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Plant function and evolutionary biology
RESEARCH ARTICLE

Gradients of light availability and leaf traits with leaf age and canopy position in 28 Australian shrubs and trees

Ian J. Wright A C , Michelle R. Leishman A , Cassia Read A B and Mark Westoby A
+ Author Affiliations
- Author Affiliations

A Department of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia.

B Current address: School of Botany, The University of Melbourne, Parkville, Vic. 3010, Australia.

C Corresponding author. Email: iwright@rna.bio.mq.edu.au

D This paper originates from a presentation at ECOFIZZ 2005, North Stradbroke Island, Queensland, Australia, November 2005.

Functional Plant Biology 33(5) 407-419 https://doi.org/10.1071/FP05319
Submitted: 31 December 2005  Accepted: 9 February 2006   Published: 2 May 2006

Abstract

Light availability generally decreases vertically downwards through plant canopies. According to optimisation theory, in order to maximise canopy photosynthesis plants should allocate leaf nitrogen per area (Narea) in parallel with vertical light gradients, and leaf mass per area (LMA) and leaf angles should decrease down through the canopy also. Many species show trends consistent with these predictions, although these are never as steep as predicted. Most studies of canopy gradients in leaf traits have concerned tall herbaceous vegetation or forest trees. But do evergreen species from open habitats also show these patterns? We quantified gradients of light availability, LMA, leaf N and phosphorus (P), and leaf angle along leaf age sequences and vertical canopy profiles, across 28 woody species from open habitats in eastern Australia. The observed trends in LMA, Narea and leaf angle largely conflicted with expectations from canopy optimisation models, whereas trends in leaf P were more consistent with optimal allocation. These discrepancies most likely relate to these species having rather open canopies with quite shallow light gradients, but also suggest that modelling the co-optimisation of resources other than nitrogen is required for understanding plant canopies.

Keywords: canopy structure, leaf angle, nitrogen, optimisation models, phosphorus, photosynthesis.


Acknowledgments

Wright, Westoby and Leishman acknowledge support for their research from the Australian Research Council, in part through the ARC–NZ Research Network for Vegetation Function. Additional funding also came from a Macquarie University Research Grant to Leishman and Wright. We are also greatly indebted to David Duncan, Angela Moles, Barbara Rice and Peter Vesk for their enthusiastic assistance in the field, and to two anonymous reviewers for their helpful comments on the manuscript.


References


Ackerly DD (1992) Light, leaf age, and leaf nitrogen concentration in a tropical vine. Oecologia 89, 596–600. open url image1

Ackerly DD (1999) Self-shading, carbon gain and leaf dynamics: a test of alternative optimality models. Oecologia 119, 300–310.
Crossref | GoogleScholarGoogle Scholar | open url image1

Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Advances in Ecological Research 30, 1–67. open url image1

Anten NPR (2002) Evolutionarily stable leaf area production in plant populations. Journal of Theoretical Biology 217, 15–32.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Anten NPR (2005) Optimal photosynthetic characteristics of individual plants in vegetation stands and implications for species coexistence. Annals of Botany 95, 495–506.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

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, 504–513.
Crossref | GoogleScholarGoogle Scholar | open url image1

Aranda I, Pardo F, Gil L, Pardos JA (2004) Anatomical basis of the change in leaf mass per area and nitrogen investment with relative irradiance within the canopy of eight temperate tree species. Acta Oecologica 25, 187–194.
Crossref | GoogleScholarGoogle Scholar | open url image1

Beadle NCW (1966) Soil phosphate and its role in molding segments of the Australian flora and vegetation, with special reference to xeromorphy and scleromorphy. Ecology 47, 992–1007. open url image1

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 Physiology 20, 179–186.
PubMed |
open url image1

Chapin FS, Kedrowski RA (1983) Seasonal changes in nitrogen and phosphorus fractions and autumn retranslocation in evergreen and deciduous Taiga trees. Ecology 64, 376–391. open url image1

Close DC, Battaglia M, Davidson NJ, Beadle CL (2004) Within-canopy gradients of nitrogen and photosynthetic activity of Eucalyptus nitens and Eucalyptus globulus in response to nitrogen nutrition. Australian Journal of Botany 52, 133–140.
Crossref | GoogleScholarGoogle Scholar | open url image1

Comeau PG, Gendron F, Letchford T (1998) A comparison of several methods for estimating light under a paper birch mixedwood stand. Canadian Journal of Forest Research 28, 1843–1850.
Crossref | GoogleScholarGoogle Scholar | open url image1

Eichelmann H, Oja V, Rasulov B, Padu E, Bichele I, Pettai H, Mand P, Kull O, Laisk A (2005) Adjustment of leaf photosynthesis to shade in a natural canopy: reallocation of nitrogen. Plant, Cell & Environment 28, 389–401.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ellsworth DS, Reich PB (1993) Canopy structure and vertical patterns of photosynthesis and related leaf traits in a deciduous forest. Oecologia 96, 169–178.
Crossref | GoogleScholarGoogle Scholar | open url image1

Escudero A, Mediavilla S (2003) Decline in photosynthetic nitrogen use efficiency with leaf age and nitrogen resorption as determinants of leaf life span. Journal of Ecology 91, 880–889.
Crossref | GoogleScholarGoogle Scholar | open url image1

Falster DS, Westoby M (2003) Leaf size and angle vary widely across species: what consequences for light interception? New Phytologist 158, 509–525.
Crossref | GoogleScholarGoogle Scholar | open url image1

Farquhar GD, Buckley TN, Miller JM (2002) Optimal stomatal control in relation to leaf area and nitrogen content. Silva Fennica 36, 625–637. open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Franklin O, Agren GI (2002) Leaf senescence and resorption as mechanisms of maximizing photosynthetic production during canopy development at N limitation. Functional Ecology 16, 727–733.
Crossref | GoogleScholarGoogle Scholar | open url image1

Givnish TJ (1982) Adaptive significance of leaf height in forest herbs. American Naturalist 120, 353–381.
Crossref | GoogleScholarGoogle Scholar | open url image1

Givnish TJ (2002) Adaptive significance of evergreen vs. deciduous leaves: solving the triple paradox. Silva Fennica 36, 703–743. open url image1

Gower ST, Reich PB, Son Y (1993) Canopy dynamics and aboveground production of five tree species with different leaf longevities. Tree Physiology 12, 327–345.
PubMed |
open url image1

Gutschick VP (1981) Evolved strategies in nitrogen acquisition by plants. American Naturalist 118, 607–637.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gutschick VP, Wiegel FW (1988) Optimizing the canopy photosynthetic rate by patterns of investment in specific leaf mass. American Naturalist 132, 67–86.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hevia F, Minoletti ML, Decker KLM, Boerner REJ (1999) Foliar nitrogen and phosphorus dynamics of three Chilean Nothofagus (Fagaceae) species in relation to leaf lifespan. American Journal of Botany 86, 447–455.
Crossref | PubMed |
open url image1

Hikosaka K (1996) Effects of leaf age, nitrogen nutrition and photon flux density on the organization of the photosynthetic apparatus in leaves of a vine (Ipomoea tricolor Cav.) grown horizontally to avoid mutual shading of leaves. Planta 198, 144–150.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hikosaka K (2003) A model of dynamics of leaves and nitrogen in a canopy: an integration of canopy photosynthesis, leaf life-span, and nitrogen use efficiency. American Naturalist 162, 149–164.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hikosaka K (2005) Leaf canopy as a dynamic system: ecophysiology and optimality in leaf turnover. Annals of Botany 95, 521–533.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hikosaka K, Hirose T (1997) Leaf angle as a strategy for light competition — optimal and evolutionarily stable light-extinction coefficient within a leaf canopy. Ecoscience 4, 501–507. open url image1

Hirose T (2005) Development of the Monsi–Saeki theory on canopy structure and function. Annals of Botany 95, 483–494.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hirose T, Werger MJA (1987) Maximizing daily canopy photosynthesis with respect to the leaf nitrogen allocation pattern in the canopy. Oecologia 72, 520–526.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hollinger DY (1989) Canopy organization and foliage photosynthetic capacity in a broad-leaved evergreen montane forest. Functional Ecology 3, 53–62. open url image1

Hom JL, Oechel WC (1983) The photosynthetic capacity nutrient content and nutrient use efficiency of different needle age classes of black spruce (Picea mariana) found in interior Alaska, USA. Canadian Journal of Forest Research 13, 834–839. open url image1

Kikuzawa K, Ackerly D (1999) Significance of leaf longevity in plants. Plant Species Biology 14, 39–45.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kitajima K, Mulkey SS, Wright SJ (1997) Decline of photosynthetic capacity with leaf age in relation to leaf longevities for five tropical canopy tree species. American Journal of Botany 84, 702–708.
Crossref |
open url image1

Kull O (2002) Acclimation of photosynthesis in canopies: models and limitations. Oecologia 133, 267–279.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kuroiwa S (1971) Total photosynthesis of a foliage in relation to inclination of leaves. In ‘Prediction and measurement of photosynthetic productivity’. (Ed. I Šetlík) pp. 79–89. (Pudoc: Wageningen)

Leuning R, Cromer RN, Rance S (1991) Spatial distributions of foliar nitrogen and phosphorus in crowns of Eucalyptus grandis. Oecologia 88, 504–510. open url image1

Machado JL, Reich PB (1999) Evaluation of several measures of canopy openness as predictors of photosynthetic photon flux density in deeply shaded conifer-dominated forest understory. Canadian Journal of Forest Research 29, 1438–1444.
Crossref | GoogleScholarGoogle Scholar | open url image1

Mediavilla S, Escudero A (2003a) Leaf life span differs from retention time of biomass and nutrients in the crowns of evergreen species. Functional Ecology 17, 541–548.
Crossref | GoogleScholarGoogle Scholar | open url image1

Mediavilla S, Escudero A (2003b) Photosynthetic capacity, integrated over the lifetime of a leaf, is predicted to be independent of leaf longevity in some tree species. New Phytologist 159, 203–211.
Crossref | GoogleScholarGoogle Scholar | open url image1

Meir P, Kruijt B, Broadmeadow M, Barbosa E, Kull O, Carswell F, Nobre A, Jarvis PG (2002) Acclimation of photosynthetic capacity to irradiance in tree canopies in relation to leaf nitrogen concentration and leaf mass per unit area. Plant, Cell & Environment 25, 343–357.
Crossref | GoogleScholarGoogle Scholar | open url image1

Milla R, Castro-Diez P, Maestro-Martinez M, Montserrat-Marti G (2005) Relationships between phenology and the remobilization of nitrogen, phosphorus and potassium in branches of eight Mediterranean evergreens. New Phytologist 168, 167–178.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Monsi M, Saeki T (1953) Über den Lichtfaktor in den Pflanzengesellschaften und seine Bedeutung für die Stoffproduktion. Japanese Journal of Botany 14, 22–52. open url image1

Mooney HA, Field C, Gulmon SL, Bazzaz FA (1981) Photosynthetic capacity in relation to leaf position in desert versus old-field annuals. Oecologia 50, 109–112.
Crossref | GoogleScholarGoogle Scholar | open url image1

Mooney HA , Gulmon SL (1979) Environmental and evolutionary constraints on the photosynthetic characteristics of higher plants. In ‘Topics in plant population biology’. (Eds OT Solbrig, S Jain, GB Johnson, PR Raven) pp. 316–337. (Columbia University Press: New York)

Muraoka H, Koizumi H (2005) Photosynthetic and structural characteristics of canopy and shrub trees in a cool-temperate deciduous broadleaved forest: implication to the ecosystem carbon gain. Agricultural and Forest Meteorology 134, 39–59.
Crossref | GoogleScholarGoogle Scholar | open url image1

Nambiar EK, Fife DN (1991) Nutrient retranslocation in temperate conifers. Tree Physiology 9, 185–207.
PubMed |
open url image1

Niinemets Ü, Cescatti A, Rodeghiero M, Tosens T (2005) Leaf internal diffusion conductance limits photosynthesis more strongly in older leaves of Mediterranean evergreen broad-leaved species. Plant, Cell & Environment 28, 1552–1566.
Crossref | GoogleScholarGoogle Scholar | open url image1

Niinemets Ü, Kull O, Tenhunen JD (1998) An analysis of light effects on foliar morphology, physiology, and light interception in temperate deciduous woody species of contrasting shade tolerance. Tree Physiology 18, 681–696.
PubMed |
open url image1

Niinemets Ü, Tenhunen JD, Beyschlag W (2004) Spatial and age-dependent modifications of photosynthetic capacity in four Mediterranean oak species. Functional Plant Biology 31, 1179–1193.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ralhan PK, Singh SP (1987) Dynamics of nutrients and leaf mass in Central Himalayan forest trees and shrubs. Ecology 68, 1974–1983. open url image1

Rambal S, Damesin C, Joffre R, Methy M, Lo Seen D (1996) Optimization of carbon gain in canopies of Mediterranean evergreen oaks. Annales Des Sciences Forestieres 53, 547–560. open url image1

Read C, Wright IJ, Westoby M (2006) Scaling up from leaf to canopy-aggregate properties in sclerophyll shrub species. Austral Ecology In press 31,
Crossref |
open url image1

Reich PB, Walters MB, Ellsworth DS (1992) Leaf life-span in relation to leaf, plant, and stand characteristics among diverse ecosystems. Ecological Monographs 62, 365–392.
Crossref |
open url image1

Schieving F, Poorter H (1999) Carbon gain in a multispecies canopy: the role of specific leaf area and photosynthetic nitrogen-use efficiency in the tragedy of the commons. New Phytologist 143, 201–211.
Crossref | GoogleScholarGoogle Scholar | open url image1

Schmid B, Bazzaz FA (1994) Crown construction, leaf dynamics, and carbon gain in two perennials with contrasting architecture. Ecological Monographs 64, 177–203.
Crossref |
open url image1

Small E (1972) Photosynthetic rates in relation to nitrogen cycling as an adaptation to nutrient deficiency in peat bog plants. Canadian Journal of Botany 50, 2227–2233. open url image1

Sterner RW , Elser JJ (2002) ‘Ecological stoichiometry. The biology of elements from molecules to the biosphere.’ (Princeton University Press: Princeton Oxford)

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. Annals of Botany 95, 507–519.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Traw MB, Ackerly DD (1995) Leaf position, light levels, and nitrogen allocation in five species of rain forest pioneer trees. American Journal of Botany 82, 1137–1143.
Crossref |
open url image1

Valladares F, Pearcy RW (1999) The geometry of light interception by shoots of Heteromeles arbutifolia morphological and physiological consequences for individual leaves. Oecologia 121, 171–182.
Crossref | GoogleScholarGoogle Scholar | open url image1

Valladares F, Pugnaire FI (1999) Tradeoffs between irradiance capture and avoidance in semi-arid environments assessed with a crown architecture model. Annals of Botany 83, 459–469.
Crossref | GoogleScholarGoogle Scholar | open url image1

Warren CR, Adams MA (2000) Trade-offs between the persistence of foliage and productivity in two Pinus species. Oecologia 124, 487–494.
Crossref |
open url image1

Warren CR, Adams MA, Chen ZL (2000) Is photosynthesis related to concentrations of nitrogen and Rubisco in leaves of Australian native plants? Australian Journal of Plant Physiology 27, 407–416.
Crossref | GoogleScholarGoogle Scholar | open url image1

Webb LJ (1968) Environment relationships of the structural types of Australian rain forest vegetation. Ecology 49, 296–311. open url image1

Werger MJA, Hirose T (1991) Leaf nitrogen distribution and whole canopy photosynthetic carbon gain in herbaceous stands. Vegetatio 97, 11–20. open url image1

Werner C, Ryel RJ, Correia O, Beyschlag W (2001) Structural and functional variability within the canopy and its relevance for carbon gain and stress avoidance. Acta Oecologica 22, 129–138.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wright IJ, Reich PB, Westoby M (2001) Strategy shifts in leaf physiology, structure and nutrient content between species of high and low rainfall, and high and low nutrient habitats. Functional Ecology 15, 423–434.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wright IJ, Westoby M (2002) Leaves at low versus high rainfall: coordination of structure, lifespan and physiology. New Phytologist 155, 403–416.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wright IJ, Westoby M (2003) Nutrient concentration, resorption and lifespan: leaf traits of Australian sclerophyll species. Functional Ecology 17, 10–19.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wright IJ, Westoby M, Reich PB (2002) Convergence towards higher leaf mass per area in dry and nutrient-poor habitats has different consequences for leaf lifespan. Journal of Ecology 90, 534–543.
Crossref | GoogleScholarGoogle Scholar | open url image1