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NOTICE: This is the author’s version of a work that was accepted for publication in Nature. Changes resulting from the publishing process, such as peer review, editing, corrections or structural formatting may not be reflected in this document. A definitive version was subsequently published in NATURE, VOL 491, (29 NOVEMBER 2012). DOI: http://dx.doi.org/10.1038/nature11688 Title: Global convergence in the vulnerability of forests to drought Choat B, Jansen S, Brodribb TJ, Cochard H, Bhaskar R, Bucci S, Delzon S, Feild TS, Gleason SM, Jacobsen AL, Lens F, Maherali H, Martinez-Vilalta J, Mayr S, Mencuccini M, Mitchell PJ, Nardini A, Pittermann J, Pratt RB, Sperry JS, Westoby M, Wright IJ, Zanne A. Summary Shifts in rainfall patterns and increasing temperatures associated with climate change are likely to cause widespread mortality of forest plants in regions where the duration and severity of droughts increase1. One primary cause of drought-induced mortality is hydraulic failure of the plant water transport system2-4. Water stress creates trapped gas emboli in this transport system, which reduces the ability of plants to supply water to leaves for photosynthetic gas exchange and can ultimately result in desiccation and death. However, at present we lack a clear picture of how thresholds to hydraulic failure vary across a broad range of species and forest environments. Using a new data synthesis of woody plants (478 species from 185 sites), we show that the majority of forest species operate with narrow hydraulic safety margins against injurious levels of water stress and therefore face a high risk of mortality if significant shifts in rainfall accompany increasing temperatures. Safety margins were largely independent of mean annual precipitation, with many species highly vulnerable to hydraulic failure regardless of their current rainfall environment. These findings provide insight into why climate induced mortality is occurring not only in arid regions but also in mesic forests not normally considered to be at risk. This is particularly relevant to projections of mortality in mesic forest species, which have constitutively low embolism resistance and are predicted to face reduced rainfall in many areas5. 1 Text Sensitivity to drought is of fundamental importance in shaping the distribution of plant species, community structure, and biogeography6-8. Drought, often in combination with other abiotic and biotic factors, underpinned many large scale forest mortality events over the past century1,9. Recent evidence suggests that rising global temperatures are already amplifying drought-induced forest dieback and affecting terrestrial net primary productivity10-14. The consequences of this mortality are potentially dramatic. For example, rapid forest collapse via drought could convert the world’s tropical forests from a net carbon sink into a large carbon source during this century5,15. Predicting how forests will respond to future climate change hinges on a quantitative understanding of the physiological mechanisms governing droughtinduced mortality at the species level. The most promising avenue for characterizing the sensitivity of plants to water stress is by quantifying the strength of the liquid (hydraulic) connection between soil and leaves through the water-transporting xylem tissue. Cavitation, a phase change from liquid water to vapour, occurs in plants because sap transported through the xylem is held under negative pressure16. The resultant air emboli block xylem conduits and reduce the ability of the plant to move water from the soil to the sites of photosynthesis17. Recent evidence indicates that the ability of woody plants to survive and recover from periods of sustained drought is strongly related to their embolism resistance2,3. This property varies widely among species and is largely determined by differences in the structure of the xylem18. Though xylem structure can acclimate to environmental variation during growth and development, subsequent acclimation of embolism resistance to environmental stress is not possible because xylem conduits are dead at maturity. Embolism resistance therefore represents a critically important trait in defining the limits of drought tolerance across woody species and for predictions of drought-induced mortality at regional and global scales. 2 The resistance of a plant to embolism is described by the relationship between xylem pressure and the loss of hydraulic conductivity due to conduit occlusion by gas emboli (Supplementary Fig. 1). The xylem pressure at which a 50% loss of conductivity occurs (Ψ50) is the most commonly used index of embolism resistance. In order to examine the vulnerability of forest biomes to drought-induced hydraulic failure we assembled a database of Ψ50 containing 478 woody species. In these analyses we broadly defined forests to include Mediterranean and savanna woodland biomes. Site climate varied widely, e.g. mean annual precipitation (MAP) ranged from 300 to 4500 mm, and mean annual temperature from -4º to 27 ºC. Data for angiosperms (flowering plants) and gymnosperms (mainly conifers) were analysed separately because of fundamental differences in xylem structure between these two groups. In drying soil, stomata initially regulate water loss from the leaves to maintain xylem pressure within a range that will protect the plant from extensive embolism and hydraulic failure in the xylem17,19. As drought continues, stomatal closure slows but does not halt the decline of xylem pressure and hydraulic capacity. If soil water is not replenished before complete hydraulic failure occurs then the plant will desiccate and die. It is therefore expected that the minimum xylem pressure observed in plants under natural conditions (Ψmin) will be strongly related to Ψ50. We observed a significant linear relationship between Ψmin and Ψ50 for both angiosperms and gymnosperms -- demonstrating that embolism resistance is tightly linked with the level of water stress experienced by plants across a broad range of environments (Fig. 1). The difference between Ψmin and Ψ50 represents the ‘safety margin’ with which the plant operates in a given environment20,21. A Ψmin equal to Ψ50 indicates an impaired vascular system that limits photosynthesis and increases the risk of catastrophic hydraulic failure. 3 Across all forest biomes, angiosperm species operated at narrow safety margins (Fig. 2). The low safety margin of many species indicates that all forest biomes would be vulnerable to loss of taxa via drought induced mortality, particularly in light of predicted increases in extreme drought events associated with global climate change22,23. This finding provides insight into why climate-induced mortality is occurring not only in arid regions but also in mesic forests not normally considered to be at risk1,5,24. Species from mesic forests are particularly vulnerable because of their constitutively low embolism resistance compared to species from drier environments. In addition, the slope of the relationship between xylem pressure and the loss of hydraulic conductivity is steeper for mesic taxa, meaning that a smaller absolute increase in water stress is required to push these plants to hydraulic failure (Supplementary Fig. 2). While angiosperms have a well documented capacity to recover from high levels of embolism by refilling xylem vessels, it is clear that this recovery can only occur if periods of drought are followed by sufficient precipitation and a return to favourable water status25. Therefore, refilling does not represent an effective strategy for mitigating the effects of severe and persistent drought. Gymnosperms maintained greater safety margins between Ψmin and Ψ50 than angiosperms across woodland and temperate forest biomes, with safety margins increasing in species with higher embolism resistance. However, this does not indicate that gymnosperms are generally immune to the possibility of hydraulic failure. In fact, species in the Pinaceae have significantly lower embolism resistance and safety margins than species in the Cupressaceae26,27. This taxonomic difference is reflected in the greater frequency of dieback events involving Pinaceae species compared with Cupressaceae in Asia, Europe, and North America1,28. A clear illustration of how species differences in embolism resistance and safety margin play out during drought is provided by the Piñon-Juniper woodlands of the south western USA. In the severe 2002-2003 drought, Pinus (Pinaceae) species suffered 4 widespread mortality while co-existing Juniperus (Cupressaceae) species with greater embolism resistance and safety margins survived12. In our dataset, Ψ50 was significantly related to MAP such that, on average, species at higher rainfall sites exhibited lower resistance to embolism (Fig. 3). Similar relationships were found between Ψ50 and climate variables that account for both the variation in potential evapotranspiration (PET) and seasonality of precipitation: Aridity Index (MAP / PET) and mean precipitation of the driest quarter (Supplementary Fig. 3). That said, a wide range of hydraulic strategies occur within any given climate region, with the greatest variation in Ψ50 occurring at sites with MAP between 300-1000 mm. These sites are characterised by high seasonality of rainfall and include savannas, seasonally dry tropical forests and Mediterranean environments. In high MAP sites, represented by tropical rainforests in our dataset, variation is compressed to less negative Ψ50. This suggests that the lower transport efficiency and higher structural ‘costs’ associated with achieving high embolism resistance render these dry forest species less competitive in highly productive, wet tropical environments18. It is clear that Ψmin and MAP are decoupled in certain cases, implying that some species growing in drier environments escape from water stress, therefore alleviating the need for high embolism resistance. There are numerous examples in the literature of species with low embolism resistance growing in areas of low rainfall or which are prone to seasonal drought. This includes riparian and ground water dependent vegetation occurring in drier regions8 and drought deciduous behaviour in dry tropical forest trees29. These plants manage to avoid very negative xylem pressures by some combination of predictable access to ground water (deep rooting phreatophytes), reduction in leaf area, and water storage in stems. However, it appears that the majority of species operate close to their functional limits regardless of these adjustments, a finding that is largely independent of rainfall environment and biome. 5 Our analyses of Ψmin and safety margin demonstrate the fundamental vulnerability of woody plant species to reduction in rainfall and increasing temperatures. The risky hydraulic strategy exhibited by many species is most likely the result of a trade-off that balances growth against risk of mortality in a given environment17,19. However, the limited genetic diversity of embolism resistance within species suggests that it is unlikely that most species will be able to adapt hydraulically to accelerated climate change30. If the tight link between embolism resistance and water availability is the product of an evolutionary response to natural selection over many generations, then the rapid pace of climate change may outstrip the capacity of populations to evolve increased embolism resistance. Such limits to adaptation could result in changes to the composition of forest and woodland communities, with potentially large loss of biodiversity in many areas. While it is evident that a number of different mechanisms (hydraulic failure, carbohydrate depletion, insect attack) are involved in drought induced mortality, these mechanisms are highly interdependent9. Embolism formation is a key mechanism of mortality because it sets the thresholds for stomatal closure, leading to limitations on photosynthesis, increased heat and light damage, and a rundown of carbohydrate reserves over longer time scales. Our results indicate that knowledge of embolism resistance is essential to predict how community structure and the distribution of species will change in response to increased aridity. Incorporating embolism resistance and safety margins into dynamic global vegetation models is not only desirable, but also now within reach, using this broad hydraulic dataset. Methods Xylem traits were compiled from published and unpublished sources. The full dataset used for these analyses contained 478 species from 185 sites, with 384 angiosperm and 94 6 gymnosperm species. Data presented for Ψ50 are from stem xylem only and therefore represent a conservative estimate of embolism resistance since roots are normally less embolism resistant than stems within a species. Ψmin data are the minimum water potential recorded for each species in the field, indicating a seasonal, rather than daily minimum value. ‘Lethal’ Ψmin values reported in manipulative trials where plants were droughted to death were not included in the database. Safety margins were calculated as the margin by which Ψmin differs from the xylem pressure causing 50% loss of hydraulic conductivity (Ψmin – Ψ50). Data presented in Fig. 1 were binned by 1.0 MPa increments of Ψ50; bins with only one data point were pooled with the next highest bin. Regression lines presented are for raw data to avoid bias associated with uneven bin size. Differences in biome means for safety margin were analysed using a general linear model, with differences between angiosperms and gymnosperms considered separately. Climate data were taken from (a) the paper in which Ψ50 data were published or (b) the WorldClim or CRU Climate Database depending on which value matched better with elevation. Relationships between Ψ50 and climate variables (MAP, AI, mean precipitation of the driest quarter) were analysed using a generalised model assessed by restricted maximum likelihood where variance was simultaneously modelled as a power function of the same climate variables. Forest biomes were assigned based on site descriptions contained in the primary sources. We defined ‘forest’ broadly to include Mediterranean, savanna and woodland environments that are not commonly classified as forests. The dataset therefore encompasses tree, shrub and liana species from vegetation communities with a significant component of woody plants. 7 References 1 Allen, C. D. et al. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecology and Management 259, 660-684 (2010). 2 Brodribb, T. J. & Cochard, H. Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiol. 149, 575-584 (2009). 3 Kursar, T. A. et al. Tolerance to low leaf water status of tropical tree seedlings is related to drought performance and distribution. Functional Ecology 23, 93-102 (2009). 4 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). 5 Phillips, O. L. et al. Drought sensitivity of the amazon rainforest. Science 323, 13441347 (2009). 6 Brodribb, T. & Hill, R. S. The importance of xylem constraints in the distribution of conifer species. New Phytol. 143, 365-372 (1999). 7 Engelbrecht, B. M. J. et al. Drought sensitivity shapes species distribution patterns in tropical forests. Nature 447, 80-82 (2007). 8 Pockman, W. T. & Sperry, J. S. Vulnerability to xylem cavitation and the distribution of Sonoran desert vegetation. Am. J. Bot. 87, 1287-1299 (2000). 9 McDowell, N. G. et al. The interdependence of mechanisms underlying climatedriven vegetation mortality. Trends in Ecology and Evolution 26, 523-532 (2011). 10 Anderegga, W. R. L. et al. The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off. Proceedings of the National Academy of Sciences of the United States of America 109, 233–237 (2012). 8 11 Bréda, N., Huc, R., Granier, A. & Dreyer, E. Temperate forest trees and stands under severe drought: A review of ecophysiological responses, adaptation processes and long-term consequences. Annals of Forest Science 63, 625-644 (2006). 12 Breshears, D. D. et al. Regional vegetation die-off in response to global-change-type drought. Proceedings of the National Academy of Sciences of the United States of America 102, 15144-15148 (2005). 13 Ciais, P. et al. Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437, 529-533 (2005). 14 Zhao, M. & Running, S. W. Drought-induced reduction in global terrestrial net primary production from 2000 through 2009. Science 329, 940-943 (2010). 15 Lewis, S. L. Tropical forests and the changing earth system. Philosophical Transactions of the Royal Society B: Biological Sciences 361, 195-210 (2006). 16 Pockman, W. T., Sperry, J. S. & O'Leary, J. W. Sustained and significant negative water pressure in xylem. Nature 378, 715-716 (1995). 17 Tyree, M. T. & Sperry, J. S. Vulnerability of xylem to cavitation and embolism. Annu. Rev. Plant Physiol. Plant Molec. Biol. 40, 19-38 (1989). 18 Sperry, J. S., Hacke, U. G. & Pittermann, J. Size and function in conifer tracheids and angiosperm vessels. Am. J. Bot. 93, 1490-1500 (2006). 19 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). 20 Alder, N. N., Sperry, J. S. & Pockman, W. T. Root and stem xylem embolism, stomatal conductance, and leaf turgor in Acer grandidentatum populations along a soil moisture gradient. Oecologia 105, 293-301 (1996). 9 21 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. Functional Ecology 23, 922-930 (2009). 22 Allison, I. et al. The Copenhagen Diagnosis: updating the world on the latest climate science. (The University of New South Wales Climate Research Centre, 2009). 23 Zhang, X. et al. Detection of human influence on twentieth-century precipitation trends. Nature 448, 461-465 (2007). 24 Meir, P. & Woodward, F. I. Amazonian rain forests and drought: Response and vulnerability. New Phytol. 187, 553-557 (2010). 25 Brodersen, C. R., McElrone, A. J., Choat, B., Matthews, M. A. & Shackel, K. A. The dynamics of embolism repair in xylem: In vivo visualizations using high-resolution computed tomography. Plant Physiol. 154, 1088-1095 (2010). 26 Delzon, S., Douthe, C., Sala, A. & Cochard, H. Mechanism of water-stress induced cavitation in conifers: Bordered pit structure and function support the hypothesis of seal capillary-seeding. Plant, Cell and Environment 33, 2101-2111 (2010). 27 Maherali, H., Pockman, W. T. & Jackson, R. B. Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology 85, 2184-2199 (2004). 28 Bigler, C., Bräker, O. U., Bugmann, H., Dobbertin, M. & Rigling, A. Drought as an inciting mortality factor in scots pine stands of the Valais, Switzerland. Ecosystems 9, 330-343 (2006). 29 Choat, B., Ball, M. C., Luly, J. G. & Holtum, J. A. M. Hydraulic architecture of deciduous and evergreen dry rainforest tree species from north-eastern Australia. Trees - Structure and Function 19, 305-311 (2005). 30 Lamy, J. B. et al. Uniform selection as a primary force reducing population genetic differentiation of cavitation resistance across a species range. PLoS ONE 6 (2011). 10 Supplementary Information is linked to the online version of the paper at www.nature.com/nature. Acknowledgements We thank the ARC-NZ Vegetation Function Network for hosting the original working group from which the data set was compiled. Author Contributions BC and SJ led the initial working group and coordinated analysis and write up of the work. All authors contributed to compilation and organization of the dataset. SG and IJW extracted climate data from WorldClim and CRU Climate Database. HM, MM and JMV assisted in statistical analyses of the dataset. Author Information The authors declare that they have no competing financial interests. Figure legends Figure 1. Minimum xylem pressure (Ψmin) as a function of embolism resistance (Ψ50) for angiosperm and gymnosperm species. The dashed line indicates the xylem pressure at which a 50% loss of hydraulic conductivity occurs. The safety margin is the distance between each point and this line. Error bars show standard deviation. Points were binned in 1.0 MPa increments for Ψ50 with a total sample size of 209 species for angiosperms and 36 species for gymnosperms. Bins were pooled with the next lowest bin if they contained only one sample. Regression lines shown were fitted to raw data (angiosperms r2 = 0.57, P < 0.0001, gymnosperms r2 = 0.59, P < 0.0001). Figure 2. Box plot of hydraulic safety margins (Ψmin – Ψ50) for angiosperm and gymnosperm species across major forest biomes, with the dashed line indicating the pressure causing a 11 50% loss of hydraulic conductivity in the stem xylem. Boxes show the median, 25th and 75th percentiles, error bars show 10th and 90th percentiles, filled symbols show outliers. Gymnosperm species were not represented in tropical forests. Significant differences (P < 0.01) between biome means are indicated by different letters above boxes with angiosperms and gymnosperms considered separately. Figure 3. Embolism resistance (Ψ50) as a function of mean annual precipitation (MAP) for angiosperm and gymnosperm species with each point representing one species (N = 384 for angiosperms and 94 for gymnosperms). A generalised model indicated Ψ50 was significantly related (P < 0.00001) to MAP for angiosperms and gymnosperms (see methods summary for details). 12