Dynamic regulation of water potential in Juniperus osteosperma mediates ecosystem carbon fluxes.

Some plants exhibit dynamic hydraulic regulation, in which the strictness of hydraulic regulation (i.e. iso/anisohydry) changes in response to environmental conditions. However, the environmental controls over iso/anisohydry and the implications of flexible hydraulic regulation for plant productivity remain unknown. In Juniperus osteosperma, a drought-resistant dryland conifer, we collected a 5-month growing season time series of in situ, high temporal-resolution plant water potential ( Ψ $$ \Psi $$ ) and stand gross primary productivity (GPP). We quantified the stringency of hydraulic regulation associated with environmental covariates and evaluated how predawn water potential contributes to empirically predicting carbon uptake. Juniperus osteosperma showed less stringent hydraulic regulation (more anisohydric) after monsoon precipitation pulses, when soil moisture and atmospheric demand were high, and corresponded with GPP pulses. Predawn water potential matched the timing of GPP fluxes and improved estimates of GPP more strongly than soil and/or atmospheric moisture, notably resolving GPP underestimation before vegetation green-up. Flexible hydraulic regulation appears to allow J. osteosperma to prolong soil water extraction and, therefore, the period of high carbon uptake following monsoon precipitation pulses. Water potential and its dynamic regulation may account for why process-based and empirical models commonly underestimate the magnitude and temporal variability of dryland GPP.

Compensatory response of ecosystem carbon-water cycling following severe drought in Southwestern China.

Climate change has increased the frequency and length of droughts, but many uncertainties remain regarding the impacts of this aridification on terrestrial ecosystem function. Vegetation water use efficiency and carbon sequestration capacity are crucial determinants that both respond to and mediate the effects of drought. However, it is important to note that the consequences of drought on these processes can persist for years. A deeper exploration of these "drought legacy effects" will help improve our understanding of how climate change alter ecosystem carbon-water cycling. Here, we investigate the spatial patterns of drought legacy effects on remotely-sensed vegetation greenness (NDVI), net primary productivity (NPP) and water use efficiency (WUE) in southwestern China, a biodiversity hotspot that was impacted by an extreme drought in 2009-2010, with a particular focus on the tradeoff between WUE and NPP. Despite widespread negative drought legacy effects in NDVI (impacting 61.26 % of the study region), there was a general increase in NPP (58.68 %) and a decrease in WUE (67.53 %) in the year following drought (2011). This drought legacy effect was most evident in forests, while drought legacies in grasslands were less common. Drought legacies were also most apparent in relatively warm and humid areas. During the study period (2002 to 2018), we found that drought impacts on WUE also lagged behind changes in NPP by 1-2 years in forests, which highlights how drought legacies may manifest differently across ecosystem processes. Our study demonstrated that severe drought conditions may significantly affect the carbon sequestration capacity and water use efficiency of vegetation in southwestern China, and that forests may compensate for the detrimental effects of water stress by increasing water use and biomass growth after drought episodes.

Cross-biome synthesis of source versus sink limits to tree growth.

Uncertainties surrounding tree carbon allocation to growth are a major limitation to projections of forest carbon sequestration and response to climate change. The prevalence and extent to which carbon assimilation (source) or cambial activity (sink) mediate wood production are fundamentally important and remain elusive. We quantified source-sink relations across biomes by combining eddy-covariance gross primary production with extensive on-site and regional tree ring observations. We found widespread temporal decoupling between carbon assimilation and tree growth, underpinned by contrasting climatic sensitivities of these two processes. Substantial differences in assimilation-growth decoupling between angiosperms and gymnosperms were determined, as well as stronger decoupling with canopy closure, aridity, and decreasing temperatures. Our results reveal pervasive sink control over tree growth that is likely to be increasingly prominent under global climate change.

Heterogeneous isotope effects decouple conifer leaf and branch sugar δ18O and δ13C.

Isotope ratios of tree-ring cellulose are a prominent tool to reconstruct paleoclimate and plant responses to environmental variation. Current models for cellulose isotope ratios assume a transfer of the environmental signals recorded in bulk leaf water to carbohydrates and ultimately into stem cellulose. However, the isotopic signal of carbohydrates exported from leaf to branch may deviate from mean leaf values if spatial heterogeneity in isotope ratios exists in the leaf. We tested whether the isotopic heterogeneity previously observed along the length of a ponderosa pine (Pinus ponderosa) leaf water was preserved in photosynthetic products. We observed an increase in both sugar and bulk tissue δ18O values along the needle, but the increase in carbohydrate δ18O values was dampened relative to the trend observed in leaf water. In contrast, δ13C values of both sugar and bulk organic matter were invariant along the needle. Phloem-exported sugar measured in the branch below the needles did not match whole-needle values of δ18O or δ13C. Instead, there was a near-constant offset observed between the branch and needle sugar δ13C values, while branch δ18O values were most similar to δ18O values observed for sugar at the base of the needle. The observed offset between the branch and needle sugar δ18O values likely arises from partial isotope oxygen exchange between sugars and water during phloem loading and transport. An improved understanding of the conditions producing differential δ13C and δ18O isotope effects between branch phloem and needle sugars could improve tree-ring-based climate reconstructions.

Rapid increases in shrubland and forest intrinsic water-use efficiency during an ongoing megadrought.

Globally, intrinsic water-use efficiency (iWUE) has risen dramatically over the past century in concert with increases in atmospheric CO2 concentration. This increase could be further accelerated by long-term drought events, such as the ongoing multidecadal "megadrought" in the American Southwest. However, direct measurements of iWUE in this region are rare and largely constrained to trees, which may bias estimates of iWUE trends toward more mesic, high elevation areas and neglect the responses of other key plant functional types such as shrubs that are dominant across much of the region. Here, we found evidence that iWUE is increasing in the Southwest at one of the fastest rates documented due to the recent drying trend. These increases were particularly large across three common shrub species, which had a greater iWUE sensitivity to aridity than Pinus ponderosa, a common tree species in the western United States. The sensitivity of both shrub and tree iWUE to variability in atmospheric aridity exceeded their sensitivity to increasing atmospheric [CO2]. The shift to more water-efficient vegetation would be, all else being equal, a net positive for plant health. However, ongoing trends toward lower plant density, diminished growth, and increasing vegetation mortality across the Southwest indicate that this increase in iWUE is unlikely to offset the negative impacts of aridification.

Long-term nitrogen isotope dynamics in Encelia farinosa reflect plant demographics and climate.

While plant δ15 N values have been applied to understand nitrogen (N) dynamics, uncertainties regarding intraspecific and temporal variability currently limit their application. We used a 28 yr record of δ15 N values from two Mojave Desert populations of Encelia farinosa to clarify sources of population-level variability. We leveraged > 3500 foliar δ15 N observations collected alongside structural, physiological, and climatic data to identify plant and environmental contributors to δ15 N values. Additional sampling of soils, roots, stems, and leaves enabled assessment of the distribution of soil N content and δ15 N, intra-plant fractionations, and relationships between soil and plant δ15 N values. We observed extensive within-population variability in foliar δ15 N values and found plant age and foliar %N to be the strongest predictors of individual δ15 N values. There were consistent differences between root, stem, and leaf δ15 N values (spanning c. 3‰), but plant and bulk soil δ15 N values were unrelated. Plant-level variables played a strong role in influencing foliar δ15 N values, and interannual relationships between climate and δ15 N values were counter to previously recognized spatial patterns. This long-term record provides insights regarding the interpretation of δ15 N values that were not available from previous large-scale syntheses, broadly enabling more effective application of foliar δ15 N values.

Seasonal and diurnal trends in progressive isotope enrichment along needles in two pine species.

The Craig-Gordon type (C-G) leaf water isotope enrichment models assume a homogeneous distribution of enriched water across the leaf surface, despite observations that Δ18 O can become increasingly enriched from leaf base to tip. Datasets of this 'progressive isotope enrichment' are limited, precluding a comprehensive understanding of (a) the magnitude and variability of progressive isotope enrichment, and (b) how progressive enrichment impacts the accuracy of C-G leaf water model predictions. Here, we present observations of progressive enrichment in two conifer species that capture seasonal and diurnal variability in environmental conditions. We further examine which leaf water isotope models best capture the influence of progressive enrichment on bulk needle water Δ18 O. Observed progressive enrichment was large and equal in magnitude across both species. The magnitude of this effect fluctuated seasonally in concert with vapour pressure deficit, but was static in the face of diurnal cycles in meteorological conditions. Despite large progressive enrichment, three variants of the C-G model reasonably successfully predicted bulk needle Δ18 O. Our results thus suggest that the presence of progressive enrichment does not impact the predictive success of C-G models, and instead yields new insight regarding the physiological and anatomical mechanisms that cause progressive isotope enrichment.

Ghosts of the past: how drought legacy effects shape forest functioning and carbon cycling.

Multi-year lags in tree drought recovery, termed 'drought legacy effects', are important for understanding the impacts of drought on forest ecosystems, including carbon (C) cycle feedbacks to climate change. Despite the ubiquity of lags in drought recovery, large uncertainties remain regarding the mechanistic basis of legacy effects and their importance for the C cycle. In this review, we identify the approaches used to study legacy effects, from tree rings to whole forests. We then discuss key knowledge gaps pertaining to the causes of legacy effects, and how the various mechanisms that may contribute these lags in drought recovery could have contrasting implications for the C cycle. Furthermore, we conduct a novel data synthesis and find that legacy effects differ drastically in both size and length across the US depending on if they are identified in tree rings versus gross primary productivity. Finally, we highlight promising approaches for future research to improve our capacity to model legacy effects and predict their impact on forest health. We emphasise that a holistic view of legacy effects - from tissues to whole forests - will advance our understanding of legacy effects and stimulate efforts to investigate drought recovery via experimental, observational and modelling approaches.

Non-structural carbohydrate pools not linked to hydraulic strategies or carbon supply in tree saplings during severe drought and subsequent recovery.

Non-structural carbohydrate (NSC) pools fluctuate based on the interplay between photosynthesis, demand from various carbon (C) sinks and tree hydraulic status. Thus, it has been hypothesized that tree species with isohydric stomatal control (i.e., trees that close stomata rapidly in response to drought) rely heavily on NSC pools to sustain metabolism, which can lead to negative physiological consequences such as C depletion. Here, we seek to use a species' degree of isohydry or anisohydry as a conceptual framework for understanding the interrelations between photosynthetic C supply, hydraulic damage and fluctuations in NSC pools. We conducted a 6-week experimental drought, followed by a 6-week recovery period, in a greenhouse on seven tree species that span the spectrum from isohydric to anisohydric. Throughout the experiment, we measured photosynthesis, hydraulic damage and NSC pools. Non-structural carbohydrate pools were remarkably stable across species and tissues-even highly isohydric species that drastically reduced C assimilation were able to maintain stored C. Despite these static NSC pools, we still inferred an important role for stored C during drought, as most species converted starches into sugars during water stress (and back again post-drought). Finally, we did not observe any linkages between C supply, hydraulic damage and NSC pools, indicating that NSC was maintained independent of variation in photosynthesis and hydraulic function. Our results advance the idea that C depletion is a rare phenomenon due to either active maintenance of NSC pools or sink limitation, and thus question the hypothesis that reductions in C assimilation necessarily lead to C depletion.

Linking drought legacy effects across scales: From leaves to tree rings to ecosystems.

Severe drought can cause lagged effects on tree physiology that negatively impact forest functioning for years. These "drought legacy effects" have been widely documented in tree-ring records and could have important implications for our understanding of broader scale forest carbon cycling. However, legacy effects in tree-ring increments may be decoupled from ecosystem fluxes due to (a) postdrought alterations in carbon allocation patterns; (b) temporal asynchrony between radial growth and carbon uptake; and (c) dendrochronological sampling biases. In order to link legacy effects from tree rings to whole forests, we leveraged a rich dataset from a Midwestern US forest that was severely impacted by a drought in 2012. At this site, we compiled tree-ring records, leaf-level gas exchange, eddy flux measurements, dendrometer band data, and satellite remote sensing estimates of greenness and leaf area before, during, and after the 2012 drought. After accounting for the relative abundance of tree species in the stand, we estimate that legacy effects led to ~10% reductions in tree-ring width increments in the year following the severe drought. Despite this stand-scale reduction in radial growth, we found that leaf-level photosynthesis, gross primary productivity (GPP), and vegetation greenness were not suppressed in the year following the 2012 drought. Neither temporal asynchrony between radial growth and carbon uptake nor sampling biases could explain our observations of legacy effects in tree rings but not in GPP. Instead, elevated leaf-level photosynthesis co-occurred with reduced leaf area in early 2013, indicating that resources may have been allocated away from radial growth in conjunction with postdrought upregulation of photosynthesis and repair of canopy damage. Collectively, our results indicate that tree-ring legacy effects were not observed in other canopy processes, and that postdrought canopy allocation could be an important mechanism that decouples tree-ring signals from GPP.

Anisohydric behavior linked to persistent hydraulic damage and delayed drought recovery across seven North American tree species.

The isohydry-anisohydry spectrum has become a popular way to characterize plant drought responses and recovery processes. Despite the proven utility of this framework for understanding the interconnected physiological changes plants undergo in response to water stress, new challenges have arisen pertaining to the traits and tradeoffs that underlie this concept. To test the utility of this framework for understanding hydraulic traits, drought physiology and recovery, we applied a 6 wk experimental soil moisture reduction to seven tree species followed by a 6 wk recovery period. Throughout, we measured hydraulic traits and monitored changes in gas exchange, leaf water potential, and hydraulic conductivity. Species' hydraulic traits were not coordinated, as some anisohydric species had surprisingly low resistance to embolism (P50 ) and negative safety margins. In addition to widespread hydraulic damage, these species also experienced reductions in photosynthesis and stem water potential during water stress, and delayed recovery time. Given that we observed no benefit of being anisohydric either during or after drought, our results indicate the need to reconsider the traits and tradeoffs that underlie anisohydric behavior, and to consider the environmental, biological and edaphic processes that could allow this strategy to flourish in forests.

Drought legacies are dependent on water table depth, wood anatomy and drought timing across the eastern US.

Severe droughts can impart long-lasting legacies on forest ecosystems through lagged effects that hinder tree recovery and suppress whole-forest carbon uptake. However, the local climatic and edaphic factors that interact to affect drought legacies in temperate forests remain unknown. Here, we pair a dataset of 143 tree ring chronologies across the mesic forests of the eastern US with historical climate and local soil properties. We found legacy effects to be widespread, the magnitude of which increased markedly in diffuse porous species, sites with deep water tables, and in response to late-season droughts (August-September). Using an ensemble of downscaled climate projections, we additionally show that our sites are projected to drastically increase in water deficit and drought frequency by the end of the century, potentially increasing the size of legacy effects by up to 65% and acting as a significant process shaping forest composition, carbon uptake and mortality.

Coarse roots prevent declines in whole-tree non-structural carbohydrate pools during drought in an isohydric and an anisohydric species.

Predicted increases in the frequency and severity of droughts have led to a renewed focus on how plants physiologically adjust to low water availability. A popular framework for understanding plant responses to drought characterizes species along a spectrum from isohydry to anisohydry based on their regulation of gas exchange and leaf water potential under drying conditions. One prediction that arises from this theory is that plant drought responses may hinge, in part, on their usage of non-structural carbohydrate (NSC) pools. For example, trees that respond to drought by closing stomates (i.e., isohydric) are predicted to deplete NSC reserves to maintain metabolism, whereas plants that keep stomata open during water stress (i.e., anisohydric), may show little change or even increases in NSC concentration. However, empirical tests of this theory largely rely on aboveground measurements of NSC, ignoring the potentially conflicting responses of root NSC pools. We sought to test these predictions by subjecting potted saplings of Quercus alba L. (an anisohydric species) and Liriodendron tulipifera L. (an isohydric species) to a 6 week experimental drought. We found that stem NSC concentrations were depleted in the isohydric L. tulipifera but maintained in the anisohydric Q. alba-as predicted. However, when scaled to whole-plant NSC content, the drought-induced decreases in stem NSCs in L. tulipifera were offset by increases in root NSCs (especially soluble sugars), resulting in no net change to whole-plant NSC content. Similarly, root sugars increased in Q. alba in response to drought. This increase was concurrent with declines in growth, suggesting a potential trade-off between allocation of photoassimilates to root sugars vs biomass during drought. Collectively, our results suggest that the responses of NSC in coarse roots can differ from stems, and indicate a prominent role of coarse roots in mitigating drought-induced declines in whole-tree NSC pools.

Soil microbial communities buffer physiological responses to drought stress in three hardwood species.

Trees possess myriad adaptations for coping with drought stress, but the extent to which their drought responses are influenced by interactions with soil microbes is poorly understood. To explore the role of microbes in mediating tree responses to drought stress, we exposed saplings of three species (Acer saccharum, Liriodendron tulipifera, and Quercus alba) to a four week experimental drought in mesocosms. Half of the pots were inoculated with a live soil slurry (i.e., a microbial inoculum derived from soils beneath the canopies of mature A. saccharum, L. tulipifera or Q. alba stands), while the other half of the pots received a sterile soil slurry. Soil microbes ameliorated drought stress in L. tulipifera by minimizing reductions in leaf water potential and by reducing photosynthetic declines. In A. saccharum, soil microbes reduced drought stress by lessening declines in leaf water potential, though these changes did not buffer the trees from declining photosynthetic rates. In Q. alba, soil microbes had no effects on leaf physiological parameters during drought stress. In all species, microbes had no significant effects on dynamic C allocation during drought stress, suggesting that microbial effects on plant physiology were unrelated to source-sink dynamics. Collectively, our results suggest that soil microbes have the potential to alter key parameters that are used to diagnose drought sensitivity (i.e., isohydry or anisohydry). To the extent that our results reflect dynamics occurring in forests, a revised perspective on plant hydraulic strategies that considers root-microbe interactions may lead to improved predictions of forest vulnerability to drought.