Skip to main content
SpringerLink
Log in

Converging patterns of vertical variability in leaf morphology and nitrogen across seven Eucalyptus plantations in Brazil and Hawaii, USA

Trees volume 28, pages 1–15 (2014)Cite this article

Abstract

Key message

Across sites in Brazil and Hawaii, LMA and N mass were strongly correlated with height and shade index, respectively, which may help simplify canopy function modeling of Eucalyptus plantations.

Abstract

Within tree canopies, leaf mass per area (LMA) and leaf nitrogen per unit area (N area) commonly increase with height. Previous research has suggested that these patterns occur as a strategy to optimize carbon gain by allocating available resources to upper canopy leaves that are exposed to greater light availability. We tested three hypotheses about the influences of height, shade index (a proxy for light), and stand age on LMA and leaf nitrogen for even-aged Eucalyptus saligna and Eucalyptus grandis × urophylla plantations in Brazil and Hawaii, USA, spanning most of the environmental conditions found across 19.6 million ha of Eucalyptus spp. plantations around the world. Shade index was developed by incorporating canopy depth (inner-crown shading) and a tree height ratio relative to neighbor trees (shading from other trees). Across all sites and ages, leaf height accounted for 45 % of the variation in LMA, whereas shade index accounted for only 6 %. A combination of both factors was slightly better in accounting for LMA variation than height alone. LMA–height relationships among sites were strongest under greater light availability and in older stands. Leaf nitrogen per unit mass (N mass) consistently decreased with shade index, whereas N area showed no consistent pattern with height or shade index. These relationships indicate that N mass is primarily driven by light, while height is the primary driver for LMA. The general relationships between LMA and leaf N mass across all sites may simplify canopy function modeling of E. saligna and E. grandis × urophylla plantations.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

39,95 €

Price includes VAT (Finland)

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  • Anderson DR (2008) Model based inference in the life sciences: a primer on evidence. Springer, New York, London

    Book  Google Scholar 

  • Anten NPR, Miyazawa K, Hikosaka K, Nagashima H, Hirose T (1998) Leaf nitrogen distribution in relation to leaf age and photon flux density in dominant and subordinate plants in dense stands of a dicotyledonous herb. Oecologia 113:314–324

    Article  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

    Article  Google Scholar 

  • Binkley D, Stape JL, Bauerle WL, Ryan MG (2010) Explaining growth of individual trees: light interception and efficiency of light use by Eucalyptus at four sites in Brazil. Forest Ecol Manag 259:1704–1713

    Article  Google Scholar 

  • 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 120:183–192

    Article  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

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Burns RM, Honkala BH (1990) Silvics of North America. U.S Department of Agriculture, Forest Service, Washington

    Google Scholar 

  • Cavaleri MA, Oberbauer SF, Ryan MG (2008) Foliar and ecosystem respiration in an old-growth tropical rain forest. Plant Cell Environ 31:473–483

    Article  CAS  PubMed  Google Scholar 

  • Cavaleri MA, Oberbauer SF, Clark DB, Clark DA, Ryan MG (2010) Height is more important than light in determining leaf morphology in a tropical forest. Ecology 91:1730–1739

    Article  PubMed  Google Scholar 

  • Ellsworth DS, Reich PB (1993) Canopy structure and vertical patterns of photosynthesis and related leaf traits in a deciduous forest. Oecologia 96:169–178

    Article  Google Scholar 

  • England JR, Attiwill PM (2006) Changes in leaf morphology and anatomy with tree age and height in the broadleaved evergreen species, Eucalyptus regnans F. Muell. Trees-Struct Funct 20:79–90

    Article  Google Scholar 

  • England JR, 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

    Article  PubMed  Google Scholar 

  • Evans JR (1983) Nitrogen and photosynthesis in the flag leaf of wheat (Triticum aestivum L.). Plant Physiol 72:297–302

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Evans JR (1986) The Relationship between carbon-dioxide-limited photosynthetic rate and ribulose-1,5-bisphosphate-carboxylase content in two nuclear-cytoplasm substitution lines of wheat, and the coordination of ribulose-bisphosphate-carboxylation and electron-transport capacities. Planta 167:351–358

    Article  CAS  PubMed  Google Scholar 

  • Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19

    Article  Google Scholar 

  • Field C (1983) Allocating leaf nitrogen for the maximization of carbon gain: leaf age as a control on the allocation program. Oecologia 56:341–347

    Article  Google Scholar 

  • Gominho J, Figueira J, Rodrigues JC, Pereira H (2001) Within-tree variation of heartwood, extractives and wood density in the Eucalypt hybrid Urograndis (Eucalyptus grandis × E. urophylla). Wood Fiber Sci 33:3–8

    CAS  Google Scholar 

  • Gower ST, Norman JM (1991) Rapid estimation of leaf-area index in conifer and broad-leaf plantations. Ecology 72:1896–1900

    Article  Google Scholar 

  • Hanson PJ, Amthor JS, Wullschleger SD, Wilson KB, Grant RF, Hartley A, Hui D, Hunt ER, Johnson DW, Kimball JS, King AW, Luo Y, McNulty SG, Sun G, Thornton PE, Wang S, Williams M, Baldocchi DD, Cushman RM (2004) Oak forest carbon and water simulations: model intercomparisons and evaluations against independent data. Ecol Monogr 74:443–489

    Article  Google Scholar 

  • Hellkvist J, Richards GP, Jarvis PG (1974) Vertical gradients of water potential and tissue water relations in Sitka spruce trees measured with pressure chamber. J Appl Ecol 11:637–667

    Article  Google Scholar 

  • Hirose T, Werger MJA (1987) Maximizing daily canopy photosynthesis with respect to the leaf nitrogen allocation pattern in the canopy. Oecologia 72:520–526

    Article  Google Scholar 

  • Hollinger DY (1989) Canopy organization and foliage photosynthetic capacity in a broad-leaved evergreen montane forest. Funct Ecol 3:53–62

    Article  Google Scholar 

  • Hsiao TC (1973) Plant responses to water stress. Annu Rev Plant Phys 24:519–570

    Article  CAS  Google Scholar 

  • Hutchison BA, Matt DR, Mcmillen RT, Gross LJ, Tajchman SJ, Norman JM (1986) The architecture of a deciduous forest canopy in eastern Tennessee, USA. J Ecol 74:635–646

    Article  Google Scholar 

  • Iglesias-Trabedo G, Wilstermann D (2008) Eucalyptus universalis. Global cultivated eucalypt forests map 2008. Version 1.0.1. In: GIT Forestry Consulting’s EUCALYPTOLOGICS. Retrieved from www.git-forestry.com [March 29th 2009]

  • Ishii H, Reynolds JH, Ford ED, Shaw DC (2000) Height growth and vertical development of an old-growth Pseudotsuga-Tsuga forest in southwestern Washington State, USA. Can J Forest Res 30:17–24

    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

    Article  PubMed  Google Scholar 

  • Iversen CM, Norby RJ (2008) Nitrogen limitation in a sweetgum plantation: implications for carbon allocation and storage. Can J Forest Res 38:1021–1032

    Article  CAS  Google Scholar 

  • Kenzo T, Ichie T, Watanabe Y, Yoneda R, Ninomiya I, Koike T (2006) Changes in photosynthesis and leaf characteristics with tree height in five dipterocarp species in a tropical rain forest. Tree Physiol 26:865–873

    Article  CAS  PubMed  Google Scholar 

  • King DA (1999) Juvenile foliage and the scaling of tree proportions, with emphasis on Eucalyptus. Ecology 80:1944–1954

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Laclau JP, Almeida JCR, Goncalves JLM, Saint-Andre L, Ventura M, Ranger J, Moreira RM, Nouvellon Y (2009) Influence of nitrogen and potassium fertilization on leaf lifespan and allocation of above-ground growth in Eucalyptus plantations. Tree Physiol 29:111–124

    Article  CAS  PubMed  Google Scholar 

  • Leverenz J, Deans JD, Ford ED, Jarvis PG, Milne R, Whitehead D (1982) Systematic spatial variation of stomatal conductance in a Sitka spruce plantation. J Appl Ecol 19:835–851

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Meinzer FC, Bond BJ, Karanian JA (2008) Biophysical constraints on leaf expansion in a tall conifer. Tree Physiol 28:197–206

    Article  PubMed  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

    Article  PubMed  Google Scholar 

  • Nobel PS (1977) Internal leaf area and cellular CO2 resistance—photosynthetic implications of variations with growth-conditions and plant species. Physiol Plant 40:137–144

    Article  CAS  Google Scholar 

  • Nobel PS, Zaragoza LJ, Smith WK (1975) Relation between mesophyll surface-area, photosynthetic rate, and illumination level during development for leaves of Plectranthus parviflorus Henckel. Plant Physiol 55:1067–1070

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nouvellon Y, Laclau JP, Epron D, Kinana A, Mabiala A, Roupsard O, Bonnefond JM, le Maire G, Marsden C, Bontemps JD, Saint-Andre L (2010) Within-stand and seasonal variations of specific leaf area in a clonal Eucalyptus plantation in the Republic of Congo. Forest Ecol Manag 259:1796–1807

    Article  Google Scholar 

  • Reich PB, Ellsworth DS, Walters MB, Vose JM, Gresham C, Volin JC, Bowman WD (1999) Generality of leaf trait relationships: a test across six biomes. Ecology 80:1955–1969

    Article  Google Scholar 

  • Rodrigo VHL, Stirling CM, Teklehaimanot Z, Nugawela A (2001) Intercropping with banana to improve fractional interception and radiation-use efficiency of immature rubber plantations. Field Crop Res 69:237–249

    Article  Google Scholar 

  • Ryan MG, Binkley D, Fownes JH, Giardina CP, Senock RS (2004) An experimental test of the causes of forest growth decline with stand age. Ecol Monogr 74:393–414

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Sack L, Melcher PJ, Liu WH, Middleton E, Pardee T (2006) How strong is intracanopy leaf plasticity in temperate deciduous trees? Am J Bot 93:829–839

    Article  PubMed  Google Scholar 

  • Scholander PF, Hammel HT, Bradstreet D, Hemmingsen EA (1965) Sap pressure in vascular plants. Science 148:339–346

    Article  CAS  PubMed  Google Scholar 

  • Smith WK, Nobel PS (1978) Influence of irradiation, soil-water potential, and leaf temperature on leaf morphology of a desert broadleaf, Encelia farinosa Gray (Compositae). Am J Bot 65:429–432

    Article  Google Scholar 

  • Stape JL, Binkley D, Ryan MG, Fonseca S, Loos RA, Takahashi EN, Silva CR, Silva SR, Hakamada RE, Ferreira JMA, Lima AMN, Gava JL, Leite FP, Andrade HB, Alves JM, Silva GGC, Azevedo MR (2010) The Brazil Eucalyptus Potential Productivity Project: influence of water, nutrients and stand uniformity on wood production. Forest Ecol Manag 259:1684–1694

    Article  Google Scholar 

  • Thomas SC, Winner WE (2002) Photosynthetic differences between saplings and adult trees: an integration of field results by meta-analysis (vol 22, p 117, 2002). Tree Physiol 22:817–817

    Article  Google Scholar 

  • Thomas D, Henson M, Joe B, Boyton S, Dickson R (2009) Review of growth and wood quality of plantation-grown Eucalyptus dunnii Maiden. Austral For 72:3–11

    Article  Google Scholar 

  • Turnbull JW (1999) Eucalypt plantations. New Forest 17:37–52

    Article  Google Scholar 

  • Walters GA (1973) Growth of Saligna eucalyptus: a spacing study after 10 years. J Forest 71:346–348

    Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

Download references

Acknowledgments

We thank the more than 100 people involved in Brazil Eucalyptus Potential Productivity Study (especially the project leader Jose Luiz Stape) and the companies that funded the work. Randy Senock, Christian Giardina, Holly Barnard, and James Fownes were particularly important in the Hawaii project, which was supported by National Science Foundation grants DEB93-06356 and DEB97-0852. MG Ryan was supported by a CSIRO McMaster’s Fellowship during the preparation of this manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. School of Forest Resources and Environmental Science, Michigan Technological University, U.J. Noblet Building, 1400 Townsend Dr, Houghton, MI, 49931, USA

    Adam P. Coble, Alisha Autio & Molly A. Cavaleri

  2. Department of Ecosystem Science and Sustainability, Colorado State University, Fort Collins, CO, 80523, USA

    Dan Binkley & Michael G. Ryan

  3. Natural Resource Ecology Laboratory, Colorado State University, Fort Collins, CO, 80523, USA

    Dan Binkley & Michael G. Ryan

  4. Emeritus, USDA Forest Service, Rocky Mountain Research Station, Fort Collins, CO, 80526, USA

    Michael G. Ryan

Authors
  1. Adam P. Coble
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alisha Autio
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Molly A. Cavaleri
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dan Binkley
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michael G. Ryan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Adam P. Coble.

Additional information

Communicated by J. Penuelas.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Coble, A.P., Autio, A., Cavaleri, M.A. et al. Converging patterns of vertical variability in leaf morphology and nitrogen across seven Eucalyptus plantations in Brazil and Hawaii, USA. Trees 28, 1–15 (2014). https://doi.org/10.1007/s00468-013-0925-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-013-0925-6

Keywords

  • Canopy position
  • Eucalyptus
  • Foliar morphology
  • Leaf mass per area
  • Leaf nitrogen
  • Vertical gradients

Search

Navigation