Drought's legacy: multiyear hydraulic deterioration underlies widespread aspen forest die‐off and portends increased future risk

Abstract

Forest mortality constitutes a major uncertainty in projections of climate impacts on terrestrial ecosystems and carbon-cycle feedbacks. Recent drought-induced, widespread forest die-offs highlight that climate change could accelerate forest mortality with its diverse and potentially severe consequences for the global carbon cycle, ecosystem services, and biodiversity. How trees die during drought over multiple years remains largely unknown and precludes mechanistic modeling and prediction of forest die-off with climate change. Here, we examine the physiological basis of a recent multiyear widespread die-off of trembling aspen (Populus tremuloides) across much of western North America. Using observations from both native trees while they are dying and a rainfall exclusion experiment on mature trees, we measure hydraulic performance over multiple seasons and years and assess pathways of accumulated hydraulic damage. We test whether accumulated hydraulic damage can predict the probability of tree survival over 2 years. We find that hydraulic damage persisted and increased in dying trees over multiple years and exhibited few signs of repair. This accumulated hydraulic deterioration is largely mediated by increased vulnerability to cavitation, a process known as cavitation fatigue. Furthermore, this hydraulic damage predicts the probability of interyear stem mortality. Contrary to the expectation that surviving trees have weathered severe drought, the hydraulic deterioration demonstrated here reveals that surviving regions of these forests are actually more vulnerable to future droughts due to accumulated xylem damage. As the most widespread tree species in North America, increasing vulnerability to drought in these forests has important ramifications for ecosystem stability, biodiversity, and ecosystem carbon balance. Our results provide a foundation for incorporating accumulated drought impacts into climate-vegetation models. Finally, our findings highlight the critical role of drought stress accumulation and repair of stress-induced damage for avoiding plant mortality, presenting a dynamic and contingent framework for drought impacts on forest ecosystems.

Tree mortality predicted from drought-induced vascular damage

“…4). This supports the hypothesis that low tree and branch conductivities seem to initially result from xylem cavitation during drought years, although other factors probably come into play to explain why these conductances might remain depressed for multiple years post-drought 20 .…”

“…Hydraulic failure through xylem cavitation has been shown to be a major mortality mechanism across a number of angiosperm species [18][19][20] . Using a combination of field physiological measurements, a plant hydraulic model 21 , a hydrologic model 22 , climate projections and multiple mortality data sets ( Supplementary Fig.…”

“…We used field measurements of plant hydraulic conductance to test for a potential threshold as a function of accumulated CWD from 2000-2013. As native branch hydraulic conductivity has been found to predict aspen stem mortality across years 20 , providing an indicator of tree hydraulic health, we tested for a threshold in hydraulic conductivity over a large spatial gradient that included both healthy and dying stands. We found a threshold during ongoing mortality where hydraulic conductivity fell rapidly as a function of accumulated CWD (Fig.…”

Tree Diseases as a Cause and Consequence of Interacting Forest Disturbances

“…Physical host wounds that act as a de facto surmounting of host physical defenses play an important role in infection [1,22,35,36]. Drought has been shown to cause physical damage to plant vascular tissues that may require multiple years to repair [37] and it is likely that other environmental stresses also cause multi-year changes in susceptibility.…”

“…Oscillating dynamics where host populations recover and provide the basis for future outbreaks are a common pattern in many tree mortality events driven by native organisms [35,51,62]. Intensifying outbreaks resulting from climate-change-associated shifts in temperature, precipitation, and resulting host-stress appears likely given documentation of landscape-level declines in host physiological status and its impact to plant defense [3,4,37].…”