During the growing season, trees allocate photoassimilates to increase their aboveground woody biomass in the stem (ABIstem). This 'carbon allocation' to structural growth is a dynamic process influenced by internal and external (e.g., climatic) drivers. While radial variability in wood formation and its resulting structure have been intensively studied, their variability along tree stems and subsequent impacts on ABIstem remain poorly understood. We collected wood cores from mature trees within a fixed plot in a well-studied temperate Fagus sylvatica L. forest. For a subset of trees, we performed regular interval sampling along the stem to elucidate axial variability in ring width (RW) and wood density (ρ), and the resulting effects on tree- and plot-level ABIstem. Moreover, we measured wood anatomical traits to understand the anatomical basis of ρ and the coupling between changes in RW and ρ during drought. We found no significant axial variability in ρ because an increase in the vessel-to-fiber ratio with smaller RW compensated for vessel tapering towards the apex. By contrast, temporal variability in RW varied significantly along the stem axis, depending on the growing conditions. Drought caused a more severe growth decrease, and wetter summers caused a disproportionate growth increase at the stem base compared with the top. Discarding this axial variability resulted in a significant overestimation of tree-level ABIstem in wetter and cooler summers, but this bias was reduced to ~2% when scaling ABIstem to the plot level. These results suggest that F. sylvatica prioritizes structural carbon sinks close to the canopy when conditions are unfavorable. The different axial variability in RW and ρ thereby indicates some independence of the processes that drive volume growth and wood structure along the stem. This refines our knowledge of carbon allocation dynamics in temperate diffuse-porous species and contributes to reducing uncertainties in determining forest carbon fixation.

Department of Ecology W Szafer Institute of Botany Polish Academy of Sciences ul Lubicz 46 31 512 Kraków Poland

Department of Environmental Systems Science Institute of Agricultural Sciences ETH Zurich 8092 Zurich Switzerland

Faculty of Forestry and Wood Sciences Czech University of Life Sciences Kamýcka Cesta 1176 CZ 165 21 Praha 6 Suchdol Czech Republic

Institute of Botany Faculty of Biology Jagiellonian University Kopernika 27 31 501 Kraków Poland

Laboratory of Plant Ecology Faculty of Bioscience Engineering Ghent University Coupure links 653 B 9000 Ghent Belgium

Swiss Federal Research Institute for Forest Snow and Landscape Research Zürcherstrasse 111 CH 8903 Birmensdorf Switzerland

Technical University of Denmark Department of Environmental Engineering Air Land and Water Resources Section Bygningstorvet 115 2800 Kgs Lyngby Denmark

See more in PubMed

Alexander MR, Rollinson CR, Babst F, Trouet V, Moore DJP (2018) Relative influences of multiple sources of uncertainty on cumulative and incremental tree-ring-derived aboveground biomass estimates. Trees Struct Funct 32:265–276.

Anfodillo T, Carraro V, Carrer M, Fior C, Rossi S (2006) Convergent tapering of xylem conduits in different woody species. New Phytol 169:279–290. PubMed

Anfodillo T, Deslauriers A, Menardi R, Tedoldi L, Petit G, Rossi S (2012) Widening of xylem conduits in a conifer tree depends on the longer time of cell expansion downwards along the stem. J Exp Bot 63:837–845. PubMed PMC

Babst F, Bouriaud O, Alexander R, Trouet V, Frank D (2014a) Toward consistent measurements of carbon accumulation: a multi-site assessment of biomass and basal area increment across Europe. Dendrochronologia 32:153–161.

Babst F, Bouriaud O, Papale D et al. (2014b) Above-ground woody carbon sequestration measured from tree rings is coherent with net ecosystem productivity at five eddy-covariance sites. New Phytol 201:1289–1303. PubMed

Babst F, Bodesheim P, Charney N et al. (2018) When tree rings go global: challenges and opportunities for retro- and prospective insight. Quat Sci Rev 197:1–20.

Bakker JD. (2005) A new, proportional method for reconstructing historical tree diameters. Can J For Res 35:2515–2520.

Bar-On YM, Phillips R, Milo R (2018) The biomass distribution on earth. Proc Natl Acad Sci USA 115:6506–6511. PubMed PMC

Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48.

Bergès L, Dupouey JL, Franc A (2000) Long-term changes in wood density and radial growth of Quercus petraea Liebl. In northern France since the middle of the nineteenth century. Trees Struct Funct 14:398–408.

Bhuyan U, Zang C, Menzel A (2017) Different responses of multispecies tree ring growth to various drought indices across Europe. Dendrochronologia 44:1–8.

Björklund J, Seftigen K, Schweingruber F et al. (2017) Cell size and wall dimensions drive distinct variability of earlywood and latewood density in northern hemisphere conifers. New Phytol 216:728–740. PubMed

Bosela M, Štefančík I, Petráš R, Vacek S (2016) The effects of climate warming on the growth of European beech forests depend critically on thinning strategy and site productivity. Agric For Meteorol 222:21–31.

Bouriaud O, Bréda N, Moguédec G, Nepveu G (2004) Modelling variability of wood density in beech as affected by ring age, radial growth and climate. Trees Struct Funct 18:264–276.

Bouriaud O, Bréda N, Dupouey J-L, Granier A (2005a) Is ring width a reliable proxy for stem-biomass increment? A case study in European beech. Can J For Res 35:2920–2933.

Bouriaud O, Leban JM, Bert D, Deleuze C (2005b) Intra-annual variations in climate influence growth and wood density of Norway spruce. Tree Physiol 25:651–660. PubMed

Bouriaud O, Teodosiu M, Kirdyanov AV, Wirth C (2015) Influence of wood density in tree-ring-based annual productivity assessments and its errors in Norway spruce. Biogeosciences 12:6205–6217.

Briffa KR, Osborn TJ, Schweingruber FH, Jones PD, Shiyatov SG, Vaganov EA (2002) Tree-ring width and density data around the northern hemisphere: part 1, local and regional climate signals. Holocene 12:737–757.

Bunn AG. (2008) A dendrochronology program library in R (dplR). Dendrochronologia 26:115–124.

Castagneri D, Petit G, Carrer M (2015) Divergent climate response on hydraulic-related xylem anatomical traits of Picea abies along a 900-m altitudinal gradient. Tree Physiol 35:1378–1387. PubMed

Chave J, Coomes D, Jansen S, Lewis SL, Swenson NG, Zanne AE (2009) Towards a worldwide wood economics spectrum. Ecol Lett 12:351–366. PubMed

Chen G, Yang Y, Robinson D (2013) Allocation of gross primary production in forest ecosystems: Allometric constraints and environmental responses. New Phytol 200:1176–1186. PubMed

Chhin S, Hogg EH, Lieffers VJ, Huang S (2010) Growth-climate relationships vary with height along the stem in lodgepole pine. Tree Physiol 30:335–345. PubMed

Cook ER, Briffa KR, Shiyatov S, Mazepa V (1990) Tree-ring standardization and growth-trend estimation In: Cook ER, Kairiukstis LA (eds) Methods of dendrochronology: applications in the environmental sciences. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 104–123.

Cosgrove DJ. (1993) Water uptake by growing cells: an assessment of the controlling roles of wall relaxation, solute uptake, and hydraulic conductance. Int J Plant Sci 154:10–21. PubMed

Cuny HE, Rathgeber CBK, Frank D et al. (2015) Woody biomass production lags stem-girth increase by over one month in coniferous forests. Nat Plants 1:1–6. PubMed

Cuny HE, Fonti P, Rathgeber CBK, Arx G, Peters RL, Frank D (2019) Couplings in cell differentiation kinetics mitigate air temperature influence on conifer wood anatomy. Plant Cell Environ 42:1222–1232. PubMed

Dalsgaard L, Mikkelsen TN, Bastrup-Birk A (2011) Sap flow for beech (Fagus sylvatica L.) in a natural and a managed forest - effect of spatial heterogeneity. J Plant Ecol 4:23–35.

De Schepper V, Steppe K (2010) Development and verification of a water and sugar transport model using measured stem diameter variations. J Exp Bot 61:2083–2099. PubMed

Dietze MC, Sala A, Carbone MS, Czimczik CI, Mantooth JA, Richardson AD, Vargas R (2014) Nonstructural carbon in Woody plants. Annu Rev Plant Biol 65:667–687. PubMed

Dye A, Plotkin AB, Bishop D, Pederson N, Poulter B, Hessl A (2016) Comparing tree-ring and permanent plot estimates of aboveground net primary production in three eastern U.S. forests. Ecosphere 7:1–13.

Eschbach W, Nogler P, Schär E, Schweingruber FH (1995) Technical advances in the radiodensitometrical determination of wood density. Dendrochronologia 13:155–168.

Esper J, Frank DC, Timonen M et al. (2012) Orbital forcing of tree-ring data. Nat Clim Chang 2:862–866.

Farrar JL. (1961) Longitudinal variation in the thickness of the annual ring. For Chron 37:323–349.

Fatichi S, Pappas C, Zscheischler J, Leuzinger S (2019) Modelling carbon sources and sinks in terrestrial vegetation. New Phytol 221:652–668. PubMed

Forrester DI, Tachauer IHH, Annighoefer P et al. (2017) Generalized biomass and leaf area allometric equations for European tree species incorporating stand structure, tree age and climate. For Ecol Manage 396:160–175.

Franceschini T, Longuetaud F, Bontemps JD, Bouriaud O, Caritey BD, Leban JM (2013) Effect of ring width, cambial age, and climatic variables on the within-ring wood density profile of Norway spruce Picea abies (L.) Karst. Trees Struct Funct 27:913–925.

Frank D, Esper J (2005) Characterization and climate response patterns of a high-elevation, multi-species tree-ring network in the European alps. Dendrochronologia 22:107–121.

Friend AD, Patrick AHE, Tim F, Rathgeber CBK, Richardson AD, Turton RH (2019) On the need to consider wood formation processes in global vegetation models and a suggested approach. Ann For Sci 76:49.

Fritts HC, Smith DG, Budelsky CA, Cardis JW (1965) The variability of ring characteristics within trees as shown by a reanalysis of four ponderosa pine. Tree Ring Bull 27:3–18.

Gärtner H, Lucchinetti S, Schweingruber FH (2015) A new sledge microtome to combine wood anatomy and tree-ring ecology. IAWA J 36:452–459.

Gea-Izquierdo G, Guibal F, Joffre R, Ourcival JM, Simioni G, Guiot J (2015) Modelling the climatic drivers determining photosynthesis and carbon allocation in evergreen Mediterranean forests using multiproxy long time series. Biogeosciences 12:3695–3712.

Guillemot J, Francois C, Hmimina G, Dufrêne E, Martin-StPaul NK, Soudani K, Marie G, Ourcival JM, Delpierre N (2017) Environmental control of carbon allocation matters for modelling forest growth. New Phytol 214:180–193. PubMed

Guilley É, Hervé JC, Huber F, Nepveu G (1999) Modelling variability of within-ring density components in Quercus petraea Liebl. With mixed-effect models and simulating the influence of contrasting silvicultures on wood density. Acta Med Bulg 56:449–458.

Harris I, Jones PD, Osborn TJ, Lister DH (2014) Updated high-resolution grids of monthly climatic observations - the CRU TS3.10 dataset. Int J Climatol 34:623–642.

Hartmann F, Rathgeber C, Fournier M, Moulia B (2017) Modelling wood formation and structure: power and limits of a morphogenetic gradient in controlling xylem cell proliferation and growth. Ann For Sci 74:1–15.

He Y, Peng S, Liu Y et al. (2019) Global vegetation biomass production efficiency constrained by models and observations. Glob Chang Biol 00:1–11. PubMed

Holmes RL. (1983) Computer-assisted quality control in tree-ring dating and measurement. Tree Ring Bull 43:69–78.

Jacquin P, Longuetaud F, Leban JM, Mothe F (2017) X-ray microdensitometry of wood: a review of existing principles and devices. Dendrochronologia 42:42–50.

Kellogg RM, Wangaard FF (1969) Variation in the cell-wall density of wood. Wood Fiber Sci 1:180–204.

Kerhoulas LP, Kane JM (2012) Sensitivity of ring growth and carbon allocation to climatic variation vary within ponderosa pine trees. Tree Physiol 32:14–23. PubMed

Klesse S, Etzold S, Frank D (2016) Integrating tree-ring and inventory-based measurements of aboveground biomass growth: research opportunities and carbon cycle consequences from a large snow breakage event in the Swiss alps. Eur J For Res 135:297–311.

Klesse S, Babst F, Lienert S et al. (2018) A combined tree-ring and vegetation model assessment of European forest growth sensitivity to inter-annual climate variability. Global Biogeochem Cycles 32:1226–1240.

Körner C. (2017) A matter of tree longevity. Science 355:130–131. PubMed

Lachaud S, Catesson AM, Bonnemain JL (1999) Structure and functions of the vascular cambium. C R Acad Sci Paris 322:633–650. PubMed

Lacointe A. (2000) Carbon allocation among tree organs: a review of basic processes and representation in functional-structural tree models. Ann For Sci 57:521–533.

Lapenis AG, Lawrence GB, Heim A, Zheng C, Shortle W (2013) Climate warming shifts carbon allocation from stemwood to roots in calcium-depleted spruce forests. Global Biogeochem Cycles 27:101–107.

Larjavaara M, Muller-Landau HC (2013) Measuring tree height: a quantitative comparison of two common field methods in a moist tropical forest. Methods Ecol Evol 4:793–801.

Larson PR. (1963) The indirect effect of drought on tracheid diameter in red pine. For Sci 9:52–62.

Lazzarin M, Zweifel R, Anten N, Sterck FJ (2018) Does phloem osmolality affect diurnal diameter changes of twigs but not of stems in Scots pine? Tree Physiol 32:275–283. PubMed

Le Quéré C, Andrew RM, Friedlingstein P et al. (2018) Global carbon budget 2017. Earth Syst Sci Data 10:405–448.

Li G, Harrison SP, Prentice IC, Falster D (2014) Simulation of tree-ring widths with a model for primary production, carbon allocation, and growth. Biogeosciences 11:6711–6724.

Litton CM, Raich JW, Ryan MG (2007) Carbon allocation in forest ecosystems. Glob Chang Biol 13:2089–2109.

Lockhart JA. (1965) An analysis of irreversible plant cell elongation. J Theor Biol 8:264–275. PubMed

Lupi C, Morin H, Deslauriers A, Rossi S (2010) Xylem phenology and wood production: resolving the chicken-or-egg dilemma. Plant Cell Environ 33:1721–1730. PubMed

Luyssaert S, Inglima I, Jung M et al. (2007) CO2 balance of boreal, temperate, and tropical forests derived from a global database. Glob Chang Biol 13:2509–2537.

Mausolf K, Härdtle W, Hertel D, Leuschner C, Fichtner A (2019) Impacts of multiple environmental change drivers no growth of European beech (Fagus sylvatica): Forest history matters. Ecosystems. doi: 10.1007/s10021-019-00419-0. DOI

Mcmurtrie RE, Dewar RC (2013) New insights into carbon allocation by trees from the hypothesis that annual wood production is maximized. New Phytol 199:981–990. PubMed

Münch E. (1930) Die stoffbewegunen in der Planze. JenaGustav Fischer.

Olson ME, Anfodillo T, Rosell JA, Petit G, Crivellaro A, Isnard S, León-Gómez C, Alvarado-Cárdenas LO, Castorena M (2014) Universal hydraulics of the flowering plants: vessel diameter scales with stem length across angiosperm lineages, habits and climates. Ecol Lett 17:988–997. PubMed

Pan Y, Birdsey RA, Fang J et al. (2011) A large and persistent carbon sink in the World’s forests. Science 333:988–994. PubMed

Park WK, Telewski FW (1993) Measuring maximum latewood density by image analysis at the cellular level. Wood Fiber Sci 25:326–332.

Parker ML, Meleskie KR (1970) Preparation of X-ray negatives of tree-ring specimens for dendrochronological analysis. Tree Ring Bull 30:11–22.

Peters RL, Groenendijk P, Vlam M, Zuidema PA (2015) Detecting long-term growth trends using tree rings: a critical evaluation of methods. Glob Chang Biol 21:2040–2054. PubMed

Peters RL, Balanzategui D, Hurley AG, Arx G, Prendin AL, Cuny HE, Björklund J, Frank DC, Fonti P (2018) RAPTOR: row and position tracheid organizer in R. Dendrochronologia 47:10–16.

Pilegaard K, Ibrom A, Courtney MS, Hummelshøj P, Jensen NO (2011) Increasing net CO2 uptake by a Danish beech forest during the period from 1996 to 2009. Agric For Meteorol 151:934–946.

Pirie MR, Fowler AM, Triggs CM (2015) Assessing the accuracy of three commonly used pith offset methods applied to Agathis australis (kauri) incremental cores. Dendrochronologia 36:60–68.

Prendin AL, Mayr S, Beikircher B, Von Arx G, Petit G (2018) Xylem anatomical adjustments prioritize hydraulic efficiency over safety as Norway spruce trees grow taller. Tree Physiol 38:1088–1097. PubMed

Prendin AL, Petit G, Carrer M, Fonti P, Björklund J, Von Arx G (2017) New research perspectives from a novel approach to quantify tracheid wall thickness. Tree Physiol 37:1–8. PubMed

Pretzsch H, Biber P, Schütze G, Kemmerer J, Uhl E (2018) Wood density reduced while wood volume growth accelerated in central European forests since 1870. For Ecol Manage 429:589–616.

Pritzkow C, Heinrich I, Grudd H, Helle G (2014) Relationship between wood anatomy, tree-ring widths and wood density of Pinus sylvestris L. and climate at high latitudes in northern Sweden. Dendrochronologia 32:295–302.

Rathgeber CBK, Rossi S, Bontemps JD (2011) Cambial activity related to tree size in a mature silver-fir plantation. Ann Bot 108:429–438. PubMed PMC

Rathgeber CBK, Cuny HE, Fonti P (2016) Biological basis of tree-ring formation: a crash course. Front Plant Sci 7:1–7. PubMed PMC

Ryan MG, Asao S, Way D (2014) Phloem transport in trees. Tree Physiol 34:1–4. PubMed

Schippers P, Sterck F, Vlam M, Zuidema PA (2015) Tree growth variation in the tropical forest: understanding effects of temperature, rainfall and CO2. Glob Chang Biol 21:2749–2761. PubMed

Schweingruber FH. (1996) Tree rings and environment - Dendroecology. Paul Haupt, Bern, Switzerland.

Sevanto S, Vesala T, Perämäki M, Nikinmaa E (2003) Sugar transport together with environmental conditions controls time lags between xylem and stem diameter changes. Plant Cell Environ 26:1257–1265.

Skomarkova MV, Vaganov EA, Mund M, Knohl A, Linke P, Boerner A, Schulze ED (2006) Inter-annual and seasonal variability of radial growth, wood density and carbon isotope ratios in tree rings of beech (Fagus sylvatica) growing in Germany and Italy. Trees Struct Funct 20:571–586.

Steppe K, Sterck F, Deslauriers A (2015) Diel growth dynamics in tree stems: linking anatomy and ecophysiology. Trends Plant Sci 20:335–343. PubMed

Sunberg B, Little CHA, Cui K, Sandberg G (1991) Level of endogenous indole-3-acetic acid in the stem of Pinus sylvestris in relation to the seasonal variation of cambial activity. Plant Cell Environ 14:241–246.

Teets A, Fraver S, Hollinger DY, Weiskittel AR, Seymour RS, Richardson AD (2018) Linking annual tree growth with eddy-flux measures of net ecosystem productivity across twenty years of observation in a mixed conifer forest. Agric For Meteorol 249:479–487.

Maaten-Theunissen M, Bouriaud O (2012) Climate–growth relationships at different stem heights in silver fir and Norway spruce. Can J For Res 42:958–969.

Arx G, Arzac A, Fonti P, Frank D, Zweifel R, Rigling A, Galiano L, Gessler A, Olano JM (2017) Responses of sapwood ray parenchyma and non-structural carbohydrates of Pinus sylvestris to drought and long-term irrigation. Funct Ecol 31:1371–1382.

Arx G, Carrer M (2014) Roxas a new tool to build centuries-long tracheid-lumen chronologies in conifers. Dendrochronologia 32:290–293.

Arx G, Crivellaro A, Prendin AL, Čufar K, Carre M (2016) Quantitative wood anatomy-practical guidelines. Front Plant Sci 7:1–13. PubMed PMC

Wang L, Payette S, Bégin Y (2002) Relationships between anatomical and densitometric characteristics of black spruce and summer temperature at tree line in northern Quebec. Can J For Res 32:477–486.

West GB, Brown JH, Enquist BJ (1999) A general model for the structure and allometry of plant vascular systems. Nature 400:664–667.

Williams CB, Anfodillo T, Crivellaro A, Lazzarin M, Dawson TE, Koch GW (2019) Axial variation of xylem conduits in the Earth’s tallest trees. Trees Struct Funct 1–13.

Williamson GB, Wiemann MC (2010) Measuring wood specific gravity... Correctly. Am J Bot 97:519–524. PubMed

Wilmking M, Hallinger M, Van Bogaert R et al. (2012) Continuously missing outer rings in woody plants at their distributional margins. Dendrochronologia 30:213–222.

Woodruff DR, Bond BJ, Meinzer FC (2004) Does turgor limit growth in tall trees? Plant Cell Environ 27:229–236.

Zuidema PA, Poulter B, Frank DC (2018) A wood biology agenda to support global vegetation modelling. Trends Plant Sci 23:1006–1015. PubMed

Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14.

Quantitative vessel mapping on increment cores: a critical comparison of image acquisition methods