A mechanism of expansion: Arctic deciduous shrubs capitalize on warming-induced nutrient availability.

Warming-induced nutrient enrichment in the Arctic may lead to shifts in leaf-level physiological properties and processes with potential consequences for plant community dynamics and ecosystem function. To explore the physiological responses of Arctic tundra vegetation to increasing nutrient availability, we examined how a set of leaf nutrient and physiological characteristics of eight plant species (representing four plant functional groups) respond to a gradient of experimental nitrogen (N) and phosphorus (P) enrichment. Specifically, we examined a set of chlorophyll fluorescence measures related to photosynthetic efficiency, performance and stress, and two leaf nutrient traits (leaf %C and %N), across an experimental nutrient gradient at the Arctic Long Term Ecological Research site, located in the northern foothills of the Brooks Range, Alaska. In addition, we explicitly assessed the direct relationships between chlorophyll fluorescence and leaf %N. We found significant differences in physiological and nutrient traits between species and plant functional groups, and we found that species within one functional group (deciduous shrubs) have significantly greater leaf %N at high levels of nutrient addition. In addition, we found positive, saturating relationships between leaf %N and chlorophyll fluorescence measures across all species. Our results highlight species-specific differences in leaf nutrient traits and physiology in this ecosystem. In particular, the effects of a gradient of nutrient enrichment were most prominent in deciduous plant species, the plant functional group known to be increasing in relative abundance with warming in this ecosystem.

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.

Temperature response of soil respiration largely unaltered with experimental warming.

The respiratory release of carbon dioxide (CO2) from soil is a major yet poorly understood flux in the global carbon cycle. Climatic warming is hypothesized to increase rates of soil respiration, potentially fueling further increases in global temperatures. However, despite considerable scientific attention in recent decades, the overall response of soil respiration to anticipated climatic warming remains unclear. We synthesize the largest global dataset to date of soil respiration, moisture, and temperature measurements, totaling >3,800 observations representing 27 temperature manipulation studies, spanning nine biomes and over 2 decades of warming. Our analysis reveals no significant differences in the temperature sensitivity of soil respiration between control and warmed plots in all biomes, with the exception of deserts and boreal forests. Thus, our data provide limited evidence of acclimation of soil respiration to experimental warming in several major biome types, contrary to the results from multiple single-site studies. Moreover, across all nondesert biomes, respiration rates with and without experimental warming follow a Gaussian response, increasing with soil temperature up to a threshold of ∼25 °C, above which respiration rates decrease with further increases in temperature. This consistent decrease in temperature sensitivity at higher temperatures demonstrates that rising global temperatures may result in regionally variable responses in soil respiration, with colder climates being considerably more responsive to increased ambient temperatures compared with warmer regions. Our analysis adds a unique cross-biome perspective on the temperature response of soil respiration, information critical to improving our mechanistic understanding of how soil carbon dynamics change with climatic warming.

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.

Leaf day respiration: low CO2 flux but high significance for metabolism and carbon balance.

Contents 986 I. 987 II. 987 III. 988 IV. 991 V. 992 VI. 995 VII. 997 VIII. 998 References 998 SUMMARY: It has been 75 yr since leaf respiratory metabolism in the light (day respiration) was identified as a low-flux metabolic pathway that accompanies photosynthesis. In principle, it provides carbon backbones for nitrogen assimilation and evolves CO2 and thus impacts on plant carbon and nitrogen balances. However, for a long time, uncertainties have remained as to whether techniques used to measure day respiratory efflux were valid and whether day respiration responded to environmental gaseous conditions. In the past few years, significant advances have been made using carbon isotopes, 'omics' analyses and surveys of respiration rates in mesocosms or ecosystems. There is substantial evidence that day respiration should be viewed as a highly dynamic metabolic pathway that interacts with photosynthesis and photorespiration and responds to atmospheric CO2 mole fraction. The view of leaf day respiration as a constant and/or negligible parameter of net carbon exchange is now outdated and it should now be regarded as a central actor of plant carbon-use efficiency.

Chlorophyll fluorescence tracks seasonal variations of photosynthesis from leaf to canopy in a temperate forest.

Accurate estimation of terrestrial gross primary productivity (GPP) remains a challenge despite its importance in the global carbon cycle. Chlorophyll fluorescence (ChlF) has been recently adopted to understand photosynthesis and its response to the environment, particularly with remote sensing data. However, it remains unclear how ChlF and photosynthesis are linked at different spatial scales across the growing season. We examined seasonal relationships between ChlF and photosynthesis at the leaf, canopy, and ecosystem scales and explored how leaf-level ChlF was linked with canopy-scale solar-induced chlorophyll fluorescence (SIF) in a temperate deciduous forest at Harvard Forest, Massachusetts, USA. Our results show that ChlF captured the seasonal variations of photosynthesis with significant linear relationships between ChlF and photosynthesis across the growing season over different spatial scales (R2  = 0.73, 0.77, and 0.86 at leaf, canopy, and satellite scales, respectively; P < 0.0001). We developed a model to estimate GPP from the tower-based measurement of SIF and leaf-level ChlF parameters. The estimation of GPP from this model agreed well with flux tower observations of GPP (R2  = 0.68; P < 0.0001), demonstrating the potential of SIF for modeling GPP. At the leaf scale, we found that leaf Fq '/Fm ', the fraction of absorbed photons that are used for photochemistry for a light-adapted measurement from a pulse amplitude modulation fluorometer, was the best leaf fluorescence parameter to correlate with canopy SIF yield (SIF/APAR, R2  = 0.79; P < 0.0001). We also found that canopy SIF and SIF-derived GPP (GPPSIF ) were strongly correlated to leaf-level biochemistry and canopy structure, including chlorophyll content (R2  = 0.65 for canopy GPPSIF and chlorophyll content; P < 0.0001), leaf area index (LAI) (R2  = 0.35 for canopy GPPSIF and LAI; P < 0.0001), and normalized difference vegetation index (NDVI) (R2  = 0.36 for canopy GPPSIF and NDVI; P < 0.0001). Our results suggest that ChlF can be a powerful tool to track photosynthetic rates at leaf, canopy, and ecosystem scales.

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.

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).

Evolutionary change in continuous reaction norms.

Understanding the evolution of reaction norms remains a major challenge in ecology and evolution. Investigating evolutionary divergence in reaction norm shapes between populations and closely related species is one approach to providing insights. Here we use a meta-analytic approach to compare divergence in reaction norms of closely related species or populations of animals and plants across types of traits and environments. We quantified mean-standardized differences in overall trait means (Offset) and reaction norm shape (including both Slope and Curvature). These analyses revealed that differences in shape (Slope and Curvature together) were generally greater than differences in Offset. Additionally, differences in Curvature were generally greater than differences in Slope. The type of taxon contrast (species vs. population), trait, organism, and the type and novelty of environments all contributed to the best-fitting models, especially for Offset, Curvature, and the total differences (Total) between reaction norms. Congeneric species had greater differences in reaction norms than populations, and novel environmental conditions increased the differences in reaction norms between populations or species. These results show that evolutionary divergence of curvature is common and should be considered an important aspect of plasticity, together with slope. Biological details about traits and environments, including cryptic variation expressed in novel environmental conditions, may be critical to understanding how reaction norms evolve in novel and rapidly changing environments.

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.

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.

Environmental controls on light inhibition of respiration and leaf and canopy daytime carbon exchange in a temperate deciduous forest.

Uncertainty in the estimation of daytime ecosystem carbon cycling due to the light inhibition of leaf respiration and photorespiration, and how these small fluxes vary through the growing season in the field, remains a confounding element in calculations of gross primary productivity and ecosystem respiration. Our study focuses on how phenology, short-term temperature changes and canopy position influence leaf-level carbon exchange in Quercus rubra L. (red oak) at Harvard Forest in central Massachusetts, USA. Using leaf measurements and eddy covariance, we also quantify the effect of light inhibition on estimates of daytime respiration at leaf and ecosystem scales. Measured rates of leaf respiration in the light and dark were highest in the early growing season and declined in response to 10-day prior air temperatures (P < 0.01), evidence of within-season thermal acclimation. Leaf respiration was significantly inhibited by light (27.1 ± 2.82% inhibited across all measurements), and this inhibition varied with the month of measurement; greater inhibition was observed in mid-summer leaves compared with early- and late-season leaves. Increases in measurement temperature led to higher rates of respiration and photorespiration, though with a less pronounced positive effect on photosynthesis; as a result, carbon-use efficiency declined with increasing leaf temperature. Over the growing season when we account for seasonally variable light inhibition and basal respiration rates, our modeling approaches found a cumulative 12.9% reduction of leaf-level respiration and a 12.8% reduction of canopy leaf respiration, resulting in a 3.7% decrease in total ecosystem respiration compared with estimates that do not account for light inhibition in leaves. Our study sheds light on the environmental controls of the light inhibition of daytime leaf respiration and how integrating this phenomenon and other small fluxes can reduce uncertainty in current and future projections of terrestrial carbon cycling.

Temperature response of respiration and respiratory quotients of 16 co-occurring temperate tree species.

The forests of the northeastern US are globally, one of the fastest growing terrestrial carbon sinks due to historical declines in large-scale agriculture, timber harvesting and fire disturbance. However, shifting range distributions of tree species with warming air temperatures are altering forest community composition and carbon dynamics. Here, we focus on respiration, a physiological process that is strongly temperature and species dependent. We specifically examined the response of respiration (R; CO2 release) to temperature in 10 broadleaved and six conifer species, as well as the respiratory quotient (RQ; ratio of CO2 released to O2 consumed) of nine broadleaved species that co-occur in the Hudson Highlands Region of New York, USA. The relationships between these physiological measurements and associated leaf traits were also explored. The rates of respiration at 20 °C were 71% higher in northern-ranged broadleaved species when compared with both central- and southern-ranged species. In contrast, the rates of respiration at 20 °C in northern-ranged conifers were 12% lower than in central-ranged conifers. The RQ of broadleaved species increased by 14% as temperatures increased from 15 °C to 35 °C. When RQ values were pooled across temperature, northern-ranged broadleaved species had 12% and 9% lower RQ values than central, and southern-ranged species, respectively, suggesting a reliance on alternative (non-carbohydrate) substrates to fulfill respiratory demands. A Pearson correlation analysis of leaf traits and respiration revealed strong correlations between leaf nitrogen, leaf mass area and R for both broadleaved and conifer species. Our results elucidate leaf trait relationships with tree physiology and reveal the various form and function strategies for species from differing range distributions. Compounded with predicted range distribution shifts and species replacement, this may reduce the carbon storage potential of northeast forests.

A gradient of nutrient enrichment reveals nonlinear impacts of fertilization on Arctic plant diversity and ecosystem function.

Rapid environmental change at high latitudes is predicted to greatly alter the diversity, structure, and function of plant communities, resulting in changes in the pools and fluxes of nutrients. In Arctic tundra, increased nitrogen (N) and phosphorus (P) availability accompanying warming is known to impact plant diversity and ecosystem function; however, to date, most studies examining Arctic nutrient enrichment focus on the impact of relatively large (>25x estimated naturally occurring N enrichment) doses of nutrients on plant community composition and net primary productivity. To understand the impacts of Arctic nutrient enrichment, we examined plant community composition and the capacity for ecosystem function (net ecosystem exchange, ecosystem respiration, and gross primary production) across a gradient of experimental N and P addition expected to more closely approximate warming-induced fertilization. In addition, we compared our measured ecosystem CO 2 flux data to a widely used Arctic ecosystem exchange model to investigate the ability to predict the capacity for CO 2 exchange with nutrient addition. We observed declines in abundance-weighted plant diversity at low levels of nutrient enrichment, but species richness and the capacity for ecosystem carbon uptake did not change until the highest level of fertilization. When we compared our measured data to the model, we found that the model explained roughly 30%-50% of the variance in the observed data, depending on the flux variable, and the relationship weakened at high levels of enrichment. Our results suggest that while a relatively small amount of nutrient enrichment impacts plant diversity, only relatively large levels of fertilization-over an order of magnitude or more than warming-induced rates-significantly alter the capacity for tundra CO 2 exchange. Overall, our findings highlight the value of measuring and modeling the impacts of a nutrient enrichment gradient, as warming-related nutrient availability may impact ecosystems differently than single-level fertilization experiments.

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.

Seasonality of foliar respiration in two dominant plant species from the Arctic tundra: response to long-term warming and short-term temperature variability.

Direct measurements of foliar carbon exchange through the growing season in Arctic species are limited, despite the need for accurate estimates of photosynthesis and respiration to characterise carbon cycling in the tundra. We examined seasonal variation in foliar photosynthesis and respiration (measured at 20°C) in two field-grown tundra species, Betula nana L. and Eriophorum vaginatum L., under ambient and long-term warming (LTW) conditions (+5°C), and the relationship of these fluxes to intraseasonal temperature variability. Species and seasonal timing drove most of the variation in photosynthetic parameters (e.g. gross photosynthesis (Agross)), respiration in the dark (Rdark) and light (Rlight), and foliar nitrogen concentration. LTW did not consistently influence fluxes through the season but reduced respiration in both species. Alongside the flatter respiratory response to measurement temperature in LTW leaves, this provided evidence of thermal acclimation. The inhibition of respiration by light increased by ~40%, with Rlight : Rdark values of ~0.8 at leaf out decreasing to ~0.4 after 8 weeks. Though LTW had no effect on inhibition, the cross-taxa seasonal decline in Rlight : Rdark greatly reduced respiratory carbon loss. Values of Rlight : Agross decreased from ~0.3 in both species to ~0.15 (B. nana) and ~0.05 (E. vaginatum), driven by decreases in respiratory rates, as photosynthetic rates remained stable. The influence of short-term temperature variability did not exhibit predictive trends for leaf gas exchange at a common temperature. These results underscore the influence of temperature on foliar carbon cycling, and the importance of respiration in controlling seasonal carbon exchange.