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

Abstract

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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Fig. 1: Physiological responses at, or prior to, mortality from drought for multiple tree species.
Fig.  2: Relationship between the tree hydraulic traits related to xylem embolism resistance and normalized NSC in aboveground woody tissue at, or prior to, mortality from drought.
Fig. 3: Physiological responses associated with hydraulic failure and carbon starvation, as defined by PLC and NSC deviation from control in 13 cases (study × species combinations) for which both data were available.

References

  1. 1.

    Allen, C. D. et al. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecol. Manag. 259, 660–684 (2010).

    Article  Google Scholar 

  2. 2.

    IPCC Climate Change 2014: Impacts, Adaptation, and Vulnerability (eds Field, C. B. et al.) (Cambridge Univ. Press, Cambridge, 2014).

  3. 3.

    McDowell, N. et al. Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol. 178, 719–739 (2008).

    Article  PubMed  Google Scholar 

  4. 4.

    Adams, H. D. et al. Ecohydrological consequences of drought- and infestation- triggered tree die-off: insights and hypotheses. Ecohydrology 5, 145–159 (2012).

    Article  Google Scholar 

  5. 5.

    Anderegg, W. R. L., Kane, J. M. & Anderegg, L. D. L. Consequences of widespread tree mortality triggered by drought and temperature stress. Nat. Clim. Change 3, 30–36 (2013).

    Article  Google Scholar 

  6. 6.

    McDowell, N. G. et al. The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends Ecol. Evol. 26, 523–532 (2011).

    Article  PubMed  Google Scholar 

  7. 7.

    McDowell, N. G. et al. Multi-scale predictions of massive conifer mortality due to chronic temperature rise. Nat. Clim. Change 6, 295–300 (2016).

    Article  Google Scholar 

  8. 8.

    Friedlingstein, P. et al. Uncertainties in CMIP5 climate projections due to carbon cycle feedbacks. J. Climate 27, 511–526 (2014).

    Article  Google Scholar 

  9. 9.

    Friend, A. D. et al. Carbon residence time dominates uncertainty in terrestrial vegetation responses to future climate and atmospheric CO2. Proc. Natl Acad. Sci. USA 111, 3280–3285 (2014).

    Article  PubMed  CAS  Google Scholar 

  10. 10.

    McDowell, N. G. et al. Evaluating theories of drought-induced vegetation mortality using a multimodel-experiment framework. New Phytol. 200, 304–321 (2013).

    Article  PubMed  CAS  Google Scholar 

  11. 11.

    Sala, A., Piper, F. & Hoch, G. Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytol. 186, 274–281 (2010).

    Article  PubMed  Google Scholar 

  12. 12.

    Hartmann, H., Ziegler, W., Kolle, O. & Trumbore, S. Thirst beats hunger – declining hydration during drought prevents carbon starvation in Norway spruce saplings. New Phytol. 200, 340–349 (2013).

    Article  PubMed  CAS  Google Scholar 

  13. 13.

    Quirk, J., McDowell, N. G., Leake, J. R., Hudson, P. J. & Beerling, D. J. Increased susceptibility to drought-induced mortality in Sequoia sempervirens (Cupressaceae) trees under Cenozoic atmosphere carbon dioxide starvation. Am. J. Bot. 100, 582–591 (2013).

    Article  PubMed  CAS  Google Scholar 

  14. 14.

    O’Brien, M. J., Leuzinger, S., Philipson, C. D., Tay, J. & Hector, A. Drought survival of tropical tree seedlings enhanced by non-structural carbohydrate levels. Nat. Clim. Change 4, 710–714 (2014).

    Article  CAS  Google Scholar 

  15. 15.

    Sevanto, S., McDowell, N. G., Dickman, L. T., Pangle, R. & Pockman, W. T. How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant Cell Environ. 37, 153–161 (2014).

    Article  PubMed  CAS  Google Scholar 

  16. 16.

    Piper, F. I. & Fajardo, A. Carbon dynamics of Acer pseudoplatanus seedlings under drought and complete darkness. Tree Physiol. 36, 1400–1408 (2016).

    PubMed  CAS  Google Scholar 

  17. 17.

    McDowell, N. G. & Sevanto, S. The mechanisms of carbon starvation: how, when, or does it even occur at all? New Phytol. 186, 264–266 (2010).

    Article  PubMed  Google Scholar 

  18. 18.

    Sala, A., Woodruff, D. R. & Meinzer, F. C. Carbon dynamics in trees: feast or famine? Tree Physiol. 32, 764–775 (2012).

    Article  PubMed  CAS  Google Scholar 

  19. 19.

    Fatichi, S., Leuzinger, S. & Koerner, C. Moving beyond photosynthesis: from carbon source to sink-driven vegetation modeling. New Phytol. 201, 1086–1095 (2014).

    Article  PubMed  CAS  Google Scholar 

  20. 20.

    Hartmann, H. Carbon starvation during drought-induced tree mortality – are we chasing a myth? J. Plant Hydraul. 2, e005 (2015).

    Article  Google Scholar 

  21. 21.

    Körner, C. Paradigm shift in plant growth control. Curr. Opin. Plant Biol. 25, 107–114 (2015).

    Article  PubMed  CAS  Google Scholar 

  22. 22.

    Martínez-Vilalta, J. et al. Dynamics of non-structural carbohydrates in terrestrial plants: a global synthesis. Ecol. Monogr. 86, 495–516 (2016).

    Article  Google Scholar 

  23. 23.

    Choat, B. et al. Global convergence in the vulnerability of forests to drought. Nature 491, 752–755 (2012).

    Article  PubMed  CAS  Google Scholar 

  24. 24.

    Skelton, R. P., West, A. G. & Dawson, T. E. Predicting plant vulnerability to drought in biodiverse regions using functional traits. Proc. Natl Acad. Sci. USA 112, 5744–5749 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. 25.

    Poorter, L. & Markesteijn, L. Seedling traits determine drought tolerance of tropical tree species. Biotropica 40, 321–331 (2008).

    Article  Google Scholar 

  26. 26.

    Meinzer, F. C., Johnson, D. M., Lachenbruch, B., McCulloh, K. A. & Woodruff, D. R. Xylem hydraulic safety margins in woody plants: coordination of stomatal control of xylem tension with hydraulic capacitance. Funct. Ecol. 23, 922–930 (2009).

    Article  Google Scholar 

  27. 27.

    McDowell, N. G. Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol. 155, 1051–1059 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. 28.

    Mitchell, P. J., O’Grady, A. P., Tissue, D. T., Worledge, D. & Pinkard, E. A. Co-ordination of growth, gas exchange and hydraulics define the carbon safety margin in tree species with contrasting drought strategies. Tree Physiol. 34, 443–458 (2014).

    Article  PubMed  CAS  Google Scholar 

  29. 29.

    Mencuccini, M., Minunno, F., Salmon, Y., Martinez-Vilalta, J. & Holtta, T. Coordination of physiological traits involved in drought-induced mortality of woody plants. New Phytol. 208, 396–409 (2015).

    Article  PubMed  CAS  Google Scholar 

  30. 30.

    O’Brien, M. J., Burslem, D., Caduff, A., Tay, J. & Hector, A. Contrasting nonstructural carbohydrate dynamics of tropical tree seedlings under water deficit and variability. New Phytol. 205, 1083–1094 (2015).

    Article  PubMed  CAS  Google Scholar 

  31. 31.

    Landhäusser, S. M. & Lieffers, V. J. Defoliation increases risk of carbon starvation in root systems of mature aspen. Trees-Struct. Funct. 26, 653–661 (2012).

    Article  CAS  Google Scholar 

  32. 32.

    Brodribb, T. J., McAdam, S. A. M., Jordan, G. J. & Martins, S. C. V. Conifer species adapt to low-rainfall climates by following one of two divergent pathways. Proc. Natl Acad. Sci. USA 111, 14489–14493 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. 33.

    Anderegg, W. R. L. et al. Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe. Proc. Natl Acad. Sci. USA 113, 5024–5029 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. 34.

    Brodribb, T. J. & Cochard, H. Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiol. 149, 575–584 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. 35.

    Anderegg, W. R. L. et al. Tree mortality predicted from drought-induced vascular damage. Nat. Geosci. 8, 367–371 (2015).

    Article  CAS  Google Scholar 

  36. 36.

    Sperry, J. S. & Love, D. M. What plant hydraulics can tell us about responses to climate-change droughts. New Phytol. 207, 14–27 (2015).

    Article  PubMed  CAS  Google Scholar 

  37. 37.

    Zeppel, M. J. B. et al. Drought and resprouting plants. New Phytol. 206, 583–589 (2015).

    Article  PubMed  Google Scholar 

  38. 38.

    Hartmann, H. & Trumbore, S. Understanding the roles of nonstructural carbohydrates in forest trees – from what we can measure to what we want to know. New Phytol. 211, 386–403 (2016).

    Article  PubMed  CAS  Google Scholar 

  39. 39.

    Oliva, J., Stenlid, J. & Martinez-Vilalta, J. The effect of fungal pathogens on the water and carbon economy of trees: implications for drought-induced mortality. New Phytol. 203, 1028–1035 (2014).

    Article  PubMed  CAS  Google Scholar 

  40. 40.

    Anderegg, W. R. L. et al. Tree mortality from drought, insects, and their interactions in a changing climate. New Phytol. 208, 674–683 (2015).

    Article  PubMed  Google Scholar 

  41. 41.

    Johnson, D. M., McCulloh, K. A., Woodruff, D. R. & Meinzer, F. C. Hydraulic safety margins and embolism reversal in stems and leaves: why are conifers and angiosperms so different? Plant Sci. 195, 48–53 (2012).

    Article  PubMed  CAS  Google Scholar 

  42. 42.

    Garcia-Forner, N. et al. Responses of two semiarid conifer tree species to reduced precipitation and warming reveal new perspectives for stomatal regulation. Plant Cell Environ. 39, 38–49 (2016).

    Article  PubMed  CAS  Google Scholar 

  43. 43.

    Martínez-Vilalta, J. & Garcia-Forner, N. Water potential regulation, stomatal behaviour and hydraulic transport under drought: deconstructing the iso/anisohydric concept. Plant Cell Environ. 40, 962–976 (2016).

    Article  PubMed  CAS  Google Scholar 

  44. 44.

    Allen, C. D., Breshears, D. D. & McDowell, N. G. On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene. Ecosphere 6, 129 (2015).

    Article  Google Scholar 

  45. 45.

    Adams, H. D. et al. Empirical and process-based approaches to climate-induced forest mortality models. Front. Plant Sci. 4, 438 (2013).

    PubMed  PubMed Central  Google Scholar 

  46. 46.

    Mackay, D. S. et al. Interdependence of chronic hydraulic dysfunction and canopy processes can improve integrated models of tree response to drought. Water Resour. Res. 51, 6156–6176 (2015).

    Article  Google Scholar 

  47. 47.

    Sperry, J. S. et al. Pragmatic hydraulic theory predicts stomatal responses to climatic water deficits. New Phytol. 212, 577–589 (2016).

    Article  PubMed  CAS  Google Scholar 

  48. 48.

    Sperry, J. S., Adler, F. R., Campbell, G. S. & Comstock, J. P. Limitation of plant water use by rhizosphere and xylem conductance: results from a model. Plant Cell Environ. 21, 347–359 (1998).

    Article  Google Scholar 

  49. 49.

    Plaut, J. A. et al. Hydraulic limits preceding mortality in a piñon-juniper woodland under experimental drought. Plant Cell Environ. 35, 1601–1617 (2012).

    Article  PubMed  Google Scholar 

  50. 50.

    Quentin, A. G. et al. Non-structural carbohydrates in woody plants compared among laboratories. Tree Physiol. 35, 1146–1165 (2015).

    PubMed  CAS  Google Scholar 

  51. 51.

    Germino, M. J. A carbohydrate quandary. Tree Physiol. 35, 1141–1145 (2015).

    PubMed  CAS  Google Scholar 

  52. 52.

    Wheeler, J. K. et al. Cutting xylem under tension or supersaturated with gas can generate PLC and the appearance of rapid recovery from embolism. Plant Cell Environ. 36, 1938–1949 (2013).

    PubMed  CAS  Google Scholar 

  53. 53.

    Nardini, A., Savi, T., Trifilò, P. & Lo Gullo, M. A. Drought Stress and the Recovery from Xylem Embolism in Woody Plants (Progress in Botany Series, Springer, Berlin, Heidelberg, 2017).

    Google Scholar 

  54. 54.

    Chave, J. et al. Towards a worldwide wood economics spectrum. Ecol. Lett. 12, 351–366 (2009).

    Article  PubMed  Google Scholar 

  55. 55.

    Zanne, A. E. et al. Global Wood Density Database Dryad Digital Repository http://hdl.handle.net/10255/dryad.235 (2009).

  56. 56.

    Kattge, J. et al. TRY - a global database of plant traits. Glob. Change Biol. 17, 2905–2935 (2011).

    Article  Google Scholar 

  57. 57.

    Niinemets, U. Components of leaf dry mass per area – thickness and density – alter leaf photosynthetic capacity in reverse directions in woody plants. New Phytol. 144, 35–47 (1999).

    Article  Google Scholar 

  58. 58.

    Niinemets, U. Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology 82, 453–469 (2001).

    Article  Google Scholar 

  59. 59.

    Domec, J. C. & Gartner, B. L. Cavitation and water storage capacity in bole xylem segments of mature and young Douglas-fir trees. Trees-Struct. Funct. 15, 204–214 (2001).

    Article  Google Scholar 

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Acknowledgements

This research was supported by the US Department of Energy, Office of Science, Biological and Environmental Research and Office of Science, Next Generation Ecosystem Experiment-Tropics, the Los Alamos National Laboratory LDRD Program, the Pacific Northwest National Laboratory LDRD Program, The EU Euforinno project, the National Science Foundation LTER Program and EF-1340624, EF-1550756 and EAR-1331408, ARC DECRA DE120100518, ARC LP0989881, ARC DP110105102, the Philecology Foundation of Fort Worth, Texas, the Center for Environmental Biology at UC Irvine through a gift from D. Bren and additional funding sources listed in the Supplementary Acknowledgements. We thank A. Boutz, S. Bucci, R. Fisher, A. Meador-Sanchez, R. Meinzer and D. White for discussions on study design, analysis and interpretation of results, and T. Ocheltree for helpful comments on the manuscript. Any use of trade, product or firm names is for descriptive purposes only and does not imply endorsement by the US government.

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A.D.C., A.H., A.K.M., A.S., B.E.E., C.D.A., C.X.U., D.A.G., D.A.W., D.T.T., G.B.G., H.D.A., H.H., J.A.P., J.D.L., J.M.K., J.M.L., J.S.S., L.D.L.A., L.T.D., M.J.B.Z., M.J.G., M.M., N.G.M., P.J.H., R.C.C., R.V., S.M.L., S.S., T.E.F., T.E.H., T.E.K., U.H., W.R.L.A. and W.T.P. designed the study. A.H., A.O.G., B.E.E., D.A.G., D.D.B., D.J.B., D.M.L., D.T.T., E.A.P., E.A.Y., F.I.P., G.B.G., H.D., H.D.A., H.H., J.A.P., J.D.L., J.M.V., J.Q., J.S.S., K.R., L.D.L.A., L.G.P., L.T.D., M.J.B.Z., M.J.G., M.J.O., M.L.G., N.G.F., N.G.M., P.J.H., P.J.M., R.E.P., S.M.L., S.S., T.E.H., T.E.K., T.J.B., U.H., W.R.L.A. and W.T.P. contributed data. H.D.A., M.J.B.Z., P.J.H. and T.E.F. analysed the data. A.D.C., A.G., A.H., A.K.M., A.O.G., A.S., B.E.E., C.D.A., C.X.U., D.A.W., D.D.B., D.J.B., D.J.L., D.M.L., D.T.T., E.A.P., F.I.P., F.R., G.B.G., H.B., H.D., H.D.A., H.H., J.D.L., J.D.M., J.M.K., J.M.V., J.Q., J.S.S., K.R., L.D.L.A., L.G.P., L.T.D., M.G.R., M.J.B.Z., M.J.G., M.J.O., M.L.G., M.M., M.V., M.W.J., N.G.F., N.G.M., P.J.H., P.J.M., R.C.C., R.V., S.M.L., S.S., T.E.F., T.E.H., T.E.K., U.H., W.R.L.A. and W.T.P. contributed to the discussion of results. A.D.C., A.G., A.H., A.O.G., A.S., B.E.E., C.D.A., C.X.U., D.A.W., D.D.B., D.J.B., D.J.L., D.T.T., E.A.P., F.I.P., F.R., G.B.G., H.B., H.D.A., H.H., J.D.M., J.M.K., J.M.L., J.M.V., K.R., L.D.L.A., L.G.P., L.T.D., M.G.R., M.J.B.Z., M.J.G., M.J.O., M.L.G., M.M., M.V., M.W.J., N.G.F., N.G.M., P.J.M., R.C.C., R.H., R.E.P., R.V., S.M.L., S.S., T.E.H., T.E.K., T.J.B., U.H. and W.R.L.A. wrote the manuscript.

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Correspondence to Henry D. Adams.

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Supplementary Methods, Supplementary Discussion, Supplementary References, Supplementary Acknowledgments, Supplementary Tables 1–7, Supplementary Figures 1–6

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Adams, H.D., Zeppel, M.J.B., Anderegg, W.R.L. et al. A multi-species synthesis of physiological mechanisms in drought-induced tree mortality. Nat Ecol Evol 1, 1285–1291 (2017). https://doi.org/10.1038/s41559-017-0248-x

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