Heatwave breaks down the linearity between sun-induced fluorescence and gross primary production.

Sun-induced fluorescence in the far-red region (SIF) is increasingly used as a remote and proximal-sensing tool capable of tracking vegetation gross primary production (GPP). However, the use of SIF to probe changes in GPP is challenged during extreme climatic events, such as heatwaves. Here, we examined how the 2018 European heatwave (HW) affected the GPP-SIF relationship in evergreen broadleaved trees with a relatively invariant canopy structure. To do so, we combined canopy-scale SIF measurements, GPP estimated from an eddy covariance tower, and active pulse amplitude modulation fluorescence. The HW caused an inversion of the photosynthesis-fluorescence relationship at both the canopy and leaf scales. The highly nonlinear relationship was strongly shaped by nonphotochemical quenching (NPQ), that is, a dissipation mechanism to protect from the adverse effects of high light intensity. During the extreme heat stress, plants experienced a saturation of NPQ, causing a change in the allocation of energy dissipation pathways towards SIF. Our results show the complex modulation of the NPQ-SIF-GPP relationship at an extreme level of heat stress, which is not completely represented in state-of-the-art coupled radiative transfer and photosynthesis models.

Multi-sensor spectral synergies for crop stress detection and monitoring in the optical domain: A review.

Remote detection and monitoring of the vegetation responses to stress became relevant for sustainable agriculture. Ongoing developments in optical remote sensing technologies have provided tools to increase our understanding of stress-related physiological processes. Therefore, this study aimed to provide an overview of the main spectral technologies and retrieval approaches for detecting crop stress in agriculture. Firstly, we present integrated views on: i) biotic and abiotic stress factors, the phases of stress, and respective plant responses, and ii) the affected traits, appropriate spectral domains and corresponding methods for measuring traits remotely. Secondly, representative results of a systematic literature analysis are highlighted, identifying the current status and possible future trends in stress detection and monitoring. Distinct plant responses occurring under shortterm, medium-term or severe chronic stress exposure can be captured with remote sensing due to specific light interaction processes, such as absorption and scattering manifested in the reflected radiance, i.e. visible (VIS), near infrared (NIR), shortwave infrared, and emitted radiance, i.e. solar-induced fluorescence and thermal infrared (TIR). From the analysis of 96 research papers, the following trends can be observed: increasing usage of satellite and unmanned aerial vehicle data in parallel with a shift in methods from simpler parametric approaches towards more advanced physically-based and hybrid models. Most study designs were largely driven by sensor availability and practical economic reasons, leading to the common usage of VIS-NIR-TIR sensor combinations. The majority of reviewed studies compared stress proxies calculated from single-source sensor domains rather than using data in a synergistic way. We identified new ways forward as guidance for improved synergistic usage of spectral domains for stress detection: (1) combined acquisition of data from multiple sensors for analysing multiple stress responses simultaneously (holistic view); (2) simultaneous retrieval of plant traits combining multi-domain radiative transfer models and machine learning methods; (3) assimilation of estimated plant traits from distinct spectral domains into integrated crop growth models. As a future outlook, we recommend combining multiple remote sensing data streams into crop model assimilation schemes to build up Digital Twins of agroecosystems, which may provide the most efficient way to detect the diversity of environmental and biotic stresses and thus enable respective management decisions.

Hybrid retrieval of crop traits from multi-temporal PRISMA hyperspectral imagery.

The recently launched and upcoming hyperspectral satellite missions, featuring contiguous visible-to-shortwave infrared spectral information, are opening unprecedented opportunities for the retrieval of a broad set of vegetation traits with enhanced accuracy through novel retrieval schemes. In this framework, we exploited hyperspectral data cubes collected by the new-generation PRecursore IperSpettrale della Missione Applicativa (PRISMA) satellite of the Italian Space Agency to develop and test a hybrid retrieval workflow for crop trait mapping. Crop traits were mapped over an agricultural area in north-east Italy (Jolanda di Savoia, FE) using PRISMA images collected during the 2020 and 2021 vegetative seasons. Leaf chlorophyll content, leaf nitrogen content, leaf water content and the corresponding canopy level traits scaled through leaf area index were estimated using a hybrid retrieval scheme based on PROSAIL-PRO radiative transfer simulations coupled with a Gaussian processes regression algorithm. Active learning algorithms were used to optimise the initial set of simulated data by extracting only the most informative samples. The accuracy of the proposed retrieval scheme was evaluated against a broad ground dataset collected in 2020 in correspondence of three PRISMA overpasses. The results obtained were positive for all the investigated variables. At the leaf level, the highest accuracy was obtained for leaf nitrogen content (LNC: r2=0.87, nRMSE=7.5%), while slightly worse results were achieved for leaf chlorophyll content (LCC: r2=0.67, nRMSE=11.7%) and leaf water content (LWC: r2=0.63, nRMSE=17.1%). At the canopy level, a significantly higher accuracy was observed for nitrogen content (CNC: r2=0.92, nRMSE=5.5%) and chlorophyll content (CCC: r2=0.82, nRMSE=10.2%), whereas comparable results were obtained for water content (CWC: r2=0.61, nRMSE=16%). The developed models were additionally tested against an independent dataset collected in 2021 to evaluate their robustness and exportability. The results obtained (i. e., LCC: r2=0.62, nRMSE=27.9%; LNC: r2=0.35, nRMSE=28.4%; LWC: r2=0.74, nRMSE=20.4%; LAI: r2=0.84, nRMSE=14.5%; CCC: r2=0.79, nRMSE=18.5%; CNC: r2=0.62, nRMSE=23.7%; CWC: r2=0.92, nRMSE=16.6%) evidence the transferability of the hybrid approach optimised through active learning for most of the investigated traits. The developed models were then used to map the spatial and temporal variability of the crop traits from the PRISMA images. The high accuracy and consistency of the results demonstrates the potential of spaceborne imaging spectroscopy for crop monitoring, paving the path towards routine retrievals of multiple crop traits over large areas that could drive more effective and sustainable agricultural practices worldwide.

Dynamics of sun-induced chlorophyll fluorescence and reflectance to detect stress-induced variations in canopy photosynthesis.

Passive measurement of sun-induced chlorophyll fluorescence (F) represents the most promising tool to quantify changes in photosynthetic functioning on a large scale. However, the complex relationship between this signal and other photosynthesis-related processes restricts its interpretation under stress conditions. To address this issue, we conducted a field campaign by combining daily airborne and ground-based measurements of F (normalized to photosynthetically active radiation), reflectance and surface temperature and related the observed changes to stress-induced variations in photosynthesis. A lawn carpet was sprayed with different doses of the herbicide Dicuran. Canopy-level measurements of gross primary productivity indicated dosage-dependent inhibition of photosynthesis by the herbicide. Dosage-dependent changes in normalized F were also detected. After spraying, we first observed a rapid increase in normalized F and in the Photochemical Reflectance Index, possibly due to the blockage of electron transport by Dicuran and the resultant impairment of xanthophyll-mediated non-photochemical quenching. This initial increase was followed by a gradual decrease in both signals, which coincided with a decline in pigment-related reflectance indices. In parallel, we also detected a canopy temperature increase after the treatment. These results demonstrate the potential of using F coupled with relevant reflectance indices to estimate stress-induced changes in canopy photosynthesis.

Exploring the spatial relationship between airborne-derived red and far-red sun-induced fluorescence and process-based GPP estimates in a forest ecosystem.

Terrestrial gross primary productivity (GPP) plays an essential role in the global carbon cycle, but the quantification of the spatial and temporal variations in photosynthesis is still largely uncertain. Our work aimed to investigate the potential of remote sensing to provide new insights into plant photosynthesis at a fine spatial resolution. This goal was achieved by exploiting high-resolution images acquired with the FLuorescence EXplorer (FLEX) airborne demonstrator HyPlant. The sensor was flown over a mixed forest, and the images collected were elaborated to obtain two independent indicators of plant photosynthesis. First, maps of sun-induced chlorophyll fluorescence (F), a novel indicator of plant photosynthetic activity, were successfully obtained at both the red and far-red peaks (r2 = 0.89 and p < 0.01, r2 = 0.77 and p < 0.01, respectively, compared to top-of-canopy ground-based measurements acquired synchronously with the overflight) over the forested study area. Second, maps of GPP and absorbed photosynthetically active radiation (APAR) were derived using a customised version of the coupled biophysical model Breathing Earth System Simulator (BESS). The model was driven with airborne-derived maps of key forest traits (i.e., leaf chlorophyll content (LCC) and leaf area index (LAI)) and meteorological data providing a high-resolution snapshot of the variables of interest across the study site. The LCC and LAI were accurately estimated (RMSE = 5.66 µg cm-2 and RMSE = 0.51 m2m-2, respectively) through an optimised Look-Up-Table-based inversion of the PROSPECT-4-INFORM radiative transfer model, ensuring the accurate representation of the spatial variation of these determinants of the ecosystem's functionality. The spatial relationships between the measured F and modelled BESS outputs were then analysed to interpret the variability of ecosystem functioning at a regional scale. The results showed that far-red F is significantly correlated with the GPP (r2 = 0.46, p < 0.001) and APAR (r2 = 0.43, p < 0.001) in the spatial domain and that this relationship is nonlinear. Conversely, no statistically significant relationships were found between the red F and the GPP or APAR (p > 0.05). The spatial relationships found at high resolution provide valuable insight into the critical role of spatial heterogeneity in controlling the relationship between the far-red F and the GPP, indicating the need to consider this heterogeneity at a coarser resolution.

Leaf and canopy photosynthesis of a chlorophyll deficient soybean mutant.

The photosynthetic, optical, and morphological characteristics of a chlorophyll-deficient (Chl-deficient) "yellow" soybean mutant (MinnGold) were examined in comparison with 2 green varieties (MN0095 and Eiko). Despite the large difference in Chl content, similar leaf photosynthesis rates were maintained in the Chl-deficient mutant by offsetting the reduced absorption of red photons by a small increase in photochemical efficiency and lower non-photochemical quenching. When grown in the field, at full canopy cover, the mutants reflected a significantly larger proportion of incoming shortwave radiation, but the total canopy light absorption was only slightly reduced, most likely due to a deeper penetration of light into the canopy space. As a consequence, canopy-scale gross primary production and ecosystem respiration were comparable between the Chl-deficient mutant and the green variety. However, total biomass production was lower in the mutant, which indicates that processes other than steady state photosynthesis caused a reduction in biomass accumulation over time. Analysis of non-photochemical quenching relaxation and gas exchange in Chl-deficient and green leaves after transitions from high to low light conditions suggested that dynamic photosynthesis might be responsible for the reduced biomass production in the Chl-deficient mutant under field conditions.

Variability of sun-induced chlorophyll fluorescence according to stand age-related processes in a managed loblolly pine forest.

Leaf fluorescence can be used to track plant development and stress, and is considered the most direct measurement of photosynthetic activity available from remote sensing techniques. Red and far-red sun-induced chlorophyll fluorescence (SIF) maps were generated from high spatial resolution images collected with the HyPlant airborne spectrometer over even-aged loblolly pine plantations in North Carolina (United States). Canopy fluorescence yield (i.e., the fluorescence flux normalized by the light absorbed) in the red and far-red peaks was computed. This quantifies the fluorescence emission efficiencies that are more directly linked to canopy function compared to SIF radiances. Fluorescence fluxes and yields were investigated in relation to tree age to infer new insights on the potential of those measurements in better describing ecosystem processes. The results showed that red fluorescence yield varies with stand age. Young stands exhibited a nearly twofold higher red fluorescence yield than mature forest plantations, while the far-red fluorescence yield remained constant. We interpreted this finding in a context of photosynthetic stomatal limitation in aging loblolly pine stands. Current and future satellite missions provide global datasets of SIF at coarse spatial resolution, resulting in intrapixel mixture effects, which could be a confounding factor for fluorescence signal interpretation. To mitigate this effect, we propose a surrogate of the fluorescence yield, namely the Canopy Cover Fluorescence Index (CCFI) that accounts for the spatial variability in canopy structure by exploiting the vegetation fractional cover. It was found that spatial aggregation tended to mask the effective relationships, while the CCFI was still able to maintain this link. This study is a first attempt in interpreting the fluorescence variability in aging forest stands and it may open new perspectives in understanding long-term forest dynamics in response to future climatic conditions from remote sensing of SIF.

Plant functional traits and canopy structure control the relationship between photosynthetic CO2 uptake and far-red sun-induced fluorescence in a Mediterranean grassland under different nutrient availability.

Sun-induced fluorescence (SIF) in the far-red region provides a new noninvasive measurement approach that has the potential to quantify dynamic changes in light-use efficiency and gross primary production (GPP). However, the mechanistic link between GPP and SIF is not completely understood. We analyzed the structural and functional factors controlling the emission of SIF at 760 nm (F760 ) in a Mediterranean grassland manipulated with nutrient addition of nitrogen (N), phosphorous (P) or nitrogen-phosphorous (NP). Using the soil-canopy observation of photosynthesis and energy (SCOPE) model, we investigated how nutrient-induced changes in canopy structure (i.e. changes in plant forms abundance that influence leaf inclination distribution function, LIDF) and functional traits (e.g. N content in dry mass of leaves, N%, Chlorophyll a+b concentration (Cab) and maximum carboxylation capacity (Vcmax )) affected the observed linear relationship between F760 and GPP. We conclude that the addition of nutrients imposed a change in the abundance of different plant forms and biochemistry of the canopy that controls F760 . Changes in canopy structure mainly control the GPP-F760 relationship, with a secondary effect of Cab and Vcmax . In order to exploit F760 data to model GPP at the global/regional scale, canopy structural variability, biodiversity and functional traits are important factors that have to be considered.

Ground-based optical measurements at European flux sites: a review of methods, instruments and current controversies.

This paper reviews the currently available optical sensors, their limitations and opportunities for deployment at Eddy Covariance (EC) sites in Europe. This review is based on the results obtained from an online survey designed and disseminated by the Co-cooperation in Science and Technology (COST) Action ESO903-"Spectral Sampling Tools for Vegetation Biophysical Parameters and Flux Measurements in Europe" that provided a complete view on spectral sampling activities carried out within the different research teams in European countries. The results have highlighted that a wide variety of optical sensors are in use at flux sites across Europe, and responses further demonstrated that users were not always fully aware of the key issues underpinning repeatability and the reproducibility of their spectral measurements. The key findings of this survey point towards the need for greater awareness of the need for standardisation and development of a common protocol of optical sampling at the European EC sites.

UAV RGB, thermal infrared and multispectral imagery used to investigate the control of terrain on the spatial distribution of dryland biocrust.

Biocrusts (topsoil communities formed by mosses, lichens, bacteria, fungi, algae, and cyanobacteria) are a key biotic component of dryland ecosystems. Whilst climate patterns control the distribution of biocrusts in drylands worldwide, terrain and soil attributes can influence biocrust distribution at landscape scale. Multi-source unmanned aerial vehicle (UAV) imagery was used to map and study biocrust ecology in a typical dryland ecosystem in central Spain. Red, green and blue (RGB) imagery was processed using structure-from-motion techniques to map terrain attributes related to microclimate and terrain stability. Multispectral imagery was used to produce accurate maps (accuracy > 80%) of dryland ecosystem components (vegetation, bare soil and biocrust composition). Finally, thermal infrared (TIR) and multispectral imagery was used to calculate the apparent thermal inertia (ATI) of soil and to evaluate how ATI was related to soil moisture (r 2 = 0.83). The relationship between soil properties and UAV-derived variables was first evaluated at the field plot level. Then, the maps obtained were used to explore the relationship between biocrusts and terrain attributes at ecosystem level through a redundancy analysis. The most significant variables that explain biocrust distribution are: ATI (34.4% of variance, F = 130.75; p < 0.001), Elevation (25.8%, F = 97.6; p < 0.001), and potential solar incoming radiation (PSIR) (52.9%, F = 200.1; p < 0.001). Differences were found between areas dominated by lichens and mosses. Lichen-dominated biocrusts were associated with areas with high slopes and low values of ATI, with soil characterized by a higher amount of soluble salts, and lower amount of organic carbon, total phosphorus (Ptot) and total nitrogen (Ntot). Biocrust-forming mosses dominated lower and moister areas, characterized by gentler slopes and higher values of ATI with soils with higher contents of organic carbon, Ptot and Ntot. This study shows the potential to use UAVs to improve our understanding of drylands and to evaluate the control that the terrain has on biocrust distribution.

rasterdiv-An Information Theory tailored R package for measuring ecosystem heterogeneity from space: To the origin and back.

Ecosystem heterogeneity has been widely recognized as a key ecological indicator of several ecological functions, diversity patterns and change, metapopulation dynamics, population connectivity or gene flow.In this paper, we present a new R package-rasterdiv-to calculate heterogeneity indices based on remotely sensed data. We also provide an ecological application at the landscape scale and demonstrate its power in revealing potentially hidden heterogeneity patterns.The rasterdiv package allows calculating multiple indices, robustly rooted in Information Theory, and based on reproducible open-source algorithms.

Characterization of fine resolution field spectrometers using solar Fraunhofer lines and atmospheric absorption features.

The accurate spectral characterization of high-resolution spectrometers is required for correctly computing, interpreting, and comparing radiance and reflectance spectra acquired at different times or by different instruments. In this paper, we describe an algorithm for the spectral characterization of field spectrometer data using sharp atmospheric or solar absorption features present in the measured data. The algorithm retrieves systematic shifts in channel position and actual full width at half-maximum (FWHM) of the instrument by comparing data acquired during standard field spectroscopy measurement operations with a reference irradiance spectrum modeled with the MODTRAN4 radiative transfer code. Measurements from four different field spectrometers with spectral resolutions ranging from 0.05 to 3.5nm are processed and the results validated against laboratory calibration. An accurate retrieval of channel position and FWHM has been achieved, with an average error smaller than the instrument spectral sampling interval.

Assessing Steady-state Fluorescence and PRI from Hyperspectral Proximal Sensing as Early Indicators of Plant Stress: The Case of Ozone Exposure.

High spectral resolution spectrometers were used to detect optical signals ofongoing plant stress in potted white clover canopies subjected to ozone fumigation. Thecase of ozone stress is used in this manuscript as a paradigm of oxidative stress. Steadystatefluorescence (Fs) and the Photochemical Reflectance Index (PRI) were investigatedas advanced hyperspectral remote sensing techniques able to sense variations in the excessenergy dissipation pathways occurring when photosynthesis declines in plants exposed to astress agent. Fs and PRI were monitored in control and ozone fumigated canopies during a21-day experiment together with the traditional Normalized Difference Vegetation Index(NDVI) and physiological measurements commonly employed by physiologists to describestress development (i.e. net CO2 assimilation, active fluorimetry, chlorophyll concentrationand visible injuries). It is shown that remote detection of an ongoing stress through Fs andPRI can be achieved in an early phase, characterized by the decline of photosynthesis. Onthe contrary, NDVI was able to detect the stress only when damage occurred. These resultsopen up new possibilities for assessment of plant stress by means of hyperspectral remotesensing.

Assessment of oak forest condition based on leaf biochemical variables and chlorophyll fluorescence.

Pedunculate oak forests (Quercus robur L.) in the Ticino Regional Park, Italy, are declining as a result of insect attacks, summer droughts and air pollution. The assessment and monitoring of forest condition can provide a basis for managing and conserving forest ecosystems and thereby avoid loss of valuable natural resources. Currently, most forest assessments are limited to ground-based visual evaluations that are local and subjective. It is therefore difficult to compare data collected by different crews or to define reliable trends over years. We examined vegetation variables that can be quantitatively estimated by remote observations and, thus, are suitable for objective monitoring over extended forested areas. We found that total chlorophyll (Chl) concentration is the most suitable variable for assessing pedunculate oak decline. It is highly correlated with visual assessments of discoloration. Furthermore, Chl concentration can be accurately estimated from leaf optical properties, making it feasible to map Chl concentration at the canopy level from satellite and airborne remote observations.

Early drought stress detection in cereals: simplex volume maximisation for hyperspectral image analysis.

Early water stress recognition is of great relevance in precision plant breeding and production. Hyperspectral imaging sensors can be a valuable tool for early stress detection with high spatio-temporal resolution. They gather large, high dimensional data cubes posing a significant challenge to data analysis. Classical supervised learning algorithms often fail in applied plant sciences due to their need of labelled datasets, which are difficult to obtain. Therefore, new approaches for unsupervised learning of relevant patterns are needed. We apply for the first time a recent matrix factorisation technique, simplex volume maximisation (SiVM), to hyperspectral data. It is an unsupervised classification approach, optimised for fast computation of massive datasets. It allows calculation of how similar each spectrum is to observed typical spectra. This provides the means to express how likely it is that one plant is suffering from stress. The method was tested for drought stress, applied to potted barley plants in a controlled rain-out shelter experiment and to agricultural corn plots subjected to a two factorial field setup altering water and nutrient availability. Both experiments were conducted on the canopy level. SiVM was significantly better than using a combination of established vegetation indices. In the corn plots, SiVM clearly separated the different treatments, even though the effects on leaf and canopy traits were subtle.

Using optical remote sensing techniques to track the development of ozone-induced stress.

In this paper, a literature review about optical remote sensing (RS) of O(3) stress is presented. Studies on O(3)-induced effects on vegetation reflectance have been conducted since late '70s based on the analysis of optical RS data. Literature review reveals that traditional RS techniques were able to detect changes in leaf and canopy reflectance related to O(3)-induced stress when visible symptoms already occurred. Only recently, advanced RS techniques using hyperspectral sensors, demonstrated the feasibility of detecting the stress in its early phase by monitoring excess energy dissipation pathways such as chlorophyll fluorescence and non-photochemical quenching (NPQ). Steady-state fluorescence (Fs), measured by exploiting the Fraunhofer line depth principle and NPQ related xanthophyll-cycle, estimated through the photochemical reflectance index (PRI) responded to O(3) fumigation before visible symptoms occurred. This opens up new possibilities for the early detection of vegetation O(3) stress by means of hyperspectral RS.

A flux-based assessment of the effects of ozone on foliar injury, photosynthesis, and yield of bean (Phaseolus vulgaris L. cv. Borlotto Nano Lingua di Fuoco) in open-top chambers.

Stomatal ozone uptake, determined with the Jarvis' approach, was related to photosynthetic efficiency assessed by chlorophyll fluorescence and reflectance measurements in open-top chamber experiments on Phaseolus vulgaris. The effects of O(3) exposure were also evaluated in terms of visible and microscopical leaf injury and plant productivity. Results showed that microscopical leaf symptoms, assessed as cell death and H(2)O(2) accumulation, preceded by 3-4 days the appearance of visible symptoms. An effective dose of ozone stomatal flux for visible leaf damages was found around 1.33 mmol O(3) m(-2). Significant linear dose-response relationships were obtained between accumulated fluxes and optical indices (PRI, NDI, DeltaF/F'(m)). The negative effects on photosynthesis reduced plant productivity, affecting the number of pods and seeds, but not seed weight. These results, besides contributing to the development of a flux-based ozone risk assessment for crops in Europe, highlight the potentiality of reflectance measurements for the early detection of ozone stress.