaluation of a new centrifuge technique for rapid generation of xylem vulnerability curves. Physiologia Plantarum 124: 410-418.
20. De Micco V, Aronne G, Baas P. 2008. Wood anatomy and hydraulic architecture of stems and twigs of some Mediterranean trees and shrubs along a mesic-xeric gradient. Trees-Structure and Function 22: 643-655.
21. Delzon S, Douthe C, Sala A, Cochard H. 2010. Mechanism of water-stress induced cavitation in conifers: bordered pit structure and function support the hypothesis of seal capillary-seeding. Plant, Cell & Environment 33: 2101-2111.
22. Domec J-C, Gartner BL. 2001. Cavitation and water storage capacity in bole xylem segments of mature and young Douglas-fir trees. Trees 15: 204-214.
23. 2 concentration. Tree Physiology 30: 1001-1015.
24. Domec J-C, Warren JM, Meinzer FC, Lachenbruch B. 2009. Safety factors for xylem failure by implosion and air-seeding within roots, trunks and branches of young and old conifer trees. IAWA Journal 30: 101-120.
25. Eilmann B, Sterck F, Wegner L, de Vries SMG, von Arx G, Mohren GMJ, den Ouden J, Sass-Klaassen U. 2014. Wood structural differences between northern and southern beech provenances growing at a moderate site. Tree Physiology 34: 882-893.
26. Ellenberg H, Leuschner C. 2010. Vegetation Mitteleuropas mit den Alpen in ökologischer, dynamischer und historischer Sicht, 6th edn. Stuttgart, Germany: Ulmer.
27. Fan DY, Jie SL, Liu CC, Zhang XY, Xu XW, Zhang SR, Xie ZQ. 2011. The trade-off between safety and efficiency in hydraulic architecture in 31 woody species in a karst area. Tree Physiology 31: 865-877.
28. Fichot R, Brignolas F, Cochard H, Ceulemans R. 2015. Vulnerability to drought-induced cavitation in poplars: synthesis and future opportunities. Plant, Cell & Environment 38: 1233-1251.
29. Fischer EM, Schär C. 2008. Future changes in daily summer temperature variability: driving processes and role for temperature extremes. Climate Dynamics 33: 917-935.
30. Führer E, Horváth L, Jagodics A, Machon A, Szabados I. 2011. Application of a new aridity index in Hungarian forestry practice. Idojaras 115: 205-216.
31. Gessler A, Keitel C, Kreuzwieser J, Matyssek R, Seiler W, Rennenberg H. 2007. Potential risks for European beech (Fagus sylvatica L.) in a changing climate. Trees - Structure and Function 21: 1-11.
32. Gleason SM, Butler DW, Waryszak P. 2013. Shifts in leaf and stem hydraulic traits across aridity gradients in Eastern Australia. International Journal of Plant Sciences 174: 1292-1301.
33. Gleason SM, Butler DW, Ziemińska K, Waryszak P, Westoby M. 2012. Stem xylem conductivity is key to plant water balance across Australian angiosperm species. Functional Ecology 26: 343-352.
34. Gleason SM, Westoby M, Jansen S, Choat B, Hacke UG, Pratt RB, Bhaskar R, Brodribb TJ, Bucci SJ, Cao KF et al. 2016. Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world's woody plant species. New Phytologist 209: 123-136.
35. Goldstein G, Bucci SJ, Scholz FG. 2013. Why do trees adjust water relations and hydraulic architecture in response to nutrient availability? Tree Physiology 33: 238-240.
36. Guet J, Fichot R, Ledee C, Laurans F, Cochard H, Delzon S, Bastien C, Brignolas F. 2015. Stem xylem resistance to cavitation is related to xylem structure but not to growth and water-use efficiency at the within-population level in Populus nigra L. Journal of Experimental Botany 66: 4643-4652.
37. Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloch KA. 2001. Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126: 457-461.
38. Hajek P, Leuschner C, Hertel D, Delzon S, Schuldt B. 2014. Trade-offs between xylem hydraulic properties, wood anatomy and yield in Populus. Tree Physiology 34: 744-756.
39. Herbette S, Wortemann R, Awad H, Huc R, Cochard H, Barigah TS. 2010. Insights into xylem vulnerability to cavitation in Fagus sylvatica L.: phenotypic and environmental sources of variability. Tree Physiology 30: 1448-1455.
40. Hertel D, Strecker T, Müller-Haubold H, Leuschner C. 2013. Fine root biomass and dynamics in beech forests across a precipitation gradient - is optimal resource partitioning theory applicable to water-limited mature trees? Journal of Ecology 101: 1183-1200.
41. Hoeber S, Leuschner C, Köhler L, Arias-Aguilar D, Schuldt B. 2014. The importance of hydraulic conductivity and wood density to growth performance in eight tree species from a tropical semi-dry climate. Forest Ecology and Management 330: 126-136.
42. Jacob D, Göttel H, Kotlarski S, Lorenz P, Sieck K. 2008. Klimaauswirkungen und Anpassung in Deutschland - Phase 1: Erstellung regionaler Klimaszenarien für Deutschland. In: Umweltbundesamt, eds. Reihe climate change. 11/2008, ISSN 1862-4359, Dessau-Roßlau, Germany. [WWW document] URL http://www.umweltbundesamt.de/publikationen/klimaauswirkungen-anpassung-in-deutschland.
43. Jacobsen AL, Pratt RB, Ewers FW, Davis SD. 2007. Cavitation resistance among 26 chaparral species of southern California. Ecological Monographs 77: 99-115.
44. Jansen S, Choat B, Pletsers A. 2009a. Morphological variation of intervessel pit membranes and implications to xylem function in angiosperms. American Journal of Botany 96: 409-419.
45. Jansen S, Dute RR, Plavcová L, Choat B. 2009b. Preparation of material for TEM examination. Prometheus Wiki, CSIRO Publishing. [WWW document] URL http://prometheuswiki.publish.csiro.au/tiki-index.php?page=Preparation+of+Material+for+TEM+Examination.
46. Jump AS, Hunt JM, Peñuelas J. 2006. Rapid climate change-related growth decline at the southern range edge of Fagus sylvatica. Global Change Biology 12: 2163-2174.
47. Kotowska MM, Hertel D, Abou Rajab Y, Barus H, Schuldt B. 2015. Patterns in hydraulic architecture from roots to branches in six tropical tree species from cacao agroforestry and their relation to wood density and stem growth. Frontiers in Plant Science 6: 1-16.
48. Kremer A, Potts BM, Delzon S. 2014. Genetic divergence in forest trees: understanding the consequences of climate change. Functional Ecology 28: 22-36.
49. Lamy JB, Delzon S, Bouche PS, Alia R, Vendramin GG, Cochard H, Plomion C. 2014. Limited genetic variability and phenotypic plasticity detected for cavitation resistance in a Mediterranean pine. New Phytologist 201: 874-886.
50. nd English edn. Amsterdam, the Netherlands: Elsevier Science.
51. Lens F, Luteyn JL, Smets E, Jansen S. 2004. Ecological trends in the wood anatomy of Vaccinioideae (Ericaceae s.l.). Flora - Morphology Distribution, Functional Ecology of Plants 199: 309-319.
52. Lens F, Sperry JS, Christman MA, Choat B, Rabaey D, Jansen S. 2011. Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer. New Phytologist 190: 709-723.
53. Leuschner C. 2009. Die Trockenheitsempfindlichkeit der Rotbuche vor dem Hintergrund des prognostizierten Klimawandels. Jahrbuch der Akademie der Wissenschaften zu Göttingen. Berlin, Germany: Walter de Gruyter. [WWW document] URL adw-digital.sub.uni-goettingen.de/bitstream/handle/11858/00-001S-0000-0007-371C-7/Article-21.pdf?sequence=1.
54. Lewis AM, Boose ER. 1995. Estimating flow rates through xylem conduits. American Journal of Botany 82: 1112-1116.
55. Lintunen A, Kalliokoski T. 2010. The effect of tree architecture on conduit diameter and frequency from small distal roots to branch tips in Betula pendula, Picea abies and Pinus sylvestris. Tree Physiology 30: 1433-1447.
56. Loepfe L, Martinez-Vilalta J, Pinol J, Mencuccini M. 2007. The relevance of xylem network structure for plant hydraulic efficiency and safety. Journal of Theoretical Biology 247: 788-803.
57. 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 & Environment 29: 571-583.
58. Markesteijn L, Poorter L, Paz H, Sack L, Bongers F. 2011. Ecological differentiation in xylem cavitation resistance is associated with stem and leaf structural traits. Plant, Cell & Environment 34: 137-148.
59. Martinez-Vilalta J, Cochard H, Mencuccini M, Sterck F, Herrero A, Korhonen JFJ, Llorens P, Nikinmaa E, Nole A, Poyatos R et al. 2009. Hydraulic adjustment of Scots pine across Europe. New Phytologist 184: 353-364.
60. McDowell NG, Allen CD. 2015. Darcy's law predicts widespread forest mortality under climate warming. Nature Climate Change 5: 669-672.
61. Meier IC, Leuschner C. 2008. Leaf size and leaf area index in Fagus sylvatica forests: competing effects of precipitation, temperature, and nitrogen availability. Ecosystems 11: 655-669.
62. Meinke I, Gerstner E, von Storch H, Marx A, Schipper H, Kottmeier C, Treffeisen R, Lemke P. 2010. Regionaler Klimaatlas Deutschland der Helmholtz-Gemeinschaft informiert im Internet über möglichen künftigen Klimawandel. DMG Mitteilungen 2: 7-9.
63. Mencuccini M, Grace J. 1995. Climate influences the leaf area/sapwood area ratio in Scots pine. Tree Physiology 15: 1-10.
64. Müller-Haubold H, Hertel D, Seidel D, Knutzen F, Leuschner C. 2013. Climate responses of aboveground productivity and allocation in Fagus sylvatica: a transect study in mature forests. Ecosystems 16: 1498-1516.
65. Nardini A, Tyree MT, Salleo S. 2001. Xylem cavitation in the leaf of Prunus laurocerasus and its impact on leaf hydraulics. Plant Physiology 125: 1700-1709.
66. Nolf M, Creek D, Duursma R, Holtum J, Mayr S, Choat B. 2015. Stem and leaf hydraulic properties are finely coordinated in three tropical rainforest tree species. Plant, Cell & Environment 38: 2652-2661.
67. Ogasa M, Miki NH, Murakami Y, Yoshikawa K. 2013. Recovery performance in xylem hydraulic conductivity is correlated with cavitation resistance for temperate deciduous tree species. Tree Physiology 33: 335-344.
68. Pammenter NW, Vander Willigen C. 1998. A mathematical and statistical analysis of the curves illustrating vulnerability of xylem to cavitation. Tree Physiology 18: 589-593.
69. Plavcová L, Jansen S, Klepsch M, Hacke UG. 2013. Nobody's perfect: can irregularities in pit structure influence vulnerability to cavitation? Frontiers in Plant Science 4: 453.
70. Poyatos R, Martínez-Vilalta J, Cermák J, Ceulemans R, Granier A, Irvine J, Köstner B, Lagergren F, Meiresonne L, Nadezhdina N et al. 2007. Plasticity in hydraulic architecture of Scots pine across Eurasia. Oecologia 153: 245-259.
71. R Development Core Team. 2013. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical computing. URL http://www.R-project.org.
72. Rigling A, Bigler C, Eilmann B, Feldmeyer-Christe E, Gimmi U, Ginzler C, Graf U, Mayer P, Vacchiano G, Weber P et al. 2013. Driving factors of a vegetation shift from Scots pine to pubescent oak in dry Alpine forests. Global Change Biology 19: 229-240.
73. Rowell DP, Jones RG. 2006. Causes and uncertainty of future summer drying over Europe. Climate Dynamics 27: 281-299.
74. Schär C, Vidale PL, Lüthi D, Frei C, Häberli C, Liniger MA, Appenzeller C. 2004. The role of increasing temperature variability in European summer heatwaves. Nature 427: 332-336.
75. Schenk HJ, Steppe K, Jansen S. 2015. Nanobubbles: a new paradigm for air-seeding in xylem. Trends in Plant Science 20: 199-205.
76. Scholz A, Klepsch M, Karimi Z, Jansen S. 2013. How to quantify conduits in wood? Frontiers in Plant Science 4: 56.
77. Schreiber SG, Hacke UG, Hamann A. 2015. Variation of xylem vessel diameters across a climate gradient: insight from a reciprocal transplant experiment with a widespread boreal tree. Functional Ecology 29: 1392-1401.
78. Sperry JS, Nichols KL, Sullivan JEM, Eastlack SE. 1994. Xylem embolism in ring-porous, diffuse-porous, and coniferous trees of Northern Utah and Interior Alaska. Ecology 75: 1736-1752.
79. Sterck FJ, Martínez-Vilalta J, Mencuccini M, Cochard H, Gerrits P, Zweifel R, Herrero A, Korhonen JFJ, Llorens P, Nikinmaa E et al. 2012. Understanding trait interactions and their impacts on growth in Scots pine branches across Europe. Functional Ecology 26: 541-549.
80. Sterck FJ, Zweifel R, Sass-Klaassen U, Chowdhury Q. 2008. Persisting soil drought reduces leaf specific conductivity in Scots pine (Pinus sylvestris) and pubescent oak (Quercus pubescens). Tree Physiology 28: 529-536.
81. Tokumoto I, Heilman JL, Schwinning S, McInnes KJ, Litvak ME, Morgan CLS, Kamps RH. 2014. Small-scale variability in water storage and plant available water in shallow, rocky soils. Plant and Soil 385: 193-204.
82. Tyree MT. 2003. Hydraulic limits on tree performance: transpiration, carbon gain and growth of trees. Trees-Structure and Function 17: 95-100.
83. Tyree MT, Davis SD, Cochard H. 1994. Biophysical perspectives of xylem evolution - is there a trade-off of hydraulic efficiency for vulnerability to dysfunction? IAWA Journal 15: 335-360.
84. Tyree MT, Sperry JS. 1989. Vulnerability of xylem to cavitation and embolism. Annual Review of Plant Physiology and Plant Molecular Biology 40: 19-38.
85. Tyree MT, Zimmermann MH. 2002. Xylem structure and the ascent of sap. Berlin, Germany: Springer.
86. Vesque J. 1876. Note sur l'anatomie du Goodenia ovate. Annales des Sciences Naturalles-Botanique et Biologie Vegetale 6: 312-326.
87. Weber P, Bugmann H, Pluess AR, Walthert L, Rigling A. 2013. Drought response and changing mean sensitivity of European beech close to the dry distribution limit. Trees - Structure and Function 27: 171-181.
88. 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 & Environment 28: 800-812.
89. Willson CJ, Manos PS, Jackson RB. 2008. Hydraulic traits are influenced by phylogenetic history in the drought-resistant, invasive genus Juniperus (Cupressaceae). American Journal of Botany 95: 299-314.
90. Wortemann R, Herbette S, Barigah TS, Fumanal B, Alia R, Ducousso A, Gomory D, Roeckel-Drevet P, Cochard H. 2011. Genotypic variability and phenotypic plasticity of cavitation resistance in Fagus sylvatica L. across Europe. Tree Physiology 31: 1175-1182.
91. Zimmermann J, Hauck M, Dulamsuren C, Leuschner C. 2015. Climate warming-related growth decline affects Fagus sylvatica, but not other broad-leaved tree species in Central European mixed forests. Ecosystems 1: 560-572.