Xylem as the main origin of stem radius changes in Eucalyptus
Roman Zweifel A B D , David M. Drew B , Fritz Schweingruber A and Geoffrey M. Downes B C
+ Author Affiliations
- Author Affiliations
A Swiss Federal Institute for Forest, Snow and Landscape Research WSL, Zuercherstrasse 111, CH-8903 Birmensdorf, Switzerland.
B CSIRO Ecosystem Sciences, Private Bag 12, Hobart, Tas. 7001, Australia.
C Forest Quality Pty Ltd PO Box 293 Huonville, Tas. 7109, Australia.
D Corresponding author. Email: roman.zweifel@natkon.ch
Functional Plant Biology 41(5) 520-534 https://doi.org/10.1071/FP13240
Submitted: 8 August 2013 Accepted: 8 December 2013 Published: 13 January 2014
Abstract
The state-of-the-art interpretation of stem radius changes (DRTotal) for tree water relations is based on knowledge from mostly slow growing tree species. The ratio between diurnal size fluctuations of the rigid xylem (DRXylem) and the respective fluctuations of the elastic bark (DRBark) is known to be small (<0.4) and is of importance for the localisation of water storage dynamics in stems. In this study, fast growing Eucalyptus globulus Labill. in Tasmania were investigated by point dendrometers in order to investigate tree water relations. Unexpectedly, DRXylem was found to be the main driver of DRTotal with the bark acting as a passive layer on top of the fluctuating xylem under most conditions. Accordingly, the ratio between the diurnal fluctuations of the two tissues was found to be much higher (0.6–1.6) than everything reported before. Based on simulations using a hydraulic plant model, the high tissue-specific elasticity of the Eucalyptus xylem was found to explain this atypical response and not osmotically-driven processes or species-specific flow resistances. The wide zone of secondary thickening xylem in various stages of lignification is proposed to be an important component of the high wood elasticity. The tissue acts as additional water storage like the bark and may positively affect the water transport efficiency.
Additional keywords: bark, cambial activity, Eucalyptus globulus, Larix decidua, lignification, phloem, point dendrometer, stem size fluctuations, Tasmania, hydraulic plant model, tree rings, tree water relations, water tension, wood growth.
References
Daudet FA, Ameglio T, Cochard H, Archilla O, Lacointe A (2005) Experimental analysis of the role of water and carbon in tree stem diameter variations. Journal of Experimental Botany 56, 135–144.De Pauw DJW, Steppe K, De Baets B (2008a) Identifiability analysis and improvement of a tree water flow and storage model. Mathematical Biosciences 211, 314–332.
| Identifiability analysis and improvement of a tree water flow and storage model.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1c%2FlvFCrtQ%3D%3D&md5=8be6953e0c0dcbd8c29814c59728deacCAS |
De Pauw DJW, Steppe K, De Baets B (2008b) Unravelling the output uncertainty of a tree water flow and storage model using several global sensitivity analysis methods. Biosystems Engineering 101, 87–99.
| Unravelling the output uncertainty of a tree water flow and storage model using several global sensitivity analysis methods.Crossref | GoogleScholarGoogle Scholar |
De Schepper V, Steppe K (2010) Development and verification of a water and sugar transport model using measured stem diameter variations. Journal of Experimental Botany 61, 2083–2099.
| Development and verification of a water and sugar transport model using measured stem diameter variations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmsVGgu7k%3D&md5=2f09b107048b106c401759a3a8ba1bf4CAS | 20176887PubMed |
De Schepper V, Steppe K (2011) Tree girdling responses simulated by a water and carbon transport model. Annals of Botany 108, 1147–1154.
| Tree girdling responses simulated by a water and carbon transport model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlGiur7N&md5=9ca8eade4849a315134552fbe2447130CAS | 21478174PubMed |
De Schepper V, van Dusschoten D, Copini P, Jahnke S, Steppe K (2012) MRI links stem water content to stem diameter variations in transpiring trees. Journal of Experimental Botany 63, 2645–2653.
| MRI links stem water content to stem diameter variations in transpiring trees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmvF2rsLY%3D&md5=225755821aa7787e71dd5393b9e1b702CAS | 22268159PubMed |
Deslauriers A, Morin H, Urbinati C, Carrer M (2003) Daily weather response of balsam fir (Abies balsamea (L.) Mill.) stem radius increment from dendrometer analysis in the boreal forests of Quebec (Canada). Trees – Structure and Function 17, 477–484.
| Daily weather response of balsam fir (Abies balsamea (L.) Mill.) stem radius increment from dendrometer analysis in the boreal forests of Quebec (Canada).Crossref | GoogleScholarGoogle Scholar |
Dixon HH, Joly J (1895) On the ascent of sap. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 186, 563–576.
| On the ascent of sap.Crossref | GoogleScholarGoogle Scholar |
Downes G, Beadle C, Worledge D (1999a) Daily stem growth patterns in irrigated Eucalyptus globulus and E. nitens in relation to climate. Trees – Structure and Function 14, 102–111.
Downes GM, Beadle C, Gensler W, Mummery D, Worledge D (1999b) Diurnal variation and radial growth of stems in young plantation eucalypts. In ‘Tree ring analysis: biological, methodological and environmental aspects’. (Eds R Wimmer, RE Vetter) pp. 83–103. (CABI Publishing Series: University of California)
Downes GM, Drew D, Battaglia M, Schulze D (2009) Measuring and modelling stem growth and wood formation: an overview. Dendrochronologia 27, 147–157.
| Measuring and modelling stem growth and wood formation: an overview.Crossref | GoogleScholarGoogle Scholar |
Drew DM, Pammenter NW (2007) Developmental rates and morphological properties of fibres in two eucalypt clones at sites differing in water availability. Southern Hemisphere Forestry Journal 69, 71–79.
| Developmental rates and morphological properties of fibres in two eucalypt clones at sites differing in water availability.Crossref | GoogleScholarGoogle Scholar |
Drew DM, O’Grady AP, Downes GM, Read J, Worledge D (2008) Daily patterns of stem size variation in irrigated and unirrigated Eucalyptus globulus. Tree Physiology 28, 1573–1581.
| Daily patterns of stem size variation in irrigated and unirrigated Eucalyptus globulus.Crossref | GoogleScholarGoogle Scholar | 18708339PubMed |
Drew DM, Downes GM, Battaglia M (2010) CAMBIUM, a process-based model of daily xylem development in Eucalyptus. Journal of Theoretical Biology 264, 395–406.
| CAMBIUM, a process-based model of daily xylem development in Eucalyptus.Crossref | GoogleScholarGoogle Scholar | 20167220PubMed |
Drew DM, Richards AE, Downes GM, Cook GD, Baker P (2011) The development of seasonal tree water deficit in Callitris intratropica. Tree Physiology 31, 953–964.
| The development of seasonal tree water deficit in Callitris intratropica.Crossref | GoogleScholarGoogle Scholar | 21558386PubMed |
Ehrenberger W, Rüger S, Fitzke R, Vollenweider P, Günthardt-Goerg M, Kuster T, Zimmermann U, Arend M (2012) Concomitant dendrometer and leaf patch pressure probe measurements reveal the effect of microclimate and soil moisture on diurnal stem water and leaf turgor variations in young oak trees. Functional Plant Biology 39, 297–305.
| Concomitant dendrometer and leaf patch pressure probe measurements reveal the effect of microclimate and soil moisture on diurnal stem water and leaf turgor variations in young oak trees.Crossref | GoogleScholarGoogle Scholar |
Etzold S, Ruehr NK, Zweifel R, Dobbertin M, Zingg A, Pluess P, Häsler R, Eugster W, Buchmann N (2011) The carbon balance of two contrasting mountain forest ecosystems in Switzerland: similar annual trends, but seasonal differences. Ecosystems 14, 1289–1309.
| The carbon balance of two contrasting mountain forest ecosystems in Switzerland: similar annual trends, but seasonal differences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFaitL%2FK&md5=a784d36a4868dd7c2949821f6f19465bCAS |
Gričar J, Čufar K (2008) Seasonal dynamics of phloem and xylem formation in silver fir and Norway spruce as affected by drought. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 55, 538–543.
| Seasonal dynamics of phloem and xylem formation in silver fir and Norway spruce as affected by drought.Crossref | GoogleScholarGoogle Scholar |
Gričar J, Zupančič M, Čufar K, Oven P (2007) Regular cambial activity and xylem and phloem formation in locally heated and cooled stem portions of Norway spruce. Wood Science and Technology 41, 463–475.
| Regular cambial activity and xylem and phloem formation in locally heated and cooled stem portions of Norway spruce.Crossref | GoogleScholarGoogle Scholar |
Gričar J, Krže L, Čufar K (2009) Number of cells in xylem, phloem and dormant cambium in silver fir (Abies alba), in trees of different vitality. IAWA Journal 30, 121–133.
| Number of cells in xylem, phloem and dormant cambium in silver fir (Abies alba), in trees of different vitality.Crossref | GoogleScholarGoogle Scholar |
Honeysett JL, Beadle CL, Turnbull CRA (1992) Evapotranspiration and growth of 2 contrasting species of eucalypts under nonlimiting and limiting water availability. Forest Ecology and Management 50, 203–216.
| Evapotranspiration and growth of 2 contrasting species of eucalypts under nonlimiting and limiting water availability.Crossref | GoogleScholarGoogle Scholar |
Hunt R, Running SW, Federer CA (1991) Extrapolating plant water flow resistances and capacitances to regional scales. Agricultural and Forest Meteorology 54, 169–195.
| Extrapolating plant water flow resistances and capacitances to regional scales.Crossref | GoogleScholarGoogle Scholar |
Irvine J, Grace J (1997) Continuous measurements of water tensions in the xylem of tree based on the elastic properties of wood. Planta 202, 455–461.
| Continuous measurements of water tensions in the xylem of tree based on the elastic properties of wood.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXltFyjt7w%3D&md5=5947c6beb4ec37ea2e355856dc277f08CAS |
Johnson DM, McCulloh KA, Woodruff DR, Meinzer FC (2012) Evidence for xylem embolism as a primary factor in dehydration-induced declines in leaf hydraulic conductance. Plant, Cell & Environment 35, 760–769.
| Evidence for xylem embolism as a primary factor in dehydration-induced declines in leaf hydraulic conductance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmtFWls7k%3D&md5=7b46664cdef3b405ed8f2131937c6754CAS |
King G, Fonti P, Nievergelt D, Buentgen U, Frank D (2013) Climatic drivers of hourly to yearly tree radius variations along a 6 degrees C natural warming gradient. Agricultural and Forest Meteorology 168, 36–46.
| Climatic drivers of hourly to yearly tree radius variations along a 6 degrees C natural warming gradient.Crossref | GoogleScholarGoogle Scholar |
Kozlowski TT, Winget CH (1964) Diurnal and seasonal variation in radii of tree stems. Ecology 45, 149–155.
| Diurnal and seasonal variation in radii of tree stems.Crossref | GoogleScholarGoogle Scholar |
Lockhart JA (1965) An analysis of irreversible plant cell elongation. Journal of Theoretical Biology 8, 264–275.
| An analysis of irreversible plant cell elongation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF2s7jvFyhsg%3D%3D&md5=19216c3e511036e23f45d4884ccc20c0CAS | 5876240PubMed |
Mencuccini M, Holtta T (2010) The significance of phloem transport for the speed with which canopy photosynthesis and belowground respiration are linked. New Phytologist 185, 189–203.
| The significance of phloem transport for the speed with which canopy photosynthesis and belowground respiration are linked.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpvFKmtg%3D%3D&md5=8cd1a2b03543f408c6f2c89e5c12c790CAS | 19825019PubMed |
Mencuccini M, Hölttä T, Sevanto S, Nikinmaa E (2013) Concurrent measurements of change in the bark and xylem diameters of trees reveal a phloem-generated turgor signal. New Phytologist 198, 1143–1154.
| Concurrent measurements of change in the bark and xylem diameters of trees reveal a phloem-generated turgor signal.Crossref | GoogleScholarGoogle Scholar | 23517018PubMed |
Milburn JA (1996) Sap ascent in vascular plants: challengers to the cohesion theory ignore the significance of immature xylem and the recycling of Munch water. Annals of Botany 78, 399–407.
| Sap ascent in vascular plants: challengers to the cohesion theory ignore the significance of immature xylem and the recycling of Munch water.Crossref | GoogleScholarGoogle Scholar |
Milne R, Young P (1985) ‘Modelling of water movement in trees.’ (IAFC Identification and System Parameter Estimation: York, UK)
Molz FJ, Klepper B (1973) On the mechanism of water-stress-induced stem deformation. Agronomy Journal 65, 304–306.
| On the mechanism of water-stress-induced stem deformation.Crossref | GoogleScholarGoogle Scholar |
Oertli JJ (1989) The plant cell’s resistance to consequences of negative turgor pressure. In ‘Structural and functional responses to environmental stress’. (Eds KH Kreeb, H Richter, TM Hinckley.) pp. 73–88. (SPB Academic Publishing: The Hague)
Petit G, Pfautsch S, Anfodillo T, Adams MA (2010) The challenge of tree height in Eucalyptus regnans: when xylem tapering overcomes hydraulic resistance. New Phytologist 187, 1146–1153.
| The challenge of tree height in Eucalyptus regnans: when xylem tapering overcomes hydraulic resistance.Crossref | GoogleScholarGoogle Scholar | 20497350PubMed |
Petit G, Anfodillo T, Carraro V, Grani F, Carrer M (2011) Hydraulic constraints limit height growth in trees at high altitude. New Phytologist 189, 241–252.
| Hydraulic constraints limit height growth in trees at high altitude.Crossref | GoogleScholarGoogle Scholar | 20840508PubMed |
Ridoutt BG, Sands R (1993) Within-tree variation in cambial anatomy and xylem cell differentiation in Eucalyptus globulus. Trees – Structure and Function 8, 18–22.
Ridoutt BG, Sands R (1994) Quantification of the processes of secondary xylem fiber development in Eucalyptus-globulus at 2 height levels. IAWA Journal 15, 417–424.
Ridoutt BG, Pharis RP, Sands R (1995) Identification and quantification of cambial region hormones of Eucalyptus globulus. Plant & Cell Physiology 36, 1143–1147.
Rossi S, Deslauriers A, Anfodillo T, Morin H, Saracino A, Motta R, Borghetti M (2006) Conifers in cold environments synchronize maximum growth rate of tree-ring formation with day length. New Phytologist 170, 301–310.
| Conifers in cold environments synchronize maximum growth rate of tree-ring formation with day length.Crossref | GoogleScholarGoogle Scholar | 16608455PubMed |
Rossi S, Deslauriers A, Anfodillo T, Carraro V (2007) Evidence of threshold temperatures for xylogenesis in conifers at high altitudes. Oecologia 152, 1–12.
| Evidence of threshold temperatures for xylogenesis in conifers at high altitudes.Crossref | GoogleScholarGoogle Scholar | 17165095PubMed |
Rossi S, Deslauriers A, Gricar J, Seo JW, Rathgeber CBK, Anfodillo T, Morin H, Levanic T, Oven P, Jalkanen R (2008) Critical temperatures for xylogenesis in conifers of cold climates. Global Ecology and Biogeography 17, 696–707.
| Critical temperatures for xylogenesis in conifers of cold climates.Crossref | GoogleScholarGoogle Scholar |
Schweingruber FH (1996) ‘Tree rings and environment. Dendroecology.’ (Paul Haupt Publishers: Berne, Germany)
Schweingruber FH, Börner A, Schulze ED (2008) ‘Atlas of woody plant stems – evolution, structure, and environmental modifications.’ (Springer-Verlag: Berlin)
Schweingruber FH, Börner A, Schulze ED (2013) ‘Atlas of stem anatomy in herbs, shrubs and trees.’ (Springer-Verlag Berlin)
Sevanto S, Vesala T, Peramaki M, Nikinmaa E (2002) Time lags for xylem and stem diameter variations in a Scots pine tree. Plant, Cell & Environment 25, 1071–1077.
| Time lags for xylem and stem diameter variations in a Scots pine tree.Crossref | GoogleScholarGoogle Scholar |
Sevanto S, Holtta T, Markkanen T, Peramaki M, Nikinmaa E, Vesala T (2005) Relationships between diurnal xylem diameter variation and environmental factors in Scots pine. Boreal Environment Research 10, 447–458.
Sevanto S, Holtta T, Holbrook NM (2011) Effects of the hydraulic coupling between xylem and phloem on diurnal phloem diameter variation. Plant, Cell & Environment 34, 690–703.
| Effects of the hydraulic coupling between xylem and phloem on diurnal phloem diameter variation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltFaksrg%3D&md5=7102ec8e9ae966b74a5f66a40fc44135CAS |
Siau JF (1984) ‘Transport processes in wood.’ (Springer: Berlin)
Steppe K, De Pauw DJW, Lemeur R, Vanrolleghem PA (2006) A mathematical model linking tree sap flow dynamics to daily stem diameter fluctuations and radial stem growth. Tree Physiology 26, 257–273.
| A mathematical model linking tree sap flow dynamics to daily stem diameter fluctuations and radial stem growth.Crossref | GoogleScholarGoogle Scholar | 16356899PubMed |
Steppe K, De Pauw DJW, Lemeur R (2008) Validation of a dynamic stem diameter variation model and the resulting seasonal changes in calibrated parameter values. Ecological Modelling 218, 247–259.
| Validation of a dynamic stem diameter variation model and the resulting seasonal changes in calibrated parameter values.Crossref | GoogleScholarGoogle Scholar |
Steppe K, Cochard H, Lacointe A, Ameglio T (2012) Could rapid diameter changes be facilitated by a variable hydraulic conductance? Plant, Cell & Environment 35, 150–157.
| Could rapid diameter changes be facilitated by a variable hydraulic conductance?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjvVWht7c%3D&md5=1957f3db9b983736385b014fbd003b0eCAS |
Teskey RO, Saveyn A, Steppe K, McGuire MA (2008) Origin, fate and significance of CO2 in tree stems. New Phytologist 177, 17–32.
White DA, Beadle CL, Worledge D (1996) Leaf water relations of Eucalyptus globulus ssp globulus and E. nitens: seasonal, drought and species effects. Tree Physiology 16, 469–476.
| Leaf water relations of Eucalyptus globulus ssp globulus and E. nitens: seasonal, drought and species effects.Crossref | GoogleScholarGoogle Scholar | 14871715PubMed |
White D, Beadle C, Worledge D, Honeysett J, Cherry M (1998) The influence of drought on the relationship between leaf and conducting sapwood area in Eucalyptus globulus and Eucalyptus nitens. Trees – Structure and Function 12, 406–414.
Wimmer R, Downes GM, Evans R (2002) Temporal variation of microfibril angle in Eucalyptus nitens grown in different irrigation regimes. Tree Physiology 22, 449–457.
| Temporal variation of microfibril angle in Eucalyptus nitens grown in different irrigation regimes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD383kslyktQ%3D%3D&md5=059290f9da985d1f4b6451a43d8339b9CAS | 11986048PubMed |
Zimmermann MH (1983) ‘Xylem structure and ascent of sap.’ (Springer: Berlin)
Zweifel R, Item H, Häsler R (2000) Stem radius changes and their relation to stored water in stems of young Norway spruce trees. Trees 15, 50–57.
| Stem radius changes and their relation to stored water in stems of young Norway spruce trees.Crossref | GoogleScholarGoogle Scholar |
Zweifel R, Item H, Häsler R (2001) Link between diurnal stem radius changes and tree water relations. Tree Physiology 21, 869–877.
| Link between diurnal stem radius changes and tree water relations.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3Mvlt12hsw%3D%3D&md5=763f1a378078f6b729860b617122f26dCAS | 11498334PubMed |
Zweifel R, Böhm JP, Häsler R (2002) Midday stomatal closure in Norway spruce – Reactions in the upper and lower crown. Tree Physiology 22, 1125–1136.
| Midday stomatal closure in Norway spruce – Reactions in the upper and lower crown.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38nlsFequg%3D%3D&md5=42881d3d162227d0453b4c5c3bba1580CAS | 12414372PubMed |
Zweifel R, Zeugin F, Zimmermann L, Newbery DM (2006) Intra-annual radial growth and water relations of trees – implications towards a growth mechanism. Journal of Experimental Botany 57, 1445–1459.
| Intra-annual radial growth and water relations of trees – implications towards a growth mechanism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtFSktL0%3D&md5=3eaf9addb15cdc9dad27352adde75e24CAS | 16556628PubMed |
Zweifel R, Steppe K, Sterck FJ (2007) Stomatal regulation by microclimate and tree water relations: interpreting ecophysiological field data with a hydraulic plant model. Journal of Experimental Botany 58, 2113–2131.
| Stomatal regulation by microclimate and tree water relations: interpreting ecophysiological field data with a hydraulic plant model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXosFektr4%3D&md5=bd2be2b8ae76abb4987f71c6dd9d960dCAS | 17490998PubMed |
Zweifel R, Eugster W, Etzold S, Dobbertin M, Buchmann N, Häsler R (2010) Link between continuous stem radius changes and net ecosystem productivity of a subalpine Norway spruce forest in the Swiss Alps. New Phytologist 187, 819–830.
| Link between continuous stem radius changes and net ecosystem productivity of a subalpine Norway spruce forest in the Swiss Alps.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cjgtVyitQ%3D%3D&md5=aca14a36255d7cabb43b88fe6f1a960dCAS | 20497351PubMed |
Zweifel R, Bangerter S, Rigling A, Sterck FJ (2012) Pine and mistletoes: how to live with a leak in the water flow and storage system? Journal of Experimental Botany 63, 2565–2578.
| Pine and mistletoes: how to live with a leak in the water flow and storage system?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmvF2rurk%3D&md5=bbe8cb0c2f8f077315f790191146d05eCAS | 22268160PubMed |
