Photosynthesis and water-use efficiency of seedlings from northern Australian monsoon forest, savanna and swamp habitats grown in a common garden
Kim A. Orchard A , Lucas A. Cernusak A C and Lindsay B. Hutley A BA School of Environmental and Life Sciences, Charles Darwin University, Darwin, NT 0909, Australia.
B School of Environmental Research, Charles Darwin University, Darwin, NT 0909, Australia.
C Corresponding author. Email: lucas.cernusak@cdu.edu.au
Functional Plant Biology 37(11) 1050-1060 https://doi.org/10.1071/FP09306
Submitted: 22 December 2009 Accepted: 6 July 2010 Published: 22 October 2010
Abstract
Islands of monsoon rainforest and Melaleuca swamp punctuate vast tracts of savanna in monsoonal northern Australia. Seedlings of species from each of these habitat associations were grown in a common garden. Monsoon forest species had higher specific leaf area, lower photosynthetic capacity and lower photosynthetic light compensation points, and required lower irradiance to achieve 50% of light-saturated photosynthesis compared with savanna or swamp species. These traits probably contribute towards greater shade tolerance beneath dense monsoon-forest canopies, whereas savanna and swamp canopies are relatively open. Swamp species, especially two Melaleuca species, had high stomatal conductance and small CO2 drawdown during photosynthesis, and more negative leaf δ13C, compared with monsoon forest and savanna species. Higher stomatal conductance increases carbon uptake during photosynthesis and a high transpiration rate would increase transport of nutrients to absorbing surfaces in the root by mass flow. Thus, a strategy of high transpiration and low water-use efficiency appears to be favoured in swamp species compared with monsoon-forest and savanna species. Instantaneous measurements of the ratio of intercellular to ambient CO2 concentrations (ci/ca) explained 81% of variation in leaf δ13C across 44 species sampled in this and other studies, suggesting that leaf δ13C generally provides a robust proxy for comparisons of ci/ca, even when applied across species.
Additional keywords: carbon isotope ratio, Melaleuca, transpiration.
Acknowledgements
We thank Sean Bellairs, Marjory King and Lisa Peters for assisting with species selection, and Quan Tien, Max Orchard, Beverley Orchard, Lance O’Connor and Melina McDowell for technical assistance. This research was supported by an Australian Postdoctoral Fellowship and Discovery grant to Lucas A. Cernusak from the Australian Research Council (DP0771427), and by a research grant from Charles Darwin University.
Anderson JE,
Williams J,
Kriedemann PE,
Austin MP, Farquhar GD
(1996) Correlations between carbon isotope discrimination and climate of native habitats for diverse eucalypt taxa growing in a common garden. Australian Journal of Plant Physiology 23, 311–320.
| Crossref | GoogleScholarGoogle Scholar |
Bach CS
(2002) Phenological patterns in monsoon rainforests in the Northern Territory, Australia. Austral Ecology 27, 477–489.
| Crossref | GoogleScholarGoogle Scholar |
Beringer J,
Hutley LB,
Tapper NJ, Cernusak LA
(2007) Savanna fires and their impact on net ecosystem productivity in North Australia. Global Change Biology 13, 990–1004.
| Crossref | GoogleScholarGoogle Scholar |
Blackman VH
(1919) The compound interest law and plant growth. Annals of Botany 33, 353–360.
Bowman DMJS, Minchin PR
(1987) Environmental relationships of woody vegetation patterns in the Australian monsoon tropics. Australian Journal of Botany 35, 151–169.
| Crossref | GoogleScholarGoogle Scholar |
Bowman DMJS, Prior LD
(2005) Why do evergreen trees dominate the Australian seasonal tropics? Australian Journal of Botany 53, 379–399.
| Crossref | GoogleScholarGoogle Scholar |
Brodribb T, Hill RS
(1998) The photosynthetic drought physiology of a diverse group of southern hemisphere conifer species is correlated with minimum seasonal rainfall. Functional Ecology 12, 465–471.
| Crossref | GoogleScholarGoogle Scholar |
Cernusak LA, Marshall JD
(2001) Responses of foliar δ13C, gas exchange, and leaf morphology to reduced hydraulic conductivity in Pinus monticola branches. Tree Physiology 21, 1215–1222.
|
CAS |
PubMed |
Cernusak LA,
Aranda J,
Marshall JD, Winter K
(2007a) Large variation in whole-plant water-use efficiency among tropical tree species. New Phytologist 173, 294–305.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cernusak LA,
Winter K,
Aranda J,
Turner BL, Marshall JD
(2007b) Transpiration efficiency of a tropical pioneer tree (Ficus insipida) in relation to soil fertility. Journal of Experimental Botany 58, 3549–3566.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Cernusak LA,
Winter K,
Aranda J, Turner BL
(2008) Conifers, angiosperm trees, and lianas: growth, whole-plant water and nitrogen use efficiency, and stable isotope composition (δ13C and δ18O) of seedlings grown in a tropical environment. Plant Physiology 148, 642–659.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Cernusak LA,
Tcherkez G,
Keitel C,
Cornwell WK, Santiago LS ,
et al
.
(2009a) Why are non-photosynthetic tissues generally 13C enriched compared to leaves in C3 plants? Review and synthesis of current hypotheses. Functional Plant Biology 36, 199–213.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Cernusak LA,
Winter K,
Aranda J,
Virgo A, Garcia M
(2009b) Transpiration efficiency over an annual cycle, leaf gas exchange and wood carbon isotope ratio of three tropical tree species. Tree Physiology 29, 1153–1161.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Cernusak LA,
Winter K, Turner BL
(2009c) Physiological and isotopic (δ13C and δ18O) responses of three tropical tree species to water and nutrient availability. Plant, Cell & Environment 32, 1441–1455.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Cernusak LA,
Winter K, Turner BL
(2010) Leaf nitrogen to phosphorus ratios of tropical trees: experimental assessment of physiological and environmental controls. New Phytologist 185, 770–779.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Chapin FS,
Schulze E-D, Mooney HA
(1990) The ecology and economics of storage in plants. Annual Review of Ecology and Systematics 21, 423–447.
| Crossref | GoogleScholarGoogle Scholar |
Cole SP,
Woo KC,
Eamus D,
Harwood CE, Haines MW
(1994) Field measurements of net photosynthesis and related parameters in 4 provenances of Acacia auriculiformis. Australian Journal of Botany 42, 457–470.
| Crossref | GoogleScholarGoogle Scholar |
Cramer MD,
Hoffmann V, Verboom GA
(2008) Nutrient availability moderates transpiration in Ehrharta calycina. The New Phytologist 179, 1048–1057.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Cramer MD,
Hawkins HJ, Verboom GA
(2009) The importance of nutritional regulation of plant water flux. Oecologia 161, 15–24.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Eamus D, Cole S
(1997) Diurnal and seasonal comparisons of assimilation, phyllode conductance and water potential, of three Acacia and one Eucalyptus species in the wet-dry tropics of Australia. Australian Journal of Botany 45, 275–290.
| Crossref | GoogleScholarGoogle Scholar |
Farquhar GD, Richards RA
(1984) Isotopic composition of plant carbon correlates with water-use efficiency in wheat genotypes. Australian Journal of Plant Physiology 11, 539–552.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Farquhar GD,
von Caemmerer S, Berry JA
(1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Farquhar GD,
Ball MC,
von Caemmerer S, Roksandic Z
(1982a) Effect of salinity and humidity on δ13C value of halophytes – evidence for diffusional isotope fractionation determined by the ratio of intercellular/atmospheric partial pressure of CO2 under different environmental conditions. Oecologia 52, 121–124.
| Crossref | GoogleScholarGoogle Scholar |
Farquhar GD,
O’Leary MH, Berry JA
(1982b) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Australian Journal of Plant Physiology 9, 121–137.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Farquhar GD,
Ehleringer JR, Hubick KT
(1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40, 503–537.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Franklin DC,
Brocklehurst PS,
Lynch D, Bowman DMJS
(2007) Niche differentiation and regeneration in the seasonally flooded Melaleuca forests of northern Australia. Journal of Tropical Ecology 23, 457–467.
| Crossref | GoogleScholarGoogle Scholar |
Hutley LB,
O’Grady AP, Eamus D
(2000) Evapotranspiration from eucalypt open-forest savanna of northern Australia. Functional Ecology 14, 183–194.
| Crossref | GoogleScholarGoogle Scholar |
Kelley G,
O’Grady AP,
Hutley LB, Eamus D
(2007) A comparison of tree water use in two contiguous vegetation communities of the seasonally dry tropics of northern Australia: the importance of site water budget to tree hydraulics. Australian Journal of Botany 55, 700–708.
| Crossref | GoogleScholarGoogle Scholar |
Ladiges PY,
Udovicic F, Nelson G
(2003) Australian biogeographical connections and the phylogeny of large genera in the plant family Myrtaceae. Journal of Biogeography 30, 989–998.
| Crossref |
Lehmann CER,
Ratnam J, Hutley LB
(2009) Which of these continents is not like the other? Comparisons of tropical savanna systems: key questions and challenges. New Phytologist 181, 508–511.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
McDonald EP,
Erickson JE, Kruger EL
(2002) Can decreased transpiration limit plant nitrogen acquisition in elevated CO2? Functional Plant Biology 29, 1115–1120.
| Crossref | GoogleScholarGoogle Scholar |
Montagu KD, Woo KC
(1999) Recovery of tree photosynthetic capacity from seasonal drought in the wet-dry tropics: the role of phyllode and canopy processes in Acacia auriculiformis. Australian Journal of Plant Physiology 26, 135–145.
| Crossref | GoogleScholarGoogle Scholar |
O’Grady AP,
Chen X,
Eamus D, Hutley LB
(2000) Composition, leaf area index and standing biomass of eucalypt open forests near Darwin in the Northern Territory, Australia. Australian Journal of Botany 48, 629–638.
| Crossref | GoogleScholarGoogle Scholar |
Price OF
(2004) Indirect evidence that frugivorous birds track fluctuating fruit resources among rainforest patches in the Northern Territory, Australia. Austral Ecology 29, 137–144.
| Crossref | GoogleScholarGoogle Scholar |
Prior LD,
Eamus D, Bowman DMJS
(2003) Leaf attributes in the seasonally dry tropics: a comparison of four habitats in northern Australia. Functional Ecology 17, 504–515.
| Crossref | GoogleScholarGoogle Scholar |
Prior LD,
Eamus D, Bowman DMJS
(2004) Tree growth rates in north Australian savanna habitats: seasonal patterns and correlations with leaf attributes. Australian Journal of Botany 52, 303–314.
| Crossref | GoogleScholarGoogle Scholar |
Read J, Farquhar GD
(1991) Comparative studies in Nothofagus (Fagaceae). 1. Leaf carbon isotope discrimination. Functional Ecology 5, 684–695.
| Crossref | GoogleScholarGoogle Scholar |
Russell-Smith J,
Yates C,
Edwards A,
Allan GE,
Cook GD,
Cooke P,
Craig R,
Heath B, Smith R
(2003) Contemporary fire regimes of northern Australia, 1997–2001: change since Aboriginal occupancy, challenges for sustainable management. International Journal of Wildland Fire 12, 283–297.
| Crossref | GoogleScholarGoogle Scholar |
Scholz FG,
Bucci SJ,
Goldstein G,
Meinzer FC,
Franco AC, Miralles-Wilhelm F
(2007) Removal of nutrient limitations by long-term fertilization decreases nocturnal water loss in savanna trees. Tree Physiology 27, 551–559.
| PubMed |
Schulze ED,
Turner NC,
Nicolle D, Schumacher J
(2006) Species differences in carbon isotope ratios, specific leaf area and nitrogen concentrations in leaves of Eucalyptus growing in a common garden compared with along an aridity gradient. Physiologia Plantarum 127, 434–444.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Seibt U,
Rajabi A,
Griffiths H, Berry JA
(2008) Carbon isotopes and water use efficiency: sense and sensitivity. Oecologia 155, 441–454.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sharkey TD,
Bernacchi CJ,
Farquhar GD, Singsaas EL
(2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant, Cell & Environment 30, 1035–1040.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Turton SM, Duff GA
(1992) Light environments and floristic composition across an open forest-rainforest boundary in northeastern Queensland. Australian Journal of Ecology 17, 415–423.
| Crossref | GoogleScholarGoogle Scholar |
Valladares F, Niinemets U
(2008) Shade tolerance, a key plant feature of complex nature and consequences. Annual Review of Ecology Evolution and Systematics 39, 237–257.
| Crossref | GoogleScholarGoogle Scholar |
Warren CR, Adams MA
(2006) Internal conductance does not scale with photosynthetic capacity: implications for carbon isotope discrimination and the economics of water and nitrogen use in photosynthesis. Plant, Cell & Environment 29, 192–201.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Warren CR,
Dreyer E,
Tausz M, Adams MA
(2006) Ecotype adaptation and acclimation of leaf traits to rainfall in 29 species of 16-year-old Eucalyptus at two common gardens. Functional Ecology 20, 929–940.
| Crossref | GoogleScholarGoogle Scholar |
Williams RJ,
Hutley LB,
Cook GD,
Russell-Smith J,
Edwards A, Chen XY
(2004) Assessing the carbon sequestration potential of mesic savannas in the Northern Territory, Australia: approaches, uncertainties and potential impacts of fire. Functional Plant Biology 31, 415–422.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Woinarski JCZ,
Brock C,
Armstrong M,
Hempel C,
Cheal D, Brennan K
(2000) Bird distribution in riparian vegetation in the extensive natural landscape of Australia’s tropical savanna: a broad-scale survey and analysis of a distributional database. Journal of Biogeography 27, 843–868.
| Crossref | GoogleScholarGoogle Scholar |
Wong S-C,
Cowan IR, Farquhar GD
(1979) Stomatal conductance correlates with photosynthetic capacity. Nature 282, 424–426.
| Crossref | GoogleScholarGoogle Scholar |