Reductions in tree performance during hotter droughts are mitigated by shifts in nitrogen cycling.

Climate warming should result in hotter droughts of unprecedented severity in this century. Such droughts have been linked with massive tree mortality, and data suggest that warming interacts with drought to aggravate plant performance. Yet how forests will respond to hotter droughts remains unclear, as does the suite of mechanisms trees use to deal with hot droughts. We used an ecosystem-scale manipulation of precipitation and temperature on piñon pine (Pinus edulis) and juniper (Juniperus monosperma) trees to investigate nitrogen (N) cycling-induced mitigation processes related to hotter droughts. We found that while negative impacts on plant carbon and water balance are manifest after prolonged drought, performance reductions were not amplified by warmer temperatures. Rather, increased temperatures for 5 years stimulated soil N cycling under piñon trees and modified tree N allocation for both species, resulting in mitigation of hotter drought impacts on tree water and carbon functions. These findings suggest that adjustments in N cycling are likely after multi-year warming conditions and that such changes may buffer reductions in tree performance during hotter droughts. The results highlight our incomplete understanding of trees' ability to acclimate to climate change, raising fundamental questions about the resistance potential of forests to long-term, compound climatic stresses.

Stem radial growth and water storage responses to heat and drought vary between conifers with differing hydraulic strategies.

We investigated stem radial growth and water storage dynamics of 2 conifer species differing in hydraulic carbon strategies, Juniperus monosperma and Pinus edulis, under conditions of ambient, drought (∼45% reduction in precipitation), heat (∼4.8 °C temperature increase), and the combination of drought + heat, in 2013 and 2014. Juniper maintained low growth across all treatments. Overall, the relatively isohydric piñon pine showed significantly greater growth and water storage recharge than the relatively anisohydric juniper across all treatments in the average climate year (2014) but no differences in the regionally dry year (2013). Piñon pine ceased growth at a constant predawn water potential across all treatments and at a less negative water potential threshold than juniper. Heat has a greater negative impact on piñon pines' growth and water storage than drought, whereas juniper was, in contrast, unaffected by heat but strongly impacted by drought. The whole-plant hydraulic carbon strategies, in this case captured using the isohydric/anisohydric concept, translate into alternative growth and water storage strategies under drought and heat conditions.

Warming combined with more extreme precipitation regimes modifies the water sources used by trees.

The persistence of vegetation under climate change will depend on a plant's capacity to exploit water resources. We analyzed water source dynamics in piñon pine and juniper trees subjected to precipitation reduction, atmospheric warming, and to both simultaneously. Piñon and juniper exhibited different and opposite shifts in water uptake depth in response to experimental stress and background climate over 3 yr. During a dry summer, juniper responded to warming with a shift to shallow water sources, whereas piñon pine responded to precipitation reduction with a shift to deeper sources in autumn. In normal and wet summers, both species responded to precipitation reduction, but juniper increased deep water uptake and piñon increased shallow water uptake. Shifts in the utilization of water sources were associated with reduced stomatal conductance and photosynthesis, suggesting that belowground compensation in response to warming and water reduction did not alleviate stress impacts for gas exchange. We have demonstrated that predicted climate change could modify water sources of trees. Warming impairs juniper uptake of deep sources during extended dry periods. Precipitation reduction alters the uptake of shallow sources following extended droughts for piñon. Shifts in water sources may not compensate for climate change impacts on tree physiology.

Tree water dynamics in a drying and warming world.

Disentangling the relative impacts of precipitation reduction and vapour pressure deficit (VPD) on plant water dynamics and determining whether acclimation may influence these patterns in the future is an important challenge. Here, we report sap flux density (FD ), stomatal conductance (Gs ), hydraulic conductivity (KL ) and xylem anatomy in piñon pine (Pinus edulis) and juniper (Juniperus monosperma) trees subjected to five years of precipitation reduction, atmospheric warming (elevated VPD) and their combined effects. No acclimation occurred under precipitation reduction: lower Gs and FD were found for both species compared to ambient conditions. Warming reduced the sensibility of stomata to VPD for both species but resulted in the maintenance of Gs and FD to ambient levels only for piñon. For juniper, reduced soil moisture under warming negated benefits of stomatal adjustments and resulted in reduced FD , Gs and KL . Although reduced stomatal sensitivity to VPD also occurred under combined stresses, reductions in Gs , FD and KL took place to similar levels as under single stresses for both species. Our results show that stomatal conductance adjustments to high VPD could minimize but not entirely prevent additive effects of warming and drying on water use and carbon acquisition of trees in semi-arid regions.

Responses of two semiarid conifer tree species to reduced precipitation and warming reveal new perspectives for stomatal regulation.

Relatively anisohydric species are predicted to be more predisposed to hydraulic failure than relatively isohydric species, as they operate with narrower hydraulic safety margins. We subjected co-occurring anisohydric Juniperus monosperma and isohydric Pinus edulis trees to warming, reduced precipitation, or both, and measured their gas exchange and hydraulic responses. We found that reductions in stomatal conductance and assimilation by heat and drought were more frequent during relatively moist periods, but these effects were not exacerbated in the combined heat and drought treatment. Counter to expectations, both species exhibited similar gs temporal dynamics in response to drought. Further, whereas P. edulis exhibited chronic embolism, J. monosperma showed very little embolism due to its conservative stomatal regulation and maintenance of xylem water potential above the embolism entry point. This tight stomatal control and low levels of embolism experienced by juniper refuted the notion that very low water potentials during drought are associated with loose stomatal control and with the hypothesis that anisohydric species are more prone to hydraulic failure than isohydric species. Because direct association of stomatal behaviour with embolism resistance can be misleading, we advocate consideration of stomatal behaviour relative to embolism resistance for classifying species drought response strategies.

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.

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.

In vivo Observation of Tree Drought Response with Low-Field NMR and Neutron Imaging.

Using a simple low-field NMR system, we monitored water content in a living tree in a greenhouse over 2 months. By continuously running the system, we observed changes in tree water content on a scale of half an hour. The data showed a diurnal change in water content consistent both with previous NMR and biological observations. Neutron imaging experiments show that our NMR signal is primarily due to water being rapidly transported through the plant, and not to other sources of hydrogen, such as water in cytoplasm, or water in cell walls. After accounting for the role of temperature in the observed NMR signal, we demonstrate a change in the diurnal signal behavior due to simulated drought conditions for the tree. These results illustrate the utility of our system to perform noninvasive measurements of tree water content outside of a temperature controlled environment.