Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW

Light-acclimation of cladode photosynthetic potentials in Casuarina glauca: trade-offs between physiological and structural investments

Ülo Niinemets A B , Aljona Lukjanova C , Ashley D. Sparrow D and Matthew H. Turnbull D
+ Author Affiliations
- Author Affiliations

A Department of Plant Physiology, Institute of Molecular and Cell Biology, University of Tartu, Riia 23, Tartu 51010, Estonia. Corresponding author. Email: ylon@ut.ee

B Centro di Ecologia Alpina, I-38040 Viote del Monte Bondone (TN), Italy.

C Institute of Forestry and Rural Engineering, Estonian Agricultural University, Kreutzwaldi 5, Tartu 51014, Estonia.

D School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch 8020, New Zealand.

Functional Plant Biology 32(7) 571-582 https://doi.org/10.1071/FP05037
Submitted: 17 February 2005  Accepted: 6 April 2005   Published: 7 July 2005

Abstract

Many arid and saline habitat species possess sparse canopies with cylindrical foliage that is considered relatively invariable along environmental gradients. However, even in sparse canopies strong gradients of light develop between the canopy top and bottom. We studied structural and photosynthetic acclimation to within-canopy light gradient in Casuarina glauca Sieb. ex Spreng., the photosynthetic organs of which are cylindrical cladodes. Seasonal average integrated quantum flux density (Qint) varied 25-fold between the canopy top and the canopy bottom. Cladode cross-sectional shape was unaffected by irradiance, but cladode dry mass per unit total area (MA) varied 2-fold within the canopy light gradient. This resulted primarily from light-dependent changes in cladode thickness (volume to total area ratio,V / AT) and to a lesser extent from changes in cladode density (D, MA = DV / AT). Nitrogen content, and the volume of mesophyll per unit surface area increased with increasing Qint and V / AT, resulting in positive scaling of foliage photosynthetic potential (capacity of photosynthetic electron transport and maximum Rubisco carboxylase activity per unit area) with light. However, nitrogen content per unit dry mass and the volume fraction of mesophyll decreased with increasing irradiance. This was explained by greater fractional investment in mechanical tissues in cladodes with greater volume to surface area ratio. This trade-off between photosynthetic and support investments reduced the cladode photosynthetic plasticity. Our study demonstrates a significant acclimation potential of species with cylindrical foliage that should be included in larger-scale carbon balance estimations of arid and saline communities.

Keywords: Casuarina, cladode anatomy, cladode photosynthesis, nitrogen content, quantitative anatomy, support costs.


Acknowledgments

ÜN was an Erskine fellow of the University of Canterbury, Christchurch, New Zealand during this study. Financial support was partly provided by the Estonian Science Foundation (grants 5702, 6022), the Estonian Ministry of Education and Science (grants 0182468As03, 0432153s02), the German Academic Exchange Service (equipment grant to ÜN), and the Province of Trento, Italy (grants DL1060 and DL3402).


References


Baldocchi DD, Harley PC (1995) Scaling carbon dioxide and water vapour exchange from leaf to canopy in a deciduous forest. II. Model testing and application. Plant, Cell and Environment 18, 1157–1173. open url image1

Barrett-Lennard E (2000) Plants in saline environments: an Australian experience. Natural Resource Management 3, 9–13. open url image1

Berg RH (1994) A calcium oxalate-secreting tissue in branchlets of the Casuarinaceae. Protoplasma 183, 29–36.
Crossref | GoogleScholarGoogle Scholar | open url image1

Cramer VA, Thorburn PJ, Fraser GW (1999) Transpiration and groundwater uptake from farm forest plots of Casuarina glauca and Eucalyptus camaldulensis in saline areas of southeast Queensland, Australia. Agricultural Water Management 39, 187–204.
Crossref | GoogleScholarGoogle Scholar | open url image1

Dunn GM, Taylor DW, Nester MR, Beetson TB (1994) Performance of twelve selected Australian tree species on a saline site in southeast Queensland. Forest Ecology and Management 70, 255–264.
Crossref | GoogleScholarGoogle Scholar | open url image1

Dutta RK, Agrawal M (2001) Litterfall, litter decomposition and nutrient release in five exotic plant species planted on coal mine spoils. Pedobiologia 45, 298–312. open url image1

Frak E, Le Roux X, Millard P, Adam B, Dreyer E, Escuit C, Sinoquet H, Vandame M, Varlet-Grancher C (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. Journal of Experimental Botany 53, 2207–2216.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gibson, AC (1996). ‘Structure–function relations of warm desert plants.’ (Springer-Verlag: Berlin)

Groom PK, Lamont BB, Markey AS (1997) Influence of leaf type and plant age on leaf structure and sclerophylly in Hakea (Proteaceae). Australian Journal of Botany 45, 827–838.
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

Haase P, Pugnaire FI, Clark SC, Incoll LD (1999) Diurnal and seasonal changes in cladode photosynthetic rate in relation to canopy age structure in the leguminous shrub Retama sphaerocarpa.  Functional Ecology 13, 640–649.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hanba YT, Miyazawa SI, Terashima I (1999) The influence of leaf thickness on the CO2 transfer conductance and leaf stable carbon isotope ratio for some evergreen tree species in Japanese warm-temperate forests. Functional Ecology 13, 632–639.
Crossref | GoogleScholarGoogle Scholar | open url image1

Koike T, Kitao M, Maruyama Y, Mori S, Lei TT (2001) Leaf morphology and photosynthetic adjustments among deciduous broad-leaved trees within the vertical canopy profile. Tree Physiology 21, 951–958.
PubMed |
open url image1

Lamont BB, Groom PK, Cowling RM (2002) High leaf mass per area of related species assemblages may reflect low rainfall and carbon isotope discrimination rather than low phosphorus and nitrogen concentrations. Functional Ecology 16, 403–412.
Crossref | GoogleScholarGoogle Scholar | open url image1

Langeland, KA ,  and  Craddock Burks, K (1998). ‘Identification and biology of non-native plants in Florida’s natural areas.’ (Gainesville, FL: University of Florida)

Le Roux X, Walcroft AS, Daudet FA, Sinoquet H, Chaves MM, Rodrigues A, Osorio L (2001) Photosynthetic light acclimation in peach leaves: importance of changes in mass : area ratio, nitrogen concentration, and leaf nitrogen partitioning. Tree Physiology 21, 377–386.
PubMed |
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 and Environment 25, 343–357.
Crossref | GoogleScholarGoogle Scholar | open url image1

Morales D, González-Rodríguez AM, Čhermák J, Jiménez MS (1996) Laurel forests in Tenerife, Canary Islands: the vertical profiles of leaf characteristics. Phyton — Annales Rei Botanicae 36, 251–263. open url image1

Moro MJ, Pugnaire FI, Haase P, Puigdefábregas J (1997) Effect of the canopy of Retama sphaerocarpa on its understorey in a semiarid environment. Functional Ecology 11, 425–431.
Crossref | GoogleScholarGoogle Scholar | open url image1

Niinemets Ü (1997) Distribution patterns of foliar carbon and nitrogen as affected by tree dimensions and relative light conditions in the canopy of Picea abies.  Trees. Structure and Function 11, 144–154. open url image1

Niinemets Ü (1999) Research review. Components of leaf dry mass per area — thickness and density — alter leaf photosynthetic capacity in reverse directions in woody plants. New Phytologist 144, 35–47.
Crossref | GoogleScholarGoogle Scholar | open url image1

Niinemets Ü (2001) Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology 82, 453–469. open url image1

Niinemets Ü, Tenhunen JD (1997) A model separating leaf structural and physiological effects on carbon gain along light gradients for the shade-tolerant species Acer saccharum.  Plant, Cell and Environment 20, 845–866.
Crossref | GoogleScholarGoogle Scholar | open url image1

Niinemets, Ü ,  and  Sack, L (2005). Structural determinants of leaf light harvesting capacity and photosynthetic potentials. In ‘Progress in botany’. In press. (Springer-Verlag: Berlin)

Niinemets Ü, Valladares F (2004) Photosynthetic acclimation to simultaneous and interacting environmental stresses along natural light gradients: optimality and constraints. Plant Biology 6, 254–268.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Niinemets Ü, Kull O, Tenhunen JD (1999a) Variability in leaf morphology and chemical composition as a function of canopy light environment in co-existing trees. International Journal of Plant Sciences 160, 837–848.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Niinemets Ü, Tenhunen JD, Canta NR, Chaves MM, Faria T, Pereira JS, Reynolds JF (1999b) Interactive effects of nitrogen and phosphorus on the acclimation potential of foliage photosynthetic properties of cork oak, Quercus suber, to elevated atmospheric CO2 concentrations. Global Change Biology 5, 455–470.
Crossref | GoogleScholarGoogle Scholar | open url image1

Niinemets Ü, Valladares F, Ceulemans R (2003) Leaf-level phenotypic variability and plasticity of invasive Rhododendron ponticum and non-invasive Ilex aquifolium co-occurring at two contrasting European sites. Plant, Cell and Environment 26, 941–956.
Crossref | GoogleScholarGoogle Scholar | 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

Nilsen, ET (1995). Stem photosynthesis: extent, patterns, and role in plant carbon economy. In ‘Plant stems: physiology and functional morphology’. pp. 223–240. (San Diego: Academic Press Inc.)

Nimz H (1974) Das Lignin der Buche — Entwurf eines Konstitutionsschemas. (Beech lignin — proposal of a constitutional scheme). Angewandte Chemie 86, 336–344. open url image1

Nobel PS, Cui M, Israel AA (1994) Light, chlorophyll, carboxylase activity and CO2 fixation at various depths in the chlorenchyma of Opuntia ficus-indica (L.) Miller under current and elevated CO2. New Phytologist 128, 315–322. open url image1

Pomar F, Merino F, Ros Barceló A (2002) O-4-Linked coniferyl and sinapyl aldehydes in lignifying cell walls are the main targets of the Wiesner (phloroglucinol–HCl) reaction. Protoplasma 220, 17–28.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rajendran K, Devaraj P (2004) Biomass and nutrient distribution and their return of Casuarina equisetifolia inoculated with biofertilizers in farm land. Biomass and Bioenergy 26, 235–249.
Crossref | GoogleScholarGoogle Scholar | open url image1

Roderick ML, Berry SL, Noble IR, Farquhar GD (1999) A theoretical approach to linking the composition and morphology with the function of leaves. Functional Ecology 13, 683–695.
Crossref | GoogleScholarGoogle Scholar | open url image1

Roderick ML, Berry SL, Noble IR (2000) A framework for understanding the relationship between environment and vegetation based on the surface area to volume ratio of leaves. Functional Ecology 14, 423–437.
Crossref | GoogleScholarGoogle Scholar | open url image1

Rokitta M, Medek D, Pope JM, Critchley C (2004) 23Na NMR microimaging: a tool for non-invasive monitoring of sodium distribution in living plants. Functional Plant Biology 31, 879–887.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ryel RJ, Beyschlag W, Caldwell MM (1993) Foliage orientation and carbon gain in two tussock grasses as assessed with a new whole-plant gas-exchange model. Functional Ecology 7, 115–124. open url image1

Sánchez-Rodríguez J, Pérez P, Martínez-Carrasco R (1999) Photosynthesis, carbohydrate levels and chlorophyll fluorescence-estimated intercellular CO2 in water-stressed Casuarina equisetifolia Forst. & Forst. Plant, Cell and Environment 22, 867–873.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sims DA, Pearcy RW (1994) Scaling sun and shade photosynthetic acclimation of Alocasia macrorrhiza to whole-plant performance. I. Carbon balance and allocation at different daily photon flux densities. Plant, Cell and Environment 17, 881–887. open url image1

Specht RL (1981) Ecophysiological principles determining the biogeography of major vegetation formations in Australia. In ‘Ecological biogeography of Australia’. (Ed. A Keast) pp. 300–333. (Dr W Junk: The Hague)

Specht RL, Rundel PW (1990) Sclerophylly and foliar nutrient status of Mediterranean-climate plant communities in southern Australia. Australian Journal of Botany 38, 459–474. open url image1

Stenberg P, Kangas T, Smolander H, Linder S (1999) Shoot structure, canopy openness, and light interception in Norway spruce. Plant, Cell and Environment 22, 1133–1142.
Crossref | GoogleScholarGoogle Scholar | open url image1

Syvertsen JP, Lloyd J, McConchie C, Kriedemann PE, Farquhar GD (1995) On the relationship between leaf anatomy and CO2 diffusion through the mesophyll of hypostomatous leaves. Plant, Cell and Environment 18, 149–157. open url image1

ter Steege H (1996) ‘Winphot 5: a program to analyze vegetation indices, light and light quality from hemispherical photographs.’ (Tropenbos Guayana Program: Tropenbos)

Valladares F, Pearcy RW (2000) The role of crown architecture for light harvesting and carbon gain in extreme light environments assessed with a realistic 3-D model. Anales Jardin Botanico de Madrid 58, 3–16. 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 MW, Zou X (2002) Soil macrofauna and litter nutrients in three tropical tree plantations on a disturbed site in Puerto Rico. Forest Ecology and Management 170, 161–171.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wilson KL , Johnson LAS (1989) Casuarinaceae. In ‘Flora of Australia’. (Ed. AS George) pp. 138–174. (Australian Government Publishing Service: Canberra)

Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z , et al. (2004) The world-wide leaf economics spectrum. Nature 428, 821–827.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yamashita N, Koike N, Ishida A (2002) Leaf ontogenetic dependence of light acclimation in invasive and native subtropical trees of different successional status. Plant, Cell and Environment 25, 1341–1356.
Crossref | GoogleScholarGoogle Scholar | open url image1