William T. Pockman

Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought?

Severe droughts have been associated with regional-scale forest mortality worldwide. Climate change is expected to exacerbate regional mortality events; however, prediction remains difficult because the physiological mechanisms underlying drought survival and mortality are poorly understood. We developed a hydraulically based theory considering carbon balance and insect resistance that allowed development and examination of hypotheses regarding survival and mortality. Multiple mechanisms may cause mortality during drought. A common mechanism for plants with isohydric regulation of water status results from avoidance of drought-induced hydraulic failure via stomatal closure, resulting in carbon starvation and a cascade of downstream effects such as reduced resistance to biotic agents. Mortality by hydraulic failure per se may occur for isohydric seedlings or trees near their maximum height. Although anisohydric plants are relatively drought-tolerant, they are predisposed to hydraulic failure because they operate with narrower hydraulic safety margins during drought. Elevated temperatures should exacerbate carbon starvation and hydraulic failure. Biotic agents may amplify and be amplified by drought-induced plant stress. Wet multidecadal climate oscillations may increase plant susceptibility to drought-induced mortality by stimulating shifts in hydraulic architecture, effectively predisposing plants to water stress. Climate warming and increased frequency of extreme events will probably cause increased regional mortality episodes. Isohydric and anisohydric water potential regulation may partition species between survival and mortality, and, as such, incorporating this hydraulic framework may be effective for modeling plant survival and mortality under future climate conditions.

Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure

Wood density (Dt), an excellent predictor of mechanical properties, is typically viewed in relation to support against gravity, wind, snow, and other environmental forces. In contrast, we show the surprising extent to which variation in Dt and wood structure is linked to support against implosion by negative pressure in the xylem pipeline. The more drought-tolerant the plant, the more negative the xylem pressure can become without cavitation, and the greater the internal load on the xylem conduit walls. Accordingly, Dt was correlated with cavitation resistance. This trend was consistent with the maintenance of a safety factor from implosion by negative pressure: conduit wall span (b) and thickness (t) scaled so that (t/b)2 was proportional to cavitation resistance as required to avoid wall collapse. Unexpectedly, trends in Dt may be as much or more related to support of the xylem pipeline as to support of the plant.

Ecosystem carbon loss with woody plant invasion of grasslands

The invasion of woody vegetation into deserts, grasslands and savannas is generally thought to lead to an increase in the amount of carbon stored in those ecosystems. For this reason, shrub and forest expansion (for example, into grasslands) is also suggested to be a substantial, if uncertain, component of the terrestrial carbon sink. Here we investigate woody plant invasion along a precipitation gradient (200 to 1,100 mm yr-1) by comparing carbon and nitrogen budgets and soil δ13C profiles between six pairs of adjacent grasslands, in which one of each pair was invaded by woody species 30 to 100 years ago. We found a clear negative relationship between precipitation and changes in soil organic carbon and nitrogen content when grasslands were invaded by woody vegetation, with drier sites gaining, and wetter sites losing, soil organic carbon. Losses of soil organic carbon at the wetter sites were substantial enough to offset increases in plant biomass carbon, suggesting that current land-based assessments may overestimate carbon sinks. Assessments relying on carbon stored from woody plant invasions to balance emissions may therefore be incorrect.

Precipitation pulses and carbon fluxes in semiarid and arid ecosystems

In the arid and semiarid regions of North America, discrete precipitation pulses are important triggers for biological activity. The timing and magnitude of these pulses may differentially affect the activity of plants and microbes, combining to influence the C balance of desert ecosystems. Here, we evaluate how a “pulse” of water influences physiological activity in plants, soils and ecosystems, and how characteristics, such as precipitation pulse size and frequency are important controllers of biological and physical processes in arid land ecosystems. We show that pulse size regulates C balance by determining the temporal duration of activity for different components of the biota. Microbial respiration responds to very small events, but the relationship between pulse size and duration of activity likely saturates at moderate event sizes. Photosynthetic activity of vascular plants generally increases following relatively larger pulses or a series of small pulses. In this case, the duration of physiological activity is an increasing function of pulse size up to events that are infrequent in these hydroclimatological regions. This differential responsiveness of photosynthesis and respiration results in arid ecosystems acting as immediate C sources to the atmosphere following rainfall, with subsequent periods of C accumulation should pulse size be sufficient to initiate vascular plant activity. Using the average pulse size distributions in the North American deserts, a simple modeling exercise shows that net ecosystem exchange of CO2 is sensitive to changes in the event size distribution representative of wet and dry years. An important regulator of the pulse response is initial soil and canopy conditions and the physical structuring of bare soil and beneath canopy patches on the landscape. Initial condition influences responses to pulses of varying magnitude, while bare soil/beneath canopy patches interact to introduce nonlinearity in the relationship between pulse size and soil water response. Building on this conceptual framework and developing a greater understanding of the complexities of these eco-hydrologic systems may enhance our ability to describe the ecology of desert ecosystems and their sensitivity to global change.

Convergence across biomes to a common rain-use efficiency.

Water availability limits plant growth and production in almost all terrestrial ecosystems. However, biomes differ substantially in sensitivity of aboveground net primary production (ANPP) to between-year variation in precipitation. Average rain-use efficiency (RUE; ANPP/precipitation) also varies between biomes, supposedly because of differences in vegetation structure and/or biogeochemical constraints. Here we show that RUE decreases across biomes as mean annual precipitation increases. However, during the driest years at each site, there is convergence to a common maximum RUE (RUEmax) that is typical of arid ecosystems. RUEmax was also identified by experimentally altering the degree of limitation by water and other resources. Thus, in years when water is most limiting, deserts, grasslands and forests all exhibit the same rate of biomass production per unit rainfall, despite differences in physiognomy and site-level RUE. Global climate models predict increased between-year variability in precipitation, more frequent extreme drought events, and changes in temperature. Forecasts of future ecosystem behaviour should take into account this convergent feature of terrestrial biomes.

Assessing the Response of Terrestrial Ecosystems to Potential Changes in Precipitation

Abstract Changes in Earths surface temperatures caused by anthropogenic emissions of greenhouse gases are expected to affect global and regional precipitation regimes. Interactions between changing precipitation regimes and other aspects of global change are likely to affect natural and managed terrestrial ecosystems as well as human society. Although much recent research has focused on assessing the responses of terrestrial ecosystems to rising carbon dioxide or temperature, relatively little research has focused on understanding how ecosystems respond to changes in precipitation regimes. Here we review predicted changes in global and regional precipitation regimes, outline the consequences of precipitation change for natural ecosystems and human activities, and discuss approaches to improving understanding of ecosystem responses to changing precipitation. Further, we introduce the Precipitation and Ecosystem Change Research Network (PrecipNet), a new interdisciplinary research network assembled to encourage and foster communication and collaboration across research groups with common interests in the impacts of global change on precipitation regimes, ecosystem structure and function, and the human enterprise.

ECOHYDROLOGICAL IMPLICATIONS OF WOODY PLANT ENCROACHMENT

Increases in the abundance or density of woody plants in historically semiarid and arid grassland ecosystems have important ecological, hydrological, and socioeconomic implications. Using a simplified water-balance model, we propose a framework for con- ceptualizing how woody plant encroachment is likely to affect components of the water cycle within these ecosystems. We focus in particular on streamflow and the partitioning of evapotranspiration into evaporation and transpiration. On the basis of this framework, we suggest that streamflow and evaporation processes are affected by woody plant en- croachment in different ways, depending on the degree and seasonality of aridity and the availability of subsurface water. Differences in landscape physiography, climate, and runoff mechanisms mediate the influence of woody plants on hydrological processes. Streamflow is expected to decline as a result of woody plant encroachment in landscapes dominated by subsurface flow regimes. Similarly, encroachment of woody plants can be expected to produce an increase in the fractional contribution of bare soil evaporation to evapotrans- piration in semiarid ecosystems, whereas such shifts may be small or negligible in both subhumid and arid ecosystems. This framework for considering the effects of woody plant encroachment highlights important ecological and hydrological interactions that serve as a basis for predicting other ecological aspects of vegetation change—such as potential changes in carbon cycling within an ecosystem. In locations where woody plant encroach- ment results in increased plant transpiration and concurrently the availability of soil water is reduced, increased accumulation of carbon in soils emerges as one prediction. Thus, explicitly considering the ecohydrological linkages associated with vegetation change pro- vides needed information on the consequences of woody plant encroachment on water yield, carbon cycling, and other processes.

ADAPTIVE VARIATION IN THE VULNERABILITY OF WOODY PLANTS TO XYLEM CAVITATION

The ability of plants to supply water to their leaves is intimately associated with survival. Water supply to leaves depends on maintaining an intact water column in the xylem from the roots to shoots. Because this hydraulic pathway is under tension, it is vulnerable to breakage through the induction of air emboli (cavitation). Although the phys- iological benefit of resistance to water-stress-induced xylem cavitation for desiccation tol- erance is clear, there is considerable interspecific variation within and across climates. To understand the adaptive significance of this variation and the potential trade-off with water transport, we compiled a database of 167 species from 50 seed plant families and examined relationships among resistance to xylem cavitation, water transport capacity (as determined by the specific conductivity of xylem ( KS)), and climate. Relationships were evaluated using standard cross-species correlations ( r). Because inferences about the adaptive significance of these correlations can be biased by the potential similarity of closely related species, we also analyzed our data using phylogenetically independent contrast correlations (PIC) calculated over a range of alternate seed plant phylogenies. Resistance to cavitation, ex- pressed as the xylem tension at which 50% of hydraulic conductivity was lost (C50), ranged from 20.18 to 29.9 MPa for angiosperms and from 21.5 to 214.1 MPa for conifers. Conifers were most resistant to cavitation, with mean C50 80% more negative than angio- sperms. In contrast, KS was 270% higher in angiosperms than conifers. Across all species, cavitation resistance increased with decreasing mean annual precipitation. However, sig- nificant phylogenetically independent contrast correlations between C50 and annual precip- itation were found within the evergreen angiosperms and conifers but not in the deciduous angiosperms. Thus, the adaptive significance of increased resistance to cavitation as a mechanism of drought tolerance may be of primary importance in evergreen angiosperms and conifers. In contrast, analysis of independent contrasts indicated that KS increased with decreasing rainfall in deciduous angiosperms, whereas there was no association between KS and water availability for evergreen angiosperms and conifers. These results suggest that the evolution of increased KS may be a critical adaptation to water limitation in de- ciduous angiosperms. Although there was a significant cross-species correlation between C50 and KS, this relationship was not supported by the independent contrast correlation, suggesting that the evolutionary basis for a trade-off between cavitation resistance and water transport capacity is weak.

Tree die‐off in response to global change‐type drought: mortality insights from a decade of plant water potential measurements

Global climate change is projected to produce warmer, longer, and more frequent droughts, referred to here as “global change-type droughts”, which have the potential to trigger widespread tree die-off. However, drought-induced tree mortality cannot be predicted with confidence, because long-term field observations of plant water stress prior to, and culminating in, mortality are rare, precluding the development and testing of mechanisms. Here, we document plant water stress in two widely distributed, co-occurring species, pinon pine (Pinus edulis) and juniper (Juniperus monosperma), over more than a decade, leading up to regional-scale die-off of pinon pine trees in response to global change-related drought. Pinon leaf water potentials remained substantially below their zero carbon assimilation point for at least 10 months prior to dying, in contrast to those of juniper, which rarely dropped below their zero-assimilation point. These data suggest that pinon mortality was driven by protracted water stress,...

How do trees die? A test of the hydraulic failure and carbon starvation hypotheses

Despite decades of research on plant drought tolerance, the physiological mechanisms by which trees succumb to drought are still under debate. We report results from an experiment designed to separate and test the current leading hypotheses of tree mortality. We show that piñon pine (Pinus edulis) trees can die of both hydraulic failure and carbon starvation, and that during drought, the loss of conductivity and carbohydrate reserves can also co-occur. Hydraulic constraints on plant carbohydrate use determined survival time: turgor loss in the phloem limited access to carbohydrate reserves, but hydraulic control of respiration prolonged survival. Our data also demonstrate that hydraulic failure may be associated with loss of adequate tissue carbohydrate content required for osmoregulation, which then promotes failure to maintain hydraulic integrity.