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      Drought and shade deplete nonstructural carbohydrate reserves in seedlings of five temperate tree species

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          Abstract

          Plants that store nonstructural carbohydrates ( NSC) may rely on carbon reserves to survive carbon‐limiting stress, assuming that reserves can be mobilized. We asked whether carbon reserves decrease in resource stressed seedlings, and if NSC allocation is related to species' relative stress tolerances. We tested the effects of stress (shade, drought, and defoliation) on NSC in seedlings of five temperate tree species ( Acer rubrum Marsh., Betula papyrifera Marsh ., Fraxinus americana L ., Quercus rubra L., and Quercus velutina Lam.). In a greenhouse experiment, seedlings were subjected to combinations of shade, drought, and defoliation. We harvested seedlings over 32–97 days and measured biomass and NSC concentrations in stems and roots to estimate depletion rates. For all species and treatments, except for defoliation, seedling growth and NSC accumulation ceased. Shade and drought combined caused total NSC decreases in all species. For shade or drought alone, only some species experienced decreases. Starch followed similar patterns as total NSC, but soluble sugars increased under drought for drought‐tolerant species. These results provide evidence that species deplete stored carbon in response to carbon limiting stress and that species differences in NSC response may be important for understanding carbon depletion as a buffer against shade‐ and drought‐induced mortality.

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          Most cited references19

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          Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality.

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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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              Carbon dynamics in trees: feast or famine?

              Research on the degree to which carbon (C) availability limits growth in trees, as well as recent trends in climate change and concurrent increases in drought-related tree mortality, have led to a renewed focus on the physiological mechanisms associated with tree growth responses to current and future climate. This has led to some dispute over the role of stored non-structural C compounds as indicators of a tree's current demands for photosynthate. Much of the uncertainty surrounding this issue could be resolved by developing a better understanding of the potential functions of non-structural C stored within trees. In addition to functioning as a buffer to reconcile temporal asynchrony between C demand and supply, the storage of non-structural C compounds may be under greater regulation than commonly recognized. We propose that in the face of environmental stochasticity, large, long-lived trees may require larger C investments in storage pools as safety margins than previously recognized, and that an important function of these pools may be to maintain hydraulic transport, particularly during episodes of severe stress. If so, survival and long-term growth in trees remain a function of C availability. Given that drought, freeze-thaw events and increasing tree height all impose additional constraints on vascular transport, the common trend of an increase in non-structural carbohydrate concentrations with tree size, drought or cold is consistent with our hypothesis. If the regulated maintenance of relatively large constitutive stored C pools in trees serves to maintain hydraulic integrity, then the minimum thresholds are expected to vary depending on the specific tissues, species, environment, growth form and habit. Much research is needed to elucidate the extent to which allocation of C to storage in trees is a passive vs. an active process, the specific functions of stored C pools, and the factors that drive active C allocation to storage.
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                Author and article information

                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                19 November 2015
                December 2015
                : 5
                : 23 ( doiID: 10.1002/ece3.2015.5.issue-23 )
                : 5711-5721
                Affiliations
                [ 1 ] Department of Plant BiologyMichigan State University East Lansing Michigan
                [ 2 ] Graduate Program in Ecology, Evolutionary Biology and BehaviorMichigan State University East Lansing Michigan
                [ 3 ] Department ForestryMichigan State University East Lansing Michigan
                Author notes
                [*] [* ] Correspondence

                Andrea J. Maguire, 480 Wilson Road, Natural Resources Building, Michigan State University, East Lansing, MI 48824.

                Tel: 517‐355‐8433; Fax: 517‐432‐1143;

                E‐mail: maguire8@ 123456msu.edu

                Article
                ECE31819
                10.1002/ece3.1819
                4813112
                27069619
                fd209bc2-1135-40d1-a1df-de39a8422f77
                © 2015 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 06 July 2015
                : 12 October 2015
                : 14 October 2015
                Page count
                Pages: 11
                Funding
                Funded by: National Science Foundation
                Award ID: DEB 0958943
                Funded by: GRFP
                Funded by: Michigan AgBioResearch
                Award ID: NRSP‐3
                Funded by: National Atmospheric Deposition Program
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                ece31819
                December 2015
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.7.2 mode:remove_FC converted:22.12.2015

                Evolutionary Biology
                carbon reserves,carbon starvation,nonstructural carbohydrates,soluble sugars,starch,stress

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