Do increasing respiratory costs explain the decline with age of forest growth rate?

Abstract

Once forests have achieved a full canopy, their growth rate declines progressively with age. This work used a global data set with estimates from a wide range of forest types, aged 20‒795 years, of their annual photosynthetic production (gross primary production, GPP) and subsequent above- plus below-ground biomass production (net primary production, NPP). Both GPP and NPP increased with increasing mean annual temperature and precipitation. GPP was then unrelated to forest age whilst NPP declined progressively with increasing age. These results implied that autotrophic respiration increases with age. It has been proposed that GPP should decline in response to increasing water stress in leaves as water is raised to greater heights as trees grow taller with age. However, trees may make substantial plastic adjustment in morphology and anatomy of newly developing leaves, xylem and fine roots to compensate for this stress and maintain GPP with age. This work reviews the possibilities that NPP declines with age as respiratory costs increase progressively in, any or all of, the construction and maintenance of more complex tissues, the maintenance of increasing amounts of live tissue within the sapwood of stems and coarse roots, the conversion of sapwood to heartwood, the increasing distance of phloem transport, increased turnover rates of fine roots, cost of supporting very tall trees that are unable to compensate fully for increased water stress in their canopies or maintaining alive competitively unsuccessful small trees.

Keywords

Primary production / Photosynthesis / Respiration / Biomass growth / Ageing

References

[1] Abdul-Hamid H, Mencuccini M. Age- and size-related changes in physiological characteristics and chemical composition of Acer pseudoplatanus and Fraxinus excelsior trees. Tree Physiol, 2009, 29: 27-38.

[2] Aloni R. Role of hormones in controlling vascular differentiation and the mechanism of lateral root initiation. Planta, 2013, 238: 819-830.

[3] Ambrose AR, Sillett SC, Dawson TE. Effects of tree height on branch hydraulics, leaf structure and gas exchange in California redwoods. Plant Cell Environ, 2009, 32: 743-757.

[4] Ambrose AR, Sillett SC, Koch GW, Van Pelt R, Antoine ME, Dawson TE. Effects of height on treetop transpiration and stomatal conductance in coast redwood (Sequoia sempervirens). Tree Physiol, 2010, 30: 1260-1272.

[5] Andersen CP, Phillips DL, Rygiewicz PT, Storm MJ. Fine root growth and mortality in different-aged ponderosa pine stands. Can J For Res, 2008, 38: 1797-1806.

[6] Anfodillo T, Petit G, Crivellaro A. Axial conduit widening in woody species: a still neglected anatomical pattern. IAWA J, 2013, 34: 352-364.

[7] Asao S, Bedoya-Arrieta R, Ryan MG. Variation in foliar respiration and wood CO₂ efflux rates among species and canopy layers in a wet tropical forest. Tree Physiol, 2015, 35: 148-159.

[8] Avery TE, Burkhart HE. Forest measurements, 2002 5 New York: McGraw Hill.

[9] Azuma W, Ishii HR, Kuroda K, Kuroda K. Function and structure of leaves contributing to increasing water storage with height in the tallest Cryptomeria japonica trees of Japan. Trees, 2016, 30: 141-152.

[10] Azuma W, Ishii HR, Masaki T. Height-related variations of leaf traits reflect strategies for maintaining photosynthetic and hydraulic homeostasis in mature and old Pinus densiflora trees. Oecologia, 2019, 189: 317-328.

[11] Baret M, Pepin S, Ward C, Pothier D. Long-term changes in stand growth dominance as related to resource acquisition and utilization in the boreal forest. For Ecol Manag, 2017, 400: 408-416.

[12] Baret M, Pepin S, Pothier D. Hydraulic limitations in dominant trees as a contributing mechanism to the age-related growth decline of boreal forest stands. For Ecol Manag, 2018, 427: 135-142.

[13] Barnard HR, Ryan MG. A test of the hydraulic limitation hypothesis in fast-growing Eucalyptus saligna. Plant Cell Environ, 2003, 26: 1235-1245.

[14] Barotto AJ, Monteoliva S, Gyenge J, Martińez-Meier A, Moreno K, Teśon N, Fernández ME. Wood density and anatomy of three Eucalyptus species: implications for hydraulic conductivity. For Syst, 2017, 26: e010.

[15] Barotto AJ, Monteoliva S, Gyenge J, Martínez-Meier A, Fernández ME. Functional relationships between wood structure and vulnerability to xylem cavitation in races of Eucalyptus globulus differing in wood density. Tree Physiol, 2018, 38: 243-251.

[16] Baruch Z, Goldstein G. Leaf construction cost, nutrient concentration, and net CO₂ assimilation of native and invasive species in Hawaii. Oecologia, 1999, 121: 183-192.

[17] Binkley D. A hypothesis about the interaction of tree dominance and stand production through stand development. For Ecol Manag, 2004, 190: 265-271.

[18] Binkley D, Kashian DM. Tree-level patterns of lodgepole pine growth and leaf area in Yellowstone National Park explaining anomalous patterns of growth dominance within stands. Ecosystems, 2015, 18: 251-259.

[19] Binkley D, Menyailo O. Binkley D, Menyailo O. Gaining insights on the effects of tree species on soils. Tree species effects on soils: implications for global change. NATO Science Series, 2005, Dordrecht: Kluwer Academic Publishing 1 16

[20] Binkley D, Stape JL, Ryan MG, Barnard HR, Fownes J. Age-related decline in forest ecosystem growth: an individual tree, stand-structure hypothesis. Ecosystems, 2002, 5: 58-67.

[21] Binkley D, Olsson U, Rochelle R, Stohlgren T, Nikolov N. Structure, production and resource use in old-growth spruce/fir forests in the Front Range of the Rocky Mountains, USA. For Ecol Manag, 2003, 172: 271-279.

[22] Binkley D, Kashian DM, Boyden S, Kay MW, Bradford JB, Arthur MA, Fornwalt PJ, Ryan MG. Patterns of growth dominance in forests of the Rocky Mountains, USA. For Ecol Manag, 2006, 236: 193-201.

[23] Binkley D, Campoe OC, Gspaltl M, Forrester DI. Light absorption and use efficiency in forests: why patterns differ for trees and stands. For Ecol Manag, 2013, 288: 5-13.

[24] Binks O, Meir P, Rowland L, da Costa ACL, Vasconcelos SS, de Oliveira SSR, Ferreira L, Mencuccini M. Limited acclimation in leaf anatomy to experimental drought in tropical rainforest trees. Tree Physiol, 2016, 36: 1550-1561.

[25] Binks O, Meir P, Rowland L, da Costa ACL, Vasconcelos SS, de Oliveira SSR, Ferreira L, Christofferson B, Nardini A, Mencuccini M. Plasticity in leaf-level water relations of tropical rainforest trees in response to experimental drought. New Phytol, 2016, 211: 477-488.

[26] Børja I, De Wit HA, Steffenrem A, Madji H. Stand age and fine root biomass, distribution and morphology in a Norway spruce chronosequence in southeast Norway. Tree Physiol, 2008, 28: 773-784.

[27] Brunner I, Godbold DL. Tree roots in a changing world. J For Res, 2007, 12: 78-82.

[28] Buckley TN, Roberts DW. How should leaf area, sapwood area and stomatal conductance vary with tree height to maximise growth?. Tree Physiol, 2006, 26: 1445-1457.

[29] Buckley TN, Sack L, Farquhar GD. Optimal plant water economy. Plant Cell Environ, 2017, 40: 881-896.

[30] Campioli M, Vicca S, Luyssaert S Biomass production efficiency controlled by management in temperate and boreal ecosystems. Nat Geosci, 2015, 8: 843-846.

[31] Campioli M, Malhi Y, Vicca S, Luyssaert S, Papale D, Peñuelas J, Reichstein M, Migliavacca M, Arain MA, Janssens IA. Evaluating the convergence between eddy-covariance and biometric methods for assessing carbon budgets of forests. Nat Commun, 2016, 7: 13717.

[32] Campoe OC, Stape JL, Nouvellon Y, Laclau J-P, Bauerle WL, Binkley D, le Maire G. Stem production, light absorption and light use efficiency between dominant and non-dominant trees of Eucalyptus grandis across a productivity gradient in Brazil. For Ecol Manag, 2013, 288: 14-20.

[33] Cannell MGR, Thornley JHM. Modelling the components of plant respiration: some guiding principles. Ann Bot, 2000, 85: 45-54.

[34] Carey EV, DeLucia EH, Ball JT. Stem maintenance and construction respiration in Pinus ponderosa grown in different concentrations of atmospheric CO₂. Tree Physiol, 1996, 16: 125-130.

[35] Carrer M, von Arx G, Castagneri D, Petit G. Distilling allometric and environmental information from time series of conduit size: the standardization issue and its relationship to tree hydraulic architecture. Tree Physiol, 2015, 35: 27-33.

[36] Celedon JM, Bohlmann J. An extended model of heartwood secondary metabolism informed by functional genomics. Tree Physiol, 2018, 38: 311-319.

[37] Chen LL, Mu XM, Yuan ZY, Deng Q, ChenYL YL, Ryan LT, Kallenbach RL. Soil nutrients and water affect the age-related fine root biomass but not production in two plantation forests on the Loess Plateau, China. J Arid Environ, 2016, 135: 173-180.

[38] Chen SY, Yen PL, Chang TC, Chang ST, Huang SK, Yeh TF. Distribution of living ray parenchyma cells and major bioactive compounds during the heartwood formation of Taiwania cryptomerioides Hayata. J Wood Chem Technol, 2018, 38: 84-95.

[39] Chin ARO, Sillett SC. Leaf acclimation to light availability supports rapid growth in tall Picea sitchensis trees. Tree Physiol, 2017, 37: 1352-1366.

[40] Claus A, George E. Effect of stand age on fine root-biomass and biomass distribution in three European chronosequences. Can J For Res, 2005, 35: 1617-1625.

[41] Coble AP, Cavaleri MA. Light drives vertical gradients of leaf morphology in a sugar maple (Acer saccharum) forest. Tree Physiol, 2014, 34: 146-158.

[42] Coble AP, Cavaleri MA. Vertical leaf mass per area gradient of mature sugar maple reflects both height-driven increases in vascular tissue and light-driven increases in palisade layer thickness. Tree Physiol, 2017, 37: 1337-1351.

[43] Coble AP, Autio A, Cavaleri MA, Binkley D, Ryan MG. Converging patterns of vertical variability in leaf morphology and nitrogen across seven Eucalyptus plantations in Brazil and Hawaii, USA. Trees, 2014, 28: 1-15.

[44] Dadzie PK, Amoah M, Frimpong-Mensah K, Oheneba-Kwarteng F. Some physical, mechanical and anatomical characteristics of stemwood and branchwood of two hardwood species used for structural applications. Mater Struct, 2016, 49: 4947-4958.

[45] de la Riva EG, Villar R, Pérez-Ramos IM, Quero JL, Matías L, Poorter L, Marañón T. Relationships between leaf mass per area and nutrient concentrations in 98 Mediterranean woody species are determined by phylogeny, habitat and leaf habit. Trees, 2018, 32: 497-510.

[46] De Micco V, Battipaglia G, Balzano A, Cherubini P, Aronne G. Are wood fibres as sensitive to environmental conditions as vessels in tree rings with intra-annual density fluctuations (IADFs) in Mediterranean species?. Trees, 2016, 30: 971-983.

[47] De Mil T, Tarelkin Y, Hahn S, Hubau W, Deklerck V, Debeir O, Van Acker J, Cannière C, Beeckman H, Van den Bulcke J. Wood density profiles and their corresponding tissue fractions in tropical angiosperm trees. Forests, 2018, 9: 763.

[48] De Schepper V, De Swaef T, Bauweraerts I, Steppe K. Phloem transport: a review of mechanisms and controls. J Exp Bot, 2013, 64: 4839-4850.

[49] del Río M, Condés S, Pretzsch H. Analyzing size-symmetric vs size-asymmetric and intra- vs inter-specific competition in beech (Fagus sylvatica L.) mixed stands. For Ecol Manag, 2014, 325: 90-98.

[50] DeLucia EH, Drake JE, Thomas RB, Gonzalez-Meler M. Forest carbon use efficiency: Is respiration a constant function of gross primary production?. Global Change Biol, 2007, 13: 1157-1167.

[51] Dlouhá J, Alméras T, Beauchéne J, Clair B, Fournier M. Biophysical dependences among functional wood traits. Funct Ecol, 2018, 32: 2652-2665.

[52] Doi BT, Binkley D, Stape JL. Does reverse growth dominance develop in old plantations of Eucalyptus saligna?. For Ecol Manag, 2010, 259: 1815-1818.

[53] Domingues TF, Ometto JPHB, Nepstad DC, Brando PM, Martinelli LA, Ehleringer JR. Ecophysiological plasticity of Amazonian trees to long-term drought. Oecologia, 2018, 187: 933-940.

[54] Drake JE, Raetz LM, Davis SC, DeLucia EH. Hydraulic limitation not declining nitrogen availability causes the age-related photosynthetic decline in loblolly pine (Pinus taeda L.). Plant Cell Environ, 2010, 33: 1756-1766.

[55] Evans JR. Leaf anatomy enables more equal access to light and CO₂ between chloroplasts. New Phytol, 1999, 143: 93-104.

[56] Ex SA, Smith FW. Wood production efficiency and growth dominance in multiaged and even-aged ponderosa pine stands. For Sci, 2014, 60: 149-156.

[57] Fellner H, Dirnberger GF, Sterba H. Specific leaf area of European Larch (Larix decidua Mill.). Trees, 2016, 30: 1237-1244.

[58] Fernández ME, Tschieder EF, Letourneau F, Gyenge JE. Why do Pinus species have different growth dominance patterns than Eucalyptus species? A hypothesis based on differential physiological plasticity. For Ecol Manag, 2011, 261: 1061-1068.

[59] Ferrio JP, Kurosawa Y, Wang MF, Mori S. Hydraulic constraints to whole-tree water use and respiration in young Cryptomeria trees under competition. Forests, 2018, 9: 449.

[60] Ford ED. Competition and stand structure in some even-aged plant monocultures. J Ecol, 1975, 63: 311-333.

[61] Fortunel C, Ruelle J, Beauchêne J, Fine PVA, Baraloto C. Wood specific gravity and anatomy of branches and roots in 113 Amazonian rainforest tree species across environmental gradients. New Phytol, 2014, 202: 79-94.

[62] Fujimaki R, Tateno R, Tokuchi N. Root development across a chronosequence in a Japanese cedar (Cryptomeria japonica D. Don) plantation. J For Res, 2007, 12: 96-102.

[63] Garnier E, Salager J-L, Laurent G, Sonié L. Relationship between photosynthesis, nitrogen and leaf structure in 14 grass species and their dependence on the basis of expression. New Phytol, 1999, 143: 119-129.

[64] Gill RA, Jackson RB. Global patterns of root turnover for terrestrial ecosystems. New Phytol, 2000, 147: 13-31.

[65] Glencross K, West PW, Nichols JD. Species shade tolerance affects tree basal area growth behaviour in two eucalypt species in thinned and unthinned even-aged monoculture. Aust For, 2016, 79: 157-167.

[66] Goulden ML, McMillan AMS, Winston GC, Rocha AV, Manies KL, Harden JW, Bond-Lamberty BP. Patterns of NPP, GPP, respiration, and NEP during boreal forest succession. Global Change Biol, 2011, 17: 855-871.

[67] Gower ST, McMurtrie RE, Murty D. Aboveground net primary production decline with stand age: potential causes. Trends Ecol Evol, 1996, 11: 378-382.

[68] Greenwood MS, Ward MH, Day ME, Adams SL, Bond BJ. Age-related trends in red spruce foliar plasticity in relation to declining productivity. Tree Physiol, 2008, 28: 225-232.

[69] Griffin KL. Calorimetric estimates of construction cost and their use in ecological studies. Funct Ecol, 1994, 8: 551-562.

[70] Gspaltl M, Bauerle W, Binkley D, Sterba H. Leaf area and light use efficiency patterns of Norway spruce under different thinning regimes and age classes. For Ecol Manag, 2013, 288: 49-59.

[71] Gyenge J, Fernández ME. Patterns of resource use efficiency in relation to intra-specific competition, size of the trees and resource availability in ponderosa pine. For Ecol Manag, 2014, 312: 231-238.

[72] Hacke UG, Spicer R, Schreiber SG, Plavcová L. An ecophysiological and developmental perspective on variation in vessel diameter. Plant Cell Environ, 2017, 40: 831-845.

[73] Hara T. Growth of individuals in plant populations. Ann Bot, 1986, 57: 55-68.

[74] Hara T. Effects of density and extinction coefficient on size variability in plant populations. Ann Bot, 1986, 57: 885-892.

[75] Hardiman BS, Gough CM, Halperin A, Hofmeister KL, Nave LE, Bohrer G, Curtis PS. Maintaining high rates of carbon storage in old forests: a mechanism linking canopy structure to forest function. For Ecol Manag, 2013, 298: 111-119.

[76] Hayek MN, Wehr R, Longo M, Hutyra LR, Wiedemann K, Munger JW, Bonal D, Saleska SR, Fitzjarrald DR, Wofsy SC. A novel correction for biases in forest eddy covariance carbon balance. Agric For Meteorol, 2018, 250: 90-101.

[77] He NP, Liu CC, Tian M, Li ML, Yang H, Yu GR, Guo DL, Smith MD, Yu Q, Hou JH. Variation in leaf anatomical traits from tropical to cold-temperate forests and linkage to ecosystem functions. Funct Ecol, 2018, 32: 10-19.

[78] Hishi T, Tateno R, Fukushima K, Fujimaki R, Itoh M, Tokuchi N. Changes in the anatomy, morphology and mycorrhizal infection of fine root systems of Cryptomeria japonica in relation to stand ageing. Tree Physiol, 2017, 37: 61-70.

[79] Hodge A, Berta G, Doussan C, Merchan F, Crespi M. Plant root growth, architecture and function. Plant Soil, 2009, 321: 153-187.

[80] Hölttä T, Kurppa M, Nikinmaa E. Scaling of xylem and phloem transport capacity and resource usage with tree size. Front Plant Sci, 2013, 4: 496.

[81] Ishii HT, Jennings GM, Sillett SC, Koch GW. Hydrostatic constraints on morphological exploitation of light in tall Sequoia sempervirens trees. Oecologia, 2008, 156: 751-763.

[82] Ishii HR, Azuma W, Kuroda K, Sillett SC. Pushing the limits to tree height: Could foliar water storage compensate for hydraulic constraints in Sequoia sempervirens?. Funct Ecol, 2014, 28: 1087-1093.

[83] Jackson RB, Mooney HA, Schulze E-D. A global budget for fine root biomass, surface area, and nutrient contents. Proc Natl Acad Sci USA, 1997, 94: 7362-7366.

[84] Jankowski A, Wyka TP, Żytkowiak R, Nihlgård B, Reich PB, Oleksyn J. Cold adaptation drives variability in needle structure and anatomy in Pinus sylvestris L. along a 1,900 km temperate–boreal transect. Funct Ecol, 2017, 31: 2212-2223.

[85] Kawai K, Okada N. Roles of major and minor vein in leaf water deficit tolerance and structural properties in 11 temperate deciduous woody species. Trees, 2018, 32: 1573-1582.

[86] Kiorapostolou N, Galiano-Pérez L, Von Arx G, Gessler A, Petit G. Structural and anatomical responses of Pinus sylvestris and Tilia platyphyllos seedlings exposed to water shortage. Trees, 2018, 32: 1211-1218.

[87] Knoblauch M, Peters WS. Münch, morphology, microfluidics—our structural problem with the phloem. Plant Cell Environ, 2010, 33: 1439-1452.

[88] Koch GW, Sillett SC, Jennings GM, Davis SD. The limits to tree height. Nature, 2004, 428: 851-854.

[89] Korol RL, Running SW, Milner KS, Hunt ER. Testing a mechanistic carbon balance model against observed tree growth. Can J For Res, 1991, 21: 1098-1105.

[90] Kramer PJ, Kozlowski TT. Physiology of woody plants, 1979, New York: Academic Press.

[91] Krasowski MJ, Lavigne MB, Szuter MA, Olesinski J, Kershaw JA, McGarrigle E. Age-related changes in survival and turnover rates of balsam fir (Abies balsamea (L.) Mill.) fine roots. Tree Physiol, 2018, 38: 865-876.

[92] Kutsch WL, Kolari P. Data quality and the role of nutrients in forest carbon-use efficiency. Nat Clim Change, 2015, 5: 959-960.

[93] Kuusk V, Niinemets Ü, Valladares F. A major trade-off between structural and photosynthetic investments operative across plant and needle ages in three Mediterranean pines. Tree Physiol, 2018, 38: 543-557.

[94] Kuusk V, Niinemets Ü, Valladares F. Structural controls on photosynthetic capacity through juvenile-to-adult transition and needle ageing in Mediterranean pines. Funct Ecol, 2018, 32: 1479-1491.

[95] Lachenbruch B, McCulloh KA. Traits, properties, and performance: how woody plants combine hydraulic and mechanical functions in a cell, tissue, or whole plant. New Phytol, 2014, 204: 747-764.

[96] Lacointe A, Minchin PEH. Modelling phloem and xylem transport within a complex architecture. Funct Plant Biol, 2008, 35: 772-780.

[97] Law BE, Ryan MG, Anthoni PM. Seasonal and annual respiration of a ponderosa pine ecosystem. Global Change Biol, 1999, 5: 169-182.

[98] Lemoine R, La Camera S, Atanassova R Source-to-sink transport of sugar and regulation by environmental factors. Front Plant Sci, 2013, 4: 1-21.

[99] Litton CM, Raich JW, Ryan MG. Carbon allocation in forest ecosystems. Global Change Biol, 2007, 13: 2089-2109.

[100] Luostarinen K, Hakkarainen K, Kaksonen H. Connection of growth and wood density with wood anatomy in downy birch grown in two different soil types. Scand J For Res, 2017, 32: 789-797.

[101] Lusk CH, Warton DI. Global meta-analysis shows that relationships of leaf mass per area with species shade tolerance depend on leaf habit and ontogeny. New Phytol, 2007, 176: 764-774.

[102] Luyssaert S, Inglima I, Jung M CO₂ balance of boreal, temperate and tropical forests derived from a global database. Global Change Biol, 2007, 13: 2509-2537.

[103] Luyssaert S, Schulze E-D, Börner A, Knohl A, Hessenmöller D, Law BE, Ciais P, Grace J. Old-growth forests as global carbon sinks. Nature, 2008, 455: 213-215.

[104] Magnani F, Mencuccini M, Grace J. Age-related decline in stand productivity: the role of structural acclimation under hydraulic constraints. Plant Cell Environ, 2000, 23: 251-263.

[105] Makkonen K, Helmisaari H-S. Fine root biomass and production in Scots pine stands in relation to stand age. Tree Physiol, 2001, 21: 193-198.

[106] Malhi Y, Baldocchi DD, Jarvis PG. The carbon balance of tropical, temperate and boreal forests. Plant Cell Environ, 1999, 22: 715-740.

[107] Martínez-Cabrera HI, Estrada-Ruiz E, Castañeda-Posadas C, Woodcock D. Wood specific gravity estimation based on wood anatomical traits: inference of key ecological characteristics in fossil assemblages. Rev Palaeobot Palynol, 2012, 187: 1-10.

[108] Martínez-Vilalta J, Korakaki E, Vanderklein D, Mencuccini M. Below-ground hydraulic conductance is a function of environmental conditions and tree size in Scots pine. Funct Ecol, 2007, 21: 1072-1083.

[109] Martínez-Vilalta J, Cochard H, Mencuccini M, Sterck F, Herrero A, Korhonen JFJ, Llorens P, Nikinmaa E, Nolè A, Ripullone F, Sass-Klassen U, Zweifel R. Hydraulic adjustment of Scots pine across Europe. New Phytol, 2009, 184: 353-364.

[110] Meir P, Grace J. Scaling relationships for woody tissue respiration in two tropical rain forests. Plant Cell Environ, 2002, 25: 963-973.

[111] Mencuccini M. Hydraulic constraints in the functional scaling of trees. Tree Physiol, 2002, 22: 553-565.

[112] Mencuccini M, Grace J. Hydraulic conductance, light interception and needle nutrient concentration in Scots pine stands and their relationship with net primary productivity. Tree Physiol, 1996, 16: 459-468.

[113] Mencuccini M, Grace J, Fioravanti M. Biomechanical and hydraulic determinants of tree structure in Scots pine: anatomical characteristics. Tree Physiol, 1997, 17: 105-113.

[114] Mencuccini M, Hölttä T, Petit G, Magnani F. Sanio’s laws revisited Size-dependent changes in the xylem architecture of trees. Ecol Lett, 2007, 10: 1084-1093.

[115] Merino J, Field C, Mooney HA. Construction and maintenance costs of mediterranean-climate evergreen and deciduous leaves II. Biochemical pathway analysis. Acta Oecol, 1984, 5: 211-229.

[116] Michaletz ST, Cheng DL, Kerkhoff AJ, Enquist BJ. Convergence of terrestrial plant production across global climate gradients. Nature, 2014, 512: 39-43.

[117] Minchin PEH, Lacointe A. New understanding on phloem physiology and possible consequences for modelling long-distance carbon transport. New Phytol, 2005, 166: 771-779.

[118] Miyashita A, Tateno M. A novel index of leaf RGR predicts tree shade tolerance. Funct Ecol, 2014, 28: 1321-1329.

[119] Mori S, Yamaji K, Ishida A Mixed-power scaling of whole-plant respiration from seedlings to giant trees. Proc Natl Acad Sci USA, 2010, 107: 1447-1451.

[120] Nabeshima E, Hiura T. Size-dependency in hydraulic and photosynthetic properties of three Acer species having different maximum sizes. Ecol Res, 2008, 23: 281-288.

[121] Nadelhoffer KJ, Raich JW. Fine root production estimates and belowground carbon allocation in forest ecosystems. Ecology, 1992, 73: 1139-1147.

[122] Nagel JM, Griffin KL, Schuster WSF, Tissue DT, Turnbull MH, Brown KJ, Whitehead D. Energy investment in leaves of red maple and co-occurring oaks within a forested watershed. Tree Physiol, 2002, 22: 859-867.

[123] Nicoll BC, Ray D. Adaptive growth of tree root systems in response to wind action and site conditions. Tree Physiol, 1996, 16: 899-904.

[124] Nicoll BC, Gardiner BA, Rayner B, Peace AJ. Anchorage of coniferous trees in relation to species, soil type, and rooting depth. Can J For Res, 2006, 36: 1871-1883.

[125] Nicoll BC, Gardiner BA, Peace AJ. Improvements in anchorage provided by the acclimation of forest trees to wind stress. Forestry, 2008, 81: 389-398.

[126] Niinemets Ü. Energy requirement for foliage formation is not constant along canopy light gradients in temperate deciduous trees. New Phytol, 1999, 141: 459-470.

[127] Niinemets Ü. Components of leaf dry mass per area—thickness and density—alter leaf photosynthetic capacity in reverse directions in woody plants. New Phytol, 1999, 144: 35-47.

[128] Niinemets Ü. Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology, 2001, 82: 453-469.

[129] Niinemets Ü. A review of light interception in plant stands from leaf to canopy in different plant functional types and in species with varying shade tolerance. Ecol Res, 2010, 25: 693-714.

[130] Niinemets Ü, Kull O. Biomass investment in leaf lamina versus lamina support in relation to growth irradiance and leaf size in temperate deciduous trees. Tree Physiol, 1999, 19: 349-358.

[131] Niinemets Ü, Kull O, Tenhunen JD. Variability in leaf morphology and chemical composition as a function of canopy light environment in coexisting deciduous trees. Int J Plant Sci, 1999, 160: 837-848.

[132] Niinemets Ü, Sparrow A, Cescatti A. Light capture efficiency decreases with increasing tree age and size in the southern hemisphere gymnosperm Agathis australis. Trees, 2005, 19: 177-190.

[133] Niklas KJ. A mechanical perspective on foliage leaf form and function. New Phytol, 1999, 143: 19-31.

[134] Noguchi K, Konôpka B, Satomura T, Kaneko S, Takahashi M. Biomass and production of fine roots in Japanese forests. J For Res, 2007, 12: 83-95.

[135] Ogawa K. Mathematical analysis of change in forest carbon use efficiency with stand development: a case study on Abies veitchii Lindl. Ecol Model, 2009, 220: 1419-1424.

[136] O’Grady AP, Eyles A, Worledge D, Battaglia M. Seasonal patterns of foliage respiration in dominant and suppressed Eucalyptus globulus canopies. Tree Physiol, 2010, 30: 957-968.

[137] Oldham AR, Sillett SC, Tomescu AMF, Koch GW. Tree hydrostatic gradient, not light availability, drives height-related variation in Sequoia sempervirens (Cupressaceae) leaf anatomy. Am J Bot, 2010, 97: 1087-1097.

[138] Osada N, Okabe Y, Hayashi D, Katsuyama T, Tokuchi N. Differences between height- and light-dependent changes in shoot traits in five deciduous tree species. Oecologia, 2014, 174: 1-12.

[139] Osazuwa-Peters OL, Wright SJ, Zanne AE. Linking wood traits to vital rates in tropical rainforest trees: insights from comparing sapling and adult wood. Am J Bot, 2017, 104: 1464-1473.

[140] Paembonan SA, Hagihara A, Hozumi K. Long-term respiration in relation to growth and maintenance processes of the aboveground parts of a Hinoki forest tree. Tree Physiol, 1992, 10: 101-110.

[141] Pangle R, Kavanagh K, Duursma R. Decline in canopy gas exchange with increasing tree height, atmospheric evaporative demand, and seasonal drought in co-occurring inland Pacific Northwest conifer species. Can J For Res, 2015, 45: 1086-1101.

[142] Penning de Vries FWT. Cooper EJ. Use of assimilates in higher plants. Photosynthesis and productivity in different ecosystems, 1975, Cambridge: Cambridge University Press 459 480

[143] Penning de Vries FWT, Brunsting AHM, van Laar HH. Products, requirements and efficiency of biosynthesis: a quantitative approach. J Theor Biol, 1974, 45: 339-377.

[144] Petit G, Anfodillo T, Mencuccini M. Tapering of xylem conduits and hydraulic limitations in sycamore (Acer pseudoplatanus) trees. New Phytol, 2008, 177: 653-664.

[145] Pfautsch S, Harbusch M, Wesolowski A, Smith R, Macfarlane C, Tjoelker MG, Reich PB, Adams MA. Climate determines vascular traits in the ecologically diverse genus Eucalyptus. Ecol Lett, 2016, 19: 240-248.

[146] Phillips NG, Ryan MG, Bond BJ, McDowell NG, Hinkley TM, Cermak J. Reliance on stored water increases with tree size in three species in the Pacific Northwest. Tree Physiol, 2003, 23: 237-245.

[147] Phillips NB, Buckley TN, Tissue DT. Capacity of old trees to respond to environmental change. J Integr Plant Biol, 2008, 11: 1355-1364.

[148] Pothier D, Margolis HA, Poliquin J, Waring RH. Relation between the permeability and the anatomy of jack pine sapwood with stand development. Can J For Res, 1989, 19: 1564-1570.

[149] Pothier D, Margolis HA, Waring RH. Patterns of change of saturated sapwood permeability and sapwood conductance with stand development. Can J For Res, 1989, 19: 432-439.

[150] Pregitzer KS, Euskirchen ES. Carbon cycling and storage in world forests: biome patterns related to forest age. Global Change Biol, 2004, 10: 2052-2077.

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

[152] Pretzsch H, Biber P. Size-symmetric versus size-asymmetric competition and growth partitioning among trees in forest stands along an ecological gradient in central Europe. Can J For Res, 2010, 40: 370-384.

[153] Räim O, Kaurilind E, Hallik L, Merilo E. Why does needle photosynthesis decline with tree height in Norway spruce?. Plant Biol, 2012, 14: 306-314.

[154] Reich PF, Eswaran H. Lal R. Global resources. Encyclopedia of soil science, 2002, New York: Marcel Dekker 607 611

[155] Reich PB, Walters MB, Ellsworth DS, Vose JM, Volin JC, Gresham C, Bowman WD. Relationship of leaf dark respiration to leaf nitrogen, specific leaf area and leaf life-span: a test across biomes and functional groups. Oecologia, 1998, 114: 471-482.

[156] Renninger HJ, Phillips N, Hodel DR. Comparative hydraulic and anatomic properties in palm trees (Washingtonia robusta) of varying heights: implications for hydraulic limitation to increased height growth. Trees, 2009, 23: 911-921.

[157] Richardson AD, Berlyn GP, Ashton PMS, Thadani R, Cameron IR. Foliar plasticity of hybrid spruce in relation to crown position and stand age. Can J Bot, 2000, 78: 305-317.

[158] Rowland L, Lobo-do-Vale RL, Christoffersen BO After more than a decade of soil moisture deficit, tropical rainforest trees maintain photosynthetic capacity, despite increased leaf respiration. Global Change Biol, 2015, 21: 4662-4672.

[159] Rungwattana K, Hietz P. Radial variation of wood functional traits reflect size-related adaptations of tree mechanics and hydraulics. Funct Ecol, 2018, 32: 260-272.

[160] Ryan MG. Growth and maintenance respiration in stems of Pinus contorta and Picea engelmanii. Can J For Res, 1990, 20: 48-57.

[161] Ryan MG, Waring RH. Maintenance respiration and stand development in a subalpine lodgepole pine forest. Ecology, 1992, 73: 2100-2108.

[162] Ryan MG, Yoder BJ. Hydraulic limits to tree growth. Bioscience, 1997, 47: 235-242.

[163] Ryan MG, Hubbard RM, Clark DA, Sanford RL. Woody-tissue respiration for Simarouba amara and Minquartia guianensis, two tropical wet forest species with different growth habits. Oecologia, 1994, 100: 213-220.

[164] Ryan MG, Binkley D, Fownes JH. Age-related decline in forest productivity: pattern and process. Adv Ecol Res, 1997, 27: 213-262.

[165] Ryan MG, Binkley D, Fownes JH, Giardina CP, Senock RS. An experimental test of the causes of forest growth decline with stand age. Ecol Monogr, 2004, 74: 393-414.

[166] Ryan MG, Phillips N, Bond BJ. The hydraulic limitation hypothesis revisited. Plant Cell Environ, 2006, 29: 367-381.

[167] Saadaoui E, Yahia KB, Dhahri S, Jamaa MLB, Khouja L. An overview of adaptive responses to drought stress in Eucalyptus spp.. For Stud, 2017, 67: 86-96.

[168] Saenger P, West PW. Determinants of some leaf characteristics of Australian mangroves. Bot J Linn Soc, 2016, 180: 530-541.

[169] Sala A, Hoch G. Height-related growth declines in ponderosa pine are not due to carbon limitation. Plant Cell Environ, 2009, 32: 22-30.

[170] Santini NS, Schmitz N, Lovelock CE. Variation in wood density and anatomy in a widespread mangrove species. Trees, 2012, 26: 1555-1563.

[171] Savage JA, Clearwater MJ, Haines DF, Klein T, Mencuccini M, Sevanto S, Turgeon R, Zhang C. Allocation, stress tolerance and carbon transport in plants: How does phloem physiology affect plant ecology?. Plant Cell Environ, 2016, 39: 709-725.

[172] Schoettle AW. Influence of tree size on shoot structure and physiology of Pinus contorta and Pinus aristata. Tree Physiol, 1994, 14: 1055-1068.

[173] Schoonmaker AS, Lieffers VJ, Landhäusser SM. Viewing forests from below: fine root mass declines relative to leaf area in aging lodgepole pine stands. Oecologia, 2016, 181: 733-747.

[174] Schwinning S, Weiner J. Mechanisms determining the degree of size asymmetry in competition among plants. Oecologia, 1998, 113: 447-455.

[175] Shu SM, Zhu WZ, Wang WZ, Jia M, Zhang YY, Sheng ZL. Effects of tree size heterogeneity on carbon sink in old forests. For Ecol Manag, 2019, 432: 637-648.

[176] Sillett SC, Van Pelt R, Koch GW, Ambrose AR, Carroll AL, Antoine ME, Mifsud BM. Increasing wood production through old age in tall trees. For Ecol Manag, 2010, 259: 976-994.

[177] Sillett SC, Van Pelt R, Carroll AL, Kramer RD, Ambrose AR, Trask D. How do tree structure and old age affect growth potential of California redwoods?. Ecol Monogr, 2015, 85: 181-212.

[178] Simonin KA, Santiago LS, Dawson TE. Fog interception by Sequoia sempervirens (D. Don) crowns decouples physiology from soil water deficit. Plant Cell Environ, 2006, 32: 882-892.

[179] Snowdon P. A ratio estimator for bias correction in logarithmic regressions. Can J For Res, 1991, 21: 720-724.

[180] Song KL, Yin YF, Salmen L, Xiao FM, Jiang XM. Changes in the properties of wood cell walls during the transformation from sapwood to heartwood. J Mater Sci, 2014, 49: 1734-1742.

[181] Speckman HN, Frank JM, Bradford JB, Miles BL, Massman WJ, Parton WJ, Ryan MG. Forest ecosystem respiration estimated from eddy covariance and chamber measurements under high turbulence and substantial tree mortality from bark beetles. Global Change Biol, 2015, 21: 708-721.

[182] Spicer R. Symplasmic networks in secondary vascular tissues: parenchyma distribution and activity supporting long-distance transport. J Exp Bot, 2014, 65: 1829-1848.

[183] Sprugel DG. Components of woody tissue respiration in young Abies amabilis (Dougl.) Forbes trees. Trees, 1990, 4: 88-95.

[184] Sterck F, Schieving F. Modelling functional trait acclimation for trees of different height in a forest light gradient: emergent patterns driven by carbon gain maximization. Tree Physiol, 2011, 31: 1024-1037.

[185] Stokes A, Fitter AH, Coutts MP. Responses of young trees to wind and shading: effects on root architecture. J Exp Bot, 1995, 46: 1139-1146.

[186] Stokes A, Nicoll BC, Coutts MP, Fitter AH. Responses of young Sitka spruce clones to mechanical perturbation and nutrition: effects on biomass allocation, root development, and resistance to bending. Can J For Res, 1997, 27: 1049-1057.

[187] Tadaki Y, Hatiya K, Tochiaki K, Miyauchi H, Matsuda U (1970) Studies on the production structure of forest (XVI) primary productivity of Abies veitchii forests in the subalpine zone of Mt Fuji. Bulletin of the Government Forest Experiment Station No 229, Tokyo

[188] Tamasi E, Stokes A, Lasserre B, Danjon F, Berthier S, Fourcaud T, Chiatante D. Influence of wind loading on root system development and architecture in oak (Quercus robur L.) seedlings. Trees, 2005, 19: 374-384.

[189] Tan Z-H, Hughes A, Sato T, Zhang Y-P, Han S-J, Kosugi Y, Goulden M, Deng X-B, Cao M, Hao Z-Q, Hu G-R, Yu G-R, Ma K-P. Quantifying forest net primary production: combining eddy flux, inventory and metabolic theory. Forest, 2017, 10: 475-482.

[190] Tang JW, Luyssaert S, Richardson AD, Kutsch W, Janssens IA. Steeper declines in forest photosynthesis than respiration explain age-driven decreases in forest growth. Proc Natl Acad Sci USA, 2014, 111: 8856-8860.

[191] Taylor D, Eamus D. Coordinating leaf functional traits with branch hydraulic conductivity: resource substitution and implications for carbon gain. Tree Physiol, 2008, 28: 1169-1177.

[192] Thompson MV, Holbrook NM. Scaling phloem transport: information transmission. Plant Cell Environ, 2004, 27: 509-519.

[193] Tschieder EF, Fernández ME, Schlicter TM, Pinazo MA, Crechi EH. Influence of growth dominance and individual tree growth efficiency on Pinus taeda stand growth. A contribution to the debate about why stands productivity declines. For Ecol Manag, 2012, 277: 116-123.

[194] Ugawa S, Miura S, Hashimoto S, Iwamoto K, Fukuda K. Changes in quantity, morphology and nitrogen content of fine roots with stand development in a subalpine fir-wave forest. J For Res, 2018, 23: 336-345.

[195] Van Bel AJE. The phloem, a miracle of ingenuity. Plant Cell Environ, 2003, 26: 125-149.

[196] Vanninen P, Mäkelä A. A fine root biomass of Scots pine stands differing in age and soil fertility in southern Finland. Tree Physiol, 1999, 19: 823-830.

[197] Weiner J. Asymmetric competition in plant populations. Trends Ecol Evol, 1990, 5: 360-364.

[198] Weiner J, Thomas SC. Size variability and competition in plant monocultures. Oikos, 1986, 47: 211-222.

[199] West PW. Use of diameter increment and basal area increment in tree growth studies. Can J For Res, 1980, 10: 71-77.

[200] West PW. Comparative growth rates of several eucalypts in mixed-species stands in southern Tasmania. N Z J For Sci, 1981, 11: 45-52.

[201] West PW. Simulation of diameter growth and mortality in regrowth eucalypt forest of southern Tasmania. For Sci, 1981, 27: 603-616.

[202] West PW. Application of regression analysis to inventory data with measurements on successive occasions. For Ecol Manag, 1995, 71: 227-234.

[203] West PW. Use of the Lorenz curve to measure size inequality and growth dominance in forest populations. Aust For, 2018, 81: 231-238.

[204] West PW, Borough CJ. Tree suppression and the self-thinning rule in a monoculture of Pinus radiata D. Don. Ann Bot, 1983, 52: 149-158.

[205] West PW, Osler GHR. Growth response to thinning and its relation to site resources in Eucalyptus regnans. Can J For Res, 1995, 25: 69-80.

[206] West PW, Smith RGB. Inter-tree competitive processes during early growth of an experimental plantation of Eucalyptus pilularis in sub-tropical Australia. For Ecol Manag, 2019, 450: 117450.

[207] West PW, Wells KF. Estimation of leaf weight of standing trees of Eucalyptus regnans F. Muell. Can J For Res, 1990, 20: 1732-1738.

[208] West PW, Ratkowsky DA, Davis AW. Problems of hypothesis testing of regressions with multiple measurements from individual sampling units. For Ecol Manag, 1984, 7: 207-224.

[209] West PW, Jackett DR, Borough CJ. Competitive processes in a monoculture of Pinus radiata D. Don. Oecologia, 1989, 81: 57-61.

[210] West PW, Glencross K, Nicols DJ. Modelling growth behaviour in monoculture in subtropical eastern Australia of two eucalypt species that differ in shade tolerance. South For, 2016, 78: 283-287.

[211] Woodruff DR, Bond BJ, Meinzer FC. Does turgor limit growth in tall trees?. Plant Cell Environ, 2004, 27: 229-236.

[212] Wright IJ, Reich PB, Westoby M The worldwide leaf economics spectrum. Nature, 2004, 428: 821-827.

[213] Xu CY, Turnbull MH, Tissue DT, Lewis JD, Carson R, Schuster WSF, Whitehead D, Walcroft AS, Li J, Griffin KL. Age-related decline of stand biomass accumulation is primarily due to mortality and not to reductions in NPP associated with individual tree physiology. J Ecol, 2012, 100: 428-440.

[214] Yoda K, Shinozaki K, Ogawa H, Hozumi K, Kira T. Estimation of the total amount of respiration in woody organs of trees and forest communities. J Biol Osaka City Univ, 1965, 16: 15-26.

[215] Yue JW, Guan JH, Yan MJ, Zhang JG, Deng L, Li GQ, Du S. Biomass carbon density in natural oak forests with different climate conditions and stand ages in northwest China. J For Res, 2018, 23: 354-362.

[216] Zaehle S. Effect of height on tree hydraulic conductance incompletely compensated by xylem tapering. Funct Ecol, 2005, 19: 359-364.

[217] Zha TS, Barr AG, Bernier P-Y, Lavigne MB Gross and aboveground net primary production at Canadian forest carbon flux sites. Agric For Meteorol, 2013, 174: 54-64.

[218] Zhang Z, Zhao P, McCarthy HR, Ouyang L, Niu J, Zhu L, Ni G, Huang Y. Hydraulic balance of a Eucalyptus urophylla plantation in response to periodic drought in low subtropical China. Front Plant Sci, 2016, 7: 1346.

[219] Zhang L, Yang J, Huang Y, Jia Z, Fang Y. Leaf venation variation and phenotypic plasticity in response to environmental heterogeneity in Parrotia subaequalis (H. T. Chang) R. M. Hao et H. T. Wei, an endemic and endangered tree species from China. Forests, 2018, 9: 247.

[220] Zhang P, Wang H, Wu Q, Yu M, Wu T. Effect of wind on the relation of leaf N, P stoichiometry with leaf morphology in Quercus species. Forests, 2018, 9: 110.

[221] Zheng Y, Zhang L, Xiao JF, Yuan WP, Yan M, Li T, Zhang ZQ. Sources of uncertainty in gross primary productivity simulated by light use efficiency models: model structure, parameters, input data, and spatial resolution. Agric For Meteorol, 2018, 263: 242-257.

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