Quantifying in situ phenotypic variability in the hydraulic properties of four tree species across their distribution range in Europe
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
29715289
PubMed Central
PMC5929519
DOI
10.1371/journal.pone.0196075
PII: PONE-D-17-25371
Knihovny.cz E-zdroje
- MeSH
- fenotyp MeSH
- lesy MeSH
- období sucha * MeSH
- podnebí MeSH
- stromy klasifikace fyziologie MeSH
- voda * MeSH
- xylém fyziologie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Evropa MeSH
- Názvy látek
- voda * MeSH
Many studies have reported that hydraulic properties vary considerably between tree species, but little is known about their intraspecific variation and, therefore, their capacity to adapt to a warmer and drier climate. Here, we quantify phenotypic divergence and clinal variation for embolism resistance, hydraulic conductivity and branch growth, in four tree species, two angiosperms (Betula pendula, Populus tremula) and two conifers (Picea abies, Pinus sylvestris), across their latitudinal distribution in Europe. Growth and hydraulic efficiency varied widely within species and between populations. The variability of embolism resistance was in general weaker than that of growth and hydraulic efficiency, and very low for all species but Populus tremula. In addition, no and weak support for a safety vs. efficiency trade-off was observed for the angiosperm and conifer species, respectively. The limited variability of embolism resistance observed here for all species except Populus tremula, suggests that forest populations will unlikely be able to adapt hydraulically to drier conditions through the evolution of embolism resistance.
BIOGECO INRA Université de Bordeaux Pessac France
Climatic Change and Climate Impacts Institute for Environmental Sciences Geneva Switzerland
Department of Forest Sciences University of Helsinki Helsinki Finland
Forest Research Centre School of Agriculture University of Lisbon Tapada da Ajuda Lisboa Portugal
Natural Resources Institute Finland Latokartanonkaari 9 Helsinki Finland
PIAF INRA Université Clermont Auvergne Clermont Ferrand France
Swiss Federal Institute for Forest Snow and Landscape Research WSL Birmensdorf Switzerland
Swiss Federal Institute of Technology ETH Planning of Landscape and Urban Systems Zurich Switzerland
Università degli Studi di Padova Dep TeSAF Legnaro Italy
Wageningen Environmental Research Wageningen The Netherlands
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Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, et al. (2010) A global overview of drought and heat induced tree mortality reveals emerging climate change risks for forests. For Ecol Manage 259:660–684.
van Mantgem PJ, Stephenson NL, Byrne JC, Daniels LD, Franklin JF, Fulé PZ, et al. (2009) Widespread increase of tree mortality rates in the western United States. Science 323:521–524. doi: 10.1126/science.1165000 PubMed DOI
Carnicer J, Coll M, Ninyerola M, Pons X, Sánchez G, Peñuelas J (2011) Widespread crown condition decline, food web disruption, and amplified tree mortality with increased climate change-type drought. PNAS 108:1474–1478. doi: 10.1073/pnas.1010070108 PubMed DOI PMC
Peng C, Ma Z, Lei X, Zhy Q, Chen H, Wang W, et al. (2011) A drought-induced pervasive increase in tree mortality across Canada’s boreal forests. Nat Clim Change 1:467–471.
Heres AM, Voltas J, Lopez BC, Claramunt B, Martínez-Vilata J (2014) Drought-induced mortality selectively affects Scots pine trees that show limited intrinsic water-use efficiency responsiveness to rising atmospheric CO2. Funct Plant Biol 41(3):244–256. PubMed
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, Cambridge.
Benito-Garzón M, Ruiz-Benito P, Zavala MA (2013) Interspecific differences in tree growth and mortality responses to environmental drivers determine potential species distributional limits in Iberian forests. Global Ecol Biogeogr 22:1141–1151.
Anderegg WRL, Flint A, Huang Ch, Flint L, Berry JA, Davis FW, et al. (2015) Tree mortality predicted from drought-induced vascular damage. Nat Geosci 8:367–371.
Salmon Y, Torres-Ruiz JM, Poyatos R, Martínez-Vilalta J, Meir P, Cochard H, et al. (2015) Balancing the risks of hydraulic failure and carbon starvation: a twig scale analysis in declining Scots pine. Plant Cell Environ 38:2575–2588. doi: 10.1111/pce.12572 PubMed DOI PMC
Anderegg WRL, Klein T, Bartlett M, Sack L, Pellegrini AF, Choat B, et al. (2016) Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe. PNAS 113(18):5024–5029. doi: 10.1073/pnas.1525678113 PubMed DOI PMC
Sperry JS, Tyree MT (1990) Water-stress-induced xylem embolism in three species of conifers. Plant Cell Environ 13:427–43.
Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent of sap Springer, Berlin
Brodribb TJ, Cochard H (2009) Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiol 149:575–584. doi: 10.1104/pp.108.129783 PubMed DOI PMC
Urli M, Porte A, Cochard H, Guengant Y, Burlett R, Delzon S (2013) Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees. Tree Physiol 33(7):672–683. doi: 10.1093/treephys/tpt030 PubMed DOI
Delzon S, Cochard H (2014) Recent advances in tree hydraulics highlight the ecological significance of the hydraulic safety margin. New Phytol 203:355–358. doi: 10.1111/nph.12798 PubMed DOI
Gleason SM, Westoby M, Jansen S, Choat B, Hacke UG, Pratt RB, et al. (2015) Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world’s woody plant species. New Phytol 209:123–136. doi: 10.1111/nph.13646 PubMed DOI
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 Environ 33(12):2101–2111. doi: 10.1111/j.1365-3040.2010.02208.x PubMed DOI PMC
Pittermann J, Choat B, Jansen S, Stuart SA, Lynn L, Dawson TE (2010) Relationships between xylem safety and hydraulic efficiency in the Cupressaceae: the evolution of pit membrane form and function. Plant Physiol 153:1919–1931. doi: 10.1104/pp.110.158824 PubMed DOI PMC
Bouche PF, Larter M, Domec JC, Burlett R, Gasson P, Jansen S, Delzon S (2014) A broad survey of xylem hydraulic safety and efficiency in conifers. J Exp Bot 65:4419–4431. doi: 10.1093/jxb/eru218 PubMed DOI PMC
Sperry JS, Hacke UG, Pittermann J (2006) Size and function in conifer tracheids and angiosperm vessels. Am J Bot 93(10):1490–1500. doi: 10.3732/ajb.93.10.1490 PubMed DOI
Choat B, Cobb AR, Jansen S (2008) Tansley Review: Structure and function of bordered pits: new discoveries and impacts on whole plant hydraulic function. New Phytol 177:608–625. doi: 10.1111/j.1469-8137.2007.02317.x PubMed DOI
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. doi: 10.1111/j.1469-8137.2010.03518.x PubMed DOI
Li S, Lens F, Espino S, Karimi Z, Klepsch M, 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(2):152–171.
Sperry JS, Hacke UG, Wheeler JK (2005) Comparative analysis of end wall resistance in xylem conduits. Plant Cell Environ 28:456–465.
Christman MA, Sperry JS (2010) Single-vessel flow measurements indicate scalariform perforation plates confer higher flow resistance than previously estimated. Plant Cell Environ 33:431–443. doi: 10.1111/j.1365-3040.2009.02094.x PubMed DOI
Maherali H, Pockman WT, Jackson RB (2004) Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology 85(8):2184–2199.
Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, et al. (2012) Global convergence in the vulnerability of forests to drought. Nature 491:752–755. doi: 10.1038/nature11688 PubMed DOI
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 1–12. PubMed
Valladares F, Gianoli E, Gómez JM (2007) Ecological limits to plant phenotypic plasticity. New Phytol 176(4):749–763. doi: 10.1111/j.1469-8137.2007.02275.x PubMed DOI
Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan E, Mathesius U, Poot P, Purugganan MD, Richards C, Valladares F (2010) Plant phenotypic plasticity in a changing climate. Trends Plant Sci 15: 684–692. doi: 10.1016/j.tplants.2010.09.008 PubMed DOI
Lindner M, Maroschek M, Netherer S, Kremer A, Barbati A, Garcia-Gonzalo J, Seidl R, Delzon S, Corona P, Kolstrom M, Lexer MJ, Marchetti M (2010) Climate change impacts, adaptive capacity, and vulnerability of European forest ecosystems. For Ecol Manag 259:698–709.
Alberto F, Bouffier L, Louvet JM, Lamy JB, Delzon S, Kremer A (2011) Adaptive responses for seed and leaf phenology in natural populations of sessile oak along an altitudinal gradient. J Evol Biol 24(7):1442–1454. doi: 10.1111/j.1420-9101.2011.02277.x PubMed DOI
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 Physiol 31(11):1164–1174. doi: 10.1093/treephys/tpr084 PubMed DOI
Martínez-Vilalta J, Cochard H, Mencuccini M, Sterck F, Herrero A, Korhonen JFJ, Llorens 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(2):353–364. doi: 10.1111/j.1469-8137.2009.02954.x PubMed DOI
Corcuera L, Cochard H, Gil-Pelegrin E, Notivol E (2011) Phenotypic plasticity in mesic populations of Pinus pinaster improves resistance to embolism (P50) under severe drought. Trees (25):1033–1042.
Wortemann R, Herbette S, Barigah TS, Fumanal B, Alia R, Ducousso A, et al. (2011) Genotypic variability and phenotypic plasticity of cavitation resistance in Fagus sylvatica L. across Europe. Tree Physiol 31:1175–1182. doi: 10.1093/treephys/tpr101 PubMed DOI
Lamy JB, Bouffier L, Burlett R, Plomion Ch, Cochard H, Delzon S (2011) Uniform selection as a primary force reducing population genetic differentiation of cavitation resistance across a species range. Plos One (8):e23476 doi: 10.1371/journal.pone.0023476 PubMed DOI PMC
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 Phytol 201:874–886. doi: 10.1111/nph.12556 PubMed DOI
Anderegg WRL (2015) Spatial and temporal variation in plant hydraulic traits and their relevance for climate change impacts on vegetation. New Phytol 205(3):1008–1014. PubMed
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Clim 25:1965–1978.
Zimmermann NE, Roberts DW (2001) Final Report of the MLP climate and biophysical mapping project, Birmensdorf.
Torres-Ruiz JM, Cochard H, Choat B, Jansen S, López R, Tomášková I, et al. (2017) Xylem resistance to embolism: presenting a simple diagnostic test for the open vessel artefact. New Phytol 215:489–499. doi: 10.1111/nph.14589 PubMed DOI
Cochard H (2002) A technique for measuring xylem hydraulic conductance under high negative pressures. Plant, Cell and Environment 25:815–819.
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 Plantarum 124:410–418.
Pammenter NW, Vander Willigen C (1998) A mathematical and statistical analysis of the curves illustrating vulnerability of xylem to cavitation. Tree Physiol 18:589–59. PubMed
Weiskittel AR, Maguire DA, Monserud RA (2007) Response of branch growth and mortality to silvicultural treatments in coastal Douglas-fir plantations: Implications for predicting tree growth. For Ecol Manage 251:182–194.
R Development Core Team (2016) R: A Language and Environment for Statistical Computing R Foundation for Statistical Computing, Vienna.
Yang S, Tyree MT (1993) Hydraulic resistance in the shoots of Acer saccharum and its influence on leaf water potential and transpiration. Tree Physiol 12:231–242. PubMed
Petit G, Anfodillo T, Mencuccini M (2008) Tapering of xylem conduits and hydraulic limitations in sycamore (Acer pseudoplatanus) trees. New Phytol 177(3):653–64. doi: 10.1111/j.1469-8137.2007.02291.x PubMed DOI
Makinen H, Saranpaa P, Linder S (2001) Effect of nutrient optimization on branch characteristics in Picea abies. Scand J Forest Res 16:354–362.
Makinen H (2002) Effect of stand density on the branch development of silver birch (Betula pendula Roth.) in central Finland. Trees Struct Funct 16:346–353.
Hatfield JL, Prueger JH (2015) Temperature extremes: Effect on plant growth and development. Weather Climate Extremes 10(A):4–10.
Lipiec J, Doussan C, Nosalewicz A, Kondracka K (2013) Effect of drought and heat stresses on plant growth and yield: a review. Int Agrophys 27(4):463–477.
Makinen H (1999) Effect of stand density on radial growth of branches of Scots pine in southern and central Finland. Can J Forest Res 29:1216–1224.
Stojnić S, Suchocka M, Benito-Garzón M, Torres-Ruiz JM, Cochard H, Bolte A, et al. (2017) Variation in xylem vulnerability to embolism in European beech from geographically marginal populations. Tree Physiol in press. PubMed
Mencuccini M, Comstock J (1997) Vulnerability to cavitation in populations of two desert species, Hymenoclea salsola and Ambrosia dumosa, from different climatic regions. J Exp Botany 48:1323–1334.
Vander Willigen C, Pammenter NW (1998) Relationship between growth and xylem hydraulic characteristics of clones of Eucalyptus spp. at contrasting sites. Tree Physiol 18: 595–600. PubMed
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(2):443–458. doi: 10.1111/nph.13798 PubMed DOI
Maherali H, De Lucia EH (2000) Xylem conductivity and vulnerability to cavitation of ponderosa pine growing in contrasting climates. Tree Physiol 20:859–867. PubMed
Martínez-Vilalta J, Piñol J (2002) Drought-induced mortality and hydraulic architecture in pine populations of the NE Iberian Peninsula. For Ecol Manage 161: 247–256.
Cornwell WK, Bhaskar R, Sack L, Cordell D, Lunch CK (2007) Adjustment of structure and function of Hawaiian Metrosideros polymorpha at high vs. low precipitation. Funct Ecol 21:1063–1071.
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 doi: 10.3389/fpls.2016.00791 PubMed DOI PMC
Ahmad HB, Lens F, Capdeville G, Burlett R, Lamarque LJ, Delzon S (2017) Intraspecific variation in embolism resistance and stem anatomy across four sunflower (Helianthus annuus L.) accessions. Physiol Plant in press. PubMed
Lexer C, Fay M, Joseph J, Nica MS, Heinze B (2005) Barrier to gene flow between two ecologically divergent Populus species, P. alba (white poplar) and P. tremula (European aspen): the role of ecology and life history in gene introgression. Mol Ecol 14: 1045–1057. doi: 10.1111/j.1365-294X.2005.02469.x PubMed DOI
Lexer C, Joseph J, van Loo M, Prenner G, Heinze B, Chase MW, et al. (2009) The use of digital image-based morphometrics to study the phenotypic mosaic in taxa with porous genomes. Taxon 58:349–364.
Delzon S, Sartore M, Burlett R, Dewar R, Loustau D (2004) Hydraulic responses to height growth in maritime pine trees. Plant Cell Environ 27(9):1077–1087.
Quantitative vessel mapping on increment cores: a critical comparison of image acquisition methods
Dryad
10.5061/dryad.b2pg468