Maite Guardiola-Claramonte

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 (≈4 °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.

Nonstructural leaf carbohydrate dynamics of Pinus edulis during drought‐induced tree mortality reveal role for carbon metabolism in mortality mechanism

Vegetation change is expected with global climate change, potentially altering ecosystem function and climate feedbacks. However, causes of plant mortality, which are central to vegetation change, are understudied, and physiological mechanisms remain unclear, particularly the roles of carbon metabolism and xylem function. We report analysis of foliar nonstructural carbohydrates (NSCs) and associated physiology from a previous experiment where earlier drought-induced mortality of Pinus edulis at elevated temperatures was associated with greater cumulative respiration. Here, we predicted faster NSC decline for warmed trees than for ambient-temperature trees. Foliar NSC in droughted trees declined by 30% through mortality and was lower than in watered controls. NSC decline resulted primarily from decreased sugar concentrations. Starch initially declined, and then increased above pre-drought concentrations before mortality. Although temperature did not affect NSC and sugar, starch concentrations ceased declining and increased earlier with higher temperatures. Reduced foliar NSC during lethal drought indicates a carbon metabolism role in mortality mechanism. Although carbohydrates were not completely exhausted at mortality, temperature differences in starch accumulation timing suggest that carbon metabolism changes are associated with time to death. Drought mortality appears to be related to temperature-dependent carbon dynamics concurrent with increasing hydraulic stress in P. edulis and potentially other similar species.

Reply to Sala: Temperature sensitivity in drought-induced tree mortality hastens the need to further resolve a physiological model of death

Our recent study (1) of pinon pine (Pinus edulis) response to change in climate, on which Sala (2) comments, documented that drought-induced mortality was temperature-sensitive. In addition, we showed that time to tree mortality was predicted by leaf-level cumulative respiration for ambient and warmer treatments. Notably, our study experimentally assessed temperature sensitivity of drought mortality by tracking individual physiological responses throughout the death process. Ambient and warmer treatments did not differ in water balance in such a manner as to drive differences in mortality, yet higher respiration rates under warmer temperatures were associated with earlier death of individual trees. Two related studies provide additional support implicating carbon starvation via respiration during protracted water stress. First, modeling of physiological responses indicated that even short droughts drove leaf water potential of pinon pine—a drought-avoiding, isohydric species—quickly below its zero-carbon assimilation point (3). Second, long-term observational measurements of predawn water potential of pinon pine documented that trees could survive shorter but not longer periods of water stress below their zero-carbon assimilation point (4).

Reply to Leuzinger et al.: Drought-induced tree mortality temperature sensitivity requires pressing forward with best available science

Forest and woodland vulnerability to tree mortality in response to future drought and warmer temperatures is emerging as a potentially critical impact of global change (1). We directly addressed this issue experimentally in our recent study (2), on which Leuzinger et al. comment (3). Notably, we showed drought-induced tree mortality was highly temperature-sensitive, raising concern about future die-off. Other experimental studies isolating the effect of warmer temperature on drought-induced tree mortality are lacking—a major knowledge gap given how directly such a relationship underpins the potential impacts of climate change. The shorter survival period under warmer temperatures quantified in our study correspondeds to a difference in leaf-level cumulative respiration—a response consistent with the temperature sensitivity of carbon dynamics driving differences in mortality. A simple projection of this sensitivity using a 103-year historical record of drought indicated that warmer temperatures (+4.3 °C) could increase die-off frequency 5-fold. Leuzinger et al. (3) note methodological concerns regarding the study, some of which are helpful in prioritizing future research to refine insights, but nonetheless do not negate the main findings. Furthermore, these concerns should not cloud the urgency with which the research community pursues additional research to develop an improved model of plant mortality.