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 C₃ plant canopies. I then present a case study of water‐use efficiency in northern Australian tree species. In general, C₃ plants face a trade‐off whereby increasing stomatal conductance for a given set of conditions will result in a higher CO₂ 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 C₃ 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 respired CO₂ 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 atmospheric CO₂. In coming decades, increases in plant water‐use efficiency caused by rising CO₂ are likely to partially mitigate impacts on plants of drought stress caused by global warming.     

A comparison of passage efficiency for native and exotic fish species over an artificial baffled ramp

This study used an experimental approach to compare the passage success of native and exotic fish species from the temperate Southern Hemisphere over an artificial baffled fish ramp designed for overcoming low-head (≤1.0 m) fish migration barriers. Passage efficiency was, on average, lower for the exotic species [koi carp (Cyprinus carpio), rudd (Scardinius erythrophthalmus) and rainbow trout (Oncorhynchus mykiss)] compared to the native species [inanga (Galaxias maculatus), redfin bully (Gobiomorphus huttoni) and common bully (Gobiomorphus cotidianus)]. Nonetheless, there was considerable variation between individual species, with rainbow trout outperforming common bully and juvenile inanga, but koi carp and rudd failing to pass any of the ramps. The differences in predicted probability of passage success between the native and exotic fish species in this study were sufficient in some cases to indicate the potential for the baffled fish ramps to operate as a selective migration barrier. Nonetheless, further testing is required to validate these results across a broader range of conditions before deployment.     

Seasonal and within‐canopy variation in shoot‐scale resource‐use efficiency trade‐offs in a Norway spruce stand

Previous leaf‐scale studies of carbon assimilation describe short‐term resource‐use efficiency (RUE) trade‐offs where high use efficiency of one resource requires low RUE of another. However, varying resource availabilities may cause long‐term RUE trade‐offs to differ from the short‐term patterns. This may have important implications for understanding canopy‐scale resource use and allocation. We used continuous gas exchange measurements collected at five levels within a Norway spruce, Picea abies (L.) karst., canopy over 3 years to assess seasonal differences in the interactions between shoot‐scale resource availability (light, water and nitrogen), net photosynthesis (A_n) and the use efficiencies of light (LUE), water (WUE) and nitrogen (NUE) for carbon assimilation. The continuous data set was used to develop and evaluate multiple regression models for predicting monthly shoot‐scale A_n. These models showed that shoot‐scale A_n was strongly dependent on light availability and was generally well described with simple one‐ or two‐parameter models. WUE peaked in spring, NUE in summer and LUE in autumn. However, the relative importance of LUE for carbon assimilation increased with canopy depth at all times. Our results suggest that accounting for seasonal and within‐canopy trade‐offs may be important for RUE‐based modelling of canopy carbon uptake.     

Phenology in a warming world: differences between native and non‐native plant species

Phenology is a harbinger of climate change, with many species advancing flowering in response to rising temperatures. However, there is tremendous variation among species in phenological response to warming, and any phenological differences between native and non‐native species may influence invasion outcomes under global warming. We simulated global warming in the field and found that non‐native species flowered earlier and were more phenologically plastic to temperature than natives, which did not accelerate flowering in response to warming. Non‐native species' flowering also became more synchronous with other community members under warming. Earlier flowering was associated with greater geographic spread of non‐native species, implicating phenology as a potential trait associated with the successful establishment of non‐native species across large geographic regions. Such phenological differences in both timing and plasticity between native and non‐natives are hypothesised to promote invasion success and population persistence, potentially benefiting non‐native over native species under climate change.     

Contrasting water sources and water‐use efficiency in coexisting desert plants in two saline‐sodic soils in northwest China

• Soil degradation resulting from various types of salinity is a major environmental problem, especially in arid and semiarid regions. Exploring the water‐related physiological traits of halophytes is useful for understanding the mechanisms of salt tolerance. This knowledge could be used to rehabilitate degraded arid lands.
• To investigate whether different types of salinity influence the water sources and water‐use efficiency of desert plants (Karelinia caspia, Tamarix hohenackeri, Nitraria sibirica, Phragmites australis, Alhagi sparsifolia, Suaeda microphylla, Kalidium foliatum) in natural environments, we measured leaf gas exchange, leaf carbon and xylem oxygen isotope composition and soil oxygen isotope composition at neutral saline‐sodic site (NSS) and alkaline saline‐sodic site (ASS) in northwest China.
• The studied plants had different xylem water oxygen isotope compositions (δ¹⁸O) and foliar carbon isotope compositions (δ¹³C), indicating that desert plants coexist through differentiation in water use patterns. Compared to that at the NSS site, the stem water in K. caspia, A. sparsifolia and S. microphylla was depleted in ¹⁸O at the ASS site, which indicates that plants can switch to obtain water from deeper soil layers when suffering environmental stress from both salinity and alkalinisation. Alhagi sparsifolia had higher δ¹³C at the ASS site than at the NSS site, while K. caspia and S. microphylla had lower δ¹³C, which may have resulted from interspecific differences in plant alkali and salt tolerance ability.
• Our results suggest that under severe salinity and alkalinity, plants may exploit deeper soil water to avoid ion toxicity resulting from high concentrations of soluble salts in the superficial soil layer. In managed lands, it is vital to select and cultivate different salt‐tolerant or alkali‐tolerant plant species in light of local conditions.

     

Seasonal responses of terrestrial ecosystem water‐use efficiency to climate change

Ecosystem water‐use efficiency (EWUE) is an indicator of carbon–water interactions and is defined as the ratio of carbon assimilation (GPP) to evapotranspiration (ET). Previous research suggests an increasing long‐term trend in annual EWUE over many regions and is largely attributed to the physiological effects of rising CO₂. The seasonal trends in EWUE, however, have not yet been analyzed. In this study, we investigate seasonal EWUE trends and responses to various drivers during 1982–2008. The seasonal cycle for two variants of EWUE, water‐use efficiency (WUE, GPP/ET), and transpiration‐based WUE (WUE_t, the ratio of GPP and transpiration), is analyzed from 0.5° gridded fields from four process‐based models and satellite‐based products, as well as a network of 63 local flux tower observations. WUE derived from flux tower observations shows moderate seasonal variation for most latitude bands, which is in agreement with satellite‐based products. In contrast, the seasonal EWUE trends are not well captured by the same satellite‐based products. Trend analysis, based on process‐model factorial simulations separating effects of climate, CO₂, and nitrogen deposition (NDEP), further suggests that the seasonal EWUE trends are mainly associated with seasonal trends of climate, whereas CO₂ and NDEP do not show obvious seasonal difference in EWUE trends. About 66% grid cells show positive annual WUE trends, mainly over mid‐ and high northern latitudes. In these regions, spring climate change has amplified the effect of CO₂ in increasing WUE by more than 0.005 gC m⁻² mm⁻¹ yr⁻¹ for 41% pixels. Multiple regression analysis further shows that the increase in springtime WUE in the northern hemisphere is the result of GPP increasing faster than ET because of the higher temperature sensitivity of GPP relative to ET. The partitioning of annual EWUE to seasonal components provides new insight into the relative sensitivities of GPP and ET to climate, CO_2, and NDEP.     

Change in terrestrial ecosystem water‐use efficiency over the last three decades

Defined as the ratio between gross primary productivity (GPP) and evapotranspiration (ET), ecosystem‐scale water‐use efficiency (EWUE) is an indicator of the adjustment of vegetation photosynthesis to water loss. The processes controlling EWUE are complex and reflect both a slow evolution of plants and plant communities as well as fast adjustments of ecosystem functioning to changes of limiting resources. In this study, we investigated EWUE trends from 1982 to 2008 using data‐driven models derived from satellite observations and process‐oriented carbon cycle models. Our findings suggest positive EWUE trends of 0.0056, 0.0007 and 0.0001 g C m^?2 mm^?1 yr^?1 under the single effect of rising CO₂ (‘CO₂’), climate change (‘CLIM’) and nitrogen deposition (‘NDEP’), respectively. Global patterns of EWUE trends under different scenarios suggest that (i) EWUE‐CO₂ shows global increases, (ii) EWUE‐CLIM increases in mainly high latitudes and decreases at middle and low latitudes, (iii) EWUE‐NDEP displays slight increasing trends except in west Siberia, eastern Europe, parts of North America and central Amazonia. The data‐driven MTE model, however, shows a slight decline of EWUE during the same period (?0.0005 g C m^?2 mm^?1 yr^?1), which differs from process‐model (0.0064 g C m^?2 mm^?1 yr^?1) simulations with all drivers taken into account. We attribute this discrepancy to the fact that the nonmodeled physiological effects of elevated CO₂ reducing stomatal conductance and transpiration (TR) in the MTE model. Partial correlation analysis between EWUE and climate drivers shows similar responses to climatic variables with the data‐driven model and the process‐oriented models across different ecosystems. Change in water‐use efficiency defined from transpiration‐based WUE_t (GPP/TR) and inherent water‐use efficiency (IWUE_t, GPP×VPD/TR) in response to rising CO₂, climate change, and nitrogen deposition are also discussed. Our analyses will facilitate mechanistic understanding of the carbon–water interactions over terrestrial ecosystems under global change.     

Interactions between CO2 enhancement and N addition on net primary productivity and water‐use efficiency in a mesocosm with multiple subtropical tree species

Carbon dioxide (CO₂) enhancement (eCO₂) and N addition (aN) have been shown to increase net primary production (NPP) and to affect water‐use efficiency (WUE) for many temperate ecosystems, but few studies have been made on subtropical tree species. This study compared the responses of NPP and WUE from a mesocosm composing five subtropical tree species to eCO₂ (700 ppm), aN (10 g N m^?2 yr^?1) and eCO₂ × aN using open‐top chambers. Our results showed that mean annual ecosystem NPP did not changed significantly under eCO₂, increased by 56% under aN and 64% under eCO₂ × aN. Ecosystem WUE increased by 14%, 55%, and 61% under eCO₂, aN and eCO₂ × aN, respectively. We found that the observed responses of ecosystem WUE were largely driven by the responses of ecosystem NPP. Statistical analysis showed that there was no significant interactions between eCO₂ and aN on ecosystem NPP (P = 0.731) or WUE (P = 0.442). Our results showed that increasing N deposition was likely to have much stronger effects on ecosystem NPP and WUE than increasing CO₂ concentration for the subtropical forests. However, different tree species responded quite differently. aN significantly increased annual NPP of the fast‐growing species (Schima superba). Nitrogen‐fixing species (Ormosia pinnata) grew significantly faster only under eCO₂ × aN. eCO₂ had no effects on annual NPP of those two species but significantly increased annual NPP of other two species (Castanopsis hystrix and Acmena acuminatissima). Differential responses of the NPP among different tree species to eCO₂ and aN will likely have significant implications on the species composition of subtropical forests under future global change.     

Ecophysiological traits of invasive alien Acacia cyclops compared to co‐occuring native species in Strandveld vegetation of the Cape Floristic Region

Tree invasions of Mediterranean‐climate ecosystems pose a significant threat to both biodiversity and functioning, by excluding native species, altering soil nutrient status and depleting water resources. In order to attain greater relative biomass associated with successful invasion in these characteristically resource‐poor environments, invasive species must have novel traits that enable better acquisition (e.g. deep roots) or exploitation of different resources (e.g. N₂ fixation) and/or more efficient use of available resources than native species. We compared the ecophysiological and morphological traits of three abundant native species to those of the invasive Australian tree species, Acacia cyclops. This species is widely invasive in the Mediterranean‐climate coastal vegetation of South Africa that includes the Strandveld vegetation type. A. cyclops had 30–50% greater foliar N concentrations (P < 0.001) in comparison with the native species and lower foliar δ¹⁵N values that may indicate N₂ fixation. Additionally, A. cyclops maintained higher photosynthetic rates over the dry summer season (ca. 15 μmol m^?2 s^?1) than the native species. These higher photosynthetic rates may result from sustained access to water due to deeper rooting abilities as indicated by the more negative δD values (P < 0.001) of A. cyclops (?43‰) in comparison with the some native species (?29 to ?37‰). Acacia cyclops did not, however, exhibit greater water use efficiencies or photosynthetic nitrogen use efficiencies (P > 0.05) compared to native species. Invasiveness of A. cyclops into this resource‐limited Mediterranean‐climate ecosystem appears to be supported by greater resource acquisition, possibly partially through N₂ fixation and greater rooting depth, rather than greater resource use efficiency or conservation.     

Century‐long apparent decrease in intrinsic water‐use efficiency with no evidence of progressive nutrient limitation in African tropical forests

Forests exhibit leaf‐ and ecosystem‐level responses to environmental changes. Specifically, rising carbon dioxide (CO₂) levels over the past century are expected to have increased the intrinsic water‐use efficiency (iWUE) of tropical trees while the ecosystem is gradually pushed into progressive nutrient limitation. Due to the long‐term character of these changes, however, observational datasets to validate both paradigms are limited in space and time. In this study, we used a unique herbarium record to go back nearly a century and show that despite the rise in CO₂ concentrations, iWUE has decreased in central African tropical trees in the Congo Basin. Although we find evidence that points to leaf‐level adaptation to increasing CO₂—that is, increasing photosynthesis‐related nutrients and decreasing maximum stomatal conductance, a decrease in leaf δ¹³C clearly indicates a decreasing iWUE over time. Additionally, the stoichiometric carbon to nitrogen and nitrogen to phosphorus ratios in the leaves show no sign of progressive nutrient limitation as they have remained constant since 1938, which suggests that nutrients have not increasingly limited productivity in this biome. Altogether, the data suggest that other environmental factors, such as increasing temperature, might have negatively affected net photosynthesis and consequently downregulated the iWUE. Results from this study reveal that the second largest tropical forest on Earth has responded differently to recent environmental changes than expected, highlighting the need for further on‐ground monitoring in the Congo Basin.     

Increasing water‐use efficiency and age‐specific growth responses of old‐growth ponderosa pine trees in the Northern Rockies

We examined radial growth responses of ponderosa pine (Pinus ponderosa var. ponderosa) between 1905–1954 and 1955–2004 to determine if the effects of increased intrinsic water‐use efficiencies (iWUE) caused by elevated atmospheric CO₂ concentrations were age‐specific. We collected 209 cores from five sites in the Northern Rockies and calculated iWUE using carbon isotope data from 1850 to 2004. Standardized radial growth responses were age dependent, with older trees exhibiting significantly higher values than younger trees during the later period at four sites and all sites combined. No significant differences in radial growth existed either for the individual sites or combined site during the earlier period. Increases in iWUE during 1955–2004 were 11% greater than during 1905–1954, and pentadal fluctuations in iWUE were significantly correlated with the radial growth of older trees from 1850 to 2004. Radial growth of younger trees and iWUE were not significantly correlated. Our results suggest that: (1) responses to elevated atmospheric CO₂ in old‐growth ponderosa forests are age‐specific; (2) radial growth increases in older trees coincided with increased iWUE; (3) ponderosa had increased growth rates in their third, fourth, and fifth centuries of life; and (4) age‐specific growth responses during 1955–2004 are unique since at least the mid‐16th century.     

Observed and modelled historical trends in the water‐use efficiency of plants and ecosystems

Plant water‐use efficiency (WUE, the carbon gained through photosynthesis per unit of water lost through transpiration) is a tracer of the plant physiological controls on the exchange of water and carbon dioxide between terrestrial ecosystems and the atmosphere. At the leaf level, rising CO₂ concentrations tend to increase carbon uptake (in the absence of other limitations) and to reduce stomatal conductance, both effects leading to an increase in leaf WUE. At the ecosystem level, indirect effects (e.g. increased leaf area index, soil water savings) may amplify or dampen the direct effect of CO₂. Thus, the extent to which changes in leaf WUE translate to changes at the ecosystem scale remains unclear. The differences in the magnitude of increase in leaf versus ecosystem WUE as reported by several studies are much larger than would be expected with current understanding of tree physiology and scaling, indicating unresolved issues. Moreover, current vegetation models produce inconsistent and often unrealistic magnitudes and patterns of variability in leaf and ecosystem WUE, calling for a better assessment of the underlying approaches. Here, we review the causes of variations in observed and modelled historical trends in WUE over the continuum of scales from leaf to ecosystem, including methodological issues, with the aim of elucidating the reasons for discrepancies observed within and across spatial scales. We emphasize that even though physiological responses to changing environmental drivers should be interpreted differently depending on the observational scale, there are large uncertainties in each data set which are often underestimated. Assumptions made by the vegetation models about the main processes influencing WUE strongly impact the modelled historical trends. We provide recommendations for improving long‐term observation‐based estimates of WUE that will better inform the representation of WUE in vegetation models.     

PdEPF1 regulates water‐use efficiency and drought tolerance by modulating stomatal density in poplar

Water deficiency is a critical environmental condition that is seriously reducing global plant production. Improved water‐use efficiency (WUE) and drought tolerance are effective strategies to address this problem. In this study, PdEPF1, a member of the EPIDERMAL PATTERNING FACTOR (EPF) family, was isolated from the fast‐growing poplar clone NE‐19 [Populus nigra × (Populus deltoides × Populus nigra)]. Significantly, higher PdEPF1 levels were detected after induction by dehydration and abscisic acid. To explore the biological functions of PdEPF1, transgenic triploid white poplars (Populus tomentosa ‘YiXianCiZhu B385’) overexpressing PdEPF1 were constructed. PdEPF1 overexpression resulted in increased water deficit tolerance and greater WUE. We confirmed that the transgenic lines with greater instantaneous WUE had approximately 30% lower transpiration but equivalent CO₂ assimilation. Lower transpiration was associated with a 28% reduction in abaxial stomatal density. PdEPF1 overexpression not only strongly enhanced WUE, but also greatly improved drought tolerance, as measured by the leaf relative water content and water potential, under limited water conditions. In addition, the growth of these oxPdEPF1 plants was less adversely affected by reduced water availability than plants with a higher stomatal density, indicating that plants with a low stomatal density may be well suited to grow in water‐scarce environments. Taken together, our data suggest that PdEPF1 improves WUE and confers drought tolerance in poplar; thus, it could be used to breed drought‐tolerant plants with increased production under conditions of water deficiency.     

Canopy radiation‐ and water‐use efficiencies as affected by elevated [CO2]

This study used an environmentally controlled plant growth facility, EcoCELLs, to measure canopy gas exchanges directly and to examine the effects of elevated [CO₂] on canopy radiation‐ and water‐use efficiencies. Sunflowers (Helianthus annus var. Mammoth) were grown at ambient (399 μmol mol^?1) and elevated [CO₂] (746 μmol mol^?1) for 53 days in EcoCELLs. Whole canopy carbon‐ and water‐fluxes were measured continuously during the period of the experiment. The results indicated that elevated [CO₂] enhanced daily total canopy carbon‐ and water‐fluxes by 53% and 11%, respectively, on a ground‐area basis, resulting in a 54% increase in radiation‐use efficiency (RUE) based on intercepted photosynthetic active radiation and a 26% increase in water‐use efficiency (WUE) by the end of the experiment. Canopy carbon‐ and water‐fluxes at both CO₂ treatments varied with canopy development. They were small at 22 days after planting (DAP) and gradually increased to the maxima at 46 DAP. When canopy carbon‐ and water‐fluxes were expressed on a leaf‐area basis, no effect of CO₂ was found for canopy water‐flux while elevated [CO₂] still enhanced canopy carbon‐flux by 29%, on average. Night‐time canopy carbon‐flux was 32% higher at elevated than at ambient [CO₂]. In addition, RUE and WUE displayed strong diurnal variations, high at noon and low in the morning or afternoon for WUE but opposite for RUE. This study provided direct evidence that plant canopy may consume more, instead of less, water but utilize both water and radiation more efficiently at elevated than at ambient [CO₂], at least during the exponential growth period as illustrated in this experiment.     

Relationship between photosynthetic phosphorus‐use efficiency and foliar phosphorus fractions in tropical tree species

How plants develop adaptive strategies to efficiently use nutrients on infertile soils is an important topic in plant ecology. It has been suggested that, with decreasing phosphorus (P) availability, plants increase photosynthetic P‐use efficiency (PPUE) (i.e., the ratio of instantaneous photosynthetic carbon assimilation rate per unit foliar P). However, the mechanism to increase PPUE remains unclear. In this study, we tested whether high PPUE is explained by an optimized allocation of P in cells among P‐containing biochemical compounds (i.e., foliar P fractions). We investigated the relationships among mass‐based photosynthetic carbon assimilation rate (A_mass), PPUE, total foliar P concentration, and foliar P fractions in 10 tree species in two tropical montane rain forests with differing soil P availability (five species on sedimentary soils and five species on P‐poorer ultrabasic serpentine soils) on Mount Kinabalu, Borneo. We chemically fractionated foliar P into the following four fractions: metabolic P, lipid P, nucleic acid P, and residual P. A_mass was positively correlated with the concentrations of total foliar P and of metabolic P across 10 tree species. Mean A_mass and mean concentrations of total foliar P and of each foliar P fraction were lower on the P‐poorer ultrabasic serpentine soils than on the sedimentary soils. There was a negative relationship between the proportion of metabolic P per total P and the proportion of lipid P per total P. PPUE was positively correlated with the ratio of metabolic P to lipid P. High PPUE is explained by the net effect of a relatively greater investment of P into P‐containing metabolites and a relatively lesser investment into phospholipids in addition to generally reduced concentrations of all P fractions. We conclude that plants optimize the allocation of P among foliar P fractions for maintaining their productivity and growth and for reducing demand for P as their adaptation to P‐poor soils.     

Identifying potentially invasive non‐native marine and brackish water species for the Arabian Gulf and Sea of Oman

Invasive non‐native species (NNS) are internationally recognized as posing a serious threat to global biodiversity, economies and human health. The identification of invasive NNS is already established, those that may arrive in the future, their vectors and pathways of introduction and spread, and hotspots of invasion are important for a targeted approach to managing introductions and impacts at local, regional and global scales. The aim of this study was to identify which marine and brackish NNS are already present in marine systems of the northeastern Arabia area (Arabian Gulf and Sea of Oman) and of these which ones are potentially invasive, and which species have a high likelihood of being introduced in the future and negatively affect biodiversity. Overall, 136 NNS were identified, of which 56 are already present in the region and a further 80 were identified as likely to arrive in the future, including fish, tunicates, invertebrates, plants and protists. The Aquatic Species Invasiveness Screening Kit (AS‐ISK) was used to identify the risk of NNS being (or becoming) invasive within the region. Based on the AS‐ISK basic risk assessment (BRA) thresholds, 36 extant and 37 horizon species (53.7% of all species) were identified as high risk. When the impact of climate change on the overall assessment was considered, the combined risk score (BRA+CCA) increased for 38.2% of all species, suggesting higher risk under warmer conditions, including the highest‐risk horizon NNS the green crab Carcinus maenas, and the extant macro‐alga Hypnea musciformis. This is the first horizon‐scanning exercise for NNS in the region, thus providing a vital baseline for future management. The outcome of this study is the prioritization of NNS to inform decision‐making for the targeted monitoring and management in the region to prevent new bio‐invasions and to control existing species, including their potential for spread.