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.LinkDoi: 10.1093/treephys/tpv005
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.
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.LinkDoi: 10.3390/f6082505
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.
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.LinkDoi: 10.1016/j.agrformet.2015.06.012
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.
Colomer-Ventura F., Martínez-Vilalta J., Zuccarini P., Escolà A., Armengot L., Castells E. (2015) Contemporary evolution of an invasive plant is associated with climate but not with herbivory. Functional Ecology. 29: 1475-1485.LinkDoi: 10.1111/1365-2435.12463
Divergence in plant traits and trait plasticity after invasion has been proposed as mechanisms favouring invasion success. Current hypotheses predict a rapid evolution in response to changes in the abiotic conditions in the area of introduction or to differences in the herbivore consumption pressure caused by a decrease in the enemies associated with the area of origin [e.g. evolution of increased competitive ability (EICA) hypothesis]. The importance of these factors in determining plant geographical divergence has not been yet simultaneously evaluated. Senecio pterophorus (Asteraceae) is a perennial shrub native to eastern South Africa and a recent invader in western South Africa (since ~100 years ago), Australia (>70-100 years) and Europe (>30 years). These areas differ in their summer drought stress [measured as the ratio of summer precipitation to potential evapotranspiration (P/PET)] and their interactions with herbivores. We performed a common garden experiment with S. pterophorus sampled throughout its entire known distributional area to determine (i) whether native and non-native populations diverge in their traits, as well as the plasticity of these traits in response to water availability and (ii) whether climate and herbivory play a role in the genetic differentiation across regions. Plants from the non-native regions were smaller and had a lower reproductive output than plants from the indigenous area. No geographical differences in phenotypic plasticity were found in response to water availability. Herbivory was not related to the plant geographical divergence. In contrast, our results are consistent with the role of climate as a driver for postinvasive evolution, as suggested by adaptation of plants to a drought cline in the native range, the analogous change in plant traits in independently invaded regions and the convergence of vegetative traits between non-native plants and native plants under similar drought conditions. Native and non-native populations of S. pterophorus differed in plant traits, but not in trait plasticity, in response to their local climatic conditions. Our results are contrary to the role of herbivory as a selective factor after invasion and highlight the importance of climate driving rapid evolution of exotic plants. © 2015 The Authors.
Garcia-Forner N., Adams H.D., Sevanto S., Collins A.D., Dickman L.T., Hudson P.J., Zeppel M.J., Jenkins M.W., Powers H., Martinez-Vilalta J., Mcdowell N.G. (2015) Responses of two semiarid conifer tree species to reduced precipitation and warming reveal new perspectives for stomatal regulation. Plant, Cell and Environment. : 0-0.LinkDoi: 10.1111/pce.12588
Relatively anisohydric species are predicted to be more predisposed to hydraulic failure than relatively isohydric species, as they operate with narrower hydraulic safety margins. We subjected co-occurring anisohydric Juniperus monosperma and isohydric Pinus edulis trees to warming, reduced precipitation, or both, and measured their gas exchange and hydraulic responses. We found that reductions in stomatal conductance and assimilation by heat and drought were more frequent during relatively moist periods, but these effects were not exacerbated in the combined heat and drought treatment. Counter to expectations, both species exhibited similar gs temporal dynamics in response to drought. Further, whereas P.edulis exhibited chronic embolism, J.monosperma showed very little embolism due to its conservative stomatal regulation and maintenance of xylem water potential above the embolism entry point. This tight stomatal control and low levels of embolism experienced by juniper refuted the notion that very low water potentials during drought are associated with loose stomatal control and with the hypothesis that anisohydric species are more prone to hydraulic failure than isohydric species. Because direct association of stomatal behaviour with embolism resistance can be misleading, we advocate consideration of stomatal behaviour relative to embolism resistance for classifying species drought response strategies. © 2015 John Wiley & Sons Ltd.
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.LinkDoi: 10.1111/nph.13646
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
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.LinkDoi: 10.1111/nph.13461
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.
Quentin A.G., Pinkard E.A., Ryan M.G., Tissue D.T., Baggett L.S., Adams H.D., Maillard P., Marchand J., Landhäusser S.M., Lacointe A., Gibon Y., Anderegg W.R.L., Asao S., Atkin O.K., Bonhomme M., Claye C., Chow P.S., Clément-Vidal A., Davies N.W., Dickman L.T., Dumbur R., Ellsworth D.S., Falk K., Galiano L., Grünzweig J.M., Hartmann H., Hoch G., Hood S., Jones J.E., Koike T., Kuhlmann I., Lloret F., Maestro M., Mansfield S.D., Martínez-Vilalta J., Maucourt M., McDowell N.G., Moing A., Muller B., Nebauer S.G., Niinemets U., Palacio S., Piper F., Raveh E., Richter A., Rolland G., Rosas T., Joanis B.S., Sala A., Smith R.A., Sterck F., Stinziano J.R., Tobias M., Unda F., Watanabe M., Way D.A., Weerasinghe L.K., Wild B., Wiley E., Woodruff D.R. (2015) Non-structural carbohydrates in woody plants compared among laboratories. Tree Physiology. 35: 1146-1165.LinkDoi: 10.1093/treephys/tpv073
Non-structural carbohydrates (NSC) in plant tissue are frequently quantified to make inferences about plant responses to environmental conditions. Laboratories publishing estimates of NSC of woody plants use many different methods to evaluate NSC. We asked whether NSC estimates in the recent literature could be quantitatively compared among studies. We also asked whether any differences among laboratories were related to the extraction and quantification methods used to determine starch and sugar concentrations. These questions were addressed by sending sub-samples collected from five woody plant tissues, which varied in NSC content and chemical composition, to 29 laboratories. Each laboratory analyzed the samples with their laboratory-specific protocols, based on recent publications, to determine concentrations of soluble sugars, starch and their sum, total NSC. Laboratory estimates differed substantially for all samples. For example, estimates for Eucalyptus globulus leaves (EGL) varied from 23 to 116 (mean = 56) mg g-1 for soluble sugars, 6-533 (mean = 94) mg g-1 for starch and 53-649 (mean = 153) mg g-1 for total NSC. Mixed model analysis of variance showed that much of the variability among laboratories was unrelated to the categories we used for extraction and quantification methods (method category R2 = 0.05-0.12 for soluble sugars, 0.10-0.33 for starch and 0.01-0.09 for total NSC). For EGL, the difference between the highest and lowest least squares means for categories in the mixed model analysis was 33 mg g-1 for total NSC, compared with the range of laboratory estimates of 596 mg g-1. Laboratories were reasonably consistent in their ranks of estimates among tissues for starch (r = 0.41-0.91), but less so for total NSC (r = 0.45-0.84) and soluble sugars (r = 0.11-0.83). Our results show that NSC estimates for woody plant tissues cannot be compared among laboratories. The relative changes in NSC between treatments measured within a laboratory may be comparable within and between laboratories, especially for starch. To obtain comparable NSC estimates, we suggest that users can either adopt the reference method given in this publication, or report estimates for a portion of samples using the reference method, and report estimates for a standard reference material. Researchers interested in NSC estimates should work to identify and adopt standard methods. © The Author 2015.
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.LinkDoi: 10.1111/pce.12572
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.
Vilà-Cabrera A., Martínez-Vilalta J., Retana J. (2015) Functional trait variation along environmental gradients in temperate and Mediterranean trees. Global Ecology and Biogeography. 24: 1377-1389.LinkDoi: 10.1111/geb.12379
Aim: Characterizing the variation of functional traits in nature is a first step towards linking environmental changes to changes in ecosystem function. Here we aim to characterize the spatial variability of major plant functional traits along wide environmental gradients in Mediterranean and temperate forests, and assess to what extent this variability differs between two dominant families in Northern Hemisphere forests: Fagaceae and Pinaceae. Location: Catalonia (north-east Iberian Peninsula). Methods: Four functional traits were selected to incorporate information on both the leaf and the wood economic spectra: maximum tree height (Hmax), wood density (WD), leaf mass per area (LMA) and nitrogen content of leaves (Nmass). We quantified the variance distribution of each functional trait across three nested ecological scales: population, species and family. Through such scales, we explored the spatial variation of functional traits through climatic and biotic gradients, as well as the covariation among traits. Results: Functional trait variability was distributed across all the ecological scales considered, but mostly at the family level, with functional traits differing markedly between Fagaceae and Pinaceae. Within families, variation in functional traits was similar or higher within species than between species. The spatial variability in functional traits was related to biotic and abiotic gradients, although this effect was quantitatively small compared with differences between families. Covariation among functional traits was not necessarily conserved across ecological scales. Trait covariation across all species was structured along the Hmax-WD and LMA-Nmass axes, but this structure was partially lost within families, where variation was mostly structured along the Hmax-LMA and WD-Nmass axes. Main conclusions: Intraspecific variation emerges as a fundamental component of functional trait structure along wide environmental gradients. Understanding the sources of intraspecific variation, as well as how it contributes to community assembly and ecosystem functioning, thus becomes a primary research question. © 2015 John Wiley & Sons Ltd.
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