Drought tolerance traits do not vary across sites differing in water availability in Banksia serrata (Proteaceae)
Ximeng Li
A , Chris J. Blackman A , Brendan Choat A , Paul D. Rymer A , Belinda E. Medlyn A and David T. Tissue A B
+ Author Affiliations
- Author Affiliations
A Hawkesbury Institute for the Environment, Western Sydney University, Locked Bag 1797, Penrith, NSW 2751, Australia.
B Corresponding author. Email: d.tissue@westernsydney.edu.au
Functional Plant Biology 46(7) 624-633 https://doi.org/10.1071/FP18238
Submitted: 4 September 2018 Accepted: 23 February 2019 Published: 9 April 2019
Abstract
Interspecific variation in plant hydraulic traits plays a major role in shaping species distributions across climates, yet variation within species is poorly understood. Here we report on intraspecific variation of hydraulic traits in Banksia serrata (L.f.) sampled from three sites characterised by contrasting climates (warm-wet, warm-dry and cool-wet). Hydraulic characteristics including vulnerability to embolism, hydraulic conductance, pressure-volume traits and key morphological traits were measured. Vulnerability to embolism in leaf and stem, defined by the water potential inducing 50 and 88% loss of hydraulic conductivity (P50 and P88 respectively), did not differ across sites. However, plants from the warm-dry environment exhibited higher stem conductivity (Ks) than the cool-wet environment. Leaf turgor loss point (TLP) did not vary among sites, but warm-dry site plants showed lower leaf capacitance (C*FT) and higher modulus of elasticity (ε) than the other two sites. Plants from the cool-wet site had lower specific leaf area (SLA) and plants from the warm-dry site had lower sapwood density (WD). Overall, key hydraulic traits were generally conserved across populations despite differences in mean site water availability, and the safety-efficiency trade-off was absent in this species. These results suggest that B. serrata has limited ability to adjust hydraulic architecture in response to environmental change and thus may be susceptible to climate change-type drought stress.
Additional keywords: drought, embolism resistance, hydraulic conductivity, intraspecific variation, morphological traits, pressure–volume.
References
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. Ecology Letters 15, 393–405.| The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta-analysis.Crossref | GoogleScholarGoogle Scholar | 22435987PubMed |
Blackman CJ (2018) Leaf turgor loss as a predictor of plant drought response strategies. Tree Physiology 38, 655–657.
| Leaf turgor loss as a predictor of plant drought response strategies.Crossref | GoogleScholarGoogle Scholar | 29726963PubMed |
Blackman CJ, Aspinwall MJ, Tissue DT, Rymer PD (2017) Genetic adaptation and phenotypic plasticity contribute to greater leaf hydraulic tolerance in response to drought in warmer climates. Tree Physiology 37, 583–592.
| Genetic adaptation and phenotypic plasticity contribute to greater leaf hydraulic tolerance in response to drought in warmer climates.Crossref | GoogleScholarGoogle Scholar | 28338733PubMed |
Bradstock RA, Myerscough PJ (1988) The survival and population response to frequent fires of two woody resprouters Banksia serrata and Isopogon anemonifolius. Australian Journal of Botany 36, 415–431.
| The survival and population response to frequent fires of two woody resprouters Banksia serrata and Isopogon anemonifolius.Crossref | GoogleScholarGoogle Scholar |
Brodribb TJ, Cochard H (2009) Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiology 149, 575–584.
| Hydraulic failure defines the recovery and point of death in water-stressed conifers.Crossref | GoogleScholarGoogle Scholar | 19011001PubMed |
Brodribb TJ, Hill RS (1999) The importance of xylem constraints in the distribution of conifer species. New Phytologist 143, 365–372.
| The importance of xylem constraints in the distribution of conifer species.Crossref | GoogleScholarGoogle Scholar |
Brodribb TJ, Holbrook NM (2003) Stomatal closure during leaf dehydration, correlation with other leaf physiological traits. Plant Physiology 132, 2166–2173.
| Stomatal closure during leaf dehydration, correlation with other leaf physiological traits.Crossref | GoogleScholarGoogle Scholar | 12913171PubMed |
Canham CA, Froend RH, Stock WD (2009) Water stress vulnerability of four Banksia species in contrasting ecohydrological habitats on the Gnangara Mound, Western Australia. Plant, Cell & Environment 32, 64–72.
| Water stress vulnerability of four Banksia species in contrasting ecohydrological habitats on the Gnangara Mound, Western Australia.Crossref | GoogleScholarGoogle 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.
| Diversity of hydraulic traits in nine Cordia species growing in tropical forests with contrasting precipitation.Crossref | GoogleScholarGoogle Scholar | 17688584PubMed |
Choat B, Drayton WM, Brodersen C, Matthews MA, Shackel KA, Wada H, McElrone AJ (2010) Measurement of vulnerability to water stress-induced cavitation in grapevine: a comparison of four techniques applied to a long-vesseled species. Plant, Cell & Environment 33, 1502–1512.
Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Hacke UG (2012) Global convergence in the vulnerability of forests to drought. Nature 491, 752–755.
| Global convergence in the vulnerability of forests to drought.Crossref | GoogleScholarGoogle Scholar | 23172141PubMed |
Choat B, Badel E, Burlett R, Delzon S, Cochard H, Jansen S (2016) Non-invasive measurement of vulnerability to drought induced embolism by X-ray microtomography. Plant Physiology 170, 273–282.
| Non-invasive measurement of vulnerability to drought induced embolism by X-ray microtomography.Crossref | GoogleScholarGoogle Scholar | 26527655PubMed |
Choat B, Brodribb TJ, Brodersen CR, Duursma RA, López R, Medlyn BE (2018) Triggers of tree mortality under drought. Nature 558, 531–539.
| Triggers of tree mortality under drought.Crossref | GoogleScholarGoogle Scholar | 29950621PubMed |
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.
| Phenotypic plasticity in mesic populations of Pinus pinaster improves resistance to xylem embolism (P50) under severe drought.Crossref | GoogleScholarGoogle Scholar |
Dai A (2013) Increasing drought under global warming in observations and models. Nature Climate Change 3, 52–58.
| Increasing drought under global warming in observations and models.Crossref | GoogleScholarGoogle Scholar |
Duursma RA, Choat B (2017) fitplc: An R package to fit hydraulic vulnerability curves. The Journal of Plant Hydraulics 4, e002
| fitplc: An R package to fit hydraulic vulnerability curves.Crossref | GoogleScholarGoogle Scholar |
Farrell C, Szota C, Arndt SK (2017) Does the turgor loss point characterize drought response in dryland plants? Plant, Cell & Environment 40, 1500–1511.
| Does the turgor loss point characterize drought response in dryland plants?Crossref | GoogleScholarGoogle Scholar |
Freestone M, Wills TJ, Read J (2015) Post-fire succession during the long-term absence of fire in coastal heathland and a test of the chronosequence survey method. Australian Journal of Botany 63, 572–580.
| Post-fire succession during the long-term absence of fire in coastal heathland and a test of the chronosequence survey method.Crossref | GoogleScholarGoogle Scholar |
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.
| Shifts in leaf and stem hydraulic traits across aridity gradients in eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Gleason SM, Blackman CJ, Cook AM, Laws CA, Westoby M (2014) Whole-plant capacitance, embolism resistance and slow transpiration rates all contribute to longer desiccation times in woody angiosperms from arid and wet habitats. Tree Physiology 34, 275–284.
| Whole-plant capacitance, embolism resistance and slow transpiration rates all contribute to longer desiccation times in woody angiosperms from arid and wet habitats.Crossref | GoogleScholarGoogle Scholar | 24550089PubMed |
Gleason SM, Westoby M, Jansen S, Choat B, Hacke UG, Pratt RB, Bhaskar R, Brodribb TJ, Bucci SJ, Cao KF (2016) Weak tradeoff between xylem safety and xylem‐specific hydraulic efficiency across the world’s woody plant species. New Phytologist 209, 123–136.
| Weak tradeoff between xylem safety and xylem‐specific hydraulic efficiency across the world’s woody plant species.Crossref | GoogleScholarGoogle Scholar | 26378984PubMed |
González-Muñoz N, Sterck F, Torres-Ruiz J, Petit G, Cochard H, von Arx G, Lintunen A, Caldeira M, Capdeville G, Copini P (2018) Quantifying in situ phenotypic variability in the hydraulic properties of four tree species across their distribution range in Europe. PLoS One 13, e0196075
| Quantifying in situ phenotypic variability in the hydraulic properties of four tree species across their distribution range in Europe.Crossref | GoogleScholarGoogle Scholar | 29715289PubMed |
Johnson DM, Berry ZC, Baker KV, Smith DD, McCulloh KA, Domec JC (2018) Leaf hydraulic parameters are more plastic in species that experience a wider range of leaf water potentials. Functional Ecology 32, 894–903.
| Leaf hydraulic parameters are more plastic in species that experience a wider range of leaf water potentials.Crossref | GoogleScholarGoogle Scholar |
Jordan GJ, Brodribb TJ, Blackman CJ, Weston PH (2013) Climate drives vein anatomy in Proteaceae. American Journal of Botany 100, 1483–1493.
| Climate drives vein anatomy in Proteaceae.Crossref | GoogleScholarGoogle Scholar | 23935111PubMed |
Kavanagh K, Bond B, Aitken S, Gartner B, Knowe S (1999) Shoot and root vulnerability to xylem cavitation in four populations of Douglas-fir seedlings. Tree Physiology 19, 31–37.
| Shoot and root vulnerability to xylem cavitation in four populations of Douglas-fir seedlings.Crossref | GoogleScholarGoogle Scholar | 12651329PubMed |
Kolb KJ, Sperry JS (1999) Differences in drought adaptation between subspecies of sagebrush (Artemisia tridentata). Ecology 80, 2373–2384.
| Differences in drought adaptation between subspecies of sagebrush (Artemisia tridentata).Crossref | GoogleScholarGoogle Scholar |
Lamy JB, Lagane F, Plomion C, Cochard H, Delzon S (2012) Micro-evolutionary patterns of juvenile wood density in a pine species. Plant Ecology 213, 1781–1792.
| Micro-evolutionary patterns of juvenile wood density in a pine species.Crossref | GoogleScholarGoogle Scholar |
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.
| Limited genetic variability and phenotypic plasticity detected for cavitation resistance in a Mediterranean pine.Crossref | GoogleScholarGoogle Scholar | 24180459PubMed |
Larter M, Pfautsch S, Domec JC, Trueba S, Nagalingum N, Delzon S (2017) Aridity drove the evolution of extreme embolism resistance and the radiation of conifer genus Callitris. New Phytologist 215, 97–112.
| Aridity drove the evolution of extreme embolism resistance and the radiation of conifer genus Callitris.Crossref | GoogleScholarGoogle Scholar | 28378882PubMed |
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.
| Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer.Crossref | GoogleScholarGoogle Scholar | 21054413PubMed |
Lenz TI, Wright IJ, Westoby M (2006) Interrelations among pressure-volume curve traits across species and water availability gradients. Physiologia Plantarum 127, 423–433.
| Interrelations among pressure-volume curve traits across species and water availability gradients.Crossref | GoogleScholarGoogle Scholar |
Li X, Blackman CJ, Choat B, Duursma RA, Rymer PD, Medlyn BE, Tissue DT (2018a) Tree hydraulic traits are coordinated and strongly linked to climate‐of‐origin across a rainfall gradient. Plant, Cell & Environment 41, 646–660.
| Tree hydraulic traits are coordinated and strongly linked to climate‐of‐origin across a rainfall gradient.Crossref | GoogleScholarGoogle Scholar |
Li X, Blackman CJ, Rymer PD, Quintans D, Duursma RA, Choat B, Medlyn BE, Tissue DT (2018b) Xylem embolism measured retrospectively is linked to canopy dieback in natural populations of Eucalyptus piperita following drought. Tree Physiology 38, 1193–1199.
| Xylem embolism measured retrospectively is linked to canopy dieback in natural populations of Eucalyptus piperita following drought.Crossref | GoogleScholarGoogle Scholar | 29757423PubMed |
Liu YY, Wang AY, An YN, Lian PY, Wu DD, Zhu JJ, Meinzer FC, Hao GY (2018) Hydraulics play an important role in causing low growth rate and dieback of aging Pinus sylvestris var. mongolica trees in plantations of Northeast China. Plant, Cell & Environment 41, 1500–1511.
| Hydraulics play an important role in causing low growth rate and dieback of aging Pinus sylvestris var. mongolica trees in plantations of Northeast China.Crossref | GoogleScholarGoogle Scholar |
Lobo A, Torres-Ruiz JM, Burlett R, Lemaire C, Parise C, Francioni C, Truffaut L, Tomášková I, Hansen JK, Kjær ED (2018) Assessing inter- and intraspecific variability of xylem vulnerability to embolism in oaks. Forest Ecology and Management 424, 53–61.
| Assessing inter- and intraspecific variability of xylem vulnerability to embolism in oaks.Crossref | GoogleScholarGoogle Scholar | 29910530PubMed |
López R, Cano FJ, Choat B, Cochard H, Gil L (2016) Plasticity in vulnerability to cavitation of Pinus canariensis occurs only at the driest end of an aridity gradient. Frontiers of Plant Science 7, 769
| Plasticity in vulnerability to cavitation of Pinus canariensis occurs only at the driest end of an aridity gradient.Crossref | GoogleScholarGoogle Scholar |
Maherali H, DeLucia EH (2000) Xylem conductivity and vulnerability to cavitation of ponderosa pine growing in contrasting climates. Tree Physiology 20, 859–867.
| Xylem conductivity and vulnerability to cavitation of ponderosa pine growing in contrasting climates.Crossref | GoogleScholarGoogle Scholar | 11303576PubMed |
Maherali H, Pockman WT, Jackson RB (2004) Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology 85, 2184–2199.
| Adaptive variation in the vulnerability of woody plants to xylem cavitation.Crossref | GoogleScholarGoogle 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 & Environment 34, 137–148.
| Ecological differentiation in xylem cavitation resistance is associated with stem and leaf structural traits.Crossref | GoogleScholarGoogle Scholar |
Martin‐StPaul N, Delzon S, Cochard H (2017) Plant resistance to drought depends on timely stomatal closure. Ecology Letters 20, 1437–1447.
| Plant resistance to drought depends on timely stomatal closure.Crossref | GoogleScholarGoogle Scholar | 28922708PubMed |
Matusick G, Ruthrof KX, Brouwers NC, Dell B, Hardy GSJ (2013) Sudden forest canopy collapse corresponding with extreme drought and heat in a mediterranean-type eucalypt forest in southwestern Australia. European Journal of Forest Research 132, 497–510.
| Sudden forest canopy collapse corresponding with extreme drought and heat in a mediterranean-type eucalypt forest in southwestern Australia.Crossref | GoogleScholarGoogle Scholar |
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 & Environment 37, 2577–2586.
| Dynamics of leaf water relations components in co‐occurring iso‐and anisohydric conifer species.Crossref | GoogleScholarGoogle Scholar |
Mencuccini M, Grace J (1995) Climate influences the leaf area/sapwood area ratio in Scots pine. Tree Physiology 15, 1–10.
| Climate influences the leaf area/sapwood area ratio in Scots pine.Crossref | GoogleScholarGoogle Scholar | 14966005PubMed |
Mitchell PJ, O’Grady AP (2015) Adaptation of leaf water relations to climatic and habitat water availability. Forests 6, 2281–2295.
| Adaptation of leaf water relations to climatic and habitat water availability.Crossref | GoogleScholarGoogle Scholar |
Nadal M, Flexas J, Gulías J (2018) Possible link between photosynthesis and leaf modulus of elasticity among vascular plants: a new player in leaf traits relationships? Ecology Letters 21, 1372–1379.
| Possible link between photosynthesis and leaf modulus of elasticity among vascular plants: a new player in leaf traits relationships?Crossref | GoogleScholarGoogle Scholar | 30027556PubMed |
Niinemets Ü (2001) Global‐scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology 82, 453–469.
| Global‐scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs.Crossref | GoogleScholarGoogle Scholar |
Pfautsch S, Harbusch M, Wesolowski A, Smith R, Macfarlane C, Tjoelker MG, Reich PB, Adams MA (2016) Climate determines vascular traits in the ecologically diverse genus Eucalyptus. Ecology Letters 19, 240–248.
| Climate determines vascular traits in the ecologically diverse genus Eucalyptus.Crossref | GoogleScholarGoogle Scholar | 26743135PubMed |
Pivovaroff AL, Sack L, Santiago LS (2014) Coordination of stem and leaf hydraulic conductance in southern California shrubs: a test of the hydraulic segmentation hypothesis. New Phytologist 203, 842–850.
| Coordination of stem and leaf hydraulic conductance in southern California shrubs: a test of the hydraulic segmentation hypothesis.Crossref | GoogleScholarGoogle Scholar | 24860955PubMed |
Pockman WT, Sperry JS (2000) Vulnerability to xylem cavitation and the distribution of Sonoran desert vegetation. American Journal of Botany 87, 1287–1299.
| Vulnerability to xylem cavitation and the distribution of Sonoran desert vegetation.Crossref | GoogleScholarGoogle Scholar | 10991900PubMed |
Poorter H, Niinemets Ü, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta‐analysis. New Phytologist 182, 565–588.
| Causes and consequences of variation in leaf mass per area (LMA): a meta‐analysis.Crossref | GoogleScholarGoogle Scholar | 19434804PubMed |
Russo SE, Jenkins KL, Wiser SK, Uriarte M, Duncan RP, Coomes DA (2010) Interspecific relationships among growth, mortality and xylem traits of woody species from New Zealand. Functional Ecology 24, 253–262.
| Interspecific relationships among growth, mortality and xylem traits of woody species from New Zealand.Crossref | GoogleScholarGoogle Scholar |
Santiago LS, De Guzman ME, Baraloto C, Vogenberg JE, Brodie M, Hérault B, Fortunel C, Bonal D (2018) Coordination and trade‐offs among hydraulic safety, efficiency and drought avoidance traits in Amazonian rainforest canopy tree species. New Phytologist 218, 1015–1024.
| Coordination and trade‐offs among hydraulic safety, efficiency and drought avoidance traits in Amazonian rainforest canopy tree species.Crossref | GoogleScholarGoogle Scholar | 29457226PubMed |
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 Phytologist 210, 443–458.
| How adaptable is the hydraulic system of European beech in the face of climate change‐related precipitation reduction?Crossref | GoogleScholarGoogle Scholar | 26720626PubMed |
Schultz HR, Matthews MA (1993) Xylem development and hydraulic conductance in sun and shade shoots of grapevine (Vitis vinifera L.): evidence that low light uncouples water transport capacity from leaf area. Planta 190, 393–406.
| Xylem development and hydraulic conductance in sun and shade shoots of grapevine (Vitis vinifera L.): evidence that low light uncouples water transport capacity from leaf area.Crossref | GoogleScholarGoogle Scholar |
Scoffoni C, Vuong C, Diep S, Cochard H, Sack L (2014) Leaf shrinkage with dehydration: coordination with hydraulic vulnerability and drought tolerance. Plant Physiology 164, 1772–1788.
| Leaf shrinkage with dehydration: coordination with hydraulic vulnerability and drought tolerance.Crossref | GoogleScholarGoogle Scholar | 24306532PubMed |
Sperry JS, Donnelly JR, Tyree MT (1988) A method for measuring hydraulic conductivity and embolism in xylem. Plant, Cell & Environment 11, 35–40.
| A method for measuring hydraulic conductivity and embolism in xylem.Crossref | GoogleScholarGoogle Scholar |
Stojnić S, Suchocka M, Benito-Garzón M, Torres-Ruiz JM, Cochard H, Bolte A, Cocozza C, Cvjetković B, De Luis M, Martinez-Vilalta J, Ræbild A (2018) Variation in xylem vulnerability to embolism in European beech from geographically marginal populations. Tree Physiology 38, 173–185.
| Variation in xylem vulnerability to embolism in European beech from geographically marginal populations.Crossref | GoogleScholarGoogle Scholar | 29182720PubMed |
Torres-Ruiz JM, Jansen S, Choat B, McElrone AJ, Cochard H, Brodribb TJ, Badel E, Burlett R, Bouche PS, Brodersen CR (2015) Direct X-ray microtomography observation confirms the induction of embolism upon xylem cutting under tension. Plant Physiology 167, 40–43.
| Direct X-ray microtomography observation confirms the induction of embolism upon xylem cutting under tension.Crossref | GoogleScholarGoogle Scholar | 25378693PubMed |
Trueba S, Pouteau R, Lens F, Feild TS, Isnard S, Olson ME, Delzon S (2017) Vulnerability to xylem embolism as a major correlate of the environmental distribution of rain forest species on a tropical island. Plant, Cell & Environment 40, 277–289.
| Vulnerability to xylem embolism as a major correlate of the environmental distribution of rain forest species on a tropical island.Crossref | GoogleScholarGoogle Scholar |
Tyree M, Hammel H (1972) The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique. Journal of Experimental Botany 23, 267–282.
| The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique.Crossref | GoogleScholarGoogle 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 Physiology 33, 672–683.
| Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees.Crossref | GoogleScholarGoogle Scholar | 23658197PubMed |
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.
| Genotypic variability and phenotypic plasticity of cavitation resistance in Fagus sylvatica L. across Europe.Crossref | GoogleScholarGoogle Scholar | 21989814PubMed |
Zhu SD, Liu H, Xu QY, Cao KF, Ye Q (2016) Are leaves more vulnerable to cavitation than branches? Functional Ecology 30, 1740–1744.
| Are leaves more vulnerable to cavitation than branches?Crossref | GoogleScholarGoogle Scholar |
Zimmermann MH (1983) ‘Xylem structure and the ascent of sap.’ (Springer: Berlin)
