Gas exchange and water-use efficiency in plant canopies

In this review, I first address the basics of gas exchange, water-use efficiency and carbon isotope discrimination in C(3)plant canopies. I then present a case study of water-use efficiency in northern Australian tree species. In general, C(3)plants face a trade-off whereby increasing stomatal conductance for a given set of conditions will result in a higherCO(2)assimilation rate, but a lower photosynthetic water-use efficiency. A common garden experiment suggested that tree species which are able to establish and grow in drier parts of northern Australia have a capacity to use water rapidly when it is available through high stomatal conductance, but that they do so at the expense of low water-use efficiency. This may explain why community-level carbon isotope discrimination does not decrease as steeply with decreasing rainfall on the North Australian Tropical Transect as has been observed on some other precipitation gradients. Next, I discuss changes in water-use efficiency that take place during leaf expansion in C(3)plant leaves. Leaf phenology has recently been recognised as a significant driver of canopy gas exchange in evergreen forest canopies, and leaf expansion involves changes in both photosynthetic capacity and water-use efficiency. Following this, I discuss the role of woody tissue respiration in canopy gas exchange and how photosynthetic refixation of respiredCO(2)can increase whole-plant water-use efficiency. Finally, I discuss the role of water-use efficiency in driving terrestrial plant responses to global change, especially the rising concentration of atmosphericCO(2). In coming decades, increases in plant water-use efficiency caused by risingCO(2)are likely to partially mitigate impacts on plants of drought stress caused by global warming

Leaf:wood allometry and functional traits together explain substantial growth rate variation in rainforest trees

Plant growth rates drive ecosystem productivity and are a central element of plant ecological strategies. For seedlings grown under controlled conditions, a large literature has firmly identified the functional traits that drive interspecific variation in growth rate. For adult plants, the corresponding knowledge is surprisingly poorly understood. Until recently it was widely assumed that the key trait drivers would be the same (e.g. specific leaf area, or SLA), but an increasing number of papers has demonstrated this not to be the case, or not generally so. New theory has provided a prospective basis for understanding these discrepancies. Here we quantified relationships between stem diameter growth rates and functional traits of adult woody plants for 41 species in an Australian tropical rainforest. From various cost-benefit considerations, core predictions included that: (i) photosynthetic rate would be positively related to growth rate; (ii) SLA would be unrelated to growth rate (unlike in seedlings where it is positively related to growth); (iii) wood density would be negatively related to growth rate; and (iv) leaf mass:sapwood mass ratio (LM:SM) in branches (analogous to a benefit:cost ratio) would be positively related to growth rate. All our predictions found support, particularly those for LM:SM and wood density; photosynthetic rate was more weakly related to stem diameter growth rates. Specific leaf area was convincingly correlated to growth rate, in fact negatively. Together, SLA, wood density and LM:SM accounted for 52 % of variation in growth rate among these 41 species, with each trait contributing roughly similar explanatory power. That low SLA species can achieve faster growth rates than high SLA species was an unexpected result but, as it turns out, not without precedent, and easily understood via cost-benefit theory that considers whole-plant allocation to different tissue types. Branch-scale leaf:sapwood ratio holds promise as an easily measurable variable that may help to understand growth rate variation. Using cost-benefit approaches teamed with combinations of leaf, wood and allometric variables may provide a path towards a more complete understanding of growth rates under field conditions

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

Great uncertainty exists in the global exchange of carbon between the atmosphere and the terrestrial biosphere. An important source of this uncertainty lies in the dependency of photosynthesis on the maximum rate of carboxylation (Vcmax) and the maximum rate of electron transport (Jmax). Understanding and making accurate prediction of C fluxes thus requires accurate characterization of these rates and their relationship with plant nutrient status over large geographic scales. Plant nutrient status is indicated by the traits: leaf nitrogen (N), leaf phosphorus (P), and specific leaf area (SLA). Correlations between Vcmax and Jmax and leaf nitrogen (N) are typically derived from local to global scales, while correlations with leaf phosphorus (P) and specific leaf area (SLA) have typically been derived at a local scale. Thus, there is no global-scale relationship between Vcmax and Jmax and P or SLA limiting the ability of global-scale carbon flux models do not account for P or SLA. We gathered published data from 24 studies to reveal global relationships of Vcmax and Jmax with leaf N, P, and SLA. Vcmax was strongly related to leaf N, and increasing leaf P substantially increased the sensitivity of Vcmax to leaf N. Jmax was strongly related to Vcmax, and neither leaf N, P, or SLA had a substantial impact on the relationship. Although more data are needed to expand the applicability of the relationship, we show leaf P is a globally important determinant of photosynthetic rates. In a model of photosynthesis, we showed that at high leaf N (3 gm−2), increasing leaf P from 0.05 to 0.22 gm−2 nearly doubled assimilation rates. Finally, we show that plants may employ a conservative strategy of Jmax to Vcmax coordination that restricts photoinhibition when carboxylation is limiting at the expense of maximizing photosynthetic rates when light is limiting

Similar patterns of leaf temperatures and thermal acclimation to warming in temperate and tropical tree canopies

As the global climate warms, a key question is how increased leaf temperatures will affect tree physiology and the coupling between leaf and air temperatures in forests. To explore the impact of increasing temperatures on plant performance in open air, we warmed leaves in the canopy of two mature evergreen forests, a temperate Eucalyptus woodland and a tropical rainforest. The leaf heaters consistently maintained leaves at a target of 4 °C above ambient leaf temperatures. Ambient leaf temperatures (Tleaf) were mostly coupled to air temperatures (Tair), but at times, leaves could be 8–10 °C warmer than ambient air temperatures, especially in full sun. At both sites, Tleaf was warmer at higher air temperatures (Tair > 25 °C), but was cooler at lower Tair, contrary to the ‘leaf homeothermy hypothesis’. Warmed leaves showed significantly lower stomatal conductance (−0.05 mol m−2 s−1 or −43% across species) and net photosynthesis (−3.91 μmol m−2 s−1 or −39%), with similar rates in leaf respiration rates at a common temperature (no acclimation). Increased canopy leaf temperatures due to future warming could reduce carbon assimilation via reduced photosynthesis in these forests, potentially weakening the land carbon sink in tropical and temperate forests

The handbook for standardised field and laboratory measurements in terrestrial climate-change experiments and observational studies

Climate change is a worldwide threat to biodiversity and ecosystem structure, functioning, and services. To understand the underlying drivers and mechanisms, and to predict the consequences for nature and people, we urgently need better understanding of the direction and magnitude of climate‐change impacts across the soil–plant–atmosphere continuum. An increasing number of climate‐change studies is creating new opportunities for meaningful and high‐quality generalisations and improved process understanding. However, significant challenges exist related to data availability and/or compatibility across studies, compromising opportunities for data re‐use, synthesis, and upscaling. Many of these challenges relate to a lack of an established “best practice” for measuring key impacts and responses. This restrains our current understanding of complex processes and mechanisms in terrestrial ecosystems related to climate change

Photosynthetic refixation in branches of Western White Pine

1. We investigated the functional controls on light-dependent refixation of respired CO2 in photosynthetic bark of Western White Pine (Pinus monticola Dougl. ex D. Don) branches.\ud \ud 2. Gross photosynthesis increased with increasing intensity of photosynthetically active radiation (PAR) to > 2000 µmol m−2 s−1 and with increasing bark surface temperature from 15 to > 45 °C. Maximum observed refixation rates were 76 ± 3% (mean ± SE) of dark respiration.\ud \ud 3. At a given temperature and irradiance, dark respiration rate was the physiological parameter that correlated most strongly with gross photosynthesis (R = 0·89, P < 0·0001, n = 43). Dark respiration rates varied 20-fold among branches. Over this range, refixation averaged 55 ± 2% of dark respiration at 25 °C and 1000 μmol PAR m−2 s−1. However, refixation was not correlated with internal CO2 concentrations in illuminated branches; these concentrations remained fairly constant.\ud \ud 4. Specific bark area, bark conductance to water vapour, bark chlorophyll a/b ratio, and bark nitrogen concentration varied markedly with canopy depth in mature trees.\ud \ud 5. Results are summarized in a simple model of refixation driven by light, temperature and dark respiration rate. The model may prove useful in assessing the quantitative significance of refixation in the carbon balance of forest trees

Isotopic and morphologic proxies for reconstructing light environment and leaf function of fossil leaves: a modern calibration in the Daintree Rainforest, Australia

Premise: Within closed‐canopy forests, vertical gradients of light and atmospheric CO2 drive variations in leaf carbon isotope ratios, leaf mass per area (LMA), and the micromorphology of leaf epidermal cells. Variations in traits observed in preserved or fossilized leaves could enable inferences of past forest canopy closure and leaf function and thereby habitat of individual taxa. However, as yet no calibration study has examined how isotopic, micro‐ and macromorphological traits, in combination, reflect position within a modern closed‐canopy forest or how these could be applied to the fossil record. Methods: Leaves were sampled from throughout the vertical profile of the tropical forest canopy using the 48.5 m crane at the Daintree Rainforest Observatory, Queensland, Australia. Carbon isotope ratios, LMA, petiole metric (i.e., petiole‐width2/leaf area, a proposed proxy for LMA that can be measured from fossil leaves), and leaf micromorphology (i.e., undulation index and cell area) were compared within species across a range of canopy positions, as quantified by leaf area index (LAI). Results: Individually, cell area, δ13C, and petiole metric all correlated with both LAI and LMA, but the use of a combined model provided significantly greater predictive power. Conclusions: Using the observed relationships with leaf carbon isotope ratio and morphology to estimate the range of LAI in fossil floras can provide a measure of canopy closure in ancient forests. Similarly, estimates of LAI and LMA for individual taxa can provide comparative measures of light environment and growth strategy of fossil taxa from within a flora.Alexander W. Cheesman, Heather Duff, Kathryn Hill, Lucas A. Cernusak, Francesca A. McInerne

Identifying drivers of leaf water and cellulose stable isotope enrichment in Eucalyptus in northern Australia

Several previous studies have investigated the use of the stable hydrogen and oxygen isotope compositions in plant materials as indicators of palaeoclimate. However, accurate interpretation relies on a detailed understanding of both physiological and environmental drivers of the variations in isotopic enrichments that occur in leaf water and associated organic compounds. To progress this aim we measured δ18O and δ2H values in eucalypt leaf and stem water and δ18O values in leaf cellulose, along with the isotopic compositions of water vapour, across a north-eastern Australian aridity gradient. Here we compare observed leaf water enrichment, along with previously published enrichment data from a similar north Australian transect, to Craig–Gordon-modelled predictions of leaf water isotopic enrichment. Our investigation of model parameters shows that observed 18O enrichment across the aridity gradients is dominated by the relationship between atmospheric and internal leaf water vapour pressure while 2H enrichment is driven mainly by variation in the water vapour—source water isotopic disequilibrium. During exceptionally dry and hot conditions (RH 37 °C) we observed strong deviations from Craig–Gordon predicted isotope enrichments caused by partial stomatal closure. The atmospheric–leaf vapour pressure relationship is also a strong predictor of the observed leaf cellulose δ18O values across one aridity gradient. Our finding supports a wider applicability of leaf cellulose δ18O composition as a climate proxy for atmospheric humidity conditions during the leaf growing season than previously documented

Thirty-eight years of CO2 fertilization has outpaced growing aridity to drive greening of Australian woody ecosystems

Climate change is projected to increase the imbalance between the supply (precipitation) and atmospheric demand for water (i.e., increased potential evapotranspiration), stressing plants in water-limited environments. Plants may be able to offset increasing aridity because rising CO2 increases water use efficiency. CO2 fertilization has also been cited as one of the drivers of the widespread “greening” phenomenon. However, attributing the size of this CO2 fertilization effect is complicated, due in part to a lack of long-term vegetation monitoring and interannual- to decadal-scale climate variability. In this study we asked the question of how much CO2 has contributed towards greening. We focused our analysis on a broad aridity gradient spanning eastern Australia's woody ecosystems. Next we analyzed 38 years of satellite remote sensing estimates of vegetation greenness (normalized difference vegetation index, NDVI) to examine the role of CO2 in ameliorating climate change impacts. Multiple statistical techniques were applied to separate the CO2-attributable effects on greening from the changes in water supply and atmospheric aridity. Widespread vegetation greening occurred despite a warming climate, increases in vapor pressure deficit, and repeated record-breaking droughts and heat waves. Between 1982–2019 we found that NDVI increased (median 11.3 %) across 90.5 % of the woody regions. After masking disturbance effects (e.g., fire), we statistically estimated an 11.7 % increase in NDVI attributable to CO2, broadly consistent with a hypothesized theoretical expectation of an 8.6 % increase in water use efficiency due to rising CO2. In contrast to reports of a weakening CO2 fertilization effect, we found no consistent temporal change in the CO2 effect. We conclude rising CO2 has mitigated the effects of increasing aridity, repeated record-breaking droughts, and record-breaking heat waves in eastern Australia. However, we were unable to determine whether trees or grasses were the primary beneficiary of the CO2-induced change in water use efficiency, which has implications for projecting future ecosystem resilience. A more complete understanding of how CO2-induced changes in water use efficiency affect trees and non-tree vegetation is needed.Sami W. Rifai, Martin G. De Kauwe, Anna M. Ukkola, Lucas A. Cernusak, Patrick Meir, Belinda E. Medlyn, and Andy J. Pitma