Keith J. Bloomfield

Convergence in the temperature response of leaf respiration across biomes and plant functional types.

Significance A major concern for terrestrial biosphere models is accounting for the temperature response of leaf respiration at regional/global scales. Most biosphere models incorrectly assume that respiration increases exponentially with rising temperature, with profound effects for predicted ecosystem carbon exchange. Based on a study of 231 species in 7 biomes, we find that the rise in respiration with temperature can be generalized across biomes and plant types, with temperature sensitivity declining as leaves warm. This finding indicates universally conserved controls on the temperature sensitivity of leaf metabolism. Accounting for the temperature function markedly lowers simulated respiration rates in cold biomes, which has important consequences for estimates of carbon storage in vegetation, predicted concentrations of atmospheric carbon dioxide, and future surface temperatures. Plant respiration constitutes a massive carbon flux to the atmosphere, and a major control on the evolution of the global carbon cycle. It therefore has the potential to modulate levels of climate change due to the human burning of fossil fuels. Neither current physiological nor terrestrial biosphere models adequately describe its short-term temperature response, and even minor differences in the shape of the response curve can significantly impact estimates of ecosystem carbon release and/or storage. Given this, it is critical to establish whether there are predictable patterns in the shape of the respiration–temperature response curve, and thus in the intrinsic temperature sensitivity of respiration across the globe. Analyzing measurements in a comprehensive database for 231 species spanning 7 biomes, we demonstrate that temperature-dependent increases in leaf respiration do not follow a commonly used exponential function. Instead, we find a decelerating function as leaves warm, reflecting a declining sensitivity to higher temperatures that is remarkably uniform across all biomes and plant functional types. Such convergence in the temperature sensitivity of leaf respiration suggests that there are universally applicable controls on the temperature response of plant energy metabolism, such that a single new function can predict the temperature dependence of leaf respiration for global vegetation. This simple function enables straightforward description of plant respiration in the land-surface components of coupled earth system models. Our cross-biome analyses shows significant implications for such fluxes in cold climates, generally projecting lower values compared with previous estimates.

Global convergence in leaf respiration from estimates of thermal acclimation across time and space

Recent compilations of experimental and observational data have documented global temperature-dependent patterns of variation in leaf dark respiration (R), but it remains unclear whether local adjustments in respiration over time (through thermal acclimation) are consistent with the patterns in R found across geographical temperature gradients. We integrated results from two global empirical syntheses into a simple temperature-dependent respiration framework to compare the measured effects of respiration acclimation-over-time and variation-across-space to one another, and to a null model in which acclimation is ignored. Using these models, we projected the influence of thermal acclimation on: seasonal variation in R; spatial variation in mean annual R across a global temperature gradient; and future increases in R under climate change. The measured strength of acclimation-over-time produces differences in annual R across spatial temperature gradients that agree well with global variation-across-space. Our models further project that acclimation effects could potentially halve increases in R (compared with the null model) as the climate warms over the 21st Century. Convergence in global temperature-dependent patterns of R indicates that physiological adjustments arising from thermal acclimation are capable of explaining observed variation in leaf respiration at ambient growth temperatures across the globe.

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 the environment and/or associated leaf traits for tropical moist forests (TMFs) in the Andes/western 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 , Na and Pa , respectively), and chlorophyll from 210 species at 18 field sites along a 3300-m elevation gradient. Western blots were used to quantify the abundance of the CO2 -fixing enzyme Rubisco. Area- and N-based rates of photosynthetic capacity at 25°C were higher in upland than lowland 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 small subset 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 photosynthetic capacity of TMFs, with variations in N allocation and Rubisco activation state further influencing photosynthetic rates and N-use efficiency of these critically important forests.

Photosynthesis-nitrogen relationships in tropical forest tree species as affected by soil phosphorus availability: A controlled environment study

Tropical soils are often characterised by low phosphorus availability and tropical forest trees typically exhibit lower area-based rates of photosynthesis (Aa) for a given area-based leaf nitrogen concentration ([N]a) compared with plants growing in higher-latitude, N-limited ecosystems. Nevertheless, to date, very few studies have assessed the effects of P deprivation per se on Aa⟷[N]a relationships in tropical trees. Our study investigated the effect of reduced soil P availability on light-saturated Aa and related leaf traits of seven Australian tropical tree species. We addressed the following questions: (1) Do contrasting species exhibit inherent differences in nutrient partitioning and morphology? (2) Does P deprivation lead to a change in the nature of the Aa⟷[N]a relationship? (3) Does P deprivation lead to an alteration in leaf nitrogen levels or N allocation within the leaf? Applying a mixed effects model, we found that for these Australian tropical tree species, removal of P from the nutrient solution decreased area-based photosynthetic capacity (Amax,a) by 18% and reduced the slope of the Amax,a⟷[N]a relationship and differences among species accounted for around 30% of response variation. Despite greater N allocation to chlorophyll, photosynthetic N use efficiency was significantly reduced in low-P plants. Collectively, our results support the view that low soil P availability can alter photosynthesis-nitrogen relationships in tropical trees.

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

Summary Leaf dark respiration (R dark) represents an important component controlling the carbon balance in tropical forests. Here, we test how nitrogen (N) and phosphorus (P) affect R dark and its relationship with photosynthesis using three widely separated tropical forests which differ in soil fertility. R dark was measured on 431 rainforest canopy trees, from 182 species, in French Guiana, Peru and Australia. The variation in R dark was examined in relation to leaf N and P content, leaf structure and maximum photosynthetic rates at ambient and saturating atmospheric CO 2 concentration. We found that the site with the lowest fertility (French Guiana) exhibited greater rates of R dark 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 R dark with the measured leaf traits. Our data indicate that no single universal scaling relationship accounts for variation in R dark across this large biogeographical space. Variability between sites in the absolute rates of R dark and the R dark : photosynthesis ratio were driven by variations in N‐ and P‐use efficiency, which were related to both taxonomic and environmental variability.

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

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 13 C isotope discrimination (Δ13 C), 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 Δ13 C and intrinsic water-use efficiency (WUEi ) vary with climate at a continental scale? (ii) What are the seasonal and spatial patterns in Δ13 C/WUEi across biomes and species? (iii) To what extent does Δ13 C 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 Δ13 C differ across seasons? We found that MAP, temperature seasonality, isothermality and annual temperature range exerted independent effects on foliar Δ13 C/WUEi . Temperature-related variables exerted larger effects than rainfall-related variables. The relative importance of photosynthesis and stomatal conductance (gs ) in determining Δ13 C differed across seasons: Δ13 C was more strongly regulated by gs during the dry-season and by photosynthetic capacity during the wet-season. Δ13 C 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 Δ13 C. Leaf Pmass showed significant positive relationship with MAP and Δ13 C only during the dry-season. For all leaf nutrient-related traits, the relationships obtained for Δ13 C with MAP or MI indicated that Δ13 C 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 Δ13 C across Australia.

Reply to Adams et al.: Empirical versus process-based approaches to modeling temperature responses of leaf respiration

Reply to Adams et al. : Empirical versus process-based approaches to modeling temperature responses of leaf respiration

A continental-scale assessment of variability in leaf traits: within species, across sites and between seasons

Plant species show considerable leaf trait variability that should be accounted for in dynamic global vegetation models (DGVMs). In particular, differences in the acclimation of leaf traits during periods more and less favourable to growth have rarely been examined. We conducted a field study of leaf trait variation at seven sites spanning a range of climates and latitudes across the Australian continent; 80 native plant species were included. We measured key traits associated with leaf structure, chemistry and metabolism during the favourable and unfavourable growing seasons. Leaf traits differed widely in the degree of seasonal variation displayed. Leaf mass per unit area (M-a) showed none. At the other extreme, seasonal variation accounted for nearly a third of total variability in dark respiration (R-dark). At the non-tropical sites, carboxylation capacity (V-cmax) at the prevailing growth temperature was typically higher in summer than in winter. When V-cmax was normalized to a common reference temperature (25 degrees C), however, the opposite pattern was observed for about 30% of the species. This suggests that metabolic acclimation is possible, but far from universal. Intraspecific variationcombining measurements of individual plants repeated at contrasting seasons, different leaves from the same individual, and multiple conspecific plants at a given sitedominated total variation for leaf metabolic traits V-cmax and R-dark. By contrast, site location was the major source of variation (53%) for M-a. Interspecific trait variation ranged from only 13% of total variation for V-cmax up to 43% for nitrogen content per unit leaf area. These findings do not support a common practice in DGVMs of assigning fixed leaf trait values to plant functional types. Trait-based models should allow for interspecific differences, together with spatial and temporal plasticity in leaf structural, chemical and metabolic traits.

Leaf Respiration in Terrestrial Biosphere Models

How leaf respiration (Rd) is represented in leading terrestrial biosphere models (TBMs ) is reviewed, followed by an overview of how emerging global datasets provide opportunities to improve parameterization of leaf Rd in large-scale models. We first outline how TBMs have historically accounted for variations in respiratory CO2 release in mature leaves, using assumed relationships between leaf nitrogen, photosynthetic capacity and Rd. The need for TBMs to account for light inhibition of Rd in mature leaves is highlighted, followed by a discussion on how Rd of upper canopy leaves is used to predict maintenance respiration in whole plants. We then outline how respiratory energy requirements of growth are accounted for in TBMs, pointing out that current assumptions on the costs of biosynthesis are based on theoretical calculations that may not be valid for all plant species and environments. The chapter then considers how improvements might be made to TBMs with respect to the parameterization of leaf Rd. We show how recently compiled datasets provide improved capacity to predict global variations in baseline Rd measured at a standard temperature, and how baseline Rd likely acclimates to sustained changes in growth temperature. Application of this dataset reveals markedly higher rates of leaf Rd than currently predicted by TBMs , suggesting that TBMs may be underestimating global plant respiratory CO2 release. The availability of a new, global dataset on short-term temperature responses of leaf Rd is highlighted. Analysis of this dataset reveals that leaf Rd does not exhibit the exponential response assumed by most TBMs; rather, the temperature-sensitivity declines as leaves warm, with convergence in the temperature-response across biomes and plant functional types . We show how equations derived from these datasets may provide the TBM community with a new framework to improve representation of mature leaf respiration in TBMs.

Thermal acclimation of leaf respiration consistent with optimal plant function

Leaf mitochondrial (9dark9) respiration (Rd) is a key process influencing the feedback between climate change and atmospheric CO2 concentration. Yet no accepted theory accounts for its widely observed acclimation to temperature. Because Rd is closely linked to the maintenance of photosynthetic capacity (Vcmax), we propose that Rd thermal acclimation is predictable via the 9co-ordination hypothesis9 whereby optimal Vcmax is just sufficient to use average available resources. Predictions are compared to a global set of measurements from 110 sites spanning all biomes. Acclimated Rd and Vcmax (at growth temperature) are predicted to increase by 3.7% and 5.5% per °C respectively; whereas after correction to 25 °C, both are predicted to decline with growth temperature. These predictions are closely and quantitatively supported by the data. Thus we provide a parsimonious theory for Rd and its thermal acclimation, whose fidelity to observations implies that field-measured Rd is driven by photosynthetic demand.