Shifts in rainfall patterns and increasing temperatures associated with climate change are likely to cause widespread forest decline in regions where droughts are predicted to increase in duration and severity. One primary cause of productivity loss and plant mortality during drought is hydraulic failure. Drought stress creates trapped gas emboli in the water transport system, which reduces the ability of plants to supply water to leaves for photosynthetic gas exchange and can ultimately result in desiccation and mortality. At present we lack a clear picture of how thresholds to hydraulic failure vary across a broad range of species and environments, despite many individual experiments. Here we draw together published and unpublished data on the vulnerability of the transport system to drought-induced embolism for a large number of woody species, with a view to examining the likely consequences of climate change for forest biomes. We show that 70% of 226 forest species from 81 sites worldwide operate with narrow hydraulic safety margins against injurious levels of drought stress and therefore potentially face long-term reductions in productivity and survival if temperature and aridity increase as predicted for many regions across the globe. Safety margins are largely independent of mean annual precipitation, showing that there is global convergence in the vulnerability of forests to drought, with all forest biomes equally vulnerable to hydraulic failure regardless of their current rainfall environment. These findings provide insight into why drought-induced forest decline is occurring not only in arid regions but also in wet forests not normally considered at drought risk
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 droughtinduced 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
SummaryThe 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 (r 2 < 0.086), no species had high efficiency and high safety, supporting the idea for a safety-efficiency tradeoff. However, many species had low efficiency and low safety. Species with low efficiency and low safety were weakly associated (r 2 < 0.02 in most cases) with higher wood density, lower leaf-to sapwood-area and shorter stature. There appears to be no persuasive explanation for the considerable number of species with both low efficiency and low safety. These species represent a real challenge for understanding the evolution of xylem.
SummaryPlant function requires effective mechanisms to regulate water transport at a variety of scales. Here, we develop a new theoretical framework describing plant responses to drying soil, based on the relationship between midday and predawn leaf water potentials. The intercept of the relationship (Λ) characterizes the maximum transpiration rate per unit of hydraulic transport capacity, whereas the slope (r) measures the relative sensitivity of the transpiration rate and plant hydraulic conductance to declining water availability.This framework was applied to a newly compiled global database of leaf water potentials to estimate the values of Λ and r for 102 plant species.Our results show that our characterization of drought responses is largely consistent within species, and that the parameters Λ and r show meaningful associations with climate across species. Parameter r was ≤1 in most species, indicating a tight coordination between the gas and liquid phases of water transport, in which canopy transpiration tended to decline faster than hydraulic conductance during drought, thus reducing the pressure drop through the plant.The quantitative framework presented here offers a new way of characterizing water transport regulation in plants that can be used to assess their vulnerability to drought under current and future climatic conditions.
Plants store large amounts of non-structural carbohydrates (NSC). While multiple functions of NSC have long been recognized, the interpretation of NSC seasonal dynamics is often based on the idea that stored NSC is a reservoir of carbon that fluctuates depending on the balance between supply via photosynthesis and demand for growth and respiration (the source-sink dynamics concept). Consequently, relatively high NSC concentrations in some plants have been interpreted to reflect excess supply relative to demand. An alternative view, however, is that NSC accumulation reflects the relatively high NSC levels required for plant survival; an important issue that remains highly controversial. Here, we assembled a new global database to examine broad patterns of seasonal NSC variation across organs (leaves, stems, and belowground), plant functional types (coniferous, drought-deciduous angiosperms, winter deciduous angiosperms, evergreen angiosperms, and herbaceous) and biomes (boreal, temperate, Mediterranean, and tropical). We compiled data from 121 studies, including seasonal measurements for 177 species under natural conditions. Our results showed that, on average, NSC account for ~10% of dry plant biomass and are highest in leaves and lowest in stems, whereas belowground organs show intermediate concentrations. Total NSC, starch, and soluble sugars (SS) varied seasonally, with a strong depletion of starch during the growing season and a general increase during winter months, particularly in boreal and temperate biomes. Across functional types, NSC concentrations were highest and most variable in herbaceous species and in conifer needles. Conifers showed the lowest stem and belowground NSC concentrations. Minimum NSC values were relatively high (46% of seasonal maximums on average for total NSC) and, in contrast to average values, were similar among biomes and functional types. Overall, although starch depletion was relatively common, seasonal depletion of total NSC or SS was rare. These results are consistent with a dual view of NSC function: whereas starch acts mostly as a reservoir for future use, soluble sugars perform immediate functions (e.g., osmoregulation) and are kept above some critical threshold. If confirmed, this dual function of NSC will have important implications for the way we understand and model plant carbon allocation and survival under stress.
Current climatic trends involve both increasing temperatures and climatic variability, with extreme events becoming more frequent. Increasing concern on extreme climatic events has triggered research on vegetation shifts. However, evidences of vegetation shifts resulting from these events are still relatively rare. Empirical evidence supports the existence of stabilizing processes minimizing and counteracting the effects of these events, reinforcing community resilience. We propose a demographic framework to understand this inertia to change based on the balance between adult mortality induced by the event and enhanced recruitment or adult survival after the event. The stabilizing processes potentially contributing to this compensation include attenuation of the adult mortality caused by the event, due to site quality variability, to tolerance, phenotypic variability, and plasticity at population level, and to facilitative interactions. Mortality compensation may also occur by increasing future survival due to beneficial effect on growth and survival of the new conditions derived from global warming and increased climatic variability, to lowered competition resulting from reduced density in affected stands, or to antagonistic release when pathogens or predators are vulnerable to the event or the ongoing climatic conditions. Finally, mortality compensation may appear by enhanced recruitment due to release of competition with established vegetation, for instance as a consequence of gap openings after event-caused mortality, or to the new conditions, which may be more favorable for seedling establishment, or to enhanced mutualistic interactions (pollination, dispersal). There are important challenges imposed by the need of long-term studies, but a research agenda focused on potentially stabilizing processes is well suited to understand the variety of responses, including lack of sudden changes and community inertia that are frequently observed in vegetation under extreme events. This understanding is crucial for the establishment of sound management strategies and actions addressed to improve ecosystem resilience under climate change scenarios.
Tree mortality is a key factor influencing forest functions and dynamics, but our understanding of the mechanisms leading to mortality and the associated changes in tree growth rates are still limited. We compiled a new pan-continental tree-ring width database from sites where both dead and living trees were sampled (2970 dead and 4224 living trees from 190 sites, including 36 species), and compared early and recent growth rates between trees that died and those that survived a given mortality event. We observed a decrease in radial growth before death in ca. 84% of the mortality events. The extent and duration of these reductions were highly variable (1-100 years in 96% of events) due to the complex interactions among study species and the source(s) of mortality. Strong and long-lasting declines were found for gymnosperms, shade- and drought-tolerant species, and trees that died from competition. Angiosperms and trees that died due to biotic attacks (especially bark-beetles) typically showed relatively small and short-term growth reductions. Our analysis did not highlight any universal trade-off between early growth and tree longevity within a species, although this result may also reflect high variability in sampling design among sites. The intersite and interspecific variability in growth patterns before mortality provides valuable information on the nature of the mortality process, which is consistent with our understanding of the physiological mechanisms leading to mortality. Abrupt changes in growth immediately before death can be associated with generalized hydraulic failure and/or bark-beetle attack, while long-term decrease in growth may be associated with a gradual decline in hydraulic performance coupled with depletion in carbon reserves. Our results imply that growth-based mortality algorithms may be a powerful tool for predicting gymnosperm mortality induced by chronic stress, but not necessarily so for angiosperms and in case of intense drought or bark-beetle outbreaks.
305I.305II.306III.310IV.311V.314VI.316VII.317VIII.318318References318 Summary Model–data comparisons of plant physiological processes provide an understanding of mechanisms underlying vegetation responses to climate. We simulated the physiology of a piñon pine–juniper woodland (Pinus edulis–Juniperus monosperma) that experienced mortality during a 5 yr precipitation‐reduction experiment, allowing a framework with which to examine our knowledge of drought‐induced tree mortality. We used six models designed for scales ranging from individual plants to a global level, all containing state‐of‐the‐art representations of the internal hydraulic and carbohydrate dynamics of woody plants. Despite the large range of model structures, tuning, and parameterization employed, all simulations predicted hydraulic failure and carbon starvation processes co‐occurring in dying trees of both species, with the time spent with severe hydraulic failure and carbon starvation, rather than absolute thresholds per se, being a better predictor of impending mortality. Model and empirical data suggest that limited carbon and water exchanges at stomatal, phloem, and below‐ground interfaces were associated with mortality of both species. The model–data comparison suggests that the introduction of a mechanistic process into physiology‐based models provides equal or improved predictive power over traditional process‐model or empirical thresholds. Both biophysical and empirical modeling approaches are useful in understanding processes, particularly when the models fail, because they reveal mechanisms that are likely to underlie mortality. We suggest that for some ecosystems, integration of mechanistic pathogen models into current vegetation models, and evaluation against observations, could result in a breakthrough capability to simulate vegetation dynamics.
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