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Xylem hydraulic safety and efficiency in relation to leaf and wood traits in three temperate Acer species differing in habitat preferences

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For three widespread European Acer species with different climate envelopes, hydraulic traits, but not wood anatomical or leaf morphological traits, were good indicators for habitat preferences.

Abstract

Prediction of drought impacts on trees requires knowledge about species differences in hydraulic traits and how the hydraulic constitution changes along water availability gradients. We studied co-occurring mature trees of three widespread European Acer species with different climate envelopes and habitat preferences for branch hydraulic (embolism resistance, hydraulic conductivity), wood anatomical (vessel diameter, vessel density, wood density) and leaf functional traits (specific leaf area, sapwood-to-leaf area ratio, foliar δ13C), and branch growth rate. Study objectives were to examine the relation between hydraulic traits and the species’ habitat preferences and to confirm several commonly anticipated trade-offs in hydraulic traits at the genus level. The species’ habitat preferences were reflected in the hydraulic traits, but not in the studied wood anatomical or leaf traits. Embolism resistance (P12, P50 and P88 values) decreased and pit conductivity (potential minus measured conductivity) increased in the sequence A. campestre–A. platanoides–A. pseudoplatanus in parallel with the species’ putative drought tolerance. As expected, a trade-off was found between branch hydraulic efficiency and safety. Wood density was related to hydraulic safety, but neither to hydraulic efficiency nor other wood anatomical traits including vessel diameter. Branch growth rate was unrelated to wood density, but linked to vessel diameter and hydraulic conductivity. The findings from the three maple species suggest that hydraulic traits may be under stronger genetic control than leaf and wood anatomical traits that exhibited a more plastic response to the environment. The former are thus better indicators of habitat preferences.

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References

  • Alder NN, Sperry JS, Pockman WT (1996) Root and stem xylem embolism, stomatal conductance, and leaf turgor in Acer grandidentatum populations along a soil moisture gradient. Oecologia 105:293–301

    Article  CAS  Google Scholar 

  • Allen CD, Breshears DD, McDowell NG (2015) On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene. Ecosphere 6:1–55

    Article  Google Scholar 

  • Anderegg WRL, Berry JA, Smith DD, Sperry JS, Anderegg LDL, Field CB (2012) The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off. Proc Natl Acad Sci USA 109:233–237

    Article  CAS  Google Scholar 

  • Anderegg WRL, Klein T, Bartlett M, Sack L, Pellegrini AFA, Choat B, Jansen S (2016) Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe. Proc Natl Acad Sci 113:5024–5029

    Article  CAS  Google Scholar 

  • Anderegg WRL, Meinzer FC (2015) Wood anatomy and plant hydraulics in a changing climate. In: Hacke U (ed) Functional and ecological Xylem anatomy. Springer, Cham

    Google Scholar 

  • Awad H, Barigah T, Badel E, Cochard H, Herbette S (2010) Poplar vulnerability to xylem cavitation acclimates to drier soil conditions. Physiol Plant 139:280–288

    CAS  PubMed  Google Scholar 

  • Brodribb TJ, Cochard H (2009) Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiol 149:575–584

    Article  CAS  Google Scholar 

  • Choat B, Brodie TW, Cobb AR, Zwieniecki MA, Holbrook NM (2006) Direct measurements of intervessel pit membrane hydraulic resistance in two angiosperm tree species. Am J Bot 93:993–1000

    Article  Google Scholar 

  • Choat B, Sack L, Holbrook NM (2007) Diversity of hydraulic traits in nine Cordia species growing in tropical forests with contrasting precipitation. New Phytologist 175:686–698

    Article  Google Scholar 

  • Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Hacke UG et al (2012) Global convergence in the vulnerability of forests to drought. Nature 491:752–755

    Article  CAS  Google Scholar 

  • Carlquist S (1977) Ecological factors in wood evolution—floristic approach. Am J Bot 64:887–896

    Article  Google Scholar 

  • Cochard H (2002) A technique for measuring xylem hydraulic conductivity under high negative pressures. Plant Plant Cell Environ J 25:815–819

    Article  Google Scholar 

  • Cochard H, Casella E, Mencuccini M (2007) Xylem vulnerability to cavitation varies among poplar and willow clones and correlates with yield. Tree Physiol 27:1761–1767

    Article  Google Scholar 

  • 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. Physiol Plant 124:410–418

    Article  CAS  Google Scholar 

  • Corcuera L, Cochard H, Gil-Pelegrin E, Notivol E (2011) Phenotypic plasticity in mesic populations of Pinus pinaster improves resistance to xylem embolism (P50) under severe drought. Trees 25:1033–1042

    Article  Google Scholar 

  • Dai A (2013) Increasing drought under global warming in observations and models. Nat Clim Change 3:52–58

    Article  Google Scholar 

  • Dietrich L, Hoch G, Kahmen A, Körner C (2018) Losing half the conductive area hardly impacts the water status of mature trees. Sci Rep 8:15006

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Dulamsuren C, Abilova SB, Bektayeva M, Eldarov M, Schuldt B, Leuschner C, Hauck M (2019) Hydraulic architecture and vulnerability to drought-induced embolism in southern boreal tree species of Inner Asia. Tree Physiol 39:463–473

    Article  Google Scholar 

  • Enquist BJ, West GB, Charnov EL, Brown JH (1999) Allometric scaling of production and life history variation in vascular plants. Nature 401:907–911

    Article  CAS  Google Scholar 

  • Fan Z-X, Zhang S-B, Hao G-Y, Slik JWF, Cao K-F (2012) Hydraulic conductivity traits predict growth rates and adult stature of 40 Asian tropical tree species better than wood density. J Ecol 100:732–741

    Article  Google Scholar 

  • Fichot R, Barigah TS, Chamaillard S, Thiec DL, Laurans F, Chochard H, Brignolas F (2010) Common trade-offs between xylem resistance to cavitation and other physiological traits do not hold among unrelated Populus deltoids x Populus nigra hybrids. Plant Cell Environ 33:1553–1568

    PubMed  Google Scholar 

  • Fischer EM, Schär C (2008) Future changes in daily summer temperature variability: driving processes and role for temperature extremes. Clim Dyn 33:917–935

    Article  Google Scholar 

  • Gleason SM, Butler DW, Ziemińska K, Waryszak P, Westoby M (2012) Stem xylem conductivity is key to plant water balance across Australian angiosperm species. Funct Ecol 26:343–352

    Article  Google Scholar 

  • Gleason SM, Westoby M, Jansen S, Choat B, Hacke UG, Pratt RB, Bhaskar R, Brodribb TJ, Bucci SJ, Cao K-F et al (2016) Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world’s woody plant species. New Phytol 209:123–136

    Article  CAS  Google Scholar 

  • Guet J, Fichot R, Lédée 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. J Experim Bot 66:4643–4652

    Article  CAS  Google Scholar 

  • Hacke UG, Sperry JS, Pittermann J (2004) Anaylsis of circular bordered pit function II. Gymnosperm tracheids with torus-margo pit membranes. Am J Bot 91:386–400

    Article  Google Scholar 

  • Hacke UG, Sperry JS, Wheeler JK, Castro L (2006) Scaling of angiosperm xylem structure with safety and efficiency. Tree Physiol 26:689–701

    Article  Google Scholar 

  • Hacke UG, Spicer R, Schreiber SG, Plavcová L (2017) An ecophysiological and developmental perspective on variation in vessel diameter. Plant Cell Environ 40:831–845

    Article  CAS  Google Scholar 

  • Hajek P, Leuschner C, Hertel D, Delzon S, Schuldt B (2014) Trade-offs between xylem hydraulic properties, wood anatomy and yield in Populus. Tree Physiol 34:744–756

    Article  Google Scholar 

  • Hajek P, Kurjak D, von Wühlisch G, Delzon S, Schuldt B (2016) Intraspecific variation in wood anatomical, hydraulic and foliar traits in ten European beech provenances differing in growth yield. Front Plant Sci 7:791

    Article  Google Scholar 

  • Hargrave KR, Kolb KJ, Ewers FW, Davis SD (1994) Conduit diameter and drought-induced embolism in Salvia-Mellifera Greene (Labiatae). New Phytol 126:695–705

    Article  Google Scholar 

  • Hartmann H, Ziegler W, Kolle O, Trumbore S (2013) Thirst beats hunger - declining hydration during drought prevents carbon starvation in Norway spruce saplings. New Phytol 200:340–349

    Article  CAS  Google Scholar 

  • 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 Physiol 30:1448–1455

    Article  Google Scholar 

  • Hietz P, Valencia R, Wright SJ (2013) Strong radial variation in wood density follows a uniform pattern in two neotropical rain forests. Funct Ecol 27:684–692

    Article  Google Scholar 

  • 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. Ecol Manag 330:126–136

    Article  Google Scholar 

  • IPCC (2013) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Campridge

    Google Scholar 

  • Jacobsen AL, Pratt RB, Ewers FW, Davis SD (2007) Cavitation resistance among 26 chaparral species of southern California. Ecol Monogr 77:99–115

    Article  Google Scholar 

  • King DA, Davies SJ, Tan S, Noor NSM (2006) The role of wood density and stem support costs in the growth and mortality of tropical trees. J Ecol 94:670–680

    Article  Google Scholar 

  • 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. Front Plant Sci 6:1–16

    Article  Google Scholar 

  • Larter M, Pfautsch S, Domec J-C, Trueba S, Nagalingum N, Delzon S (2017) Aridity drove the evolution of extreme embolism the radiation of conifer genus Callitris. New Phytol 215:97–112

    Article  Google Scholar 

  • 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 Phytol 190:709–723

    Article  Google Scholar 

  • Leuschner C, Ellenberg H (2017) Ecology of central European forests—vegetation ecology of central Europe, vol I. Springer, Cham

    Book  Google Scholar 

  • Li S, Lens F, Espino S, Karimi MK, Schenk HJ, Schmitt M, Schuldt B, Jansen S (2016) Intervessel pit membrane thickness as a key determinant of embolism resistance in angiosperm xylem. IAWA J 37:152–171

    Article  Google Scholar 

  • Maherali H, DeLucia EH (2000) Xylem conductivity and vulnerability to cavitation of ponderosa pine growing in contrasting climates. Tree Physiol 20:859–867

    Article  CAS  Google Scholar 

  • Maherali H, Williams BL, Paige KN, DeLucia EH (2002) Hydraulic differentiation of Ponderosa pine populations along a climate gradient is not associated with ecotypic divergence. Funct Ecol 16:510–521

    Article  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 J 29:571–583

    Article  Google Scholar 

  • 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 Environ 34:137–148

    Article  Google Scholar 

  • Martínez-Cabrera HI, Schenk HJ, Cevallos-Ferriz SRS, Jones CS (2011) Integration of vessel traits, wood density, and height in angiosperm shrubs and trees. Am J Bot 98:915–922

    Article  Google Scholar 

  • Martínez-Vilalta J, Cochard H, Mencuccini M, Sterck F, Herrero A, Korhonen JFJ, Llorenz P, Nikinmaa E, Nolè A, Poyatos R, Ripullone F, Sass-Klaassen U, Zweifel R (2009) Hydraulic adjustment of Scots pine across Europe. New Phytol 184:353–364

    Article  Google Scholar 

  • McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG et al (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739

    Article  Google Scholar 

  • Neumann M, Mues V, Moreno A, Hasenauer H, Seidl R (2017) Climate variability drives recent tree mortality in Europe. Global Change Biol 23:4788–4797

    Article  Google Scholar 

  • 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 Physiol 33:335–344

    Article  Google Scholar 

  • Pammenter NW, Vander Willigen C (1998) A mathematical and statistical analysis of the curves illustrating vulnerability of xylem to cavitation. Tree Physiol 18:589–593

    Article  Google Scholar 

  • Poorter L, Mcdonald I, Alarcon A, Fichtler E, Licona J-C, Pena-Claros M et al (2010) The importance of wood traits and hydraulic conductivity for the performance and life history strategies of 42 rainforest tree species. New Phytol 185:481–492

    Article  Google Scholar 

  • Poyatos R, Martínez-Vilalta J, Čermák J, Ceulemans R, Granier A, Irvine J, Köstner B, Lagergren F, Meiresonne L, Nadezhdina N, Zimmermann R, Llorens P, Mencuccini M (2007) Plasticity in hydraulic architecture of Scots pine across Europe. Oecologia 153:245–259

    Article  CAS  Google Scholar 

  • Rowland L, da Costa ACL, Galbraith DR, Oliveira RS, Binks OJ, Oliveira AAR, Pullen AM, Doughty CE, Metcalfe DB, Vasconcelos SS et al (2015) Death from drought in tropical forests is triggered by hydraulics not carbon starvation. Nature 528:119–122

    Article  CAS  Google Scholar 

  • Salmon Y, Torres-Ruiz JM, Poyatos R, Martinez-Vilalta J, Meir P, Cochard H, Mencuccini M (2015) Balancing the risks of hydraulic failure and carbon starvation: a twig scale analysis in declining Scots pine. Plant Cell Environ 38:2575–2588

    Article  CAS  Google Scholar 

  • San-Miguel-Ayanz J, de Rigo D, Caudullo G, Houston Durrant T, Mauri A, Tinner W, Ballian D, Beck P, Birks HJB, Eaton E et al (2016) European atlas of forest tree species. Publications Office of the European Union, Luxembourg

    Google Scholar 

  • Schreiber SG, Hacke UG, Chamberland S, Lowe CW, Kamelchuk D, Bräutigam K, Campbell MM, Thomas BR (2016) Leaf size serves as a proxy for xylem vulnerability to cavitation in plantation trees. Plant Cell Environ 39:272–281

    Article  CAS  Google Scholar 

  • 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 beeach in the face of climate change-related precipitation reduction. New Phytol 210:443–548

    Article  Google Scholar 

  • Skelton RP, West AG, Dawson TE (2015) Predicting plant vulnerability to drought in biodiverse regions using functional traits. Proc Natl Acad Sci 112:5744–5749

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Sterck FJ, Martínez-Vilalta J, Mencuccini M, Cochard H, Gerrits P, Zweifel R, Herrero A, Korhonen JFJ, Llorens P, Nikinmaa E, Nolè A, Poyatos R, Ripullone F, Sass-Klaassen U (2012) Understanding trait interactions and their impacts on growth in Scots pine branches across Europe. Funct Ecol 26:541–549

    Article  Google Scholar 

  • Tissier J, Lambs L, Peltier J-P, Marigo G (2004) Relationship between hydraulic traits and habitat preference for six Acer species occurring in the French Alps. Ann For Sci 61:81–86

    Article  Google Scholar 

  • Togashi HF, Prentice IC, Evans BJ, Forrester DI, Drake P, Feikema P, Brooksbank K, Eamus D, Tylor D (2015) Morphological and moisture availability controls of the leaf area-to-sapwood area ratio: analysis of measurements on Australian trees. Ecol Evolut 5:1263–1270

    Article  Google Scholar 

  • Torres-Ruiz JM, Cochard H, Fonseca E, Badel E, Gazarini L, Vaz M (2017) Differences in functional and xylem anatomical features allow Cistus species to co-occur and cope differently with drought in the Mediterranean region. Tree Physiol 37:755–766

    Article  Google Scholar 

  • Trifilò P, Casolo V, Raimondo F, Petrussa E, Boscutti F, Lo Gullo MA, Nardini A (2017) Effects of prolonged drought on stem non-structural carbohydrates content and post-drought hydraulic recovery in Laurus nobilis L.: The possible link between carbon starvation and hydraulic failure. Plant Physiol Biochem 120:232–241

    Article  Google Scholar 

  • Tyree MT, Sperry JS (1989) Vulnerability of xylem to cavitation and embolism. Ann Rev Plant Biol 40:19–38

    Article  Google Scholar 

  • Urli M, Porté AJ, Cochard H, Guengant Y, Burlett R, Delzon S (2013) Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees. Tree Physiol 33:672–683

    Article  CAS  Google Scholar 

  • White FM (1991) Viscous fluid flow, 2nd edn. McGraw-Hill, New York

    Google Scholar 

  • Willson CJ, Jackson RB (2006) Xylem cavitation caused by drought and freezing stress in four co-occurring Juniperus species. Physiol Plant 127:374–382

    Article  CAS  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 

  • Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    Article  CAS  Google Scholar 

  • Yoshimura K, Saiki S-T, Yazaki K, Ogasa MY, Shirai M, Nakano T, Yoshimura J, Ishida A (2016) The dynamics of carbon stored in xylem sapwood to drought-induced hydraulic stress in mature trees. Sci Rep 6:24513

    Article  CAS  Google Scholar 

  • Ziemińska K, Butler DW, Gleason SM, Wright IJ, Westoby M (2013) Fibre wall and lumen fractions drive wood density variation across 24 Australian angiosperms. AoB Plants 5:plt046

    Article  Google Scholar 

  • Zimmermann MH (1983) Xylem structure and the ascent of sap. Springer, Berlin

    Book  Google Scholar 

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Acknowledgements

We would like to thank Ana Sapoznikova for preparing all transverse sections for wood anatomical analyses, and Jürgen Köhler for branch sample collection. The constructive comments by two anonymous reviewers helped to improve the manuscript.

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  1. Plant Ecology, Albrecht von Haller Institute for Plant Sciences, University of Goettingen, Untere Karspüle 2, 37073, Göttingen, Germany

    Katja Schumann, Christoph Leuschner & Bernhard Schuldt

  2. Julius-von-Sachs-Institute of Biological Sciences, Chair of Ecophysiology and Vegetation Ecology, University of Würzburg, Julius-von-Sachs-Platz 3, 97082, Würzburg, Germany

    Bernhard Schuldt

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Schumann, K., Leuschner, C. & Schuldt, B. Xylem hydraulic safety and efficiency in relation to leaf and wood traits in three temperate Acer species differing in habitat preferences. Trees 33, 1475–1490 (2019). https://doi.org/10.1007/s00468-019-01874-x

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