Plasticity of photosynthetic heat tolerance in plants adapted to thermally contrasting biomes.

In many biomes, plants are subject to heatwaves, potentially causing irreversible damage to the photosynthetic apparatus. Field surveys have documented global, temperature-dependent patterns in photosynthetic heat tolerance (PHT ); however, it remains unclear if these patterns reflect acclimation in PHT or inherent differences among species adapted to contrasting habitats. To address these unknowns, we quantified seasonal variations in Tcrit (high temperature where minimal chlorophyll-a fluorescence rises rapidly, reflecting disruption to photosystem II) in 62 species native to 6 sites from 5 thermally contrasting biomes across Australia. Tcrit and leaf fatty acid (FA) composition (important for membrane stability) were quantified in three temperature-controlled glasshouses in 20 of those species. Tcrit was greatest at hot field sites and acclimated seasonally (summer > winter, increasing on average 0.34 °C per °C increase in growth temperature). The glasshouse study showed that Tcrit was inherently higher in species from warmer habitats (increasing 0.16 °C per °C increase in origin annual mean maximum temperature) and acclimated to increasing growth temperature (0.24 °C °C-1 ). Variations in Tcrit were positively correlated with the relative abundance of saturated FAs, with FAs accounting for 40% of Tcrit variation. These results highlight the importance of both plastic adjustments and inherent differences determining contemporary continent-wide patterns in PHT .

Phosphorus deficiency alters scaling relationships between leaf gas exchange and associated traits in a wide range of contrasting Eucalyptus species.

Phosphorus (P) limitation is known to have substantial impacts on leaf metabolism. However, uncertainty remains around whether P deficiency alters scaling functions linking leaf metabolism to associated traits. We investigated the effect of P deficiency on leaf gas exchange and related leaf traits in 17 contrasting Eucalyptus species that exhibit inherent differences in leaf traits. Saplings were grown under controlled-environment conditions in a glasshouse, where they were subjected to minus and plus P treatments for 15 weeks. P deficiency decreased P concentrations and increased leaf mass per area (LMA) of newly-developed leaves. Rates of photosynthesis (A) and respiration (R) were also reduced in P-deficient plants compared with P-fertilised plants. By contrast, P deficiency had little effect on the temperature sensitivity of R. Irrespective of P treatment, on a log-log basis A and R scaled positively with increasing leaf nitrogen concentration [N] and negatively with increasing LMA. Although P deficiency had limited impact on A-R-LMA relationships, rates of CO2 exchange per unit N were consistently lower in P-deficient plants. Our results highlight the importance of P supply for leaf carbon metabolism and show how P deficiencies (i.e. when excluding confounding genotypic and environmental effects) can have a direct effect on commonly used leaf trait scaling relationships.

Macromolecular rate theory (MMRT) provides a thermodynamics rationale to underpin the convergent temperature response in plant leaf respiration.

Temperature is a crucial factor in determining the rates of ecosystem processes, for example, leaf respiration (R) - the flux of plant respired CO2 from leaves to the atmosphere. Generally, R increases exponentially with temperature and formulations such as the Arrhenius equation are widely used in earth system models. However, experimental observations have shown a consequential and consistent departure from an exponential increase in R. What are the principles that underlie these observed patterns? Here, we demonstrate that macromolecular rate theory (MMRT), based on transition state theory (TST) for enzyme-catalyzed kinetics, provides a thermodynamic explanation for the observed departure and the convergent temperature response of R using a global database. Three meaningful parameters emerge from MMRT analysis: the temperature at which the rate of respiration would theoretically reach a maximum (the optimum temperature, Topt ), the temperature at which the respiration rate is most sensitive to changes in temperature (the inflection temperature, Tinf ) and the overall curvature of the log(rate) versus temperature plot (the change in heat capacity for the system, ΔCP‡). On average, the highest potential enzyme-catalyzed rates of respiratory enzymes for R are predicted to occur at 67.0 ± 1.2°C and the maximum temperature sensitivity at 41.4 ± 0.7°C from MMRT. The average curvature (average negative ΔCP‡) was -1.2 ± 0.1 kJ mol-1  K-1 . Interestingly, Topt , Tinf and ΔCP‡ appear insignificantly different across biomes and plant functional types, suggesting that thermal response of respiratory enzymes in leaves could be conserved. The derived parameters from MMRT can serve as thermal traits for plant leaves that represent the collective temperature response of metabolic respiratory enzymes and could be useful to understand regulations of R under a warmer climate. MMRT extends the classic TST to enzyme-catalyzed reactions and provides an accurate and mechanistic model for the short-term temperature response of R around the globe.

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 (R d) and temperature dependencies. This allows characterisation of baseline R d, 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 R d to whole-plant respiration R p, driven with meteorological forcings spanning uncertainty across climate change models. For pre-industrial estimates, new baseline R d increases R p and especially in the tropics. Compared to new baseline, revised instantaneous response decreases R p for mid-latitudes, while acclimation lowers this for the tropics with increases elsewhere. Under global warming, new R d estimates amplify modelled respiration increases, although partially lowered by acclimation. Future measurements will refine how R d aggregates to whole-plant respiration. Our analysis suggests R p could be around 30% higher than existing estimates.

Nitrogen and phosphorus availabilities interact to modulate leaf trait scaling relationships across six plant functional types in a controlled-environment study.

Nitrogen (N) and phosphorus (P) have key roles in leaf metabolism, resulting in a strong coupling of chemical composition traits to metabolic rates in field-based studies. However, in such studies, it is difficult to disentangle the effects of nutrient supply per se on trait-trait relationships. Our study assessed how high and low N (5 mM and 0.4 mM, respectively) and P (1 mM and 2 µM, respectively) supply in 37 species from six plant functional types (PTFs) affected photosynthesis (A) and respiration (R) (in darkness and light) in a controlled environment. Low P supply increased scaling exponents (slopes) of area-based log-log A-N or R-N relationships when N supply was not limiting, whereas there was no P effect under low N supply. By contrast, scaling exponents of A-P and R-P relationships were altered by P and N supply. Neither R : A nor light inhibition of leaf R was affected by nutrient supply. Light inhibition was 26% across nutrient treatments; herbaceous species exhibited a lower degree of light inhibition than woody species. Because N and P supply modulates leaf trait-trait relationships, the next generation of terrestrial biosphere models may need to consider how limitations in N and P availability affect trait-trait relationships when predicting carbon exchange.

Optimising UK urban road verge contributions to biodiversity and ecosystem services with cost-effective management.

Urban road verges can contain significant biodiversity, contribute to structural connectivity between other urban greenspaces, and due to their proximity to road traffic are well placed to provide ecosystem services. Using the UK as a case study we review and critically evaluate a broad range of evidence to assess how this considerable potential can be enhanced despite financial, contractual and public opinion constraints. Reduced mowing frequency and other alterations would enhance biodiversity, aesthetics and pollination services, whilst delivering costs savings and potentially being publically acceptable. Retaining mature trees and planting additional ones is favourable to residents and would enhance biodiversity, pollution and climate regulation, carbon storage, and stormwater management. Optimising these services requires improved selection of tree species, and creating a more diverse tree stock. Due to establishment costs additional tree planting and maintenance could benefit from payment for ecosystem service schemes. Verges could also provide areas for cultivation of biofuels and possibly food production. Maximising the contribution of verges to urban biodiversity and ecosystem services is economical and becoming an increasingly urgent priority as the road network expands and other urban greenspace is lost, requiring enhancement of existing greenspace to facilitate sustainable urban development.

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.

Thermal limits of leaf metabolism across biomes.

High-temperature tolerance in plants is important in a warming world, with extreme heat waves predicted to increase in frequency and duration, potentially leading to lethal heating of leaves. Global patterns of high-temperature tolerance are documented in animals, but generally not in plants, limiting our ability to assess risks associated with climate warming. To assess whether there are global patterns in high-temperature tolerance of leaf metabolism, we quantified Tcrit (high temperature where minimal chlorophyll a fluorescence rises rapidly and thus photosystem II is disrupted) and Tmax (temperature where leaf respiration in darkness is maximal, beyond which respiratory function rapidly declines) in upper canopy leaves of 218 plant species spanning seven biomes. Mean site-based Tcrit values ranged from 41.5 °C in the Alaskan arctic to 50.8 °C in lowland tropical rainforests of Peruvian Amazon. For Tmax , the equivalent values were 51.0 and 60.6 °C in the Arctic and Amazon, respectively. Tcrit and Tmax followed similar biogeographic patterns, increasing linearly (˜8 °C) from polar to equatorial regions. Such increases in high-temperature tolerance are much less than expected based on the 20 °C span in high-temperature extremes across the globe. Moreover, with only modest high-temperature tolerance despite high summer temperature extremes, species in mid-latitude (~20-50°) regions have the narrowest thermal safety margins in upper canopy leaves; these regions are at the greatest risk of damage due to extreme heat-wave events, especially under conditions when leaf temperatures are further elevated by a lack of transpirational cooling. Using predicted heat-wave events for 2050 and accounting for possible thermal acclimation of Tcrit and Tmax , we also found that these safety margins could shrink in a warmer world, as rising temperatures are likely to exceed thermal tolerance limits. Thus, increasing numbers of species in many biomes may be at risk as heat-wave events become more severe with climate change.

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

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 variability in leaf respiration in relation to climate, plant functional types and leaf traits.

Leaf dark respiration (Rdark ) is an important yet poorly quantified component of the global carbon cycle. Given this, we analyzed a new global database of Rdark and associated leaf traits. Data for 899 species were compiled from 100 sites (from the Arctic to the tropics). Several woody and nonwoody plant functional types (PFTs) were represented. Mixed-effects models were used to disentangle sources of variation in Rdark . Area-based Rdark at the prevailing average daily growth temperature (T) of each site increased only twofold from the Arctic to the tropics, despite a 20°C increase in growing T (8-28°C). By contrast, Rdark at a standard T (25°C, Rdark (25) ) was threefold higher in the Arctic than in the tropics, and twofold higher at arid than at mesic sites. Species and PFTs at cold sites exhibited higher Rdark (25) at a given photosynthetic capacity (Vcmax (25) ) or leaf nitrogen concentration ([N]) than species at warmer sites. Rdark (25) values at any given Vcmax (25) or [N] were higher in herbs than in woody plants. The results highlight variation in Rdark among species and across global gradients in T and aridity. In addition to their ecological significance, the results provide a framework for improving representation of Rdark in terrestrial biosphere models (TBMs) and associated land-surface components of Earth system models (ESMs).

Modelling short-rotation coppice and tree planting for urban carbon management - a citywide analysis.

The capacity of urban areas to deliver provisioning ecosystem services is commonly overlooked and underutilized. Urban populations have globally increased fivefold since 1950, and they disproportionately consume ecosystem services and contribute to carbon emissions, highlighting the need to increase urban sustainability and reduce environmental impacts of urban dwellers. Here, we investigated the potential for increasing carbon sequestration, and biomass fuel production, by planting trees and short-rotation coppice (SRC), respectively, in a mid-sized UK city as a contribution to meeting national commitments to reduce CO 2 emissions.Iterative GIS models were developed using high-resolution spatial data. The models were applied to patches of public and privately owned urban greenspace suitable for planting trees and SRC, across the 73 km2 area of the city of Leicester. We modelled tree planting with a species mix based on the existing tree populations, and SRC with willow and poplar to calculate biomass production in new trees, and carbon sequestration into harvested biomass over 25 years.An area of 11 km2 comprising 15% of the city met criteria for tree planting and had the potential over 25 years to sequester 4200 tonnes of carbon above-ground. Of this area, 5·8 km2 also met criteria for SRC planting and over the same period this could yield 71 800 tonnes of carbon in harvested biomass.The harvested biomass could supply energy to over 1566 domestic homes or 30 municipal buildings, resulting in avoided carbon emissions of 29 236 tonnes of carbon over 25 years when compared to heating by natural gas. Together with the net carbon sequestration into trees, a total reduction of 33 419 tonnes of carbon in the atmosphere could be achieved in 25 years by combined SRC and tree planting across the city. Synthesis and applications. We demonstrate that urban greenspaces in a typical UK city are underutilized for provisioning ecosystem services by trees and especially SRC, which has high biomass production potential. For urban greenspace management, we recommend that planting SRC in urban areas can contribute to reducing food-fuel conflicts on agricultural land and produce renewable energy sources close to centres of population and demand.

Urban tree effects on soil organic carbon.

Urban trees sequester carbon into biomass and provide many ecosystem service benefits aboveground leading to worldwide tree planting schemes. Since soils hold ∼75% of ecosystem organic carbon, understanding the effect of urban trees on soil organic carbon (SOC) and soil properties that underpin belowground ecosystem services is vital. We use an observational study to investigate effects of three important tree genera and mixed-species woodlands on soil properties (to 1 m depth) compared to adjacent urban grasslands. Aboveground biomass and belowground ecosystem service provision by urban trees are found not to be directly coupled. Indeed, SOC enhancement relative to urban grasslands is genus-specific being highest under Fraxinus excelsior and Acer spp., but similar to grasslands under Quercus robur and mixed woodland. Tree cover type does not influence soil bulk density or C∶N ratio, properties which indicate the ability of soils to provide regulating ecosystem services such as nutrient cycling and flood mitigation. The trends observed in this study suggest that genus selection is important to maximise long-term SOC storage under urban trees, but emerging threats from genus-specific pathogens must also be considered.

Thermal acclimation of shoot respiration in an Arctic woody plant species subjected to 22 years of warming and altered nutrient supply.

Despite concern about the status of carbon (C) in the Arctic tundra, there is currently little information on how plant respiration varies in response to environmental change in this region. We quantified the impact of long-term nitrogen (N) and phosphorus (P) treatments and greenhouse warming on the short-term temperature (T) response and sensitivity of leaf respiration (R), the high-T threshold of R, and associated traits in shoots of the Arctic shrub Betula nana in experimental plots at Toolik Lake, Alaska. Respiration only acclimated to greenhouse warming in plots provided with both N and P (resulting in a ~30% reduction in carbon efflux in shoots measured at 10 and 20 °C), suggesting a nutrient dependence of metabolic adjustment. Neither greenhouse nor N+P treatments impacted on the respiratory sensitivity to T (Q10 ); overall, Q10 values decreased with increasing measuring T, from ~3.0 at 5 °C to ~1.5 at 35 °C. New high-resolution measurements of R across a range of measuring Ts (25-70 °C) yielded insights into the T at which maximal rates of R occurred (Tmax ). Although growth temperature did not affect Tmax , N+P fertilization increased Tmax values ~5 °C, from 53 to 58 °C. N+P fertilized shoots exhibited greater rates of R than nonfertilized shoots, with this effect diminishing under greenhouse warming. Collectively, our results highlight the nutrient dependence of thermal acclimation of leaf R in B. nana, suggesting that the metabolic efficiency allowed via thermal acclimation may be impaired at current levels of soil nutrient availability. This finding has important implications for predicting carbon fluxes in Arctic ecosystems, particularly if soil N and P become more abundant in the future as the tundra warms.

High-resolution temperature responses of leaf respiration in snow gum (Eucalyptus pauciflora) reveal high-temperature limits to respiratory function.

We tested whether snow gum (Eucalyptus pauciflora) trees growing in thermally contrasting environments exhibit generalizable temperature (T) response functions of leaf respiration (R) and fluorescence (Fo). Measurements were made on pot-grown saplings and field-grown trees (growing between 1380 and 2110 m a.s.l.). Using a continuous, high-resolution protocol, we quantified T response curves of R and Fo--these data were used to identify an algorithm for modelling R-T curves at subcritical T's and establish variations in heat tolerance. For the latter, we quantified Tmax [T where R is maximal] and Tcrit [T where Fo rises rapidly]. Tmax ranged from 51 to 57 °C, varying with season (e.g. winter summer). Tcrit ranged from 41 to 49 °C in summer and from 58 to 63 °C in winter. Thus, surprisingly, leaf energy metabolism was more heat-tolerant in trees experiencing ice-encasement in winter than warmer conditions in summer. A polynomial model fitted to log-transformed R data provided the best description of the T-sensitivity of R (between 10 and 45 °C); using these model fits, we found that the negative slope of the Q10 -T relationship was greater in winter than in summer. Collectively, our results (1) highlight high-T limits of energy metabolism in E. pauciflora and (2) provide a framework for improving representation of T-responses of leaf R in predictive models.