, Volume 182, Issue 3, pp 713–730 | Cite as

Hydraulic constraints modify optimal photosynthetic profiles in giant sequoia trees

  • Anthony R. Ambrose
  • Wendy L. Baxter
  • Christopher S. Wong
  • Stephen S. O. Burgess
  • Cameron B. Williams
  • Rikke R. Næsborg
  • George W. Koch
  • Todd E. Dawson
Physiological ecology - original research


Optimality theory states that whole-tree carbon gain is maximized when leaf N and photosynthetic capacity profiles are distributed along vertical light gradients such that the marginal gain of nitrogen investment is identical among leaves. However, observed photosynthetic N gradients in trees do not follow this prediction, and the causes for this apparent discrepancy remain uncertain. Our objective was to evaluate how hydraulic limitations potentially modify crown-level optimization in Sequoiadendron giganteum (giant sequoia) trees up to 90 m tall. Leaf water potential (Ψ l ) and branch sap flow closely followed diurnal patterns of solar radiation throughout each tree crown. Minimum leaf water potential correlated negatively with height above ground, while leaf mass per area (LMA), shoot mass per area (SMA), leaf nitrogen content (%N), and bulk leaf stable carbon isotope ratios (δ13C) correlated positively with height. We found no significant vertical trends in maximum leaf photosynthesis (A), stomatal conductance (g s), and intrinsic water-use efficiency (A/g s), nor in branch-averaged transpiration (E L), stomatal conductance (G S), and hydraulic conductance (K L). Adjustments in hydraulic architecture appear to partially compensate for increasing hydraulic limitations with height in giant sequoia, allowing them to sustain global maximum summer water use rates exceeding 2000 kg day−1. However, we found that leaf N and photosynthetic capacity do not follow the vertical light gradient, supporting the hypothesis that increasing limitations on water transport capacity with height modify photosynthetic optimization in tall trees.


Sequoiadendron giganteum Sap flow Hydraulic conductance Tree size Hydraulic limitation Xylem conduit widening 



We are grateful to the Save the Redwoods League, which supported this work through the Redwoods and Climate Change Initiative. We thank Rob York with the UC Berkeley Center for Forestry for permission to work at Whitaker’s Forest. We also thank the US National Park Service, California State Parks, California Department of Forestry and Fire Protection, and US Forest Service for research permissions and support. We thank Stephen Sillett for valuable help with field measurements, data analysis, and reviewing earlier versions of the manuscript, and Bob Van Pelt, Marie Antoine, Jim Campbell-Spickler, Russell Kramer, Tobe Sherrill, and Bryan Kotwica for field assistance. We also thank two anonymous reviewers for comments and suggestions that substantially improved the manuscript.

Author contribution statement

ARA, WLB, CSW and TED conceived and designed the study. ARA, SSOB, WLB, CSW, CBW, RRN, GWK and TED conducted the fieldwork. ARA, and SSOB analyzed the data. ARA wrote the manuscript; all others provided editorial advice and feedback.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

442_2016_3705_MOESM1_ESM.jpg (1 mb)
Supplementary material 1 (JPEG 1052 kb)


  1. Ambrose AR, Sillett SC, Dawson TE (2009) Effects of tree height on branch hydraulic, leaf structure and gas exchange in California redwoods. Plant, Cell Environ 32:743–757CrossRefGoogle Scholar
  2. Ambrose AR, Sillett SC, Koch GW, Van Pelt R, Antoine ME, Dawson TE (2010) Effects of height on treetop transpiration and stomatal conductance in coast redwood (Sequoia sempervirens). Tree Physiol 30:1260–1272CrossRefPubMedGoogle Scholar
  3. Amthor JS (1994) Scaling CO2-photosynthesis relationships from the leaf to the canopy. Photosynth Res 39:321–350CrossRefPubMedGoogle Scholar
  4. Anfodillo T, Carrao V, Carrer M, Fior C, Rossi S (2006) Convergent tapering of xylem conduits in different woody species. New Phytol 169:279–290CrossRefPubMedGoogle Scholar
  5. Anten NPR, Schieving F, Werger MJA (1995) Patterns of light and nitrogen distribution in relation to whole canopy carbon gain in C3 and C4 mono- and dicotyledonous species. Oecologia 101:504–513CrossRefGoogle Scholar
  6. Bond BJ, Farnsworth BT, Coulombe RA, Winner WE (1999) Foliage physiology and biochemistry in response to light gradients in conifers with varying shade tolerance. Oecologia 120:183–192CrossRefGoogle Scholar
  7. Brodribb TJ, Field TS (2000) Stem hydraulic supply is linked to leaf photosynthetic capacity: evidence from New Caledonian and Tasmanian rainforests. Plant Cell Environ 23:1381–1388CrossRefGoogle Scholar
  8. Brodribb TJ, Field TS, Jordan GJ (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiol 144:1890–1898CrossRefPubMedPubMedCentralGoogle Scholar
  9. Buck AL (1981) New equations for computing vapor pressure and enhancement factor. J Appl Meteorol 20:1527–1532CrossRefGoogle Scholar
  10. Buckley TN, Warren CR (2014) The role of mesophyll conductance in the economics of nitrogen and water use in photosynthesis. Photosynth Res 119:77–88CrossRefPubMedGoogle Scholar
  11. Buckley TM, Cescatti A, Farquhar GD (2013) What does optimization theory actually predict about crown profiles of photosynthetic capacity when models incorporate greater realism? Plant Cell Environ 36:1547–1563CrossRefPubMedGoogle Scholar
  12. Burgess SSO, Dawson TE (2008) Using branch and basal trunk sap flow measurements to estimate whole-plant water capacitance: a caution. Plant Soil 305:5–13CrossRefGoogle Scholar
  13. Burgess SSO, Adams MA, Turner NC, Beverly CR, Ong CK, Khan AAH, Bleby TM (2001) An improved heat pulse method to measure low and reverse rates of sap flow in woody plants. Tree Physiol 21:589–598CrossRefPubMedGoogle Scholar
  14. Burgess SSO, Pittermann J, Dawson TE (2006) Hydraulic efficiency and safety of branch xylem increases with height in Sequoia sempervirens (D.Don) crowns. Plant Cell Environ 29:229–239CrossRefPubMedGoogle Scholar
  15. Cavaleri MA, Obserbauer SF, Clark DB, Clark DA, Ryan MG (2010) Height is more important than light in determining leaf morphology in a tropical forest. Ecology 91:1730–1739CrossRefPubMedGoogle Scholar
  16. Cermák J, Kucera J, Bauerle WL, Phillips N, Hinkley TM (2007) Tree water storage and its diurnal dynamics related to sap flow and changes in stem volume in old-growth Douglas-fir trees. Tree Physiol 27:181–198CrossRefPubMedGoogle Scholar
  17. Chin ARO, Sillett SC (2016) Phenotypic plasticity of leaves enhances water-stress tolerance and promotes hydraulic conductivity in a tall conifer. Am J Bot 103:796–807CrossRefPubMedGoogle Scholar
  18. Coble AP, Cavaleri MA (2015) Light acclimation optimizes leaf functional traits despite height-related constraints in a canopy shading experiment. Oecologia 177:1131–1143CrossRefPubMedGoogle Scholar
  19. Coble AP, Autio A, Cavaleri MA, Binkley D, Ryan MG (2014) Converging patterns of vertical variability in leaf morphology and nitrogen across seven Eucalyptus plantations in Brazil and Hawaii, USA. Trees 28:1–15CrossRefGoogle Scholar
  20. Dewar RD, Taravainen L, Parker K, Wallin G, McMurtrie RE (2012) Why does leaf nitrogen decline within tree canopies less rapidly than light? An explanation from optimization subject to a lower bound on leaf mass per area. Tree Physiol 32:520–534CrossRefPubMedGoogle Scholar
  21. 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 Nat Acad Sci USA 105:12069–12074CrossRefPubMedPubMedCentralGoogle Scholar
  22. Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19CrossRefGoogle Scholar
  23. Farquhar GD (1989) Models of integrated photosynthesis of cell and leaves. Philosophical Trans Royal Soc Lond Ser B 323:357–367CrossRefGoogle Scholar
  24. Farquhar GD, O’Leary MH, Berry JA (1982) On the relationships between carbon isotope discrimination and the intercellular carbon dioxide concentrations in leaves. Aust J Plant Physiol 9:121–137CrossRefGoogle Scholar
  25. Field CB (1983) Allocating leaf nitrogen for maximization of carbon gain: leaf age as a control on the allocation program. Oecologia 56:341–347CrossRefGoogle Scholar
  26. Field CB, Mooney HA (1986) The photosynthesis-nitrogen relationship in wild plants. In: Givnish TJ (ed) On the economy of plant form and function. Cambridge University Press, Cambridge, pp 25–55Google Scholar
  27. Flexas J, Ribas-Carbo M, Diaz-Espejo A, Galmés J, Medrano H (2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant Cell Environ 31:602–621CrossRefPubMedGoogle Scholar
  28. Goldstein GG, Andrade JL, Meinzer FC, Holbrook NM, Cavalier J, Jackon P, Celis A (1998) Stem water storage and diurnal patterns of water use in tropical forest canopy trees. Plant Cell Environ 21:397–406CrossRefGoogle Scholar
  29. Han Q (2011) Height-related decreases in mesophyll conductance, leaf photosynthesis and compensating adjustments associated with leaf nitrogen concentrations in Pinus densiflora. Tree Physiol 31:976–984CrossRefPubMedGoogle Scholar
  30. Hassiotou F, Ludwig M, Renton M, Veneklaas EJ, Evans JR (2009) Influence of leaf dry mass per area, CO2, and irradiance on mesophyll conductance in schlerophylls. J Exp Bot 60:23030–23140CrossRefGoogle Scholar
  31. Hatton TJ, Catchpole EA, Vertessey RA (1990) Integration of sap-flow velocity in elliptical streams. Tree Physiol 11:185–196CrossRefGoogle Scholar
  32. Hellkvist J, Richards GP, Jarvis PG (1974) Vertical gradients of water potential and tissue water relations in Sitka spruce trees measured with the pressure chamber. J Appl Ecol 11:637–667CrossRefGoogle Scholar
  33. Hirose T, Werger MJA (1987) Maximizing daily canopy photosynthesis with respect to the leaf nitrogen allocation pattern in the canopy. Oecologia 72:520–526CrossRefGoogle Scholar
  34. Hirose T, Ackerly DD, Traw MB, Ramseier D, Bazzaz FA (1997) CO2, elevation, canopy photosynthesis, and optimal leaf area index. Ecology 78:2339–2350Google Scholar
  35. Hollinger DY (1996) Optimality and nitrogen allocation in a tree canopy. Tree Physiol 16:627–634CrossRefPubMedGoogle Scholar
  36. Hsaio TC (1973) Plant responses to water stress. Ann Rev Plant Physiol 24:519–570CrossRefGoogle Scholar
  37. Hubbard RM, Bond BJ, Ryan MG (1999) Evidence that hydraulic conductance limits photosynthesis in old Pinus ponderosa trees. Tree Physiol 19:165–172CrossRefPubMedGoogle Scholar
  38. 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 22:575–581CrossRefPubMedGoogle Scholar
  39. Ishii HT, Jennings GM, Sillett SC, Koch GW (2008) Hydrostatic constraints on morphological exploitation of light in tall Sequoia sempervirens trees. Oecologia 156:751–763CrossRefPubMedGoogle Scholar
  40. Ishii HR, Azuma W, Kuroda K, Sillett SC (2014) Pushing the limits to tree height: could foliar water storage compensate for hydraulic constraints in Sequoia sempervirens? Funct Ecol 28:1087–1093CrossRefGoogle Scholar
  41. Jarvis PG, McNaughton KG (1986) Stomatal control of transpiration: scaling up from leaf to region. Adv Ecol Res 15:1–49CrossRefGoogle Scholar
  42. Jerez M, Dean TJ, Roberts SD, Evans DL (2004) Patterns of branch permeability with crown depth among loblolly pine families differing in growth rate and crown size. Trees 18:145–150CrossRefGoogle Scholar
  43. Kattge J, Knorr W, Raddatz T, Wirth C (2009) Quantifying photosynthetic capacity and its relationship to leaf nitrogen content for global-scale terrestrial biosphere models. Glob Change Biol 15:976–991CrossRefGoogle Scholar
  44. Katul G, Leuning R, Oren R (2003) Relationship between plant hydraulic and biochemical properties derived from a steady-state coupled water and carbon transport model. Plant Cell Environ 26:339–350CrossRefGoogle Scholar
  45. Koch GW, Sillett SC, Jennings GM, Davis SD (2004) The limits to tree height. Nature 428:851–854CrossRefPubMedGoogle Scholar
  46. Lemoine D, Cochard H, Granier A (2002) Within crown variation in hydraulic architecture in beech (Fagus sylvatica L.): evidence for a stomatal control of xylem embolism. Ann For Sci 59:19–27CrossRefGoogle Scholar
  47. Lloyd J, Patiño S, Paiva RQ et al (2010) Optimisation of photosynthetic carbon gain and within-canopy gradients of associated foliar traits for Amazon forest trees. Biogeosciences 7:1833–1859CrossRefGoogle Scholar
  48. Marshall JD, Monserud RA (2003) Foliage height influences specific leaf area of three conifer species. Can J For Res 33:164–170CrossRefGoogle Scholar
  49. McDowell NG, Bond BJ, Dickman LT, Ryan MG, Whitehead D (2011) Relationship between tree height and carbon isotope discrimination. In: Lachenbruch B, Dawson TE (eds) Meinzer FC. Size- and age-related changes in tree structure and function. Spring, Berlin, pp 255–286Google Scholar
  50. Meinzer FC, Bond BJ, Warren JM, Woodruff DR (2005) Does water transport scale universally with tree size? Funct Ecol 19:558–565CrossRefGoogle Scholar
  51. Meinzer FC, Bond BJ, Karanian JA (2008) Biophysical constraints on leaf expansion in a tall conifer. Tree Physiol 28:197–206CrossRefPubMedGoogle Scholar
  52. Meir P, Kruijt B, Broadmeadow M, Barbosa E, Kull O, Carswell F, Nobre A, Jarvis P (2002) Acclimation of photosynthetic capacity to irradiance in tree canopies in relation to leaf nitrogen and leaf mass per unit area. Plant Cell Environ 25:343–357CrossRefGoogle Scholar
  53. Mullin LP, Sillett SC, Koch GW, Tu KP, Antoine ME (2009) Physiological consequences of height-related morphological variation in Sequoia sempervirens foliage. Tree Physiol 29:999–1010CrossRefPubMedGoogle Scholar
  54. Nadezhdina N, Cermák J, Ceulemans R (2002) Radial patterns of sap flow in woody stems of dominant and understory species: scaling errors associated with positioning of sensors. Tree Physiol 22:907–918CrossRefPubMedGoogle Scholar
  55. Nardini A, Grego F, Trifilò P, Salleo S (2010) Changes of xylem sap ionic content and stem hydraulics in response to irradiance in Laurus nobilis. Tree Physiol 30:628–635CrossRefPubMedGoogle Scholar
  56. Niinemets Ü (1999) Components of leaf dry mass per area—thickness and density—alter leaf photosynthetic capacity in reverse directions in woody plants. New Phytol 144:35–47CrossRefGoogle Scholar
  57. Niinemets Ü (2007) Photosynthesis and resource distribution through plant canopies. Plant Cell Environ 30:1052–1071CrossRefPubMedGoogle Scholar
  58. Niinemets Ü (2010) 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 25:693–714CrossRefGoogle Scholar
  59. Niinemets Ü (2012) Optimization of foliage photosynthetic capacity in tree canopies: towards identifying missing constraints. Tree Physiol 32:505–509CrossRefPubMedGoogle Scholar
  60. Niinemets U, Diaz-Espejo A, Flexas J, Galmes J, Warren CR (2009) Role of mesophyll diffusion in constraining potential photosynthetic productivity in the field. J Exp Bot 60:2249–2270CrossRefPubMedGoogle Scholar
  61. Niinemets Ü, Keenan TF, Hallik L (2015) A worldwide analysis of within-canopy variations in leaf structural, chemical and physiological traits across plant functional types. New Phytol 205:973–993CrossRefPubMedGoogle Scholar
  62. Nonami H, Boyer JS (1990) Wall extensibility and cell hydraulic conductivity decrease in enlarging stem tissues at low water potentials. Plant Physiol 93:1610–1619CrossRefPubMedPubMedCentralGoogle Scholar
  63. Oldham AR, Sillett SC, Temescu AMF, Koch GW (2010) The hydrostatic gradient, not light availability, drives height-related variation in Sequoia sempervirens (Cupressaceae) leaf anatomy. Am J Bot 97:1087–1097CrossRefPubMedGoogle Scholar
  64. Oren R, Werk KS, Schulze E-D (1986) Relationships between foliage and conducting xylem in Picea abies (L.) Karst. Trees 1:61–69CrossRefGoogle Scholar
  65. Parkhurst DF (1994) Diffusion of CO2 and other gases inside leaves. New Phytol 126:49–479CrossRefGoogle Scholar
  66. Peltoniemi MS, Duursma RA, Medlyn BE (2012) Co-optimal distribution of leaf nitrogen and hydraulic conductance in plant canopies. Tree Physiol 32:510–519CrossRefPubMedGoogle Scholar
  67. Petit G, Pfautsch S, Anfodillo T, Adams MA (2010) The challenge of tree height in Eucalyptus regans: when xylem tapering overcomes hydraulic resistance. New Phytol 187:1146–1153CrossRefPubMedGoogle Scholar
  68. Phillips N, Nagchaudhuri A, Oren R, Katul G (1997) Time constant for water transport in loblolly pine trees estimated from time series of evaporative demand and stem sapflow. Trees 11:412–419CrossRefGoogle Scholar
  69. Phillips N, Bond BJ, McDowell NG, Ryan MG (2002) Canopy and hydraulic conductance in young, mature and old Douglas-fir trees. Tree Physiol 22:205–211CrossRefPubMedGoogle Scholar
  70. Phillips NG, Ryan MG, Bond BJ, McDowell NG, Hinkley TM, Cermák J (2003) Reliance on stored water increases with tree size in three species in the Pacific Northwest. Tree Physiol 23:237–245CrossRefPubMedGoogle Scholar
  71. Poorter H, Niinemets Ü, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588CrossRefPubMedGoogle Scholar
  72. Reich PB, Ellsworth DS, Walters MB (1998) Leaf structure (specific leaf area) modulates photosynthesis-nitrogen relations: evidence from within and across species and functional groups. Funct Ecol 12:948–958CrossRefGoogle Scholar
  73. Rijkers T, Pons TL, Bongers F (2000) The effect of tree height and light availability on photosynthetic leaf traits of four neotropical species differing in shade tolerance. Funct Ecol 14:77–86CrossRefGoogle Scholar
  74. Ryan MG, Yoder BJ (1997) Hydraulic limits to tree height and tree growth. Bioscience 47:235–242CrossRefGoogle Scholar
  75. Ryan MG, Bond BJ, Law BE, Hubbard RM, Woodruff D, Cienciala E, Kucera J (2000) Transpiration and whole-tree conductance in ponderosa pine trees of different heights. Oecologia 124:553–560CrossRefGoogle Scholar
  76. Ryan MG, Phillips N, Bond BJ (2006) The hydraulic limitation hypothesis revisited. Plant Cell Environ 29:367–381CrossRefPubMedGoogle Scholar
  77. Sands PJ (1995) Modeling canopy production. I. Optimal distribution of photosynthetic resources. Aust J Plant Physiol 22:593–601CrossRefGoogle Scholar
  78. Santiago LS, Kitajima K, Wright SJ, Mulkey SS (2004) Coordinated changes in photosynthesis, water relations and leaf nutritional traits of canopy trees along a precipitation gradient in lowland tropical forest. Oecologia 139:495–502CrossRefPubMedGoogle Scholar
  79. Sillett SC, Van Pelt R, Carroll AL, Kramer RD, Ambrose AR, Trask D (2015) How do tree structure and old age affect growth potential of California redwoods? Ecol Monogr 85:181–212CrossRefGoogle Scholar
  80. Simonin KA, Santiago LS, Dawson TE (2009) Fog interception by Sequoia sempervirens (D. Don) crowns decouples physiology from soil water deficit. Plant Cell Environ 32:882–892CrossRefPubMedGoogle Scholar
  81. Sprugel DG, Hinkley TM, Schaap W (1991) The theory and practice of branch autonomy. Annu Rev Ecol Syst 22:309–334CrossRefGoogle Scholar
  82. Stockoff BA (1994) Maximization of daily canopy photosynthesis: effects of herbivory on optimal nitrogen distribution. J Theor Biol 169:209–220CrossRefGoogle Scholar
  83. Tyree MT, Ewers FW (1991) The hydraulic architecture of trees and other woody plants. New Phytol 119:345–360CrossRefGoogle Scholar
  84. Woodruff DR, Bond BJ, Meinzer FC (2004) Does turgor limit growth in tall trees? Plant, Cell Environ 27:229–1236CrossRefGoogle Scholar
  85. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827CrossRefPubMedGoogle Scholar
  86. Wright IJ, Leisham MR, Read C, Westoby M (2006) Gradients in light availability and leaf traits with leaf age and canopy position in 28 Australian shrubs and trees. Funct Plant Biol 43:407–419CrossRefGoogle Scholar
  87. Wullschleger SD, Meinzer FC, Vertessey RA (1998) A review of whole-plant water use studies in trees. Tree Physiol 18:499–512CrossRefPubMedGoogle Scholar
  88. Zeppel M (2013) Convergence of tree water use and hydraulic architecture in water-limited regions: a review and synthesis. Ecohydrology 6:889–900Google Scholar
  89. Zhang Y, Equiza MA, Zheng Q, Tyree MT (2011) Factors controlling plasticity of leaf morphology in Robinia pseudoacacia: III. Biophysical constraints on leaf expansion under long-term water stress. Physiol Plant 143:367–374CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Anthony R. Ambrose
    • 1
  • Wendy L. Baxter
    • 1
  • Christopher S. Wong
    • 1
  • Stephen S. O. Burgess
    • 2
  • Cameron B. Williams
    • 1
  • Rikke R. Næsborg
    • 1
  • George W. Koch
    • 3
  • Todd E. Dawson
    • 1
  1. 1.Department of Integrative BiologyUniversity of CaliforniaBerkeleyUSA
  2. 2.School of Plant BiologyUniversity of Western AustraliaPerthAustralia
  3. 3.Department of Biological SciencesNorthern Arizona UniversityFlagstaffUSA

Personalised recommendations