Skip to main content
SpringerLink
Log in

Relationships Between Tree Height and Carbon Isotope Discrimination

  • Chapter
  • First Online:
Book cover Size- and Age-Related Changes in Tree Structure and Function

Part of the book series: Tree Physiology ((TREE,volume 4))

Abstract

Understanding how tree size impacts leaf- and crown-level gas exchange is essential to predicting forest yields and carbon and water budgets. The stable carbon isotope ratio (δ13C) of organic matter has been used to examine the relationship of gas exchange to tree size for a host of species because it carries a temporally integrated signature of foliar photosynthesis and stomatal conductance. The carbon isotope composition of leaves reflects discrimination against 13C relative to 12C during photosynthesis and is the net result of the balance of change in CO2 supply and demand at the sites of photosynthesis within the leaf mesophyll. Interpreting the patterns of changes in δ13C with tree size are not always clear, however, because multiple factors that regulate gas exchange and carbon isotope discrimination (Δ) co-vary with height, such as solar irradiance and hydraulic conductance. Here we review 36 carbon isotope datasets from 38 tree species and conclude that there is a consistent, linear decline of Δ with height. The most parsimonious explanation of this result is that gravitational constraints on maximum leaf water potential set an ultimate boundary on the shape and sign of the relationship. These hydraulic constraints are manifest both over the long term through impacts on leaf structure, and over diel periods via impacts on stomatal conductance, photosynthesis and leaf hydraulic conductance. Shading induces a positive offset to the linear decline, consistent with light limitations reducing carbon fixation and increasing partial pressures of CO2 inside of the leaf, p c at a given height. Biome differences between tropical and temperate forests were more important in predicting Δ and its relationship to height than wood type associated with being an angiosperm or gymnosperm. It is not yet clear how leaf internal conductance varies with leaf mass area, but some data in particularly tall, temperate conifers suggest that photosynthetic capacity may not vary dramatically with height when compared between tree-tops, while stomatal and leaf internal conductances do decline in unison with height within canopy gradients. It is also clear that light is a critical variable low in the canopy, whereas hydrostatic constraints dominate the relationship between Δ and height in the upper canopy. The trend of increasing maximum height with decreasing minimum Δ suggests that trees that become particularly tall may be adapted to tolerate particularly low values of p c.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 299.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 299.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Addington RN, Donovan LA, Mitchell RJ, Vose JM, Pecot SD, Jack SB, Hacke UG, Sperry JS, Oren R (2006) Adjustments in hydraulic architecture of Pinus palustris maintain similar stomatal conductance in xeric and mesic habitats. Plant Cell Environ 29:535–545

    PubMed  CAS  Google Scholar 

  • Allen RB, Clinton PW, Davis MR (1997) Cation storage and availability along a Nothofagus forest development sequence in New Zealand. Can J For Res 27:323–330

    CAS  Google Scholar 

  • Ambrose AR, Sillett SC, Dawson TE (2009) Effects of tree height on branch hydraulics, leaf structure and gas exchange in California redwoods. Plant Cell Environ 32:743–757

    PubMed  Google Scholar 

  • Badeck F-W, Tcherkez G, Nogues S, Piel C, Ghashghaie J (2007) Post-photosynthetic fractionation of stable carbon isotopes between plant organs – a widespread phenomenon. Rapid Commun Mass Spectrom 19:1381–1391

    Google Scholar 

  • Baldocchi DD, Wilson KB, Gu L (2002) How the environment, canopy structure and canopy physiological functioning influence carbon, water and energy fluxes of a temperate broad-leaved deciduous forest – an assessment with the biophysical model CANOAK. Tree Physiol 22:1065–1077

    PubMed  CAS  Google Scholar 

  • Barbour MM, McDowell NG, Tcherkez G, Bickford C, Hanson D (2007) High frequency measurements reveal rapid post-illumination changes in the carbon isotope composition of leaf-respired CO2. Plant Cell Environ 30:469–482

    PubMed  CAS  Google Scholar 

  • Barnard HR, Ryan MG (2003) A test of the hydraulic limitation hypothesis in fast-growing Eucalyptus saligna. Plant Cell Environ 26:1235–1245

    Google Scholar 

  • Bauerle WL, Hinckley TM, Cermak J, Kucera J, Bible K (1999) The canopy water relations of old-growth Douglas-fir trees. Trees 13:211–217

    Google Scholar 

  • Bickford CP, McDowell NG, Hanson DT (2009) High resolution field measurements of diurnal carbon isotope discrimination and internal conductance in a semi-arid species, Juniperus monosperma. Plant Cell Environ 32:796–810

    PubMed  CAS  Google Scholar 

  • Bickford CP, Hanson DT, McDowell NG (2010) Influence of diurnal variation in mesophyll conductance on modelled 13C discrimination: results from a field study. J Exp Bot 61:3223–3233

    PubMed  CAS  Google Scholar 

  • Bloom AJ, Chapin FS III, Mooney HA (1985) Resource limitation in plants – an economic analogy. Annu Rev Ecol Syst 16:363–392

    Google Scholar 

  • Bonan GB (2008) Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320:1444–1449

    PubMed  CAS  Google Scholar 

  • Bond BJ (2000) Age-related changes in photosynthesis of woody plants. Trends Plant Sci 5:349–353

    PubMed  CAS  Google Scholar 

  • Bond BJ, Farnsworth BT, Coulombe RA, Winner WE (1999) Foliage physiology and biochemistry in response to radiation gradients in conifers with varying shade tolerance. Oecologia 199:183–192

    Google Scholar 

  • Bond BJ, Czarnomski NM, Cooper C, Day ME, Greenwood MS (2007) Developmental decline in height growth in Douglas-fir. Tree Physiol 27:441–453

    PubMed  Google Scholar 

  • Bond BJ, Meinzer FC, Brooks JR (2008) How trees influence the hydrological cycle in forest ecosystems. In: Wood PJ, Hannah DM, Sadler JP (eds.) Hydroecology and ecohydrology: past, present and future. Wiley, London, pp 7–28

    Google Scholar 

  • Bowling D, McDowell NG, Bond BJ, Law BE, Ehleringer JR (2002) 13C content of ecosystem respiration is linked to precipitation and vapor pressure deficit. Oecologia 131:113–124

    Google Scholar 

  • Brandes E, Kodama N, Whittaker K, Weston C, Rennenberg H, Keitel C, Adams MA, Gessler A (2006) Short-term variation in the isotopic composition of organic matter allocated from the leaves to the stem of Pinus sylvestris: effects of photosynthetic and postphotosynthetic carbon isotope fractionation. Glob Change Biol 12:1922–1939

    Google Scholar 

  • Broadmeadow MSJ, Griffiths H, Maxwell C, Borland AM (1992) The carbon isotope ratio of plant organic material reflects temporal and spatial variations in CO2 within tropical forest formations in Trinidad. Oecologia 89:435–441

    Google Scholar 

  • Brooks JR, Flanagan LB, Varney GT, Ehleringer JR (1997a) Vertical gradients in photosynthetic gas exchange characteristics and refixation of respired CO2 within boreal forest canopies. Tree Physiol 17:1–12

    PubMed  Google Scholar 

  • Brooks JR, Flanagan LB, Buchmann N, Ehleringer JR (1997b) Carbon isotope composition of boreal plants: functional grouping of life forms. Oecologia 110:301–311

    Google Scholar 

  • Brugnoli E, Farquhar GD (2000) Photosynthetic fractionation of carbon isotopes. In: Leegood RC, Sharkey TD, von Caemmerer S (eds.) Photosynthesis: physiology and metabolism. Kluwer, Dordrecht, pp 399–434

    Google Scholar 

  • Buchmann N, Kao W-Y, Ehleringer J (1997a) Influence of stand structure on carbon-13 of vegetation, soils, and canopy air within deciduous and evergreen forests in Utah, United States. Oecologia 110:109–119

    Google Scholar 

  • Buchmann N, Guehl JM, Barigah TS, Ehleringer JR (1997b) Interseasonal comparison of CO2 concentrations, isotopic composition, and carbon cycling in an Amazonian rainforest (French Guiana). Oecologia 110:120–131

    Google Scholar 

  • Buckley TN, Roberts DW (2006) How should leaf area, sapwood area and stomatal conductance vary with tree height to maximize growth? Tree Physiol 26:145–157

    PubMed  Google Scholar 

  • Burgess SSO, Dawson TE (2007) Predicting the limits to tree height using statistical regressions of leaf traits. New Phytol 174:626–636

    PubMed  CAS  Google Scholar 

  • Campbell GS, Norman JM (1998) An introduction to environmental biophysics, 2nd edn. Springer, New York, 286 pp

    Google Scholar 

  • Carswell FE, Meir P, Wandelli EV, Bonates LCM, Kruijt B, Barbosa EM, Nobre AD, Grace J, Jarvis PG (2000) Photosynthetic capacity in a central Amazonian rain forest. Tree Physiol 20:179–186

    PubMed  Google Scholar 

  • Cavaleri MA, Oberbauer SF, Clark DB, Clark DA, Ryan MG (2010) Height is the primary determinant of leaf morphology in a tropical rain forest canopy. Ecology 91:1730–1739

    PubMed  Google Scholar 

  • Cernusak LA, Tcherkez G, Keitel C, Cornwell WK, Santiago LS, Knohl A, Barbour MM, Williams DG, Reich PB, Ellsworth DS, Dawson TE, Griffiths HG, Farquhar GD, Wright IJ (2009) Why are non-photosynthetic tissues generally 13C enriched compared to leaves in C3 plants? Review and synthesis of current hypotheses. Funct Plant Biol 36:199–213

    CAS  Google Scholar 

  • Craig H (1957) Isotopic standards for carbon and oxygen and correction factors for mass spectrometric analysis of carbon dioxide. Geochim Cosmochim Acta 12:133–149

    CAS  Google Scholar 

  • Davis MR, Allen RB, Clinton PW (2003) Carbon storage along a stand development sequence in a New Zealand Nothofagus forest. For Ecol Manag 177:313–321

    Google Scholar 

  • Day ME, Greenwood MS, Diaz-Sala C (2002) Age- and size-related trends in woody plant shoot development: regulatory pathways and evidence for genetic control. Tree Physiol 22:507–513

    PubMed  CAS  Google Scholar 

  • Delzon S, Sartore M, Burlett R, Dewar R, Loustau D (2004) Hydraulic responses to height growth in maritime pine trees. Plant Cell Environ 27:1077–1087

    Google Scholar 

  • Domec JC, Lachenbruch B, Meinzer FC, Woodruff DR, Warren JM, McCulloh KA (2008) Maximum height in a conifer is associated with conflicting requirements for xylem design. Proc Natl Acad Sci U S A 105:12069–12074

    PubMed  CAS  Google Scholar 

  • Donovan LA, Ehleringer JR (1994) Carbon isotope discrimination, water-use efficiency, growth, and mortality in a natural shrub population. Oecologia 100:347–354

    Google Scholar 

  • Duursma RA, Marshall JD (2006) Vertical canopy gradients in δ13C correspond with leaf nitrogen content in a mixed-species conifer forest. Trees 20:496–506

    Google Scholar 

  • Ehleringer JR (1993) Carbon and water relations in desert plants: an isotopic perspective. In: Ehleringer JR, Hall AE, Farquhar GD (eds.) Stable isotopes and plant carbon/water relations. Academic, San Diego, pp 155–172

    Google Scholar 

  • Ehleringer JR, Field CB, Lin Z-F, Kuo C-Y (1986) Leaf carbon isotope and mineral composition in subtropical plants along an irradiance cline. Oecologia 70:520–526

    Google Scholar 

  • England JM, Attiwill PM (2007) Changes in sapwood permeability and anatomy with tree age and height in the broad-leaved evergreen species Eucalyptus regnans. Tree Physiol 27:1113–1124

    PubMed  Google Scholar 

  • Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust J Plant Physiol 9:121–137

    CAS  Google Scholar 

  • Field C, Mooney HA (1986) The photosynthesis–nitrogen relationship in wild plants. In: Givnish TJ (ed.) On the economy of form and function. Cambridge University Press, Cambridge, pp 25–55

    Google Scholar 

  • Francey RJ, Farquhar GD (1982) An explanation of 13C/12C variations in tree rings. Nature 297:2831

    Google Scholar 

  • Francey RJ, Gifford RM, Sharkey TD, Weir B (1985) Physiological influences on carbon isotope discrimination in huon pine (Lagarostrobos franklinii). Oecologia 66:211–218

    Google Scholar 

  • Geßler A, Schrempp S, Matzarakis A, Mayer H, Rennenberg H, Adams MA (2001) Radiation modifies the effect of water availability on the carbon isotope composition of beech (Fagus sylvatica). New Phytol 150:653–664

    Google Scholar 

  • Gessler A, Brandes E, Buchmann N, Helle G, Rennenberg H, Barnard RL (2009) Tracing carbon and oxygen isotope signals from newly assimilated sugars in the leaves to the tree-ring archive. Plant Cell Environ 32:780–795

    PubMed  CAS  Google Scholar 

  • Gower ST, McMurtrie RE, Murty D (1996) Aboveground net primary production decline with stand age: potential causes. Trends Ecol Evol 11:378–382

    PubMed  CAS  Google Scholar 

  • Greenwood MS, Ward M, Day ME, Adams S, Bond BJ (2008) Age-related trends in red spruce foliar plasticity in relation to declining productivity. Tree Physiol 28:225–232

    PubMed  CAS  Google Scholar 

  • Grulke NE, Retzlaff WA (2001) Changes in physiological attributes of ponderosa pine from seedling to mature tree. Tree Physiol 21:275–286

    PubMed  CAS  Google Scholar 

  • Hacke UG, Stiller V, Sperry JS, Pittermann J, McCulloh K (2001) Cavitation fatigue: embolism and refilling cycles can weaken the cavitation resistance of xylem. Plant Physiol 125:779–786

    PubMed  CAS  Google Scholar 

  • Hanba YT, Mori S, Lei TT, Koike T, Wada E (1997) Variations in leaf δ13C along a vertical profile of irradiance in a temperate Japanese forest. Oecologia 110:253–261

    Google Scholar 

  • Harlow BA, Marshall JD, Robinson AP (2006) A multi-species comparison of δ13C from whole wood, extractive-free wood and holocellulose. Tree Physiol 26:767–774

    PubMed  CAS  Google Scholar 

  • He C-X, Li J-Y, Zhou P, Guo M, Zheng Q-S (2008) Changes of leaf morphological, anatomical structure and carbon isotope ratio with the height of the wangtian tree (Parashorea chinensis) in Xishuangbanna, China. J Integr Plant Biol 50:168–173

    PubMed  Google Scholar 

  • Heaton THE, Crossley A (1995) Carbon isotope variations in a plantation of Sitka spruce, and the effect of acid mist. Oecologia 103:109–117

    Google Scholar 

  • Helle G, Schleser GH (2004) Beyond CO2-fixation by Rubisco – an interpretation of 13C/12C variations in tree rings from novel intra-seasonal studies on broad-leaf trees. Plant Cell Environ 27:367–380

    CAS  Google Scholar 

  • Hubbard RM, Bond BJ, Ryan MG (1999) Evidence that hydraulic limitation explains differences in photosynthesis between young and old Pinus ponderosa. Tree Physiol 19:165–172

    PubMed  Google Scholar 

  • Hubbard RM, Bond BJ, Senock RS, Ryan MG (2002) Effects of branch height on leaf gas exchange, branch hydraulic conductance and branch sap flux in open-grown ponderosa pine. Tree Physiol 22:575–581

    PubMed  Google Scholar 

  • Hultine KR, Marshall JD (2000) Altitude trends in conifer leaf morphology and stable isotope composition. Oecologia 123:32–40

    Google Scholar 

  • IPCC (2007) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change, IPCC Secretariat, Geneva, Switzerland

    Google Scholar 

  • Ishii H (2011) How do changes in leaf/shoot morphology and crown architecture affect growth and physiological function of large, old trees? In: Meinzer FC, Lachenbruch B, Dawson TE (eds.) Size- and age-related changes in tree structure and function. Springer, Dordrecht

    Google Scholar 

  • Ishii HT, Ford ED, Kennedy MC (2007) Physiological and ecological implications of adaptive reiteration as a mechanism for crown maintenance after trees reach maximum size. Tree Physiol 27:455–462

    PubMed  Google Scholar 

  • Ishii HT, Jennings GM, Sillett SC, Koch GW (2008) Hydrostatic constraints on morphological exploitation of light in tall Sequoia sempervirens trees. Oecologia 156:751–763

    PubMed  Google Scholar 

  • Keeling CD, Bacastow RB, Carter AF, Piper SC, Whorf TP, Heimann M, Mook WG, Roeloffzen H, Peterson H (1989) A three-dimensional model of atmospheric CO2 transport based on observed winds:1. Analysis of observational data. In: Peterson DH (ed.) Aspects of climate variability in the Pacific and the western Americas, Geophysical monographs. American Geophysical Union, Washington, DC, pp 165–236

    Google Scholar 

  • Koch GW, Sillett SC, Jennings GM, Davis SD (2004) The limits to tree height. Nature 428:851–854

    PubMed  CAS  Google Scholar 

  • Kolb TE, Stone JE (2000) Differences in leaf gas exchange and water relations among species and tree sizes in an Arizona pine-oak forest. Tree Physiol 20:1–12

    PubMed  Google Scholar 

  • Körner C (2007) The use of ‘altitude’ in ecological research. Trends Ecol Evol 22:569–574

    PubMed  Google Scholar 

  • Le Roux X, Bariac T, Sinoquet H, Genty B, Piel C, Mariotti A, Girardin C, Richard P (2001) Spatial distribution of leaf water-use efficiency and carbon isotope discrimination within an isolated tree crown. Plant Cell Environ 24:1021–1032

    Google Scholar 

  • Leavitt SW, Long A (1988) Stable carbon isotope chronologies from trees in the southwestern United States. Glob Biogeochem Cycles 2:189–198

    CAS  Google Scholar 

  • Leavitt SW, Long A (1991) Seasonal stable-carbon isotope variability in tree rings: possible paleoenvironmental signals. Chem Geol 87:59–70

    CAS  Google Scholar 

  • Livingston NJ, Whitehead D, Kelliher FM, Wang Y-P, Grace JC, Walcroft AS, Byers JN, Mcseveny TM, Millard P (1998) Nitrogen allocation and carbon isotope fractionation in relation to intercepted radiation and position in a young Pinus radiata D. Don tree. Plant Cell Environ 21:795–803

    CAS  Google Scholar 

  • Lloyd J, Kruijt B, Hollinger DY, Grace J, Francey RJ, Wong SC, Kelliher FM, Miranda AC, Farquhar GD, Gash JH, Vygodskaya NN, Wright IR, Miranda HS, Schulze ED (1996) Vegetation effects on the isotopic composition of atmospheric CO2 at local and regional scales: theoretical aspects and a comparison between rain forest in Amazonia and boreal forest in Siberia. Aust J Plant Physiol 23:371–399

    Google Scholar 

  • Lloyd J, Kruijt B, Hollinger DY, Grace J, Francey RJ, Wong SC, Kelliher FM, Miranda AC, Farquhar GD, Gash JH, Vygodskaya NN, Wright IR, Miranda HS, Schulze ED (1997) An alternative interpretation of the appropriateness and correct means for the evaluation of CO2 recycling indices. Aust J Plant Physiol 24:399–405

    Google Scholar 

  • Lloyd J, Patino S, Paiva RQ, Nardoto GB, Quesada CA, Santos AJB, Baker TR, Brand WA, Hilke I, Gielmann H, Raessler M, Luizao FJ, Martinelli LA, Mercado LM (2009) Variations in leaf physiological properties within Amazon forest canopies. Biogeosci Discuss 6:4639–4692

    Google Scholar 

  • Loader NJ, Robertson I, McCarroll D (2003) Comparisons of stable carbon isotope ratios in the whole-wood, cellulose and lignin of oak tree-rings. Palaeogeog Palaeoclimatol Palaeoecol 196:394–407

    Google Scholar 

  • Macfarlane C, Warren CR, White DA, Adams MA (1999) A rapid and simple method for processing wood to crude cellulose for analysis of stable carbon isotopes in tree rings. Tree Physiol 19:831–835

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Major JE, Mosseler A, Barsi DC, Campbell M (2007) Comparative nutrient economy, stable isotopes, and related adaptive traits in Picea rubens, Picea mariana, and their hybrids. Trees 21:677–692

    CAS  Google Scholar 

  • Marshall JD, Monserud RA (2003) Foliage height influences specific leaf area of three conifer species. Can J For Res 33:164–170

    Google Scholar 

  • Martinelli LA, Almeida S, Brown IF, Moreira MZ, Victoria RL, Sternberg LSL, Ferreira CAC, Thomas WW (1998) Stable carbon isotope ratio of tree leaves, boles and fine litter in a tropical forest in Rondonia, Brazil. Oecologia 114:170–179

    Google Scholar 

  • Martínez-Vilalta J, Vanderklein D, Mencuccini M (2007a) Tree height and age-related decline in growth in Scots pine (Pinus sylvestris L.). Oecologia 150:529–544

    PubMed  Google Scholar 

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

    Google Scholar 

  • McCracken IJ (1980) Mountain climate in the Craigieburn Range, New Zealand. In: Benecke U, Davis MR (eds.) Mountain environments and subalpine growth. New Zealand Forest Service Forestry Research Institute Technical Paper 70, pp 41–60

    Google Scholar 

  • McDowell NG, Phillips N, Lunch CK, Bond BJ, Ryan MG (2002a) An investigation of hydraulic limitation and compensation in large, old Douglas-fir trees. Tree Physiol 22:763–774

    PubMed  CAS  Google Scholar 

  • McDowell NG, Barnard HR, Bond BJ, Hinckley T, Hubbard RM, Ishii H, Köstner B, Magnani F, Marshall JD, Meinzer FC, Phillips N, Ryan MG, Whitehead D (2002b) The relationship between tree height and leaf area: sapwood area ratio. Oecologia 132:12–20

    Google Scholar 

  • McDowell NG, Licata J, Bond BJ (2005) Environmental sensitivity of gas exchange in different-sized trees. Oecologia 145:9–20

    PubMed  Google Scholar 

  • McDowell NG, Adams HA, Bailey JD, Hess M, Kolb TE (2006) Homeostatic maintenance of ponderosa pine gas exchange in response to stand density changes. Ecol Appl 16:1164–1182

    PubMed  Google Scholar 

  • McDowell NG, Allen C, Marshall L (2010) Growth, carbon isotope discrimination, and mortality across a ponderosa pine elevation transect. Glob Change Biol 16:399–415

    Google Scholar 

  • Medina E, Minchin P (1980) Stratification of 13C-values of leaves in Amazonian rain forests. Oecologia 45:377–378

    Google Scholar 

  • Meinzer FC, Grantz DA (1990) Stomatal and hydraulic conductance in growing sugarcane: stomatal adjustment to water transport capacity. Plant Cell Environ 13:383–388

    Google Scholar 

  • Mencuccini M (2003) The ecological significance of long distance water transport: short-term regulation and long-term acclimation across plant growth forms. Plant Cell Environ 26:163–182

    Google Scholar 

  • Mencuccini M, Comstock J (1999) Variability in hydraulic architecture and gas exchange of common bean (Phaseolus vulgaris) cultivars under well-watered conditions: interactions with leaf size. Aust J Plant Physiol 26:115–124

    Google Scholar 

  • Mencuccini M, Grace J (1996a) Hydraulic conductance, light interception and needle nutrient concentration in Scots pine stands and their relation with net primary productivity. Tree Physiol 16:459–468

    PubMed  CAS  Google Scholar 

  • Mencuccini M, Grace J (1996b) Developmental patterns of aboveground hydraulic conductance in a Scots pine (Pinus sylvestris L.) age sequence. Plant Cell Environ 19:939–948

    Google Scholar 

  • Mencuccini M, Martinez-Vilalta J, Vanderklein D, Hamid HA, Korakaki E, Lee S, Michiels B (2005) Size-mediated ageing reduces vigour in trees. Ecol Lett 8:1183–1190

    PubMed  CAS  Google Scholar 

  • Monserud RA, Marshall JD (2001) Time-series analysis of δ13C from tree rings. I. Time trends and autocorrelation. Tree Physiol 21:1087–1102

    PubMed  CAS  Google Scholar 

  • Mullin LP, Sillett SC, Koch GW, Tu KP, Antoine ME (2009) Physiological consequences of height-related morphological variation in Sequoia sempervirens foliage. Tree Physiol 29:999–1010

    PubMed  Google Scholar 

  • Niinemets U (2002) Stomatal conductance alone does not explain the decline in foliar photosynthetic rates with increasing tree age and size in Picea abies and Pinus sylvestris. Tree Physiol 22:515–535

    PubMed  Google Scholar 

  • Ogée J, Barbour MM, Wingate L, Bert D, Bosc A, Stievenard M, Lambrot C, Pierre M, Bariac T, Loustau D, Dewar RC (2009) A single-substrate model to interpret intra-annual stable isotope signals in tree-ring cellulose. Plant Cell Environ 32:1071–1090

    PubMed  Google Scholar 

  • Oldham AR (2008) Height-associated variation in leaf anatomy of tall redwoods: potential impacts on whole-tree carbon balance. M.A. thesis, Humboldt State University, 59 pp

    Google Scholar 

  • Ometto JPHB, Flanagan LB, Martinelli LA, Moreira MZ, Higuchi N, Ehleringer JR (2002) Carbon isotope discrimination in forest and pasture ecosystems of the Amazon Basin, Brazil. Glob Biogeochem Cycles 16:1109–1119

    Google Scholar 

  • Parker GG, Davis MM, Chapotin SM (2002) Canopy light transmittance in Douglas-fir-western hemlock stands. Tree Physiol 22:147–157

    PubMed  Google Scholar 

  • Phillips N, Bond BJ, McDowell NG, Ryan MG (2002) Canopy and hydraulic conductance in young, mature, and old Douglas-fir trees. Tree Physiol 22:205–211

    PubMed  Google Scholar 

  • Phillips N, Bond BJ, McDowell NG, Ryan MG, Schauer A (2003) Leaf area compounds height-related hydraulic costs of water transport in Oregon White Oak trees. Funct Ecol 17:832–840

    Google Scholar 

  • Pons TL, Flexas J, von Caemmerer S, Evans JR, Genty B, Ribas-Carbo M, Brugnoli E (2009) Estimating mesophyll conductance to CO2: methodology, potential errors, and recommendations. J Exp Bot 60:2217–2234

    PubMed  CAS  Google Scholar 

  • Poorter L, Bongers F, Sterck FJ, Wöll H (2005) Beyond the regeneration phase: differentiation of height-light trajectories among tropical tree species. J Ecol 93:256–267

    Google Scholar 

  • Ryan MG, Yoder BJ (1997) Hydraulic limits to tree height and tree growth. Bioscience 47:235–242

    Google Scholar 

  • Ryan MG, Binkley D, Fownes JH (1997) Age-related decline in forest productivity: pattern and process. Adv Ecol Res 27:213–262

    Google Scholar 

  • Ryan MG, Phillips N, Bond BJ (2006) The hydraulic limitation hypothesis revisited. Plant Cell Environ 29:367–381

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Samuelson LJ, McLemore PC III, Somers GL (2003) Relationship between foliar δ13C and hydraulic pathway length in Pinus palustris. For Sci 49(5):790–798

    Google Scholar 

  • Schäfer KVR, Oren R, Tenhunen JD (2000) The effect of tree height on crown level stomatal conductance. Plant Cell Environ 23:365–375

    Google Scholar 

  • Schleser GH (1990) Investigations of the δ13C pattern in leaves of Fagus sylvatica L. J Exp Bot 41:565–572

    CAS  Google Scholar 

  • Schleser GH (1992) δ13C pattern in a forest tree as an indicator of carbon transfer in trees. Ecology 73:1922–1925

    Google Scholar 

  • Schoettle AW (1994) Influence of tree size on shoot structure and physiology of Pinus contorta and Pinus aristata. Tree Physiol 14:1055–1068

    PubMed  Google Scholar 

  • Schulze E-D, Williams RJ, Farquhar GD, Schulze W, Langridge J, Miller JM, Walker BH (1998) Carbon and nitrogen isotope discrimination and nitrogen nutrition of trees along a rainfall gradient in northern Australia. Aust J Plant Physiol 25:413–425

    Google Scholar 

  • Seibt U, Rajabi A, Griffiths H, Berry JA (2008) Carbon isotopes and water-use efficiency: sense and sensitivity. Oecologia 155:441–454

    PubMed  Google Scholar 

  • Sperry JS, Hacke U, Oren R, Comstock J (2002) Water deficits and hydraulic limits to leaf water supply. Plant Cell Environ 25:251–263

    PubMed  Google Scholar 

  • Sperry JS, Hacke UG, Pittermann J (2006) Size and function in conifer tracheids and angiosperm vessels. Am J Bot 93:1490–1500

    PubMed  Google Scholar 

  • Steppe K, Niinemets Ü, Teskey RO (2011) Tree size- and age-related changes in leaf physiology and their influence on carbon gain. In: Meinzer FC, Lachenbruch B, Dawson TE (eds.) Size- and age-related changes in tree structure and function. Springer, Dordrecht

    Google Scholar 

  • Sternberg L da SL, Mulkey SS, Wright SJ (1989) Ecological interpretation of leaf carbon isotope ratios: influence of recycled carbon dioxide. Ecology 70:1317–1324

    Google Scholar 

  • Tate KR, Scott NA, Ross DJ, Parshotam A, Claydon JJ (2000) Plant effects on soil carbon storage and turnover in a montane beech (Nothofagus) forest and adjacent tussock grassland in New Zealand. Aust J Soil Res 38:685–698

    Google Scholar 

  • Tenhunen JD, Lange OL, Gebel J, Beyschlag W, Weber JA (1984) Changes in photosynthetic capacity, carboxylation efficiency, and CO2 compensation point associated with midday stomatal closure and midday depression of net CO2 exchange of leaves of Quercus suber. Planta 162:193–203

    CAS  Google Scholar 

  • Terashima I, Araya T, Miyazawa S, Sone K, Yano S (2005) Construction and maintenance of the optimal photosynthetic systems of the leaf, herbaceous plant, and tree: an eco-developmental treatise. Ann Bot 95:507–519

    PubMed  CAS  Google Scholar 

  • Thomas SC (2011) Age-related changes in tree growth and functional biology: the role of reproduction. In: Meinzer FC, Lachenbruch B, Dawson TE (eds.) Size- and age-related changes in tree structure and function. Springer, Dordrecht

    Google Scholar 

  • Thomas SC, Bazzaz FA (1999) Asymptotic height as a predictor of photosynthetic characteristics in Malaysian rain forest trees. Ecology 80:1607–1622

    Google Scholar 

  • Vitousek PM, Field CB, Matson PA (1990) Variation in foliar δ13C in Hawaiian Metrosideros polymorpha: a case of internal resistance? Oecologia 84:362–370

    Google Scholar 

  • Ward JK, Harris JM, Cerling TE, Wiedenhoeft A, Lott MJ, Dearing M-D, Coltrain JB, Ehleringer JR (2005) Carbon starvation in glacial trees recovered from the La Brea tar pits, southern California. Proc Natl Acad Sci U S A 102:690–694

    PubMed  CAS  Google Scholar 

  • Waring RH, Silvester WB (1994) Variation in foliar 13C values within the crowns of Pinus radiata trees. Tree Physiol 14:1203–1213

    PubMed  Google Scholar 

  • Warren CR, Adams MA (2000) Water availability and branch length determine δ13C in foliage of Pinus pinaster. Tree Physiol 20:637–643

    PubMed  Google Scholar 

  • Warren CR, Adams MA (2006) Internal conductance does not scale with photosynthetic capacity: implications for carbon isotope discrimination and the economics of water and nitrogen use in photosynthesis. Plant Cell Environ 29:192–201

    PubMed  CAS  Google Scholar 

  • Warren CR, McGrath JF, Adams MA (2001) Water availability and carbon isotope discrimination in conifers. Oecologia 127:476–486

    Google Scholar 

  • Warren CR, Ethier GJ, Livingston NJ, Grant NJ, Turpin DH, Harrison DL, Black TA (2003) Transfer conductance in second growth Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco) canopies. Plant Cell Environ 26:1215–1227

    CAS  Google Scholar 

  • Whitehead D (1998) Regulation of stomatal conductance and transpiration in forest canopies. Tree Physiol 18:633–644

    PubMed  Google Scholar 

  • Winner WE, Thomas S, Berry J, Bond BJ, Cooper CE, Hinckley TM, Ehleringer JR, Fessenden JE, Lamb B, McCarthy S, McDowell NG, Phillips N, Williams M (2004) Canopy carbon gain and water use: analysis of old-growth conifers in the Pacific Northwest. Ecosystems 7:482–497

    Google Scholar 

  • Woodruff DR, Meinzer FC (2011) Size-dependent changes in biophysical control of tree growth: the role of turgor. In: Meinzer FC, Lachenbruch B, Dawson TE (eds.) Size- and age-related changes in tree structure and function. Springer, Dordrecht

    Google Scholar 

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

    Google Scholar 

  • Woodruff DR, Meinzer FC, Lachenbruch B, Johnson DM (2009) Coordination of leaf structure and gas exchange along a height gradient in a tall conifer. Tree Physiol 29:261–272

    PubMed  CAS  Google Scholar 

  • Xu ZH, Saffigna PG, Farquhar GD, Simpson JA, Haines RJ, Walker S, Osborne DO, Guinto D (2000) Carbon isotope discrimination and oxygen isotope composition in clones of the F1 hybrid between slash pine and Caribbean pine in relation to tree growth, water-use efficiency and foliar nutrient concentration. Tree Physiol 20:1209–1218

    PubMed  CAS  Google Scholar 

  • Yoder BJ, Ryan MG, Waring RH, Schoettle AW, Kaufmann MR (1994) Evidence of reduced photosynthetic rates in old trees. For Sci 40(3):513–527

    Google Scholar 

  • Zhang J, Fins L, Marshall JD (1994) Stable carbon isotope discrimination, photosynthetic gas exchange, and growth differences among western larch families. Tree Physiol 14:53l–539

    Google Scholar 

Download references

Acknowledgments

We are grateful to the hundreds of scientists who have devoted long and challenging hours accessing tall trees to understand the fundamental constraints to tree size. We appreciate the generous provision of unpublished canopy-top samples from Maurizio Mencuccini, Walter Oechel, and Eladio Cornejo-Oviedo, and Renee Brooks for analyses of these samples. We are grateful for the shotgun assistance of Julian Licata and Andrew Schauer. Thoughtful edits were provided from three anonymous reviewers. Funding support during the writing of this manuscript was provided by DOE-BER and LANL-LDRD (N.G.M and L.T.H.), the National Science Foundation (DEB-0110142 and DEB-0823380, B.J.B.), a Hayward Scholarship from Landcare Research New Zealand (M.G.R.) and the Foundation for Research Science and Technology New Zealand (D.W.).

Author information

Authors and Affiliations

  1. Earth and Environmental Sciences Division, Los Alamos National Lab, MS-J495, Los Alamos, NM, 87544, USA

    Nate G. McDowell & Lee T. Dickman

  2. Department of Forest Ecosystems and Society, Oregon State University, 330 Richardson Hall, Corvallis, OR, 97331, USA

    Barbara J. Bond

  3. Laboratory for Studies of the Forest Carbon Cycle, Rocky Mountain Research Station, USDA Forest Service, 240 West Prospect Road, Fort Collins, CO, 80526, USA

    Michael G. Ryan

  4. Colorado State University, Fort Collins, CO, 80523, USA

    Michael G. Ryan

  5. Landcare Research, 40, Lincoln, 7640, New Zealand

    David Whitehead

Authors
  1. Nate G. McDowell
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Barbara J. Bond
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lee T. Dickman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michael G. Ryan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. David Whitehead
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nate G. McDowell .

Editor information

Editors and Affiliations

  1. Forestry Sciences Lab., Ecosystem Processes Program, USDA Forest Service, SW. Jefferson Way 3200, Corvallis, 97331, Oregon, USA

    Frederick C. Meinzer

  2. , Department of Wood Science and Engineeri, Oregon State University, Richardson Hall 119, Corvallis, 97331, Oregon, USA

    Barbara Lachenbruch

  3. Dept. Integrative Biology, University of California, Berkeley, Berkeley, 94720, California, USA

    Todd E. Dawson

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

McDowell, N.G., Bond, B.J., Dickman, L.T., Ryan, M.G., Whitehead, D. (2011). Relationships Between Tree Height and Carbon Isotope Discrimination. In: Meinzer, F., Lachenbruch, B., Dawson, T. (eds) Size- and Age-Related Changes in Tree Structure and Function. Tree Physiology, vol 4. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-1242-3_10

Download citation

Publish with us

Policies and ethics

Search

Navigation