Exceptional heat and atmospheric dryness amplified losses of primary production during the 2020 U.S. Southwest hot drought.

Earth's ecosystems are increasingly threatened by "hot drought," which occurs when hot air temperatures coincide with precipitation deficits, intensifying the hydrological, physiological, and ecological effects of drought by enhancing evaporative losses of soil moisture (SM) and increasing plant stress due to higher vapor pressure deficit (VPD). Drought-induced reductions in gross primary production (GPP) exert a major influence on the terrestrial carbon sink, but the extent to which hotter and atmospherically drier conditions will amplify the effects of precipitation deficits on Earth's carbon cycle remains largely unknown. During summer and autumn 2020, the U.S. Southwest experienced one of the most intense hot droughts on record, with record-low precipitation and record-high air temperature and VPD across the region. Here, we use this natural experiment to evaluate the effects of hot drought on GPP and further decompose those negative GPP anomalies into their constituent meteorological and hydrological drivers. We found a 122 Tg C (>25%) reduction in GPP below the 2015-2019 mean, by far the lowest regional GPP over the Soil Moisture Active Passive satellite record. Roughly half of the estimated GPP loss was attributable to low SM (likely a combination of record-low precipitation and warming-enhanced evaporative depletion), but record-breaking VPD amplified the reduction of GPP, contributing roughly 40% of the GPP anomaly. Both air temperature and VPD are very likely to continue increasing over the next century, likely leading to more frequent and intense hot droughts and substantially enhancing drought-induced GPP reductions.

Temperature memory and non-structural carbohydrates mediate legacies of a hot drought in trees across the southwestern USA.

Trees are long-lived organisms that integrate climate conditions across years or decades to produce secondary growth. This integration process is sometimes referred to as 'climatic memory.' While widely perceived, the physiological processes underlying this temporal integration, such as the storage and remobilization of non-structural carbohydrates (NSC), are rarely explicitly studied. This is perhaps most apparent when considering drought legacies (perturbed post-drought growth responses to climate), and the physiological mechanisms underlying these lagged responses to climatic extremes. Yet, drought legacies are likely to become more common if warming climate brings more frequent drought. To quantify the linkages between drought legacies, climate memory and NSC, we measured tree growth (via tree ring widths) and NSC concentrations in three dominant species across the southwestern USA. We analyzed these data with a hierarchical mixed effects model to evaluate the time-scales of influence of past climate (memory) on tree growth. We then evaluated the role of climate memory and the degree to which variation in NSC concentrations were related to forward-predicted growth during the hot 2011-2012 drought and subsequent 4-year recovery period. Populus tremuloides exhibited longer climatic memory compared to either Pinus edulis or Juniperus osteosperma, but following the 2011-2012 drought, P. tremuloides trees with relatively longer memory of temperature conditions showed larger (more negative) drought legacies. Conversely, Pinus edulis trees with longer temperature memory had smaller (less negative) drought legacies. For both species, higher NSC concentrations followed more negative (larger) drought legacies, though the relevant NSC fraction differed between P. tremuloides and P. edulis. Our results suggest that differences in tree NSC are also imprinted upon tree growth responses to climate across long time scales, which also underlie tree resilience to increasingly frequent drought events under climate change.

Divergent responses of primary production to increasing precipitation variability in global drylands.

Interannual variability in precipitation has increased globally as climate warming intensifies. The increased variability impacts both terrestrial plant production and carbon (C) sequestration. However, mechanisms driving these changes are largely unknown. Here, we examined mechanisms underlying the response of aboveground net primary production (ANPP) to interannual precipitation variability in global drylands with mean annual precipitation (MAP) <500 mm year-1 , using a combined approach of data synthesis and process-based modeling. We found a hump-shaped response of ANPP to precipitation variability along the MAP gradient. The response was positive when MAP < ~300 mm year-1 and negative when MAP was higher than this threshold, with a positive peak at 140 mm year-1 . Transpiration and subsoil water content mirrored the response of ANPP to precipitation variability; evaporation responded negatively and water loss through runoff and drainage responded positively to precipitation variability. Mean annual temperature, soil type, and plant physiological traits all altered the magnitude but not the pattern of the response of ANPP to precipitation variability along the MAP gradient. By extrapolating to global drylands (<500 mm year-1  MAP), we estimated that ANPP would increase by 15.2 ± 6.0 Tg C year-1 in arid and hyper-arid lands and decrease by 2.1 ± 0.5 Tg C year-1 in dry sub-humid lands under future changes in interannual precipitation variability. Thus, increases in precipitation variability will enhance primary production in many drylands in the future.

Temporal controls on crown nonstructural carbohydrates in southwestern US tree species.

In trees, large uncertainties remain in how nonstructural carbohydrates (NSCs) respond to variation in water availability in natural, intact ecosystems. Variation in NSC pools reflects temporal fluctuations in supply and demand, as well as physiological coordination across tree organs in ways that differ across species and NSC fractions (e.g., soluble sugars vs starch). Using landscape-scale crown (leaves and twigs) NSC concentration measurements in three foundation tree species (Populus tremuloides, Pinus edulis, Juniperus osteosperma), we evaluated in situ, seasonal variation in NSC responses to moisture stress on three timescales: short-term (via predawn water potential), seasonal (via leaf δ13C) and annual (via current year's ring width index). Crown NSC responses to moisture stress appeared to depend on hydraulic strategy, where J. osteosperma appears to regulate osmotic potentials (via higher sugar concentrations), P. edulis NSC responses suggest respiratory depletion and P. tremuloides responses were consistent with direct sink limitations. We also show that overly simplistic models can mask seasonal and tissue variation in NSC responses, as well as strong interactions among moisture stress at different timescales. In general, our results suggest large seasonal variation in crown NSC concentrations reflecting the multiple cofunctions of NSCs in plant tissues, including storage, growth and osmotic regulation of hydraulically vulnerable leaves. We emphasize that crown NSC pool size cannot be viewed as a simple physiological metric of stress; in situ NSC dynamics are complex, varying temporally, across species, among NSC fractions and among tissue types.

Montane forest productivity across a semiarid climatic gradient.

High-elevation montane forests are disproportionately important to carbon sequestration in semiarid climates where low elevations are dry and characterized by low carbon density ecosystems. However, these ecosystems are increasingly threatened by climate change with seasonal implications for photosynthesis and forest growth. As a result, we leveraged eddy covariance data from six evergreen conifer forest sites in the semiarid western United States to extrapolate the status of carbon sequestration within a framework of projected warming and drying. At colder locations, the seasonal evolution of gross primary productivity (GPP) was characterized by a single broad maximum during the summer that corresponded to snow melt-derived moisture and a transition from winter dormancy to spring activity. Conversely, winter dormancy was transient at warmer locations, and GPP was responsive to both winter and summer precipitation such that two distinct GPP maxima were separated by a period of foresummer drought. This resulted in a predictable sequence of primary limiting factors to GPP beginning with air temperature in winter and proceeding to moisture and leaf area during the summer. Due to counteracting winter (positive) and summer (negative) GPP responses to warming, leaf area index and moisture availability were the best predictors of annual GPP differences across sites. Overall, mean annual GPP was greatest at the warmest site due to persistent vegetation photosynthetic activity throughout the winter. These results indicate that the trajectory of this region's carbon sequestration will be sensitive to reduced or delayed summer precipitation, especially if coupled to snow drought and earlier soil moisture recession, but summer precipitation changes remain highly uncertain. Given the demonstrated potential for seasonally offsetting responses to warming, we project that decadal semiarid montane forest carbon sequestration will remain relatively stable in the absence of severe disturbance.

Reevaluating growing season length controls on net ecosystem production in evergreen conifer forests.

Growing season length (GSL) is a key unifying concept in ecology that can be estimated from eddy covariance-derived estimates of net ecosystem production (NEP). Previous studies disagree on how increasing GSLs may affect NEP in evergreen coniferous forests, potentially due to the variety of methods used to quantify GSL from NEP. We calculated GSL and GSL-NEP regressions at eleven evergreen conifer sites across a broad climatic gradient in western North America using three common approaches: (1) variable length (3-7 days) regressions of day of year versus NEP, (2) a smoothed threshold approach, and (3) the carbon uptake period, followed by a new approach of a method-averaged ensemble. The GSL and the GSL-NEP relationship differed among methods, resulting in linear relationships with variable sign, slope, and statistical significance. For all combinations of sites and methods, the GSL explained between 6% and 82% of NEP with p-values ranging from 0.45 to < 0.01. These results demonstrate the variability among GSL methods and the importance of selecting an appropriate method to accurately project the ecosystem carbon cycling response to longer growing seasons in the future. To encourage this approach in future studies, we outline a series of best practices for GSL method selection depending on research goals and the annual NEP dynamics of the study site(s). These results contribute to understanding growing season dynamics at ecosystem and continental scales and underscore the potential for methodological variability to influence forecasts of the evergreen conifer forest response to climate variability.

Climate sensitivity functions and net primary production: A framework for incorporating climate mean and variability.

Understanding controls on net primary production (NPP) has been a long-standing goal in ecology. Climate is a well-known control on NPP, although the temporal differences among years within a site are often weaker than the spatial pattern of differences across sites. Climate sensitivity functions describe the relationship between an ecological response (e.g., NPP) and both the mean and variance of its climate driver (e.g., aridity index), providing a novel framework for understanding how climate trends in both mean and variance vary with NPP over time. Nonlinearities in these functions predict whether an increase in climate variance will have a positive effect (convex nonlinearity) or negative effect (concave nonlinearity) on NPP. The influence of climate variance may be particularly intense at ecosystem transition zones, if species reach physiological thresholds that create nonlinearities at these ecotones. Long-term data collected at the confluence of three dryland ecosystems in central New Mexico revealed that each ecosystem exhibited a unique climate sensitivity function that was consistent with long-term vegetation change occurring at their ecotones. Our analysis suggests that rising temperatures in drylands could alter the nonlinearities that determine the relative costs and benefits of variance in precipitation for primary production.

CO2 exchange and evapotranspiration across dryland ecosystems of southwestern North America.

Global-scale studies suggest that dryland ecosystems dominate an increasing trend in the magnitude and interannual variability of the land CO2 sink. However, such analyses are poorly constrained by measured CO2 exchange in drylands. Here we address this observation gap with eddy covariance data from 25 sites in the water-limited Southwest region of North America with observed ranges in annual precipitation of 100-1000 mm, annual temperatures of 2-25°C, and records of 3-10 years (150 site-years in total). Annual fluxes were integrated using site-specific ecohydrologic years to group precipitation with resulting ecosystem exchanges. We found a wide range of carbon sink/source function, with mean annual net ecosystem production (NEP) varying from -350 to +330 gCm-2 across sites with diverse vegetation types, contrasting with the more constant sink typically measured in mesic ecosystems. In this region, only forest-dominated sites were consistent carbon sinks. Interannual variability of NEP, gross ecosystem production (GEP), and ecosystem respiration (Reco ) was larger than for mesic regions, and half the sites switched between functioning as C sinks/C sources in wet/dry years. The sites demonstrated coherent responses of GEP and NEP to anomalies in annual evapotranspiration (ET), used here as a proxy for annually available water after hydrologic losses. Notably, GEP and Reco were negatively related to temperature, both interannually within site and spatially across sites, in contrast to positive temperature effects commonly reported for mesic ecosystems. Models based on MODIS satellite observations matched the cross-site spatial pattern in mean annual GEP but consistently underestimated mean annual ET by ~50%. Importantly, the MODIS-based models captured only 20-30% of interannual variation magnitude. These results suggest the contribution of this dryland region to variability of regional to global CO2 exchange may be up to 3-5 times larger than current estimates.

Plant, microbial and ecosystem carbon use efficiencies interact to stabilize microbial growth as a fraction of gross primary production.

The carbon use efficiency of plants (CUEa ) and microorganisms (CUEh ) determines rates of biomass turnover and soil carbon sequestration. We evaluated the hypothesis that CUEa and CUEh counterbalance at a large scale, stabilizing microbial growth (µ) as a fraction of gross primary production (GPP). Collating data from published studies, we correlated annual CUEa , estimated from satellite imagery, with locally determined soil CUEh for 100 globally distributed sites. Ecosystem CUEe , the ratio of net ecosystem production (NEP) to GPP, was estimated for each site using published models. At the ecosystem scale, CUEa and CUEh were inversely related. At the global scale, the apparent temperature sensitivity of CUEh with respect to mean annual temperature (MAT) was similar for organic and mineral soils (0.029°C-1 ). CUEa and CUEe were inversely related to MAT, with apparent sensitivities of -0.009 and -0.032°C-1 , respectively. These trends constrain the ratio µ : GPP (= (CUEa  × CUEh )/(1 - CUEe )) with respect to MAT by counterbalancing the apparent temperature sensitivities of the component processes. At the ecosystem scale, the counterbalance is effected by modulating soil organic matter stocks. The results suggest that a µ : GPP value of c. 0.13 is a homeostatic steady state for ecosystem carbon fluxes at a large scale.

Warm spring reduced carbon cycle impact of the 2012 US summer drought.

The global terrestrial carbon sink offsets one-third of the world's fossil fuel emissions, but the strength of this sink is highly sensitive to large-scale extreme events. In 2012, the contiguous United States experienced exceptionally warm temperatures and the most severe drought since the Dust Bowl era of the 1930s, resulting in substantial economic damage. It is crucial to understand the dynamics of such events because warmer temperatures and a higher prevalence of drought are projected in a changing climate. Here, we combine an extensive network of direct ecosystem flux measurements with satellite remote sensing and atmospheric inverse modeling to quantify the impact of the warmer spring and summer drought on biosphere-atmosphere carbon and water exchange in 2012. We consistently find that earlier vegetation activity increased spring carbon uptake and compensated for the reduced uptake during the summer drought, which mitigated the impact on net annual carbon uptake. The early phenological development in the Eastern Temperate Forests played a major role for the continental-scale carbon balance in 2012. The warm spring also depleted soil water resources earlier, and thus exacerbated water limitations during summer. Our results show that the detrimental effects of severe summer drought on ecosystem carbon storage can be mitigated by warming-induced increases in spring carbon uptake. However, the results also suggest that the positive carbon cycle effect of warm spring enhances water limitations and can increase summer heating through biosphere-atmosphere feedbacks.

Terrestrial carbon balance in a drier world: the effects of water availability in southwestern North America.

Global modeling efforts indicate semiarid regions dominate the increasing trend and interannual variation of net CO2 exchange with the atmosphere, mainly driven by water availability. Many semiarid regions are expected to undergo climatic drying, but the impacts on net CO2 exchange are poorly understood due to limited semiarid flux observations. Here we evaluated 121 site-years of annual eddy covariance measurements of net and gross CO2 exchange (photosynthesis and respiration), precipitation, and evapotranspiration (ET) in 21 semiarid North American ecosystems with an observed range of 100 - 1000 mm in annual precipitation and records of 4-9 years each. In addition to evaluating spatial relationships among CO2 and water fluxes across sites, we separately quantified site-level temporal relationships, representing sensitivity to interannual variation. Across the climatic and ecological gradient, photosynthesis showed a saturating spatial relationship to precipitation, whereas the photosynthesis-ET relationship was linear, suggesting ET was a better proxy for water available to drive CO2 exchanges after hydrologic losses. Both photosynthesis and respiration showed similar site-level sensitivity to interannual changes in ET among the 21 ecosystems. Furthermore, these temporal relationships were not different from the spatial relationships of long-term mean CO2 exchanges with climatic ET. Consequently, a hypothetical 100-mm change in ET, whether short term or long term, was predicted to alter net ecosystem production (NEP) by 64 gCm(-2) yr(-1). Most of the unexplained NEP variability was related to persistent, site-specific function, suggesting prioritization of research on slow-changing controls. Common temporal and spatial sensitivity to water availability increases our confidence that site-level responses to interannual weather can be extrapolated for prediction of CO2 exchanges over decadal and longer timescales relevant to societal response to climate change.

Root-associated fungal community response to drought-associated changes in vegetation community.

Recent droughts in southwestern USA have led to large-scale mortality of piñon (Pinus edulis) in piñon-juniper woodlands. Piñon mortality alters soil moisture, nutrient and carbon availability, which could affect the root-associated fungal (RAF) communities and therefore the fitness of the remaining plants. We collected fine root samples at a piñon-juniper woodland and a juniper savannah site in central New Mexico. Roots were collected from piñon and juniper (Juniperus monosperma) trees whose nearest neighbors were live piñon, live juniper or dead piñon. RAF communities were analyzed by 454 pyrosequencing of the universal fungal ITS region. The most common taxa were Hypocreales and Chaetothyriales. More than 10% of ITS sequences could not be assigned taxonomy at the phylum level. Two of the unclassified OTUs significantly differed between savanna and woodland, had few like sequences in GenBank and formed new fungal clades with other unclassified RAF from arid plants, highlighting how little study has been done on the RAF of arid ecosystems. Plant host or neighbor did not affect RAF community composition. However, there was a significant difference between RAF communities from woodland vs. savanna, indicating that abiotic factors such as temperature and aridity might be more important in structuring these RAF communities than biotic factors such as plant host or neighbor identity. Ectomycorrhizal fungi (EM) were present in juniper as well as piñon in the woodland site, in contrast with previous research, but did not occur in juniper savanna, suggesting a potential shared EM network with juniper. RAF richness was lower in hosts that were neighbors of the opposite host. This may indicate competitive exclusion between fungi from different hosts. Characterizing these communities and their responses to environment and plant neighborhood is a step toward understanding the effects of drought on a biome that spans 19,000,000 ha of southwestern USA.

Supply and demand processes as controls over needle monoterpene synthesis and concentration in Douglas fir [Pseudotsuga menziesii (Mirb.) Franco].

We measured the relative control that resource availability (as a supply-side control) and wounding (as a demand-side control) exert on patterns of monoterpene synthesis and concentration in Douglas fir [Pseudotsuga menziesii (Mirb.) Franco] needles. While supply-side controls should alter monoterpene production due to changes in the availability of substrate (carbohydrates), demand-side controls alter the need for a defensive product. We examined these relationships by measuring constitutive (preformed) and wound-induced rates of monoterpene synthesis and pool sizes in trees grown under ambient and elevated (ambient +200 µmol mol-1) CO2, ambient and elevated (ambient +4°C) temperature, and in trees grown under four levels of nitrogen fertilization (0, 50, 100 and 200 µg g-1 N by weight). Monoterpene pool size decreased at elevated CO2, increased at elevated temperature and did not change in response to nitrogen fertilization. Overall, we did not find that foliar nitrogen, carbon balance, or rate of monoterpene synthesis alone were consistent predictors of monoterpene concentration in current-year Douglas fir needles. In addition, despite a wound-induced decrease in monoterpene pool size, we found no evidence for induction of monoterpene synthesis in response to wounding. The influence of either resource availability or wounding on rates of monoterpene synthesis or accumulation cannot be explained by traditional supply-side or demand-side controls. We conclude that monoterpene synthesis in first-year Douglas fir needles is controlled by fairly conservative genetic mechanisms and is influenced more by past selection than by current resource state.

Patterns of induced and constitutive monoterpene production in conifer needles in relation to insect herbivory.

Studies were conducted to determine whether herbivore-induced synthesis of monoterpenes occurs in the needles of ponderosa pine (Pinus ponderosa Lawson), lodgepole pine (P. contorta Douglas var. latifolia Engelmann), white fir (Abies concolor Lindl. and Gordon) and Engelmann spruce [Picea engelmanii (Parry) Engelm.]. In the needles of all species except Engelmann spruce, simulated herbivory significantly induced the activity of monoterpene cyclases 4-8 days after wounding. In ponderosa pine, real herbivory by last-instar tiger moth larvae (Halisdota ingens Hy. Edwards: Lepidoptera) induced a significantly larger response (4.5-fold increase in monoterpene cyclase activity) than did simulated herbivory (2.5-fold increase). To our knowledge, this is the first report of herbivore-induced increases in monoterpene synthesis in needle tissue. Despite this increase in monoterpene synthesis, we observed no significant increase in total monoterpene pool size in wounded needles compared to controls. Large increases in the rate of monoterpene volatilization were observed in response to wounding. We conclude that the volatile losses caused by tissue damage compensate for herbivore-induced monoterpene synthesis, resulting in no change in pool size. Tiger moth larvae consume ponderosa pine needles in a pattern that begins at the tip and proceeds downward to midway along the needle, at which point they move to an undamaged needle. Constitutive monoterpene concentrations and monoterpene cyclase activities were highest in the lower half of ponderosa pine needles. The monoterpene profile also differed between the upper and lower needle halves, the lower half possessing an additional one to four monoterpene forms. We propose that the increasing gradient in monoterpene concentrations and number of monoterpenes along the needle from tip to base deters feeding beyond the midway point and provides time for the induction of increased cyclase activity and production of new monoterpenes. The induction of new monoterpene synthesis may have a role in replacing monoterpenes lost through damage-induced volatilization and preventing extreme compromise of the constitutive defense system.