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

Author Posting. © The Author(s), 2016. This is the author's version of the work. It is posted here by permission of John Wiley & Sons for personal use, not for redistribution. The definitive version was published in Global Change Biology 23 (2017): 2874-2886, doi: 10.1111/gcb.13590.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.This research was supported by U.S. Department of Energy Office of Biological and Environmental Research Grant DE-SC0006951, National Science Foundation Grants DBI-959333 and AGS-1005663, and the University of Chicago and the MBL Lillie Research Innovation Award to J. Tang, National Science Foundation of China Grants (41671421) to Y. Zhang, and China Scholarship Council (CSC) to H. Yang.2017-12-1

Evolutionary change in continuous reaction norms

Abstract 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 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

Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity

Phenotypic plasticity is ubiquitous and generally regarded as a key mechanism for enabling organisms to survive in the face of environmental change. Because no organism is infinitely or ideally plastic, theory suggests that there must be limits (for example, the lack of ability to produce an optimal trait) to the evolution of phenotypic plasticity, or that plasticity may have inherent significant costs. Yet numerous experimental studies have not detected widespread costs. Explicitly differentiating plasticity costs from phenotype costs, we re-evaluate fundamental questions of the limits to the evolution of plasticity and of generalists vs specialists. We advocate for the view that relaxed selection and variable selection intensities are likely more important constraints to the evolution of plasticity than the costs of plasticity. Some forms of plasticity, such as learning, may be inherently costly. In addition, we examine opportunities to offset costs of phenotypes through ontogeny, amelioration of phenotypic costs across environments, and the condition-dependent hypothesis. We propose avenues of further inquiry in the limits of plasticity using new and classic methods of ecological parameterization, phylogenetics and omics in the context of answering questions on the constraints of plasticity. Given plasticity's key role in coping with environmental change, approaches spanning the spectrum from applied to basic will greatly enrich our understanding of the evolution of plasticity and resolve our understanding of limits

A reporting format for leaf-level gas exchange data and metadata

Leaf-level gas exchange data support the mechanistic understanding of plant fluxes of carbon and water. These fluxes inform our understanding of ecosystem function, are an important constraint on parameterization of terrestrial biosphere models, are necessary to understand the response of plants to global environmental change, and are integral to efforts to improve crop production. Collection of these data using gas analyzers can be both technically challenging and time consuming, and individual studies generally focus on a small range of species, restricted time periods, or limited geographic regions. The high value of these data is exemplified by the many publications that reuse and synthesize gas exchange data, however the lack of metadata and data reporting conventions make full and efficient use of these data difficult. Here we propose a reporting format for leaf-level gas exchange data and metadata to provide guidance to data contributors on how to store data in repositories to maximize their discoverability, facilitate their efficient reuse, and add value to individual datasets. For data users, the reporting format will better allow data repositories to optimize data search and extraction, and more readily integrate similar data into harmonized synthesis products. The reporting format specifies data table variable naming and unit conventions, as well as metadata characterizing experimental conditions and protocols. For common data types that were the focus of this initial version of the reporting format, i.e., survey measurements, dark respiration, carbon dioxide and light response curves, and parameters derived from those measurements, we took a further step of defining required additional data and metadata that would maximize the potential reuse of those data types. To aid data contributors and the development of data ingest tools by data repositories we provided a translation table comparing the outputs of common gas exchange instruments. Extensive consultation with data collectors, data users, instrument manufacturers, and data scientists was undertaken in order to ensure that the reporting format met community needs. The reporting format presented here is intended to form a foundation for future development that will incorporate additional data types and variables as gas exchange systems and measurement approaches advance in the future. The reporting format is published in the U.S. Department of Energy's ESS-DIVE data repository, with documentation and future development efforts being maintained in a version control system

Contrasting effects of long term versus short-term nitrogen addition on photosynthesis and respiration in the Arctic

We examined the effects of short (<1–4 years) and long-term (22 years) nitrogen (N) and/or phosphorus (P) addition on the foliar CO2 exchange parameters of the Arctic species Betula nana and Eriophorum vaginatum in northern Alaska. Measured variables included: the carboxylation efficiency of Rubisco (Vcmax), electron transport capacity (Jmax), dark respiration (Rd), chlorophyll a and b content (Chl), and total foliar N (N). For both B. nana and E. vaginatum, foliar N increased by 20–50 % as a consequence of 1–22 years of fertilisation, respectively, and for B. nana foliar N increase was consistent throughout the whole canopy. However, despite this large increase in foliar N, no significant changes in Vcmax and Jmax were observed. In contrast, Rd was significantly higher (>25 %) in both species after 22 years of N addition, but not in the shorter-term treatments. Surprisingly, Chl only increased in both species the first year of fertilisation (i.e. the first season of nutrients applied), but not in the longer-term treatments. These results imply that: (1) under current (low) N availability, these Arctic species either already optimize their photosynthetic capacity per leaf area, or are limited by other nutrients; (2) observed increases in Arctic NEE and GPP with increased nutrient availability are caused by structural changes like increased leaf area index, rather than increased foliar photosynthetic capacity and (3) short-term effects (1–4 years) of nutrient addition cannot always be extrapolated to a larger time scale, which emphasizes the importance of long-term ecological 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 (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

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