A synthesis of bias and uncertainty in sap flow methods

Flo V., Martinez-Vilalta J., Steppe K., Schuldt B., Poyatos R. (2019) A synthesis of bias and uncertainty in sap flow methods. Agricultural and Forest Meteorology. 271: 362-374.
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Doi: 10.1016/j.agrformet.2019.03.012

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Sap flow measurements with thermometric methods are widely used to measure transpiration in plants. Different method families exist depending on how they apply heat and track sapwood temperature (heat pulse, heat dissipation, heat field deformation or heat balance). These methods have been calibrated for many species, but a global assessment of their uncertainty and reliability has not yet been conducted. Here we perform a meta-analysis of 290 individual calibration experiments assembled from the literature to assess calibration performance and how this varies across methods, experimental conditions and wood properties (density and porosity types). We used different metrics to characterize mean accuracy (closeness of the measurements to the true, reference value), proportional bias (resulting from an effect of measured flow on the magnitude of the error), linearity in the relationship between measurements and reference values, and precision (reproducibility and repeatability). We found a large intra- and inter-method variability in calibration performance, with a low proportion of this variability explained by species. Calibration performance was best when using stem segments. We did not find evidence of strong effects of wood density or porosity type in calibration performance. Dissipation methods showed lower accuracy and higher proportional bias than the other methods but they showed relatively high linearity and precision. Pulse methods also showed significant proportional bias, driven by their overestimation of low flows. These results suggest that Dissipation methods may be more appropriate to assess relative sap flow (e.g., treatment effects within a study) and Pulse methods may be more suitable to quantify absolute flows. Nevertheless, all sap flow methods showed high precision, allowing potential correction of the measurements when a study-specific calibration is performed. Our understanding of how sap flow methods perform across species would be greatly improved if experimental conditions and wood properties, including changes in wood moisture, were better reported. © 2019 Elsevier B.V.

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Correction to: Below-ground hydraulic constraints during drought-induced decline in Scots pine (Annals of Forest Science, (2018), 75, 4, (100), 10.1007/s13595-018-0778-7)

Poyatos R., Aguadé D., Martínez-Vilalta J. (2019) Correction to: Below-ground hydraulic constraints during drought-induced decline in Scots pine (Annals of Forest Science, (2018), 75, 4, (100), 10.1007/s13595-018-0778-7). Annals of Forest Science. 76: 0-0.
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Doi: 10.1007/s13595-019-0825-z

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The article was published without the submitted data availability statement linking readers to a public repository. Due to publication modifications, the information appears missing in the original article. The following corrects previous version of the statement: Data availability The datasets generated and/or analysed during the current study are available in Zenodo Repository (Poyatos et al. 2018). The datasets were not peer reviewed. The original article has been corrected. © 2019, INRA and Springer-Verlag France SAS, part of Springer Nature.

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Applying the eco-hydrological equilibrium hypothesis to model root distribution in water-limited forests

Cabon A., Martínez-Vilalta J., Martínez de Aragón J., Poyatos R., De Cáceres M. (2018) Applying the eco-hydrological equilibrium hypothesis to model root distribution in water-limited forests. Ecohydrology. : 0-0.
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Doi: 10.1002/eco.2015

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Drought is a key driver of vegetation dynamics, but plant water-uptake patterns and consequent plant responses to drought are poorly understood at large spatial scales. The capacity of vegetation to use soil water depends on its root distribution (RD). However, RD is extremely variable in space and difficult to measure in the field, which hinders accurate predictions of water fluxes and vegetation dynamics. We propose a new method to estimate RD within water balance models, assuming that vegetation is at eco-hydrological equilibrium (EHE). EHE conditions imply that vegetation optimizes RD such that transpiration is maximized within the limits of bearable drought stress, characterized here by species-specific hydraulic thresholds. Optimized RD estimates were validated against RD estimates obtained by model calibration from sap flow or soil moisture from 38 forest plots in Catalonia (NE Spain). In water-limited plots, optimized RD was similar to calibrated RD, but estimates diverged with higher water availability, suggesting that the EHE may not be assumed when water is not limiting. Thereafter, we applied the optimization procedure at the regional scale, to estimate RD for the water-limited forests of Catalonia. Regional variations of optimum RD reproduced many expected patterns in response to climate, soil physical properties, forest structure, and species hydraulic traits. We conclude that RD optimization, based on the EHE hypothesis and a simple description of plant hydraulics, produces realistic estimates of RD that can be used for model parameterization and shows promise to improve our ability to forecast vegetation dynamics under increased drought. © 2018 John Wiley & Sons, Ltd.

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Below-ground hydraulic constraints during drought-induced decline in Scots pine

Poyatos R., Aguadé D., Martínez-Vilalta J. (2018) Below-ground hydraulic constraints during drought-induced decline in Scots pine. Annals of Forest Science. 75: 0-0.
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Doi: 10.1007/s13595-018-0778-7

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Key message: Below-crown hydraulic resistance, a proxy for below-ground hydraulic resistance, increased during drought in Scots pine, but larger increases were not associated to drought-induced defoliation. Accounting for variable below-ground hydraulic conductance in response to drought may be needed for accurate predictions of forest water fluxes and drought responses in xeric forests. Context: Hydraulic deterioration is an important trigger of drought-induced tree mortality. However, the role of below-ground hydraulic constraints remains largely unknown. Aims: We investigated the association between drought-induced defoliation and seasonal dynamics of below-crown hydraulic resistance (a proxy for below-ground hydraulic resistance), associated to variations in water supply and demand in a field population of Scots pine (Pinus sylvestris L.) Methods: Below-crown hydraulic resistance (rbc) of defoliated and non-defoliated pines was obtained from the relationship between maximum leaf-specific sap flow rates and maximum stem pressure difference estimated from xylem radius variations. The percent contribution of rbc to whole-tree hydraulic resistance (%rbc) was calculated by comparing stem water potential variations with the water potential difference between the leaves and the soil. Results: rbc and %rbc increased with drought in both defoliated and non-defoliated pines. However, non-defoliated trees showed larger increases in rbc between spring and summer. The difference between defoliation classes is unexplained by differences in root embolism, and it is possibly related to seasonal changes in other properties of the roots and the soil-root interface. Conclusion: Our results highlight the importance of increasing below-ground hydraulic constraints during summer drought but do not clearly link drought-induced defoliation with severe below-ground hydraulic impairment in Scots pine. © 2018, INRA and Springer-Verlag France SAS, part of Springer Nature.

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Gap-filling a spatially explicit plant trait database: Comparing imputation methods and different levels of environmental information

Poyatos R., Sus O., Badiella L., Mencuccini M., Martínez-Vilalta J. (2018) Gap-filling a spatially explicit plant trait database: Comparing imputation methods and different levels of environmental information. Biogeosciences. 15: 2601-2617.
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Doi: 10.5194/bg-15-2601-2018

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The ubiquity of missing data in plant trait databases may hinder trait-based analyses of ecological patterns and processes. Spatially explicit datasets with information on intraspecific trait variability are rare but offer great promise in improving our understanding of functional biogeography. At the same time, they offer specific challenges in terms of data imputation. Here we compare statistical imputation approaches, using varying levels of environmental information, for five plant traits (leaf biomass to sapwood area ratio, leaf nitrogen content, maximum tree height, leaf mass per area and wood density) in a spatially explicit plant trait dataset of temperate and Mediterranean tree species (Ecological and Forest Inventory of Catalonia, IEFC, dataset for Catalonia, north-east Iberian Peninsula, 31 900 km2). We simulated gaps at different missingness levels (10-80 %) in a complete trait matrix, and we used overall trait means, species means, k nearest neighbours (kNN), ordinary and regression kriging, and multivariate imputation using chained equations (MICE) to impute missing trait values. We assessed these methods in terms of their accuracy and of their ability to preserve trait distributions, multi-trait correlation structure and bivariate trait relationships. The relatively good performance of mean and species mean imputations in terms of accuracy masked a poor representation of trait distributions and multivariate trait structure. Species identity improved MICE imputations for all traits, whereas forest structure and topography improved imputations for some traits. No method performed best consistently for the five studied traits, but, considering all traits and performance metrics, MICE informed by relevant ecological variables gave the best results. However, at higher missingness (> 30 %), species mean imputations and regression kriging tended to outperform MICE for some traits. MICE informed by relevant ecological variables allowed us to fill the gaps in the IEFC incomplete dataset (5495 plots) and quantify imputation uncertainty. Resulting spatial patterns of the studied traits in Catalan forests were broadly similar when using species means, regression kriging or the best-performing MICE application, but some important discrepancies were observed at the local level. Our results highlight the need to assess imputation quality beyond just imputation accuracy and show that including environmental information in statistical imputation approaches yields more plausible imputations in spatially explicit plant trait datasets. © 2018 Author(s).

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The role of defoliation and root rot pathogen infection in driving the mode of drought-related physiological decline in Scots pine (Pinus sylvestris L.)

Aguade D., Poyatos R., Gomez M., Oliva J., Martinez-Vilalta J. (2015) The role of defoliation and root rot pathogen infection in driving the mode of drought-related physiological decline in Scots pine (Pinus sylvestris L.). Tree Physiology. 35: 229-242.
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Doi: 10.1093/treephys/tpv005

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Drought-related tree die-off episodes have been observed in all vegetated continents. Despite much research effort, however, the multiple interactions between carbon starvation, hydraulic failure and biotic agents in driving tree mortality under field conditions are still not well understood. We analysed the seasonal variability of non-structural carbohydrates (NSCs) in four organs (leaves, branches, trunk and roots), the vulnerability to embolism in roots and branches, native embolism (percentage loss of hydraulic conductivity (PLC)) in branches and the presence of root rot pathogens in defoliated and non-defoliated individuals in a declining Scots pine (Pinus sylvestris L.) population in the NE Iberian Peninsula in 2012, which included a particularly dry and warm summer. No differences were observed between defoliated and non-defoliated pines in hydraulic parameters, except for a higher vulnerability to embolism at pressures below-2 MPa in roots of defoliated pines. No differences were found between defoliation classes in branch PLC. Total NSC (TNSC, soluble sugars plus starch) values decreased during drought, particularly in leaves. Defoliation reduced TNSC levels across tree organs, especially just before (June) and during (August) drought. Root rot infection by the fungal pathogen Onnia P. Karst spp. was detected but it did not appear to be associated to tree defoliation. However, Onnia infection was associated with reduced leaf-specific hydraulic conductivity and sapwood depth, and thus contributed to hydraulic impairment, especially in defoliated pines. Infection was also associated with virtually depleted root starch reserves during and after drought in defoliated pines. Moreover, defoliated and infected trees tended to show lower basal area increment. Overall, our results show the intertwined nature of physiological mechanisms leading to drought-induced mortality and the inherent difficulty of isolating their contribution under field conditions. © The Author 2015. Published by Oxford University Press. All rights reserved.

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Comparative drought responses of Quercus ilex L. and Pinus sylvestris L. In a montane forest undergoing a vegetation shift

Aguade D., Poyatos R., Rosas T., Martinez-Vilalta J. (2015) Comparative drought responses of Quercus ilex L. and Pinus sylvestris L. In a montane forest undergoing a vegetation shift. Forests. 6: 2505-2529.
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Doi: 10.3390/f6082505

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Different functional and structural strategies to cope with water shortage exist both within and across plant communities. The current trend towards increasing drought in many regions could drive some species to their physiological limits of drought tolerance, potentially leading to mortality episodes and vegetation shifts. In this paper, we study the drought responses of Quercus ilex and Pinus sylvestris in a montane Mediterranean forest where the former species is replacing the latter in association with recent episodes of drought-induced mortality. Our aim was to compare the physiological responses to variations in soil water content (SWC) and vapor pressure deficit (VPD) of the two species when living together in a mixed stand or separately in pure stands, where the canopies of both species are completely exposed to high radiation and VPD. P. sylvestris showed typical isohydric behavior, with greater losses of stomatal conductance with declining SWC and greater reductions of stored non-structural carbohydrates during drought, consistent with carbon starvation being an important factor in the mortality of this species. On the other hand, Q. ilex trees showed a more anisohydric behavior, experiencing more negative water potentials and higher levels of xylem embolism under extreme drought, presumably putting them at higher risk of hydraulic failure. In addition, our results show relatively small changes in the physiological responses of Q. ilex in mixed vs. pure stands, suggesting that the current replacement of P. sylvestris by Q. ilex will continue. © 2015 by the authors.

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Coupling a water balance model with forest inventory data to predict drought stress: The role of forest structural changes vs. climate changes

Caceres M.D., Martinez-Vilalta J., Coll L., Llorens P., Casals P., Poyatos R., Pausas J.G., Brotons L. (2015) Coupling a water balance model with forest inventory data to predict drought stress: The role of forest structural changes vs. climate changes. Agricultural and Forest Meteorology. 213: 77-90.
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Doi: 10.1016/j.agrformet.2015.06.012

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Mechanistic water balance models can be used to predict soil moisture dynamics and drought stress in individual forest stands. Predicting current and future levels of plant drought stress is important not only at the local scale, but also at larger, landscape to regional, scales, because these are the management scales at which adaptation and mitigation strategies are implemented. To obtain reliable predictions of soil moisture and plant drought stress over large extents, water balance models need to be complemented with detailed information about the spatial variation of vegetation and soil attributes. We designed, calibrated and validated a water balance model that produces annual estimates of drought intensity and duration for all plant cohorts in a forest stand. Taking Catalonia (NE Spain) as a case study, we coupled this model with plot records from two Spanish forest inventories in which species identity, diameter and height of plant cohorts were available. Leaf area index of each plant cohort was estimated from basal area using species-specific relationships. Vertical root distribution for each species in each forest plot was estimated by determining the distribution that maximized transpiration in the model, given average climatic conditions, soil attributes and stand density. We determined recent trends (period 1980-2010) in drought stress for the main tree species in Catalonia; where forest growth and densification occurs in many areas as a result of rural abandonment and decrease of forest management. Regional increases in drought stress were detected for most tree species, although we found high variation in stress changes among individual forest plots. Moreover, predicted trends in tree drought stress were mainly due to changes in leaf area occurred between the two forest inventories rather than to climatic trends. We conclude that forest structure needs to be explicitly considered in assessments of plant drought stress patterns and trends over large geographic areas, and that forest inventories are useful sources of data provided that reasonably good estimates of soil attributes and root distribution are available. Our approach coupled with recent improvements in forest survey technologies may allow obtaining spatially continuous and precise assessments of drought stress. Further efforts are needed to calibrate drought-related demographic processes before water balance and drought stress estimates can be fully used for the accurate prediction of drought impacts. © 2015 Elsevier B.V.

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Balancing the risks of hydraulic failure and carbon starvation: A twig scale analysis in declining Scots pine

Salmon Y., Torres-Ruiz J.M., Poyatos R., Martinez-Vilalta J., Meir P., Cochard H., Mencuccini M. (2015) Balancing the risks of hydraulic failure and carbon starvation: A twig scale analysis in declining Scots pine. Plant, Cell and Environment. : 0-0.
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Doi: 10.1111/pce.12572

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Understanding physiological processes involved in drought-induced mortality is important for predicting the future of forests and for modelling the carbon and water cycles. Recent research has highlighted the variable risks of carbon starvation and hydraulic failure in drought-exposed trees. However, little is known about the specific responses of leaves and supporting twigs, despite their critical role in balancing carbon acquisition and water loss. Comparing healthy (non-defoliated) and unhealthy (defoliated) Scots pine at the same site, we measured the physiological variables involved in regulating carbon and water resources. Defoliated trees showed different responses to summer drought compared with non-defoliated trees. Defoliated trees maintained gas exchange while non-defoliated trees reduced photosynthesis and transpiration during the drought period. At the branch scale, very few differences were observed in non-structural carbohydrate concentrations between health classes. However, defoliated trees tended to have lower water potentials and smaller hydraulic safety margins. While non-defoliated trees showed a typical response to drought for an isohydric species, the physiology appears to be driven in defoliated trees by the need to maintain carbon resources in twigs. These responses put defoliated trees at higher risk of branch hydraulic failure and help explain the interaction between carbon starvation and hydraulic failure in dying trees. Understanding the physiological responses of leaves to drought is crucial since they are the site of both photosynthesis and transpiration, and hence play key roles in balancing the risks of carbon starvation and hydraulic failure. Co-occurring healthy and unhealthy Scots pines showed different responses to summer drought: while healthy trees showed a typical response to drought for an isohydric species, atypical physiology in unhealthy trees appears to be driven by the need to maintain carbohydrate availability in needles and twigs. These responses put unhealthy trees at higher risk of branch hydraulic failure and help to explain the interaction between carbon-starvation and hydraulic failure in dying trees. © 2015 John Wiley & Sons Ltd.

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A new look at water transport regulation in plants

Martinez-Vilalta J., Poyatos R., Aguade D., Retana J., Mencuccini M. (2014) A new look at water transport regulation in plants. New Phytologist. : 0-0.
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Doi: 10.1111/nph.12912

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Plant function requires effective mechanisms to regulate water transport at a variety of scales. Here, we develop a new theoretical framework describing plant responses to drying soil, based on the relationship between midday and predawn leaf water potentials. The intercept of the relationship (Λ) characterizes the maximum transpiration rate per unit of hydraulic transport capacity, whereas the slope (σ) measures the relative sensitivity of the transpiration rate and plant hydraulic conductance to declining water availability. This framework was applied to a newly compiled global database of leaf water potentials to estimate the values of Λ and σ for 102 plant species. Our results show that our characterization of drought responses is largely consistent within species, and that the parameters Λ and σ show meaningful associations with climate across species. Parameter σ was ≤1 in most species, indicating a tight coordination between the gas and liquid phases of water transport, in which canopy transpiration tended to decline faster than hydraulic conductance during drought, thus reducing the pressure drop through the plant. The quantitative framework presented here offers a new way of characterizing water transport regulation in plants that can be used to assess their vulnerability to drought under current and future climatic conditions. © 2014 New Phytologist Trust.

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