Variation in photosynthetic traits related to access to water in semiarid Australian woody species
Rachael H. Nolan A B , Tonantzin Tarin A , Kendal A. Fairweather A , James Cleverly A and Derek Eamus AA School of Life Sciences, University of Technology Sydney, PO Box 123, Broadway, NSW 2007, Australia.
B Corresponding author. Email: rachael.nolan@uts.edu.au
Functional Plant Biology 44(11) 1087-1097 https://doi.org/10.1071/FP17096
Submitted: 17 October 2016 Accepted: 11 July 2017 Published: 15 August 2017
Abstract
Low soil water content can limit photosynthesis by reducing stomatal conductance. Here, we explore relationships among traits pertaining to carbon uptake and pre-dawn leaf water potential (as an index of soil water availability) across eight species found in semiarid central Australia. We found that as pre-dawn leaf water potential declined, stomatal limitations to photosynthesis increased, as did foliar nitrogen, which enhanced photosynthesis. Nitrogen-fixing Acacia species had higher foliar nitrogen concentrations compared with non-nitrogen fixing species, although there was considerable variability of traits within the Acacia genus. From principal component analysis we found that the most dissimilar species was Acacia aptaneura Maslin & J.E.Reid compared with both Eucalyptus camaldulensis Dehnh. and Corymbia opaca. (D.J.Carr & S.G.M.Carr) K.D.Hill & L.A.S.Johnson, having both the largest foliar N content, equal largest leaf mass per area and experiencing the lowest pre-dawn water potential of all species. A. aptaneura has shallow roots and grows above a hardpan that excludes access to groundwater, in contrast to E. camaldulensis and C. opaca, which are known to access groundwater. We conclude that ecohydrological niche separation is an important factor driving the variability of within-biome traits related to carbon gain. These observations have important implications for global vegetation models, which are parameterised with many of the traits measured here, but are often limited by data availability.
Additional keywords: carbon uptake, gas exchange, photosynthesis, respiration, water-use efficiency, Vcmax.
References
Atkin OK, Tjoelker MG (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends in Plant Science 8, 343–351.| Thermal acclimation and the dynamic response of plant respiration to temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXls1CjtLk%3D&md5=bfcd6e18c93ebde62eeae8604bbe253cCAS |
Ausplots TERN (2013) AusPlots Rangelands, ver. 2/2017. Available at: http://www.aekos.org.au/collection/adelaide.edu.au/ausplotsrangelands. TERN ÆKOS Data Portal, rights owned by University of Adelaide (http://www.adelaide.edu.au) [Accessed 6 February 2014].
Blackman CJ, Gleason SM, Chang Y, Cook AM, Laws C, Westoby M (2014) Leaf hydraulic vulnerability to drought is linked to site water availability across a broad range of species and climates. Annals of Botany 114, 435–440.
| Leaf hydraulic vulnerability to drought is linked to site water availability across a broad range of species and climates.Crossref | GoogleScholarGoogle Scholar |
Bowman D, Boggs GS, Prior LD, Krull ES (2007) Dynamics of Acacia aneura-Triodia boundaries using carbon (14C and δ13C) and nitrogen (δ15N) signatures in soil organic matter in central Australia. The Holocene 17, 311–318.
| Dynamics of Acacia aneura-Triodia boundaries using carbon (14C and δ13C) and nitrogen (δ15N) signatures in soil organic matter in central Australia.Crossref | GoogleScholarGoogle Scholar |
Bowman D, Boggs GS, Prior LD (2008) Fire maintains an Acacia aneura shrubland–Triodia grassland mosaic in central Australia. Journal of Arid Environments 72, 34–47.
| Fire maintains an Acacia aneura shrubland–Triodia grassland mosaic in central Australia.Crossref | GoogleScholarGoogle Scholar |
Cano FJ, Lopez R, Warren CR (2014) Implications of the mesophyll conductance to CO2 for photosynthesis and water-use efficiency during long-term water stress and recovery in two contrasting Eucalyptus species. Plant, Cell & Environment 37, 2470–2490.
| Implications of the mesophyll conductance to CO2 for photosynthesis and water-use efficiency during long-term water stress and recovery in two contrasting Eucalyptus species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhslOksrfM&md5=073b2e55085a03c9f0f6ed927af2c74eCAS |
Cernusak LA, Hutley LB, Beringer J, Holtum JAM, Turner BL (2011) Photosynthetic physiology of eucalypts along a sub-continental rainfall gradient in northern Australia. Agricultural and Forest Meteorology 151, 1462–1470.
| Photosynthetic physiology of eucalypts along a sub-continental rainfall gradient in northern Australia.Crossref | GoogleScholarGoogle Scholar |
Chen C, Cleverly J, Zhang L, Yu Q, Eamus D (2016) Modelling seasonal and inter-annual variations in carbon and water fluxes in an arid-zone Acacia savanna woodland, 1981–2012. Ecosystems 19, 625–644.
| Modelling seasonal and inter-annual variations in carbon and water fluxes in an arid-zone Acacia savanna woodland, 1981–2012.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xhtl2jsLk%3D&md5=b908d86403a8411de554bfb92dde23d5CAS |
Cleverly J (2011) Alice Springs Mulga OzFlux site. TERN OzFlux: Australian and New Zealand Flux Research and Monitoring Network. Available at: hdl.handle.net/102.100.100/8697. [Accessed 15 July 2017].
Cleverly J (2013) Ti Tree East OzFlux Site. TERN OzFlux: Australian and New Zealand Flux Research and Monitoring Network. Available at: hdl.handle.net/102.100.100/11135. [Accessed 15 July 2017].
Cleverly J, Eamus D, Luo QY, Coupe NR, Kljun N, Ma XL, Ewenz C, Li LH, Yu Q, Huete A (2016a) The importance of interacting climate modes on Australia’s contribution to global carbon cycle extremes. Scientific Reports 6, 23113
| The importance of interacting climate modes on Australia’s contribution to global carbon cycle extremes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XktlGqu7s%3D&md5=114db3bac26e8ce54f668c91e6c66aaeCAS |
Cleverly J, Eamus D, Restrepo-Coupe N, Chen C, Maes W, Li L, Faux R, Santini NS, Rumman R, Yu Q, Huete A (2016b) Soil moisture controls on phenology and productivity in a semi-arid critical zone. Science of the Total Environment 568, 1227–1237.
| Soil moisture controls on phenology and productivity in a semi-arid critical zone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XoslalsLo%3D&md5=3915a03bf82b77f8e47ad654fd865dc6CAS |
Cleverly J, Eamus D, Van Gorsel E, Chen C, Rumman R, Luo QY, Coupe NR, Li LH, Kljun N, Faux R, Yu Q, Huete A (2016c) Productivity and evapotranspiration of two contrasting semiarid ecosystems following the 2011 global carbon land sink anomaly. Agricultural and Forest Meteorology 220, 151–159.
| Productivity and evapotranspiration of two contrasting semiarid ecosystems following the 2011 global carbon land sink anomaly.Crossref | GoogleScholarGoogle Scholar |
Cook PG, O’Grady AP (2006) Determining soil and ground water use of vegetation from heat pulse, water potential and stable isotope data. Oecologia 148, 97–107.
| Determining soil and ground water use of vegetation from heat pulse, water potential and stable isotope data.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283hvVSrsA%3D%3D&md5=1fbb9e1f568a825e8d7616b58055f098CAS |
Cook PG, O’Grady AP, Wischusen JDH, Duguid A, Fass T, Eamus D (2008) Ecohydrology of sand plain woodlands in central Australia. Report to Natural Heritage Trust, Project no. 2005/147. Australia.
Duursma RA (2015) Plantecophys – an R package for analysing and modelling leaf gas exchange data. PLoS One 10, e0143346
| Plantecophys – an R package for analysing and modelling leaf gas exchange data.Crossref | GoogleScholarGoogle Scholar |
Eamus D, Hatton T, Cook P, Colvin C (2006) ‘Ecohydrology: vegetation function, water and resource management.’ (CSIRO Publishing: Melbourne)
Eamus D, Cleverly J, Boulain N, Grant N, Faux R, Villalobos-Vega R (2013) Carbon and water fluxes in an arid-zone Acacia savanna woodland: an analyses of seasonal patterns and responses to rainfall events. Agricultural and Forest Meteorology 182–183, 225–238.
| Carbon and water fluxes in an arid-zone Acacia savanna woodland: an analyses of seasonal patterns and responses to rainfall events.Crossref | GoogleScholarGoogle Scholar |
Erskine PD, Stewart GR, Turnbull MH, Unkovich M, Pate JS (1996) Water availability – a physiological constraint on nitrate utilization in plants of Australian semi-arid mulga woodlands. Plant, Cell & Environment 19, 1149–1159.
| Water availability – a physiological constraint on nitrate utilization in plants of Australian semi-arid mulga woodlands.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmvFKhtrg%3D&md5=c46d59dee019946fbda6b483ef6b8bafCAS |
Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78, 9–19.
| Photosynthesis and nitrogen relationships in leaves of C3 plants.Crossref | GoogleScholarGoogle Scholar |
Farquhar GD, Sharkey TD (1982) Stomatal conductance and photsynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 33, 317–345.
| Stomatal conductance and photsynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XktlKjs7o%3D&md5=10ee7a0a323eb4ff0e0cedf045e75e3aCAS |
Farquhar GD, Caemmerer SV, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90.
| A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXksVWrt7w%3D&md5=6db882a9dac8dc5a797c6c3206d6450cCAS |
Hinckley TM, Lassoie JP, Running SW (1978) Temporal and spatial variations in water status of forest trees. Forest Science 24, 1–72.
Islam M, Adams MA (1999) Mineral content and nutritive value of native grasses and the response to added phosphorus in a Pilbara rangeland. Tropical Grasslands 33, 193–200.
James JJ, Alder NN, Muhling KH, Lauchli AE, Shackel KA, Donovan LA, Richards JH (2006) High apoplastic solute concentrations in leaves alter water relations of the halophytic shrub, Sarcobatus vermiculatus. Journal of Experimental Botany 57, 139–147.
| High apoplastic solute concentrations in leaves alter water relations of the halophytic shrub, Sarcobatus vermiculatus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlCmsbvP&md5=f438ef00827603432678b14f7e35b4a3CAS |
Johnson RW, Burrows WH (1981) Acacia open forests, woodlands and shrublands. In ‘Australian vegetation’. (Ed. RH Groves) pp. 198–226. (Cambridge University Press: Cambridge, UK)
Kavanagh KL, Pangle R, Schotzko AD (2007) Nocturnal transpiration causing disequilibrium between soil and stem predawn water potential in mixed conifer forests of Idaho. Tree Physiology 27, 621–629.
| Nocturnal transpiration causing disequilibrium between soil and stem predawn water potential in mixed conifer forests of Idaho.Crossref | GoogleScholarGoogle Scholar |
Kirschbaum MUF, Harms B, Mathers NJ, Dalal RC (2008) Soil carbon and nitrogen changes after clearing mulga (Acacia aneura) vegetation in Queensland, Australia: observations, simulations and scenario analysis. Soil Biology & Biochemistry 40, 392–405.
| Soil carbon and nitrogen changes after clearing mulga (Acacia aneura) vegetation in Queensland, Australia: observations, simulations and scenario analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlajs7fN&md5=74e7d9c48f5f07fce8637e0a099c2b7fCAS |
Krinner G, Viovy N, de Noblet-Ducoudre N, Ogee J, Polcher J, Friedlingstein P, Ciais P, Sitch S, Prentice IC (2005) A dynamic global vegetation model for studies of the coupled atmosphere-biosphere system. Global Biogeochemical Cycles 19, GB1015
| A dynamic global vegetation model for studies of the coupled atmosphere-biosphere system.Crossref | GoogleScholarGoogle Scholar |
Lewis JD, Phillips NG, Logan BA, Hricko CR, Tissue DT (2011) Leaf photosynthesis, respiration and stomatal conductance in six Eucalyptus species native to mesic and xeric environments growing in a common garden. Tree Physiology 31, 997–1006.
| Leaf photosynthesis, respiration and stomatal conductance in six Eucalyptus species native to mesic and xeric environments growing in a common garden.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVCls7jP&md5=c4ea4d3380eb56db47f6cb5937b9cdf9CAS |
Lindeman RH, Merenda PF, Gold RZ (1980) ‘Introduction to bivariate and multivariate analysis.’ (Scott Foresman: Glenview IL, USA)
Manzoni S, Vico G, Katul G, Palmroth S, Porporato A (2014) Optimal plant water-use strategies under stochastic rainfall. Water Resources Research 50, 5379–5394.
| Optimal plant water-use strategies under stochastic rainfall.Crossref | GoogleScholarGoogle Scholar |
Maslin BR, Reid JB (2012) A taxonomic revision of Mulga (Acacia aneura and its close relatives: Fabaceae) in Western Australia. Nuytsia 22, 129–267.
McDowell NG (2011) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiology 155, 1051–1059.
| Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXksFOrtro%3D&md5=7637e3563e535a1299844f8410955c70CAS |
McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytologist 178, 719–739.
| Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought?Crossref | GoogleScholarGoogle Scholar |
Misson L, Tu KP, Boniello RA, Goldstein AH (2006) Seasonality of photosynthetic parameters in a multi-specific and vertically complex forest ecosystem in the Sierra Nevada of California. Tree Physiology 26, 729–741.
| Seasonality of photosynthetic parameters in a multi-specific and vertically complex forest ecosystem in the Sierra Nevada of California.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlvFars7c%3D&md5=5a71c6c7da57ac7ca6b2a52f0a846e04CAS |
Nicholas AMM, Franklin DC, Bowman DMJS (2011) Floristic uniformity across abrupt boundaries between Triodia hummock grassland and Acacia shrubland on an Australian desert sandplain. Journal of Arid Environments 75, 1090–1096.
| Floristic uniformity across abrupt boundaries between Triodia hummock grassland and Acacia shrubland on an Australian desert sandplain.Crossref | GoogleScholarGoogle Scholar |
Nolan RH, Fairweather KA, Tarin T, Santini NS, Cleverly J, Faux R, Eamus D (2017) Divergence in plant water-use strategies in semi-arid woody species. Functional Plant Biology 44,
| Divergence in plant water-use strategies in semi-arid woody species.Crossref | GoogleScholarGoogle Scholar |
O’Grady AP, Cook PG, Eamus D, Duguid A, Wischusen JDH, Fass T, Worldege D (2009) Convergence of tree water use within an arid-zone woodland. Oecologia 160, 643–655.
| Convergence of tree water use within an arid-zone woodland.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1Mvis1Wjsw%3D%3D&md5=d070cbb932ac2f2952425b53fc98d05fCAS |
Poorter H, Niinemets U, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytologist 182, 565–588.
| Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis.Crossref | GoogleScholarGoogle Scholar |
Poulter B, Frank D, Ciais P, Myneni RB, Andela N, Bi J, Broquet G, Canadell JG, Chevallier F, Liu YY, Running SW, Sitch S, van der Werf GR (2014) Contribution of semi-arid ecosystems to interannual variability of the global carbon cycle. Nature 509, 600–603.
| Contribution of semi-arid ecosystems to interannual variability of the global carbon cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXoslCrt7g%3D&md5=8f4cb49a08fac095152d63e44db8359dCAS |
Prior LD, Eamus D, Bowman D (2003) Leaf attributes in the seasonally dry tropics: a comparison of four habitats in northern Australia. Functional Ecology 17, 504–515.
| Leaf attributes in the seasonally dry tropics: a comparison of four habitats in northern Australia.Crossref | GoogleScholarGoogle Scholar |
Prior LD, Bowman D, Eamus D (2004) Seasonal differences in leaf attributes in Australian tropical tree species: family and habitat comparisons. Functional Ecology 18, 707–718.
| Seasonal differences in leaf attributes in Australian tropical tree species: family and habitat comparisons.Crossref | GoogleScholarGoogle Scholar |
R Development Core Team (2016) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna) Available at http://www.R-project.org/ [Verified 6 May 2017].
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. Ecology Letters 11, 793–801.
| Scaling of respiration to nitrogen in leaves, stems and roots of higher land plants.Crossref | GoogleScholarGoogle Scholar |
Reynolds JF, Kemp PR, Ogle K, Fernandez RJ (2004) Modifying the ‘pulse-reserve’ paradigm for deserts of North America: precipitation pulses, soil water, and plant responses. Oecologia 141, 194–210.
| Modifying the ‘pulse-reserve’ paradigm for deserts of North America: precipitation pulses, soil water, and plant responses.Crossref | GoogleScholarGoogle Scholar |
Santini NS, Cleverly J, Faux R, Lestrange C, Rumman R, Eamus D (2016) Xylem traits and water-use efficiency of woody species co-occurring in the Ti Tree Basin arid zone. Trees 30, 295–303.
| Xylem traits and water-use efficiency of woody species co-occurring in the Ti Tree Basin arid zone.Crossref | GoogleScholarGoogle Scholar |
Schulze ED, Nicolle D, Boerner A, Lauerer M, Aas G, Schulze I (2014) Stable carbon and nitrogen isotope ratios of Eucalyptus and Acacia species along a seasonal rainfall gradient in Western Australia. Trees 28, 1125–1135.
| Stable carbon and nitrogen isotope ratios of Eucalyptus and Acacia species along a seasonal rainfall gradient in Western Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXotlylsLc%3D&md5=20bbb59e5b6ca97b06899e33b6b236f7CAS |
Schuur EAG (2003) Productivity and global climate revisited: the sensitivity of tropical forest growth to precipitation. Ecology 84, 1165–1170.
| Productivity and global climate revisited: the sensitivity of tropical forest growth to precipitation.Crossref | GoogleScholarGoogle Scholar |
Shi H, Li L, Eamus D, Cleverly J, Huete A, Beringer J, Yu Q, Van Gorsel E, Hutley L (2014) Intrinsic climate dependency of ecosystem light and water-use-efficiencies across Australian biomes. Environmental Research Letters 9, 104002
| Intrinsic climate dependency of ecosystem light and water-use-efficiencies across Australian biomes.Crossref | GoogleScholarGoogle Scholar |
Silvertown J, Araya Y, Gowing D (2015) Hydrological niches in terrestrial plant communities: a review. Journal of Ecology 103, 93–108.
| Hydrological niches in terrestrial plant communities: a review.Crossref | GoogleScholarGoogle Scholar |
Stewart JD, Elabidine AZ, Bernier PY (1995) Stomatal and mesophyll limitations of photosynthesis in black spruce seedlings during multiple cycles of drought. Tree Physiology 15, 57–64.
| Stomatal and mesophyll limitations of photosynthesis in black spruce seedlings during multiple cycles of drought.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c%2Fnslentw%3D%3D&md5=31bee01869a53ad145da7177012eb85fCAS |
Tardieu F, Simonneau T (1998) Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modelling isohydric and anisohydric behaviours. Journal of Experimental Botany 49, 419–432.
| Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modelling isohydric and anisohydric behaviours.Crossref | GoogleScholarGoogle Scholar |
Taylor D, Eamus D (2008) Coordinating leaf functional traits with branch hydraulic conductivity: resource substitution and implications for carbon gain. Tree Physiology 28, 1169–1177.
| Coordinating leaf functional traits with branch hydraulic conductivity: resource substitution and implications for carbon gain.Crossref | GoogleScholarGoogle Scholar |
Tezara W, Colombo R, Coronel I, Marin O (2011) Water relations and photosynthetic capacity of two species of Calotropis in a tropical semi-arid ecosystem. Annals of Botany 107, 397–405.
| Water relations and photosynthetic capacity of two species of Calotropis in a tropical semi-arid ecosystem.Crossref | GoogleScholarGoogle Scholar |
Van Etten EJB (2009) Inter-annual rainfall variability of arid Australia: greater than elsewhere? The Australian Geographer 40, 109–120.
| Inter-annual rainfall variability of arid Australia: greater than elsewhere?Crossref | GoogleScholarGoogle Scholar |
Villeneuve S, Cook PG, Shanafield M, Wood C, White N (2015) Groundwater recharge via infiltration through an ephemeral riverbed, central Australia. Journal of Arid Environments 117, 47–58.
| Groundwater recharge via infiltration through an ephemeral riverbed, central Australia.Crossref | GoogleScholarGoogle Scholar |
Vogan PJ, Maherali H (2014) Increased photosynthetic capacity as a mechanism of drought adaptation in C3 plants. International Journal of Plant Sciences 175, 1033–1041.
| Increased photosynthetic capacity as a mechanism of drought adaptation in C3 plants.Crossref | GoogleScholarGoogle Scholar |
Walker AP, Berkerman AP, Gu L, Kattage J, Cernusak LA, Domingues TF, Scales JC, Wohlfahrt G, Wullschleger SD, Woodward FI (2014) The relationship of leaf photosynthetic traits – V cmax and J max – to leaf nitrogen, leaf phosphorus, and specific leaf area: a meta-analysis and modeling study. Ecology and Evolution 4, 3218–3235.
| The relationship of leaf photosynthetic traits – V cmax and J max – to leaf nitrogen, leaf phosphorus, and specific leaf area: a meta-analysis and modeling study.Crossref | GoogleScholarGoogle Scholar |
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.
| Strategy shifts in leaf physiology, structure and nutrient content between species of high- and low-rainfall and high- and low-nutrient habitats.Crossref | GoogleScholarGoogle Scholar |
Wright IJ, Reich PB, Atkin OK, Lusk CH, Tjoelker MG, Westoby M (2006) Irradiance, temperature and rainfall influence leaf dark respiration in woody plants: evidence from comparisons across 20 sites. New Phytologist 169, 309–319.
| Irradiance, temperature and rainfall influence leaf dark respiration in woody plants: evidence from comparisons across 20 sites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlKntLo%3D&md5=9fdc558045b085137fffc0b6a7ad3a35CAS |