Variation in bulk-leaf ¹³C discrimination, leaf traits and water-use efficiency–trait relationships along a continental-scale climate gradient in Australia

© 2017 John Wiley & Sons Ltd Large spatial and temporal gradients in rainfall and temperature occur across Australia. This heterogeneity drives ecological differentiation in vegetation structure and ecophysiology. We examined multiple leaf-scale traits, including foliar 13C isotope discrimination (Δ13C), rates of photosynthesis and foliar N concentration and their relationships with multiple climate variables. Fifty-five species across 27 families were examined across eight sites spanning contrasting biomes. Key questions addressed include: (i) Does Δ13C and intrinsic water-use efficiency (WUEi) vary with climate at a continental scale? (ii) What are the seasonal and spatial patterns in Δ13C/WUEi across biomes and species? (iii) To what extent does Δ13C reflect variation in leaf structural, functional and nutrient traits across climate gradients? and (iv) Does the relative importance of assimilation and stomatal conductance in driving variation in Δ13C differ across seasons? We found that MAP, temperature seasonality, isothermality and annual temperature range exerted independent effects on foliar Δ13C/WUEi. Temperature-related variables exerted larger effects than rainfall-related variables. The relative importance of photosynthesis and stomatal conductance (gs) in determining Δ13C differed across seasons: Δ13C was more strongly regulated by gs during the dry-season and by photosynthetic capacity during the wet-season. Δ13C was most strongly correlated, inversely, with leaf mass area ratio among all leaf attributes considered. Leaf Nmass was significantly and positively correlated with MAP during dry- and wet-seasons and with moisture index (MI) during the wet-season but was not correlated with Δ13C. Leaf Pmass showed significant positive relationship with MAP and Δ13C only during the dry-season. For all leaf nutrient-related traits, the relationships obtained for Δ13C with MAP or MI indicated that Δ13C at the species level reliably reflects the water status at the site level. Temperature and water availability, not foliar nutrient content, are the principal factors influencing Δ13C across Australia

Reduced global plant respiration due to the acclimation of leaf dark respiration coupled to photosynthesis

Leaf dark respiration (Rd) acclimates to environmental changes. However, the magnitude, controls and time scales of acclimation remain unclear and are inconsistently treated in ecosystem models. We hypothesized that Rd and Rubisco carboxylation capacity (Vcmax) at 25°C (Rd,25, Vcmax,25) are coordinated so that Rd,25 variations support Vcmax,25 at a level allowing full light use, with Vcmax,25 reflecting daytime conditions (for photosynthesis), and Rd,25/Vcmax,25 reflecting night-time conditions (for starch degradation and sucrose export). We tested this hypothesis temporally using a 5-yr warming experiment, and spatially using an extensive field-measurement data set. We compared the results to three published alternatives: Rd,25 declines linearly with daily average prior temperature; Rd at average prior night temperatures tends towards a constant value; and Rd,25/Vcmax,25 is constant. Our hypothesis accounted for more variation in observed Rd,25 over time (R2 = 0.74) and space (R2 = 0.68) than the alternatives. Night-time temperature dominated the seasonal time-course of Rd, with an apparent response time scale of c. 2 wk. Vcmax dominated the spatial patterns. Our acclimation hypothesis results in a smaller increase in global Rd in response to rising CO2 and warming than is projected by the two of three alternative hypotheses, and by current models

Scaling leaf respiration with nitrogen and phosphorus in tropical forests across two continents

Leaf dark respiration (Rdark) represents an important component controlling the carbon balance in tropical forests. Here, we test how nitrogen (N) and phosphorus (P) affect Rdark and its relationship with photosynthesis using three widely separated tropical forests which differ in soil fertility. Rdark was measured on 431 rainforest canopy trees, from 182 species, in French Guiana, Peru and Australia. The variation in Rdark was examined in relation to leaf N and P content, leaf structure and maximum photosynthetic rates at ambient and saturating atmospheric CO2 concentration. We found that the site with the lowest fertility (French Guiana) exhibited greater rates of Rdark per unit leaf N, P and photosynthesis. The data from Australia, for which there were no phylogenetic overlaps with the samples from the South American sites, yielded the most distinct relationships of Rdark with the measured leaf traits. Our data indicate that no single universal scaling relationship accounts for variation in Rdark across this large biogeographical space. Variability between sites in the absolute rates of Rdark and the Rdark : photosynthesis ratio were driven by variations in N- and P-use efficiency, which were related to both taxonomic and environmental variability

Coordination of photosynthetic traits across soil and climate gradients

"Least-cost theory" posits that C3 plants should balance rates of photosynthetic water loss and carboxylation in relation to the relative acquisition and maintenance costs of resources required for these activities. Here we investigated the dependency of photosynthetic traits on climate and soil properties using a new Australia-wide trait dataset spanning 528 species from 67 sites. We tested the hypotheses that plants on relatively cold or dry sites, or on relatively more fertile sites, would typically operate at greater CO2 drawdown (lower ratio of leaf internal to ambient CO2 , Ci :Ca ) during light-saturated photosynthesis, and at higher leaf N per area (Narea ) and higher carboxylation capacity (Vcmax 25 ) for a given rate of stomatal conductance to water vapour, gsw . These results would be indicative of plants having relatively higher water costs than nutrient costs. In general, our hypotheses were supported. Soil total phosphorus (P) concentration and (more weakly) soil pH exerted positive effects on the Narea -gsw and Vcmax 25 -gsw slopes, and negative effects on Ci :Ca . The P effect strengthened when the effect of climate was removed via partial regression. We observed similar trends with increasing soil cation exchange capacity and clay content, which affect soil nutrient availability, and found that soil properties explained similar amounts of variation in the focal traits as climate did. Although climate typically explained more trait variation than soil did, together they explained up to 52% of variation in the slope relationships and soil properties explained up to 30% of the variation in individual traits. Soils influenced photosynthetic traits as well as their coordination. In particular, the influence of soil P likely reflects the Australia's geologically ancient low-relief landscapes with highly leached soils. Least-cost theory provides a valuable framework for understanding trade-offs between resource costs and use in plants, including limiting soil nutrients

Intraspecfic variation in cold-temperature metabolic phenotypes of Arabidopsis lyrata ssp petraea

Atmospheric temperature is a key factor in determining the distribution of a plant species. Alongside this, plant populations growing at the margin of their range may exhibit traits that indicate genetic differentiation and adaptation to their local abiotic environment. We investigated whether geographically separated marginal populations of Arabidopsis lyrata ssp. petraea have distinct metabolic phenotypes associated with exposure to cold temperatures. Seeds of A. petraea were obtained from populations along a latitudinal gradient, namely Wales, Sweden and Iceland and grown in a controlled cabinet environment. Mannose, glucose, fructose, sucrose and raffinose concentrations were different between cold treatments and populations, especially in the Welsh population, but polyhydric alcohol concentrations were not. The free amino acid compositions were population specific, with fold differences in most amino acids, especially in the Icelandic populations, with gross changes in amino acids, particularly those associated with glutamine metabolism. Metabolic fingerprints and profiles were obtained. Principal component analysis (PCA) of metabolite fingerprints revealed metabolic characteristic phenotypes for each population and temperature. It is suggested that amino acids and carbohydrates were responsible for discriminating populations within the PCA. Metabolite fingerprinting and profiling has proved to be sufficiently sensitive to identify metabolic differences between plant populations at different atmospheric temperatures. These findings show that there is significant natural variation in cold metabolism among populations of A. l. petraea which may signify plant adaptation to local climates

Higher thermal acclimation potential of respiration but not photosynthesis in two alpine Picea taxa in contrast to two lowland congeners

The members of the genus Picea form a dominant component in many alpine and boreal forests which are the major sink for atmospheric CO2. However, little is known about the growth response and acclimation of CO2 exchange characteristics to high temperature stress in Picea taxa from different altitudes. Gas exchange parameters and growth characteristics were recorded from four year old seedlings of two alpine (Picea likiangensis vars. rubescens and linzhiensis) and two lowland (P. koraiensis and P. meyeri) taxa. Seedlings were grown at moderate (25°C/15°C) and high (35°C/25°C) day/night temperatures, for four months. The approximated biomass increment (ΔD2H) for all taxa decreased under high temperature stress, associated with decreased photosynthesis and increased respiration. However, the two alpine taxa exhibited lower photosynthetic acclimation and higher respiratory acclimation than either lowland taxon. Moreover, higher leaf dry mass per unit area (LMA) and leaf nitrogen content per unit area (Narea), and a smaller change in the nitrogen use efficiency of photosynthesis (PNUE) for lowland taxa indicated that these maintained higher homeostasis of photosynthesis than alpine taxa. The higher respiration rates produced more energy for repair and maintenance biomass, especially for higher photosynthetic activity for lowland taxa, which causes lower respiratory acclimation. Thus, the changes of ΔD2H for alpine spruces were larger than that for lowland spruces. These results indicate that long term heat stress negatively impact on the growth of Picea seedlings, and alpine taxa are more affected than low altitude ones by high temperature stress. Hence the altitude ranges of Picea taxa should be taken into account when predicting changes to carbon fluxes in warmer conditions

Leaf-level photosynthetic capacity in lowland Amazonian and high elevation, Andean tropical moist forests of Peru

We examined whether variations in photosynthetic capacity are linked to variations in theenvironment and/or associated leaf traits for tropical moist forests (TMFs) in the Andes/west-ern Amazon regions of Peru. We compared photosynthetic capacity (maximal rate of carboxylation of Rubisco (Vcmax),and the maximum rate of electron transport (Jmax)), leaf mass, nitrogen (N) and phosphorus(P) per unit leaf area (Ma,Naand Pa, respectively), and chlorophyll from 210 species at 18field sites along a 3300-m elevation gradient. Western blots were used to quantify the abun-dance of the CO₂-fixing enzyme Rubisco. Area- and N-based rates of photosynthetic capacity at 25°C were higher in upland than low-land TMFs, underpinned by greater investment of N in photosynthesis in high-elevation trees. Soil [P] and leaf Pa were key explanatory factors for models of area-based Vcmax and Jmax but did not account for variations in photosynthetic N-use efficiency. At any given Na and Pa, the fraction of N allocated to photosynthesis was higher in upland than lowland species. For a smallsubset of lowland TMF trees examined, a substantial fraction of Rubisco was inactive. These results highlight the importance of soil- and leaf-P in defining the photosyntheticcapacity of TMFs, with variations in N allocation and Rubisco activation state further influenc-ing photosynthetic rates and N-use efficiency of these critically important forests

Implications of improved representations of plant respiration in a changing climate

Land-atmosphere exchanges influence atmospheric CO2. Emphasis has been on describing photosynthetic CO2 uptake, but less on respiration losses. New global datasets describe upper canopy dark respiration (Rd) and temperature dependencies. This allows characterisation of baseline Rd, instantaneous temperature responses and longer-term thermal acclimation effects. Here we show the global implications of these parameterisations with a global gridded land model. This model aggregates Rd to whole-plant respiration Rp, driven with meteorological forcings spanning uncertainty across climate change models. For pre-industrial estimates, new baseline Rd increases Rp and especially in the tropics. Compared to new baseline, revised instantaneous response decreases Rp for mid-latitudes, while acclimation lowers this for the tropics with increases elsewhere. Under global warming, new Rd estimates amplify modelled respiration increases, although partially lowered by acclimation. Future measurements will refine how Rd aggregates to whole-plant respiration. Our analysis suggests Rp could be around 30% higher than existing estimates

Solar radiation and functional traits explain the decline of forest primary productivity along a tropical elevation gradient

One of the major challenges in ecology is to understand how ecosystems respond to changes in environmental conditions, and how taxonomic and functional diversity mediate these changes. In this study, we use a trait-spectra and individual-based model, to analyse variation in forest primary productivity along a 3.3 km elevation gradient in the Amazon-Andes. The model accurately predicted the magnitude and trends in forest productivity with elevation, with solar radiation and plant functional traits (leaf dry mass per area, leaf nitrogen and phosphorus concentration, and wood density) collectively accounting for productivity variation. Remarkably, explicit representation of temperature variation with elevation was not required to achieve accurate predictions of forest productivity, as trait variation driven by species turnover appears to capture the effect of temperature. Our semi-mechanistic model suggests that spatial variation in traits can potentially be used to estimate spatial variation in productivity at the landscape scale

Twenty-Two Years of Warming, Fertilisation and Shading of Subarctic Heath Shrubs Promote Secondary Growth and Plasticity but Not Primary Growth

Most manipulation experiments simulating global change in tundra were short-term or did not measure plant growth directly. Here, we assessed the growth of three shrubs (Cassiope tetragona, Empetrum hermaphroditum and Betula nana) at a subarctic heath in Abisko (Northern Sweden) after 22 years of warming (passive greenhouses), fertilisation (nutrients addition) and shading (hessian fabric), and compare this to observations from the first decade of treatment. We assessed the growth rate of current-year leaves and apical stem (primary growth) and cambial growth (secondary growth), and integrated growth rates with morphological measurements and species coverage. Primary- and total growth of Cassiope and Empetrum were unaffected by manipulations, whereas growth was substantially reduced under fertilisation and shading (but not warming) for Betula. Overall, shrub height and length tended to increase under fertilisation and warming, whereas branching increased mostly in shaded Cassiope. Morphological changes were coupled to increased secondary growth under fertilisation. The species coverage showed a remarkable increase in graminoids in fertilised plots. Shrub response to fertilisation was positive in the short-term but changed over time, likely because of an increased competition with graminoids. More erected postures and large, canopies (requiring enhanced secondary growth for stem reinforcement) likely compensated for the increased light competition in Empetrum and Cassiope but did not avoid growth reduction in the shade intolerant Betula. The impact of warming and shading on shrub growth was more conservative. The lack of growth enhancement under warming suggests the absence of long-term acclimation for processes limiting biomass production. The lack of negative effects of shading on Cassiope was linked to morphological changes increasing the photosynthetic surface. Overall, tundra shrubs showed developmental plasticity over the longer term. However, such plasticity was associated clearly with growth rate trends only in fertilised plots