Skip to main content
Log in

Concentrative nitrogen allocation to sun-lit branches and the effects on whole-plant growth under heterogeneous light environments

  • Physiological ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

We investigated the nitrogen and carbohydrate allocation patterns of trees under heterogeneous light environments using saplings of the devil maple tree (Acer diabolicum) with Y-shaped branches. Different branch groups were created: all branches of a sapling exposed to full light (L-branches), all branches exposed to full shade (S-branches), and half of the branches of a sapling exposed to light (HL-branches) and the other half exposed to shade (HS-branches). Throughout the growth period, nitrogen was preferentially allocated to HL-branches, whereas nitrogen allocation to HS-branches was suppressed compared to L- and S-branches. HL-branches with the highest leaf nitrogen content (Narea) also had the highest rates of growth, and HS-branches with the lowest Narea had the lowest observed growth rates. In addition, net nitrogen assimilation, estimated using a photosynthesis model, was strongly correlated with branch growth and whole-plant growth. In contrast, patterns of photosynthate allocation to branches and roots were not affected by the light conditions of the other branch. These observations suggest that tree canopies develop as a result of resource allocation patterns, where the growth of sun-lit branches is favoured over shaded branches, which leads to enhanced whole-plant growth in heterogeneous light environments. Our results indicate that whole-plant growth is enhanced by the resource allocation patterns created for saplings in heterogeneous light environments.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Barbaroux C, Breda N, Dufrene E (2003) Distribution of above-ground and below-ground carbohydrate reserves in adult trees of two contrasting broad-leaved species (Quercus petraea and Fagus sylvatica). New Phytol 157:605–615

    Article  Google Scholar 

  • Beaudet M, Messier C (1998) Growth and morphological responses of yellow birch, sugar maple, and beech seedlings growing under a natural light gradient. Can J For Res 28:1007–1015

    Article  Google Scholar 

  • Brooks RJ, Schulte PJ, Bond BJ, Coulombe R, Domec JC, Hinckley TM, McDowell N, Phillips N (2003) Does foliage on the same branch compete for the same water? Experiments on Douglas-fir trees. Trees 17:101–108

    Google Scholar 

  • Dyckmans J, Flessa H (2001) Influence of tree internal N status on uptake and translocation of C and N in beech: a dual 13C and 15N labeling approach. Tree Physiol 21:395–401

    Article  PubMed  CAS  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 

  • Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90

    Article  CAS  Google Scholar 

  • Frak E, Le Roux X, Millard P, Adam B, Dreyer E, Escuit C, Sinoquet E, Grancher CV, Vandame M (2002) Spatial distribution of leaf nitrogen and photosynthetic capacity within the foliage of individual trees: disentangling the effects of local light quality, leaf irradiance, and transpiration. J Exp Bot 53:2207–2216

    Article  PubMed  CAS  Google Scholar 

  • Goulet J, Messier C, Nikinmaa E (2000) Effect of branch position and light availability on shoot growth of understory sugar maple and yellow birch saplings. Botany 78:1077–1085

    Article  Google Scholar 

  • Henriksson J (2001) Differential shading of branches or whole trees: survival, growth, and reproduction. Oecologia 126:482–486

    Article  Google Scholar 

  • Hollinger DY (1996) Optimality and nitrogen allocation in a tree canopy. Tree Physiol 16:627–634

    Article  PubMed  Google Scholar 

  • Johnson IR, Thornley JH, Frantz JM, Bugbee B (2010) A model of canopy photosynthesis incorporating protein distribution through the canopy and its acclimation to light, temperature and CO2. Ann Bot 106:735–749

    Article  PubMed  CAS  Google Scholar 

  • Kuppers M, Timm H, Orth F, Stegemann J, Stober R, Schneider H, Paliwal K, Karunaichamy K, Ortiz R (1996) Effects of light environment and successional status on lightfleck use by understory trees of temperate and tropical forests. Tree Physiol 16:69–80

    Article  PubMed  Google Scholar 

  • Lacointe A, Deleens E, Ameglio T, Saint-Joanis B, Lelarge C, Vandame M, Song GC, Daudet FA (2004) Testing the branch autonomy theory: a 13C/14C double-labelling experiment on differentially shaded branches. Plant Cell Environ 27:1159–1168

    Article  CAS  Google Scholar 

  • Le Roux X, Lacointe A, Escobar-Gutierrez A, Le Dizes S (2001) Carbon-based models of individual tree growth: a critical appraisal. Ann For Sci 58:469–506

    Article  Google Scholar 

  • Millard P, Grelet G (2010) Nitrogen storage and remobilization by trees: ecophysiological relevance in a changing world. Tree Physiol 30:1083–1095

    Article  PubMed  CAS  Google Scholar 

  • Miyashita A, Sugiura D, Sawakami K, Ichihashi R, Tani T, Tateno M (2012) Long-term, short-interval measurements of the frequency distributions of the photosynthetically active photon flux density and net assimilation rate of leaves in a cool-temperate forest. Agric For Meteorol 152:1–10

    Article  Google Scholar 

  • Niinemets U, Kull O, Tenhunen JD (2004) Within-canopy variation in the rate of development of photosynthetic capacity is proportional to integrated quantum flux density in temperate deciduous trees. Plant Cell Environ 27:293–313

    Article  CAS  Google Scholar 

  • Niinemets U (2007) Photosynthesis and resource distribution through plant canopies. Plant Cell Environ 30:1052–1071

    Article  PubMed  CAS  Google Scholar 

  • Pepin S, Livingston NJ, Whitehead D (2002) Responses of transpiration and photosynthesis to reversible changes in photosynthetic foliage area in western red cedar (Thuja plicata) seedlings. Tree Physiol 22:363–371

    Article  PubMed  CAS  Google Scholar 

  • Poorter H, Pepin S, Rijkers T, De Jong Y, Evans JR, Korner C (2006) Construction costs, chemical composition and payback time of high-and low-irradiance leaves. J Exp Bot 57:355–371

    Article  PubMed  CAS  Google Scholar 

  • Reich PB, Tjoelker MG, Pregitzer KS, Wright IJ, Oleksyn J, Machado JL (2008) Scaling of respiration to nitrogen in leaves, stems and roots of higher land plants. Ecol Lett 11:793–801

    Article  PubMed  Google Scholar 

  • Remphrey WR, Bartlett GA, Davidson CG (2002) Shoot morphology and fate of buds in relation to crown location in young Fraxinus pennsylvanica var. subintegerrima. Botany 80:1274–1282

    Article  Google Scholar 

  • Sakai S (1990) The relationship between bud scale morphology and indeterminate and determinate growth patterns in Acer (Aceraceae). Can. J. Bot 68:144–148

    Article  Google Scholar 

  • Sprugel DG, Hinckley TM, Schaap W (1991) The theory and practice of branch autonomy. Annu Rev Ecol Syst 22:309–334

    Article  Google Scholar 

  • Sprugel DG (2002) When branch autonomy fails: Milton’s Law of resource availability and allocation. Tree Physiol 22:1119–1124

    Article  PubMed  Google Scholar 

  • Stoll P, Schmid B (1998) Plant foraging and dynamic competition between branches of Pinus sylvestris in contrasting light environments. J Ecol 86:934–945

    Article  Google Scholar 

  • Sugiura D, Tateno M (2011) Optimal leaf-to-root ratio and leaf nitrogen content determined by light and nitrogen availabilities. PLoS ONE 6:e22236

    Article  PubMed  CAS  Google Scholar 

  • Takenaka A (1994) A simulation model of tree architecture development based on growth response to local light environment. J Plant Res 107:321–330

    Article  Google Scholar 

  • Takenaka A (2000) Shoot growth responses to light microenvironment and correlative inhibition in tree seedlings under a forest canopy. Tree Physiol 20:987–991

    Article  PubMed  CAS  Google Scholar 

  • Tsutsumi T (1989) Forest ecology. Asakura Syoten, Tokyo

    Google Scholar 

  • Umeki K, Seino T, Lim EM, Honjo T (2006) Patterns of shoot mortality in Betula platyphylla in northern Japan. Tree Physiol 26:623–632

    Article  PubMed  Google Scholar 

  • Vertregt N, Penning de Vries FWT (1987) A rapid method for determining the efficiency of biosynthesis of plant biomass. J Theor Biol 128:109–119

    Article  Google Scholar 

  • Vose JM, Ryan MG (2002) Seasonal respiration of foliage, fine roots, and woody tissues in relation to growth, tissue N, and photosynthesis. Glob Change Biol 8:182–193

    Article  Google Scholar 

  • Warren CR, Livingston NJ, Turpin DH (2003) Responses of gas exchange to reversible changes in whole-plant transpiration rate in two conifer species. Tree Physiol 23:793–803

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto T (2001) The effects of shading on translocation of 13C-photosynthates among 2-year-old branches during the rapid growth stage of cherry, pear, apple and Japanese persimmon fruit. J Jpn Soc Hortic Sci 70:170–177

    Article  CAS  Google Scholar 

  • Young TP, Hubbell SP (1991) Crown asymmetry, treefalls, and repeat disturbance of broad-leaved forest gaps. Ecology 72:1464–1471

    Article  Google Scholar 

Download references

Acknowledgments

We greatly thank T. Hachiya, K. Noguchi, and I. Terashima for their assistance of nitrogen analyses. We also thank for K. Koyama for his valuable comments on the early draft. This study was supported by a fellowship from the Japan Society for the Promotion of Science (JSPS) for Japanese Junior Scientists.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. Sugiura.

Additional information

Communicated by Ylo Niinemets.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 68 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sugiura, D., Tateno, M. Concentrative nitrogen allocation to sun-lit branches and the effects on whole-plant growth under heterogeneous light environments. Oecologia 172, 949–960 (2013). https://doi.org/10.1007/s00442-012-2558-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-012-2558-7

Keywords

Navigation