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      Dead or dying? Quantifying the point of no return from hydraulic failure in drought‐induced tree mortality

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          Summary

          • Determining physiological mechanisms and thresholds for climate‐driven tree die‐off could help improve global predictions of future terrestrial carbon sinks. We directly tested for the lethal threshold in hydraulic failure – an inability to move water due to drought‐induced xylem embolism – in a pine sapling experiment.

          • In a glasshouse experiment, we exposed loblolly pine ( Pinus taeda) saplings ( n = 83) to drought‐induced water stress ranging from mild to lethal. Before rewatering to relieve drought stress, we measured native hydraulic conductivity and foliar color change. We monitored all measured individuals for survival or mortality.

          • We found a lethal threshold at 80% loss of hydraulic conductivity – a point of hydraulic failure beyond which it is more likely trees will die, than survive, and describe mortality risk across all levels of water stress. Foliar color changes lagged behind hydraulic failure – best predicting when trees had been dead for some time, rather than when they were dying.

          • Our direct measurement of native conductivity, while monitoring the same individuals for survival or mortality, quantifies a continuous probability of mortality risk from hydraulic failure. Predicting tree die‐off events and understanding the mechanism involved requires knowledge not only of when trees are dead, but when they begin dying – having passed the point of no return.

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          The interdependence of mechanisms underlying climate-driven vegetation mortality.

          Climate-driven vegetation mortality is occurring globally and is predicted to increase in the near future. The expected climate feedbacks of regional-scale mortality events have intensified the need to improve the simple mortality algorithms used for future predictions, but uncertainty regarding mortality processes precludes mechanistic modeling. By integrating new evidence from a wide range of fields, we conclude that hydraulic function and carbohydrate and defense metabolism have numerous potential failure points, and that these processes are strongly interdependent, both with each other and with destructive pathogen and insect populations. Crucially, most of these mechanisms and their interdependencies are likely to become amplified under a warmer, drier climate. Here, we outline the observations and experiments needed to test this interdependence and to improve simulations of this emergent global phenomenon. Copyright © 2011 Elsevier Ltd. All rights reserved.
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            A multi-species synthesis of physiological mechanisms in drought-induced tree mortality

            Widespread tree mortality associated with drought has been observed on all forested continents and global change is expected to exacerbate vegetation vulnerability. Forest mortality has implications for future biosphere-atmosphere interactions of carbon, water and energy balance, and is poorly represented in dynamic vegetation models. Reducing uncertainty requires improved mortality projections founded on robust physiological processes. However, the proposed mechanisms of drought-induced mortality, including hydraulic failure and carbon starvation, are unresolved. A growing number of empirical studies have investigated these mechanisms, but data have not been consistently analysed across species and biomes using a standardized physiological framework. Here, we show that xylem hydraulic failure was ubiquitous across multiple tree taxa at drought-induced mortality. All species assessed had 60% or higher loss of xylem hydraulic conductivity, consistent with proposed theoretical and modelled survival thresholds. We found diverse responses in non-structural carbohydrate reserves at mortality, indicating that evidence supporting carbon starvation was not universal. Reduced non-structural carbohydrates were more common for gymnosperms than angiosperms, associated with xylem hydraulic vulnerability, and may have a role in reducing hydraulic function. Our finding that hydraulic failure at drought-induced mortality was persistent across species indicates that substantial improvement in vegetation modelling can be achieved using thresholds in hydraulic function.
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              Temperature sensitivity of drought-induced tree mortality portends increased regional die-off under global-change-type drought.

              Large-scale biogeographical shifts in vegetation are predicted in response to the altered precipitation and temperature regimes associated with global climate change. Vegetation shifts have profound ecological impacts and are an important climate-ecosystem feedback through their alteration of carbon, water, and energy exchanges of the land surface. Of particular concern is the potential for warmer temperatures to compound the effects of increasingly severe droughts by triggering widespread vegetation shifts via woody plant mortality. The sensitivity of tree mortality to temperature is dependent on which of 2 non-mutually-exclusive mechanisms predominates--temperature-sensitive carbon starvation in response to a period of protracted water stress or temperature-insensitive sudden hydraulic failure under extreme water stress (cavitation). Here we show that experimentally induced warmer temperatures (approximately 4 degrees C) shortened the time to drought-induced mortality in Pinus edulis (piñon shortened pine) trees by nearly a third, with temperature-dependent differences in cumulative respiration costs implicating carbon starvation as the primary mechanism of mortality. Extrapolating this temperature effect to the historic frequency of water deficit in the southwestern United States predicts a 5-fold increase in the frequency of regional-scale tree die-off events for this species due to temperature alone. Projected increases in drought frequency due to changes in precipitation and increases in stress from biotic agents (e.g., bark beetles) would further exacerbate mortality. Our results demonstrate the mechanism by which warmer temperatures have exacerbated recent regional die-off events and background mortality rates. Because of pervasive projected increases in temperature, our results portend widespread increases in the extent and frequency of vegetation die-off.
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                Author and article information

                Contributors
                William.hammond@okstate.edu
                Journal
                New Phytol
                New Phytol
                10.1111/(ISSN)1469-8137
                NPH
                The New Phytologist
                John Wiley and Sons Inc. (Hoboken )
                0028-646X
                1469-8137
                08 July 2019
                September 2019
                : 223
                : 4 ( doiID: 10.1111/nph.v223.4 )
                : 1834-1843
                Affiliations
                [ 1 ] Plant Biology, Ecology and Evolution Oklahoma State University Stillwater OK 74078 USA
                [ 2 ] School of Biological Sciences University of Utah Salt Lake City UT 84112 USA
                [ 3 ] Department of Natural Resource Ecology and Management Oklahoma State University Stillwater OK 74078 USA
                Author notes
                [*] [* ] Author for correspondence:

                William M. Hammond

                Tel: +1 405 471 7203

                Email: William.hammond@ 123456okstate.edu

                Author information
                https://orcid.org/0000-0002-2904-810X
                https://orcid.org/0000-0003-4223-5169
                https://orcid.org/0000-0003-4277-770X
                https://orcid.org/0000-0001-6551-3331
                https://orcid.org/0000-0001-9630-4305
                Article
                NPH15922 2018-27725
                10.1111/nph.15922
                6771894
                31087656
                fb92434b-1fba-4173-ac12-8dadd8a7f2ac
                © 2019 The Authors. New Phytologist © 2019 New Phytologist Trust

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 03 August 2018
                : 05 May 2019
                Page count
                Figures: 4, Tables: 0, Pages: 10, Words: 9013
                Funding
                Funded by: Oklahoma NSF EPSCoR Research Infrastructure Improvement Award
                Award ID: OIA‐1301789
                Funded by: USDA National Institute of Food and Agriculture, Agricultural and Food Research Initiative Competitive Programme, Ecosystem Services and Agro‐ecosystem Management
                Award ID: 2018‐67019‐27850
                Funded by: David and Lucile Packard Foundation
                Funded by: National Science Foundation
                Award ID: 1714972
                Award ID: 1802880
                Funded by: Division of Graduate Education
                Award ID: 1144467
                Funded by: University of Utah Global Change and Sustainability Center
                Categories
                Full Paper
                Research
                Full Papers
                Custom metadata
                2.0
                nph15920
                September 2019
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.6.9 mode:remove_FC converted:01.10.2019

                Plant science & Botany
                climate change,drought,ecophysiology,foliar color,hydraulic failure,tree die‐off,tree mortality,tree physiology

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