Differential physiological responses to environmental change promote woody shrub expansion

© The Author(s), 2013. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Ecology and Evolution 3 (2013): 1149–1162, doi:10.1002/ece3.525.Direct and indirect effects of warming are increasingly modifying the carbon-rich vegetation and soils of the Arctic tundra, with important implications for the terrestrial carbon cycle. Understanding the biological and environmental influences on the processes that regulate foliar carbon cycling in tundra species is essential for predicting the future terrestrial carbon balance in this region. To determine the effect of climate change impacts on gas exchange in tundra, we quantified foliar photosynthesis (Anet), respiration in the dark and light (RD and RL, determined using the Kok method), photorespiration (PR), carbon gain efficiency (CGE, the ratio of photosynthetic CO2 uptake to total CO2 exchange of photosynthesis, PR, and respiration), and leaf traits of three dominant species – Betula nana, a woody shrub; Eriophorum vaginatum, a graminoid; and Rubus chamaemorus, a forb – grown under long-term warming and fertilization treatments since 1989 at Toolik Lake, Alaska. Under warming, B. nana exhibited the highest rates of Anet and strongest light inhibition of respiration, increasing CGE nearly 50% compared with leaves grown in ambient conditions, which corresponded to a 52% increase in relative abundance. Gas exchange did not shift under fertilization in B. nana despite increases in leaf N and P and near-complete dominance at the community scale, suggesting a morphological rather than physiological response. Rubus chamaemorus, exhibited minimal shifts in foliar gas exchange, and responded similarly to B. nana under treatment conditions. By contrast, E. vaginatum, did not significantly alter its gas exchange physiology under treatments and exhibited dramatic decreases in relative cover (warming: −19.7%; fertilization: −79.7%; warming with fertilization: −91.1%). Our findings suggest a foliar physiological advantage in the woody shrub B. nana that is further mediated by warming and increased soil nutrient availability, which may facilitate shrub expansion and in turn alter the terrestrial carbon cycle in future tundra environments.This study was supported by the National Science Foundation #0732664; Australian Research Council DP0986823; and Marsden Fund of the Royal Society of New Zealand

Bringing the Kok effect to light: A review on the integration of daytime respiration and net ecosystem exchange

Net ecosystem exchange (NEE) represents the difference between carbon assimilated through photosynthesis, or gross primary productivity (GPP), and carbon released via ecosystem respiration (ER). NEE, measured via eddy covariance and chamber techniques, must be partitioned into these fluxes to accurately describe and understand the carbon dynamics of an ecosystem. GPP and daytime ER may be significantly overestimated if the light inhibition of foliar mitochondrial respiration, or “Kok effect,” is not accurately estimated and further integrated into ecosystem measurements. The light inhibition of respiration, a composite effect of multiple cellular pathways, is reported to cause between 25‐100% inhibition of foliar mitochondrial respiration, and for this reason needs to be considered when estimating larger carbon fluxes. Partitioning of respiration between autotrophic and heterotrophic respiration, and applying these scaled respiratory fluxes to the ecosystem‐level proves to be difficult, and the integration of light inhibition into single and continuous measures of ecosystem respiration will require new interpretations and analysis of carbon exchange in terrestrial ecosystems

Diel- and temperature-driven variation of leaf dark respiration rates and metabolite levels in rice

Leaf respiration in the dark (R-dark) is often measured at a single time during the day, with hot-acclimation lowering R-dark at a common measuring temperature. However, it is unclear whether the diel cycle influences the extent of thermal acclimation of R-dark, or how temperature and time of day interact to influence respiratory metabolites. To examine these issues, we grew rice under 25 degrees C : 20 degrees C, 30 degrees C : 25 degrees C and 40 degrees C : 35 degrees C day : night cycles, measuring R-dark and changes in metabolites at five time points spanning a single 24-h period. R-dark differed among the treatments and with time of day. However, there was no significant interaction between time and growth temperature, indicating that the diel cycle does not alter thermal acclimation of R-dark. Amino acids were highly responsive to the diel cycle and growth temperature, and many were negatively correlated with carbohydrates and with organic acids of the tricarboxylic acid (TCA) cycle. Organic TCA intermediates were significantly altered by the diel cycle irrespective of growth temperature, which we attributed to light-dependent regulatory control of TCA enzyme activities. Collectively, our study shows that environmental disruption of the balance between respiratory substrate supply and demand is corrected for by shifts in TCA-dependent metabolites.Peer reviewe

Drought increases heat tolerance of leaf respiration in Eucalyptus globulus saplings grown under both ambient and elevated atmospheric [CO₂] and temperature

Climate change is resulting in increasing atmospheric [CO₂], rising growth temperature (T), and greater frequency/severity of drought, with each factor having the potential to alter the respiratory metabolism of leaves. Here, the effects of elevated atmospheric [CO₂], sustained warming, and drought on leaf dark respiration (R(dark)), and the short-term T response of R(dark) were examined in Eucalyptus globulus. Comparisons were made using seedlings grown under different [CO₂], T, and drought treatments. Using high resolution T-response curves of R(dark) measured over the 15-65 °C range, it was found that elevated [CO₂], elevated growth T, and drought had little effect on rates of R(dark) measured at T <35 °C and that there was no interactive effect of [CO₂], growth T, and drought on T response of R(dark). However, drought increased R(dark) at high leaf T typical of heatwave events (35-45 °C), and increased the measuring T at which maximal rates of R(dark) occurred (Tmax) by 8 °C (from 52 °C in well-watered plants to 60 °C in drought-treated plants). Leaf starch and soluble sugars decreased under drought and elevated growth T, respectively, but no effect was found under elevated [CO₂]. Elevated [CO₂] increased the Q₁₀ of R(dark) (i.e. proportional rise in R(dark) per 10 °C) over the 15-35 °C range, while drought increased Q₁₀ values between 35 °C and 45 °C. Collectively, the study highlights the dynamic nature of the T dependence of R dark in plants experiencing future climate change scenarios, particularly with respect to drought and elevated [CO₂].This work was funded by the Australian Research Council (ARC FT0991448, DP1093759, and CE140100008, to OKA; and DP0879531, to DTT). This project is supported by funding from the Australian Government Department of Agriculture, Fisheries and Forestry under its Forest Industries Climate Change Research Fund programme. Support for the renovation of the Hawkesbury Forest Experiment tree chambers to improve T and humidity control of the WTC was provided as part of an initiative of the Australian Government through the Education Investment Fund supporting research infrastructure

Leaf- and cell-level carbon cycling responses to a nitrogen and phosphorus gradient in two Arctic tundra species

Premise of the study: Consequences of global climate change are detectable in the historically nitrogen- and phosphorus-limited Arctic tundra landscape and have implications for the terrestrial carbon cycle. Warmer temperatures and elevated soil nutrient availability associated with increased microbial activity may influence rates of photosynthesis and respiration. Methods: This study examined leaf-level gas exchange, cellular ultrastructure, and related leaf traits in two dominant tundra species, Betula nana, a woody shrub, and Eriophorum vaginatum, a tussock sedge, under a 3-yr-old treatment gradient of nitrogen (N) and phosphorus (P) fertilization in the North Slope of Alaska. Key results: Respiration increased with N and P addition—the highest rates corresponding to the highest concentrations of leaf N in both species. The inhibition of respiration by light ("Kok effect") significantly reduced respiration rates in both species (P < 0.001), ranged from 12–63% (mean 34%), and generally decreased with fertilization for both species. However, in both species, observed rates of photosynthesis did not increase, and photosynthetic nitrogen use efficiency generally decreased under increasing fertilization. Chloroplast and mitochondrial size and density were highly sensitive to N and P fertilization (P < 0.001), though species interactions indicated divergent cellular organizational strategies. Conclusions: Results from this study demonstrate a species-specific decoupling of respiration and photosynthesis under N and P fertilization, implying an alteration of the carbon balance of the tundra ecosystem under future conditions

Molecular and physiological responses during thermal acclimation of leaf photosynthesis and respiration in rice

To further our understanding of how sustained changes in temperature affect the carbon economy of rice (Oryza sativa), hydroponically grown plants of the IR64 cultivar were developed at 30°C/25°C (day/night) before being shifted to 25/20°C or 40/35°C. Leaf messenger RNA and protein abundance, sugar and starch concentrations, and gas‐exchange and elongation rates were measured on preexisting leaves (PE) already developed at 30/25°C or leaves newly developed (ND) subsequent to temperature transfer. Following a shift in growth temperature, there was a transient adjustment in metabolic gene transcript abundance of PE leaves before homoeostasis was reached within 24 hr, aligning with Rdark (leaf dark respiratory CO2 release) and An (net CO2 assimilation) changes. With longer exposure, the central respiratory protein cytochrome c oxidase (COX) declined in abundance at 40/35°C. In contrast to Rdark, An was maintained across the three growth temperatures in ND leaves. Soluble sugars did not differ significantly with growth temperature, and growth was fastest with extended exposure at 40/35°C. The results highlight that acclimation of photosynthesis and respiration is asynchronous in rice, with heat‐acclimated plants exhibiting a striking ability to maintain net carbon gain and growth when exposed to heat‐wave temperatures, even while reducing investment in energy‐conserving respiratory pathways.Peer reviewe

Light inhibition of foliar respiration in response to soil water availability and seasonal changes in temperature Mediterranean holm oak. (quercus ilex forest)

In the present study we investigated variations in leaf respiration in darkness (RD) and light (RL), and associated traits in response to season, and along a gradient of soil moisture, in Mediterranean woodland dominated by holm oak (Quercus ilex L.) in central and north-eastern Spain respectively. On seven occasions during the year in the central Spain site, and along the soil moisture gradient in north-eastern Spain, we measured rates of leaf RD, RL (using the Kok method), light-saturated photosynthesis (A) and related light response characteristics, leaf mass per unit area (MA) and leaf nitrogen (N) content. At the central Spain site, significant seasonal changes in soil water content and ambient temperature (T) were associated with changes in MA, foliar N, A and stomatal conductance. RD measured at the prevailing daily T and in instantaneous R-T responses, displayed signs of partial acclimation and was not significantly affected by time of year. RL was always less than, and strongly related to, RD, and RL/RD did not vary significantly or systematically with seasonal changes in T or soil water content. Averaged over the year, RL/RD was 0.66 ± 0.05 s.e. (n = 14) at the central Spain site. At the north-eastern Spain site, the soil moisture gradient was characterised by increasing MA and RD, and reduced foliar N, A, and stomatal conductance as soil water availability decreased. Light inhibition of R occurred across all sites (mean RL/RD = 0.69 ± 0.01 s.e. (n = 18)), resulting in ratios of RL/A being lower than for RD/A. Importantly, the degree of light inhibition was largely insensitive to changes in soil water content. Our findings provide evidence for a relatively constrained degree of light inhibition of R (RL/RD ~ 0.7, or inhibition of ~30%) across gradients of water availability, although combined impacts of seasonal changes in both T and soil water content increase the range of values expressed. The findings thus have implications in terms of the assumptions made by predictive models that seek to account for light inhibition of R, and for our understanding of how environmental gradients impact on leaf trait relationships in Mediterranean plant communities

Updated respiration routines alter spatio-temporal patterns of carbon cycling in a global land surface model

We updated the routines used to estimate leaf maintenance respiration (MR) in the Energy Land Model (ELM) using a comprehensive global respiration data base. The updated algorithm includes a temperature acclimating base rate, an updated instantaneous temperature response, and new plant functional type specific parameters. The updated MR algorithm resulted in a very large increase in global MR of 16.1 Pg (38%), but the signal was not geographically uniform. The increase was concentrated in the tropics and humid warm-temperate forests. The increase in MR led to large but proportionally smaller decreases in global net primary production (19%) and in average global leaf area index (15%). The effect on global gross primary production (GPP) was a more modest 5.7 Pg (4%). A detailed site level analysis also demonstrated a wide range of effects the updated algorithm can have on the seasonal cycle of GPP. Output from the updated and old models did not differ markedly in how closely they matched a suite of benchmarks. Given the substantial impact on the land surface carbon cycle, a neutral influence on model benchmarks, and better alignment with empirical evidence, an MR algorithm similar to the one presented here should be adopted into ELM

Exploring high temperature responses of photosynthesis and respiration to improve heat tolerance in wheat

High temperatures account for major wheat yield losses annually and, as the climate continues to warm, these losses will probably increase. Both photosynthesis and respiration are the main determinants of carbon balance and growth in wheat, and both are sensitive to high temperature. Wheat is able to acclimate photosynthesis and respiration to high temperature, and thus reduce the negative affects on growth. The capacity to adjust these processes to better suit warmer conditions stands as a potential avenue toward reducing heat-induced yield losses in the future. However, much remains to be learnt about such phenomena. Here, we review what is known of high temperature tolerance in wheat, focusing predominantly on the high temperature responses of photosynthesis and respiration. We also identify the many unknowns that surround this area, particularly with respect to the high temperature response of wheat respiration and the consequences of this for growth and yield. It is concluded that further investigation into the response of photosynthesis and respiration to high temperature could present several methods of improving wheat high temperature tolerance. Extending our knowledge in this area could also lead to more immediate benefits, such as the enhancement of current crop models

Exploring high temperature responses of photosynthesis and respiration to improve heat tolerance in wheat

High temperatures account for major wheat yield losses annually and, as the climate continues to warm, these losses will probably increase. Both photosynthesis and respiration are the main determinants of carbon balance and growth in wheat, and both are sensitive to high temperature. Wheat is able to acclimate photosynthesis and respiration to high temperature, and thus reduce the negative affects on growth. The capacity to adjust these processes to better suit warmer conditions stands as a potential avenue toward reducing heat-induced yield losses in the future. However, much remains to be learnt about such phenomena. Here, we review what is known of high temperature tolerance in wheat, focusing predominantly on the high temperature responses of photosynthesis and respiration. We also identify the many unknowns that surround this area, particularly with respect to the high temperature response of wheat respiration and the consequences of this for growth and yield. It is concluded that further investigation into the response of photosynthesis and respiration to high temperature could present several methods of improving wheat high temperature tolerance. Extending our knowledge in this area could also lead to more immediate benefits, such as the enhancement of current crop models