Robert E. Pangle

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.

Drought predisposes piñon–juniper woodlands to insect attacks and mortality

To test the hypothesis that drought predisposes trees to insect attacks, we quantified the effects of water availability on insect attacks, tree resistance mechanisms, and mortality of mature piñon pine (Pinus edulis) and one-seed juniper (Juniperus monosperma) using an experimental drought study in New Mexico, USA. The study had four replicated treatments (40 × 40 m plot/replicate): removal of 45% of ambient annual precipitation (H2 O-); irrigation to produce 125% of ambient annual precipitation (H2 O+); a drought control (C) to quantify the impact of the drought infrastructure; and ambient precipitation (A). Piñon began dying 1 yr after drought initiation, with higher mortality in the H2 O- treatment relative to other treatments. Beetles (bark/twig) were present in 92% of dead trees. Resin duct density and area were more strongly affected by treatments and more strongly associated with piñon mortality than direct measurements of resin flow. For juniper, treatments had no effect on insect resistance or attacks, but needle browning was highest in the H2 O- treatment. Our results provide strong evidence that ≥ 1 yr of severe drought predisposes piñon to insect attacks and increases mortality, whereas 3 yr of the same drought causes partial canopy loss in juniper.

Hydraulic limits preceding mortality in a piñon–juniper woodland under experimental drought

Drought-related tree mortality occurs globally and may increase in the future, but we lack sufficient mechanistic understanding to accurately predict it. Here we present the first field assessment of the physiological mechanisms leading to mortality in an ecosystem-scale rainfall manipulation of a piñon-juniper (Pinus edulis-Juniperus monosperma) woodland. We measured transpiration (E) and modelled the transpiration rate initiating hydraulic failure (E(crit) ). We predicted that isohydric piñon would experience mortality after prolonged periods of severely limited gas exchange as required to avoid hydraulic failure; anisohydric juniper would also avoid hydraulic failure, but sustain gas exchange due to its greater cavitation resistance. After 1 year of treatment, 67% of droughted mature piñon died with concomitant infestation by bark beetles (Ips confusus) and bluestain fungus (Ophiostoma spp.); no mortality occurred in juniper or in control piñon. As predicted, both species avoided hydraulic failure, but safety margins from E(crit) were much smaller in piñon, especially droughted piñon, which also experienced chronically low hydraulic conductance. The defining characteristic of trees that died was a 7 month period of near-zero gas exchange, versus 2 months for surviving piñon. Hydraulic limits to gas exchange, not hydraulic failure per se, promoted drought-related mortality in piñon pine.

A multi-species synthesis of physiological mechanisms in drought-induced tree mortality

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 drought-induced 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.The mechanisms underlying drought-induced tree mortality are not fully resolved. Here, the authors show that, across multiple tree species, loss of xylem conductivity above 60% is associated with mortality, while carbon starvation is not universal.

Regulation and acclimation of leaf gas exchange in a piñon–juniper woodland exposed to three different precipitation regimes

Leaf gas-exchange regulation plays a central role in the ability of trees to survive drought, but forecasting the future response of gas exchange to prolonged drought is hampered by our lack of knowledge regarding potential acclimation. To investigate whether leaf gas-exchange rates and sensitivity to drought acclimate to precipitation regimes, we measured the seasonal variations of leaf gas exchange in a mature piñon-juniper Pinus edulis-Juniperus monosperma woodland after 3 years of precipitation manipulation. We compared trees receiving ambient precipitation with those in an irrigated treatment (+30% of ambient precipitation) and a partial rainfall exclusion (-45%). Treatments significantly affected leaf water potential, stomatal conductance and photosynthesis for both isohydric piñon and anisohydric juniper. Leaf gas exchange acclimated to the precipitation regimes in both species. Maximum gas-exchange rates under well-watered conditions, leaf-specific hydraulic conductance and leaf water potential at zero photosynthetic assimilation all decreased with decreasing precipitation. Despite their distinct drought resistance and stomatal regulation strategies, both species experienced hydraulic limitation on leaf gas exchange when precipitation decreased, leading to an intraspecific trade-off between maximum photosynthetic assimilation and resistance of photosynthesis to drought. This response will be most detrimental to the carbon balance of piñon under predicted increases in aridity in the southwestern USA.

Methodology and performance of a rainfall manipulation experiment in a piñon–juniper woodland

Climate models predict that water limited regions around the world will become drier and warmer in the near future, including southwestern North America. We developed a large-scale experimental system that allows testing of stand level impacts of precipitation changes. Four treatments were applied to 1600 m2 plots (40 m × 40 m), each with three replicates in a pinon pine (Pinus edulis) and juniper (Juniper monosperma) ecosystem. These species have extensive root systems, requiring large-scale manipulation to effectively alter soil water availability. Treatments consisted of: (1) irrigation plots that receive supplemental water additions, (2) drought plots that receive 55% of ambient rainfall, (3) cover-control plots that receive ambient precipitation, but allow determination of treatment infrastructure artifacts, and (4) ambient control plots. Our drought structures effectively reduced soil water potential and volumetric water content compared to the ambient, cover-control, and water addition plots. Drought and cover-control plots experienced an average increase in maximum soil and ground-level air temperature of 1–4°C during the growing season compared to ambient plots, and concurrent short-term diurnal increases in maximum air temperature were also observed directly above and below plastic structures. Our drought and irrigation treatments significantly influenced tree predawn water potential and canopy transpiration, with drought treatment trees exhibiting significant decreases in physiological function compared to ambient and irrigated trees. Supplemental irrigation resulted in a significant increase in both plant water potential and canopy transpiration compared to trees in the other treatments. This experimental design allows manipulation of plant water stress at the tree/stand scale, permits a wide range of drought conditions, and provides prolonged drought conditions comparable to historical droughts in the past—drought events for which wide-spread mortality in both these species was observed.

Carbohydrate dynamics and mortality in a piñon-juniper woodland under three future precipitation scenarios

Drought-induced forest mortality is an increasing global problem with wide-ranging consequences, yet mortality mechanisms remain poorly understood. Depletion of non-structural carbohydrate (NSC) stores has been implicated as an important mechanism in drought-induced mortality, but experimental field tests are rare. We used an ecosystem-scale precipitation manipulation experiment to evaluate leaf and twig NSC dynamics of two co-occurring conifers that differ in patterns of stomatal regulation of water loss and recent mortality: the relatively desiccation-avoiding piñon pine (Pinus edulis) and the relatively desiccation-tolerant one-seed juniper (Juniperus monosperma). Piñon pine experienced 72% mortality after 13-25 months of experimental drought and juniper experienced 20% mortality after 32-47 months. Juniper maintained three times more NSC in the foliage than twigs, and converted NSC to glucose and fructose under drought, consistent with osmoregulation requirements to maintain higher stomatal conductance during drought than piñon. Despite these species differences, experimental drought caused decreased leaf starch content in dying trees of both species (P < 0.001). Average dry-season leaf starch content was also a good predictor of drought-survival time for both species (R(2)  = 0.93). These results, along with observations of drought-induced reductions to photosynthesis and growth, support carbon limitation as an important process during mortality of these two conifer species.

Storage and transpiration have negligible effects on δ13C of stem CO2 efflux in large conifer trees

Stem respiration rates are often quantified by measuring the CO(2) efflux from stems into chambers. It has been suggested that these measurements underestimate respiration because some of the respired CO(2) can be either retained or transported upwards in the transpiration stream. If the stem CO(2) efflux does not represent all respired CO(2), then the interpretation of its isotopic signal may be compromised as well. The C-isotope composition of the respired CO(2) and the measured efflux could differ due to (i) the release of CO(2) produced elsewhere into the stem and transported upwards in xylem water (soil CO(2) or root respired CO(2)); (ii) the retention or release of CO(2) storage pools within the tree stem and (iii) the removal of CO(2) by the transpiration stream. We investigated the effects of these processes in large conifer trees using two manipulative experiments: a labelling experiment and a crown removal experiment. The labelling experiment used an extreme enrichment of dissolved CO(2) in soil water to assess the C uptake by the roots. In this experiment, we found no contamination of the stem CO(2) pool despite clear evidence that the water itself had been taken up. The crown removal experiment tested for vertical CO(2) flux in xylem water by eliminating transpiration. Here, we found no change in the delta(13)C of stem CO(2) efflux (delta(EA); P > 0.05). We concluded that for these large conifers, sap-flow influenced neither delta(13)C of stem efflux nor that of the stem CO(2) pool. By parameterizing Henrys Law for conditions inside the stem, we estimated the transport flux to represent 1-3% of the stem CO(2) efflux to the atmosphere. Finally, assuming a 2 per thousand difference between delta(13)C of root and stem respiration, we estimated that potential contamination of delta(EA) by root respired CO(2) would be < 0.1 per thousand. Thus, neither the release of soil or root CO(2), nor storage in the stem, nor vertical transport of CO(2) in the xylem sap had any detectable influence on delta(13)C of the CO(2) measured in stem efflux.

Prolonged experimental drought reduces plant hydraulic conductance and transpiration and increases mortality in a piñon–juniper woodland

Plant hydraulic conductance (ks) is a critical control on whole-plant water use and carbon uptake and, during drought, influences whether plants survive or die. To assess long-term physiological and hydraulic responses of mature trees to water availability, we manipulated ecosystem-scale water availability from 2007 to 2013 in a piñon pine (Pinus edulis) and juniper (Juniperus monosperma) woodland. We examined the relationship between ks and subsequent mortality using more than 5 years of physiological observations, and the subsequent impact of reduced hydraulic function and mortality on total woody canopy transpiration (EC) and conductance (GC). For both species, we observed significant reductions in plant transpiration (E) and ks under experimentally imposed drought. Conversely, supplemental water additions increased E and ks in both species. Interestingly, both species exhibited similar declines in ks under the imposed drought conditions, despite their differing stomatal responses and mortality patterns during drought. Reduced whole-plant ks also reduced carbon assimilation in both species, as leaf-level stomatal conductance (gs) and net photosynthesis (An) declined strongly with decreasing ks. Finally, we observed that chronically low whole-plant ks was associated with greater canopy dieback and mortality for both piñon and juniper and that subsequent reductions in woody canopy biomass due to mortality had a significant impact on both daily and annual canopy EC and GC. Our data indicate that significant reductions in ks precede drought-related tree mortality events in this system, and the consequence is a significant reduction in canopy gas exchange and carbon fixation. Our results suggest that reductions in productivity and woody plant cover in piñon–juniper woodlands can be expected due to reduced plant hydraulic conductance and increased mortality of both piñon pine and juniper under anticipated future conditions of more frequent and persistent regional drought in the southwestern United States.

Integrating ecophysiology and forest landscape models to improve projections of drought effects under climate change.

Fundamental drivers of ecosystem processes such as temperature and precipitation are rapidly changing and creating novel environmental conditions. Forest landscape models (FLM) are used by managers and policy-makers to make projections of future ecosystem dynamics under alternative management or policy options, but the links between the fundamental drivers and projected responses are weak and indirect, limiting their reliability for projecting the impacts of climate change. We developed and tested a relatively mechanistic method to simulate the effects of changing precipitation on species competition within the LANDIS-II FLM. Using data from a field precipitation manipulation experiment in a piñon pine (Pinus edulis) and juniper (Juniperus monosperma) ecosystem in New Mexico (USA), we calibrated our model to measurements from ambient control plots and tested predictions under the drought and irrigation treatments against empirical measurements. The model successfully predicted behavior of physiological variables under the treatments. Discrepancies between model output and empirical data occurred when the monthly time step of the model failed to capture the short-term dynamics of the ecosystem as recorded by instantaneous field measurements. We applied the model to heuristically assess the effect of alternative climate scenarios on the piñon-juniper ecosystem and found that warmer and drier climate reduced productivity and increased the risk of drought-induced mortality, especially for piñon. We concluded that the direct links between fundamental drivers and growth rates in our model hold great promise to improve our understanding of ecosystem processes under climate change and improve management decisions because of its greater reliance on first principles.