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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Changes in tree resistance, recovery and resilience across three successive extreme droughts in the northeast Iberian Peninsula

Serra-Maluquer X., Mencuccini M., Martínez-Vilalta J. (2018) Changes in tree resistance, recovery and resilience across three successive extreme droughts in the northeast Iberian Peninsula. Oecologia. : 1-12.
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Doi: 10.1007/s00442-018-4118-2

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Understanding which variables affect forest resilience to extreme drought is key to predict future dynamics under ongoing climate change. In this study, we analyzed how tree resistance, recovery and resilience to drought have changed along three consecutive droughts and how they were affected by species, tree size, plot basal area (as a proxy for competition) and climate. We focused on the three most abundant pine species in the northeast Iberian Peninsula: Pinus halepensis, P. nigra and P. sylvestris during the three most extreme droughts recorded in the period 1951–2010 (occurred in 1986, 1994, and 2005–2006). We cored trees from permanent sample plots and used dendrochronological techniques to estimate resistance (ability to maintain growth level during drought), recovery (growth increase after drought) and resilience (capacity to recover pre-drought growth levels) in terms of tree stem basal area increment. Mixed-effects models were used to determine which tree- and plot-level variables were the main determinants of resistance, recovery and resilience, and to test for differences among the studied droughts. Larger trees were significantly less resistant and resilient. Plot basal area effects were only observed for resilience, with a negative impact only during the last drought. Resistance, recovery and resilience differed across the studied drought events, so that the studied populations became less resistant, less resilient and recovered worse during the last two droughts. This pattern suggests an increased vulnerability to drought after successive drought episodes. © 2018 Springer-Verlag GmbH Germany, part of Springer Nature

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A multi-species synthesis of physiological mechanisms in drought-induced tree mortality

Adams, H.D., Zeppel, M.J.B., Anderegg, W.R.L., Hartmann, H., Landhäusser, S.M., Tissue, D.T., Huxman, T.E., Hudson, P.J., Franz, T.E., Allen, C.D., Anderegg, L.D.L., Barron-Gafford, G.A., Beerling, D.J., Breshears, D.D., Brodribb, T.J., Bugmann, H., Cobb, R.C., Collins, A.D., Dickman, L.T., Duan, H., Ewers, B.E., Galiano, L., Galvez, D.A., Garcia-Forner, N., Gaylord, M.L., Germino, M.J., Gessler, A., Hacke, U.G., Hakamada, R., Hector, A., Jenkins, M.W., Kane, J.M., Kolb, T.E., Law, D.J., Lewis, J.D., Limousin, J.-M., Love, D.M., Macalady, A.K., Martínez-Vilalta, J., Mencuccini, M., Mitchell, P.J., Muss, J.D., O'Brien, M.J., O'Grady, A.P., Pangle, R.E., Pinkard, E.A., Piper, F.I., Plaut, J.A., Pockman, W.T., Quirk, J., Reinhardt, K., Ripullone, F., Ryan, M.G., Sala, A., Sevanto, S., Sperry, J.S., Vargas, R., Vennetier, M., Way, D.A., Xu, C., Yepez, E.A., McDowell, N.G. (2017) A multi-species synthesis of physiological mechanisms in drought-induced tree mortality. Nature Ecology and Evolution. 1: 1285-1291.
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Doi: 10.1038/s41559-017-0248-x

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Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world's woody plant species

Gleason S.M., Westoby M., Jansen S., Choat B., Hacke U.G., Pratt R.B., Bhaskar R., Brodribb T.J., Bucci S.J., Cao K.-F., Cochard H., Delzon S., Domec J.-C., Fan Z.-X., Feild T.S., Jacobsen A.L., Johnson D.M., Lens F., Maherali H., Martinez-Vilalta J., Mayr S., Mcculloh K.A., Mencuccini M., Mitchell P.J., Morris H., Nardini A., Pittermann J., Plavcova L., Schreiber S.G., Sperry J.S., Wright I.J., Zanne A.E. (2015) Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world's woody plant species. New Phytologist. : 0-0.
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Doi: 10.1111/nph.13646

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The evolution of lignified xylem allowed for the efficient transport of water under tension, but also exposed the vascular network to the risk of gas emboli and the spread of gas between xylem conduits, thus impeding sap transport to the leaves. A well-known hypothesis proposes that the safety of xylem (its ability to resist embolism formation and spread) should trade off against xylem efficiency (its capacity to transport water). We tested this safety-efficiency hypothesis in branch xylem across 335 angiosperm and 89 gymnosperm species. Safety was considered at three levels: the xylem water potentials where 12%, 50% and 88% of maximal conductivity are lost. Although correlations between safety and efficiency were weak (r2

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Coordination of physiological traits involved in drought-induced mortality of woody plants

Mencuccini M., Minunno F., Salmon Y., Martinez-Vilalta J., Holtta T. (2015) Coordination of physiological traits involved in drought-induced mortality of woody plants. New Phytologist. : 0-0.
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Doi: 10.1111/nph.13461

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Accurate modelling of drought-induced mortality is challenging. A steady-state model is presented integrating xylem and phloem transport, leaf-level gas exchange and plant carbohydrate consumption during drought development. A Bayesian analysis of parameter uncertainty based on expert knowledge and a literature review is carried out. The model is tested by combining six data compilations covering 170 species using information on sensitivities of xylem conductivity, stomatal conductance and leaf turgor to water potential. The possible modes of plant failure at steady state are identified (i.e. carbon (C) starvation, hydraulic failure and phloem transport failure). Carbon starvation occurs primarily in the parameter space of isohydric stomatal control, whereas hydraulic failure is prevalent in the space of xylem susceptibility to embolism. Relative to C starvation, phloem transport failure occurs under conditions of low sensitivity of photosynthesis and high sensitivity of growth to plant water status. These three failure modes are possible extremes along two axes of physiological vulnerabilities, one characterized by the balance of water supply and demand and the other by the balance between carbohydrate sources and sinks. Because the expression of physiological vulnerabilities is coordinated, we argue that different failure modes should occur with roughly equal likelihood, consistent with predictions using optimality theory. © 2015 New Phytologist Trust.

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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.

Llegeix més

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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Evaluating theories of drought-induced vegetation mortality using a multimodel-experiment framework

Mcdowell N.G., Fisher R.A., Xu C., Domec J.C., Holtta T., Mackay D.S., Sperry J.S., Boutz A., Dickman L., Gehres N., Limousin J.M., Macalady A., Martinez-Vilalta J., Mencuccini M., Plaut J.A., Ogee J., Pangle R.E., Rasse D.P., Ryan M.G., Sevanto S., Waring R.H., Williams A.P., Yepez E.A., Pockman W.T. (2013) Evaluating theories of drought-induced vegetation mortality using a multimodel-experiment framework. New Phytologist. 200: 304-321.
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Doi: 10.1111/nph.12465

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Summary: Model-data comparisons of plant physiological processes provide an understanding of mechanisms underlying vegetation responses to climate. We simulated the physiology of a piñon pine-juniper woodland (Pinus edulis-Juniperus monosperma) that experienced mortality during a 5 yr precipitation-reduction experiment, allowing a framework with which to examine our knowledge of drought-induced tree mortality. We used six models designed for scales ranging from individual plants to a global level, all containing state-of-the-art representations of the internal hydraulic and carbohydrate dynamics of woody plants. Despite the large range of model structures, tuning, and parameterization employed, all simulations predicted hydraulic failure and carbon starvation processes co-occurring in dying trees of both species, with the time spent with severe hydraulic failure and carbon starvation, rather than absolute thresholds per se, being a better predictor of impending mortality. Model and empirical data suggest that limited carbon and water exchanges at stomatal, phloem, and below-ground interfaces were associated with mortality of both species. The model-data comparison suggests that the introduction of a mechanistic process into physiology-based models provides equal or improved predictive power over traditional process-model or empirical thresholds. Both biophysical and empirical modeling approaches are useful in understanding processes, particularly when the models fail, because they reveal mechanisms that are likely to underlie mortality. We suggest that for some ecosystems, integration of mechanistic pathogen models into current vegetation models, and evaluation against observations, could result in a breakthrough capability to simulate vegetation dynamics. © 2013 New Phytologist Trust.

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Drought-induced defoliation and long periods of near-zero gas exchange play a key role in accentuating metabolic decline of Scots pine

Poyatos R., Aguade D., Galiano L., Mencuccini M., Martinez-Vilalta J. (2013) Drought-induced defoliation and long periods of near-zero gas exchange play a key role in accentuating metabolic decline of Scots pine. New Phytologist. 200: 388-401.
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Doi: 10.1111/nph.12278

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Summary: Drought-induced defoliation has recently been associated with the depletion of carbon reserves and increased mortality risk in Scots pine (Pinus sylvestris). We hypothesize that defoliated individuals are more sensitive to drought, implying that potentially higher gas exchange (per unit of leaf area) during wet periods may not compensate for their reduced photosynthetic area. We measured sap flow, needle water potentials and whole-tree hydraulic conductance to analyse the drought responses of co-occurring defoliated and nondefoliated Scots pines in northeast Spain during typical (2010) and extreme (2011) drought conditions. Defoliated Scots pines showed higher sap flow per unit leaf area during spring, but were more sensitive to summer drought, relative to nondefoliated pines. This pattern was associated with a steeper decline in soil-to-leaf hydraulic conductance with drought and an enhanced sensitivity of canopy conductance to soil water availability. Near-homeostasis in midday water potentials was observed across years and defoliation classes, with minimum values of -2.5 MPa. Enhanced sensitivity to drought and prolonged periods of near-zero gas exchange were consistent with low levels of carbohydrate reserves in defoliated trees. Our results support the critical links between defoliation, water and carbon availability, and their key roles in determining tree survival and recovery under drought. © 2013 New Phytologist Trust.

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Global convergence in the vulnerability of forests to drought

Choat B., Jansen S., Brodribb T.J., Cochard H., Delzon S., Bhaskar R., Bucci S.J., Feild T.S., Gleason S.M., Hacke U.G., Jacobsen A.L., Lens F., Maherali H., Martínez-Vilalta J., Mayr S., Mencuccini M., Mitchell P.J., Nardini A., Pittermann J., Pratt R.B., Sperry J.S., Westoby M., Wright I.J., Zanne A.E. (2012) Global convergence in the vulnerability of forests to drought. Nature. 491: 752-755.
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Doi: 10.1038/nature11688

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Shifts in rainfall patterns and increasing temperatures associated with climate change are likely to cause widespread forest decline in regions where droughts are predicted to increase in duration and severity. One primary cause of productivity loss and plant mortality during drought is hydraulic failure. Drought stress creates trapped gas emboli in the water transport system, which reduces the ability of plants to supply water to leaves for photosynthetic gas exchange and can ultimately result in desiccation and mortality. At present we lack a clear picture of how thresholds to hydraulic failure vary across a broad range of species and environments, despite many individual experiments. Here we draw together published and unpublished data on the vulnerability of the transport system to drought-induced embolism for a large number of woody species, with a view to examining the likely consequences of climate change for forest biomes. We show that 70% of 226 forest species from 81 sites worldwide operate with narrow (

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