The impacts of rising vapour pressure deficit in natural and managed ecosystems.

An exponential rise in the atmospheric vapour pressure deficit (VPD) is among the most consequential impacts of climate change in terrestrial ecosystems. Rising VPD has negative and cascading effects on nearly all aspects of plant function including photosynthesis, water status, growth and survival. These responses are exacerbated by land-atmosphere interactions that couple VPD to soil water and govern the evolution of drought, affecting a range of ecosystem services including carbon uptake, biodiversity, the provisioning of water resources and crop yields. However, despite the global nature of this phenomenon, research on how to incorporate these impacts into resilient management regimes is largely in its infancy, due in part to the entanglement of VPD trends with those of other co-evolving climate drivers. Here, we review the mechanistic bases of VPD impacts at a range of spatial scales, paying particular attention to the independent and interactive influence of VPD in the context of other environmental changes. We then evaluate the consequences of these impacts within key management contexts, including water resources, croplands, wildfire risk mitigation and management of natural grasslands and forests. We conclude with recommendations describing how management regimes could be altered to mitigate the otherwise highly deleterious consequences of rising VPD.

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.

A framework for incorporating ecology into Earth System Models is urgently needed.

This commentary considers the benefits of a new framework to incorporate ecological processes in Earth System Models (ESMs) to both Earth system science and to ecology. Adding ecological processes to ESMs skillfully will likely improve the long-term performance of these models. The rigor required to achieve this will prompt ecologists to test complex ecological hypotheses on regional and global scales. Some candidate processes are suggested.

Precipitation alters the CO2 effect on water-use efficiency of temperate forests.

Increasing water-use efficiency (WUE), the ratio of carbon gain to water loss, is a key mechanism that enhances carbon uptake by terrestrial vegetation under rising atmospheric CO2 (ca ). Existing theory and empirical evidence suggest a proportional WUE increase in response to rising ca as plants maintain a relatively constant ratio between the leaf intercellular (ci ) and ambient (ca ) partial CO2 pressure (ci /ca ). This has been hypothesized as the main driver of the strengthening of the terrestrial carbon sink over the recent decades. However, proportionality may not characterize CO2 effects on WUE on longer time-scales and the role of climate in modulating these effects is uncertain. Here, we evaluate long-term WUE responses to ca and climate from 1901 to 2012 CE by reconstructing intrinsic WUE (iWUE, the ratio of photosynthesis to stomatal conductance) using carbon isotopes in tree rings across temperate forests in the northeastern USA. We show that iWUE increased steadily from 1901 to 1975 CE but remained constant thereafter despite continuously rising ca . This finding is consistent with a passive physiological response to ca and coincides with a shift to significantly wetter conditions across the region. Tree physiology was driven by summer moisture at multi-decadal time-scales and did not maintain a constant ci /ca in response to rising ca indicating that a point was reached where rising CO2 had a diminishing effect on tree iWUE. Our results challenge the mechanism, magnitude, and persistence of CO2 's effect on iWUE with significant implications for projections of terrestrial productivity under a changing climate.

Integrating the evidence for a terrestrial carbon sink caused by increasing atmospheric CO2.

Atmospheric carbon dioxide concentration ([CO2 ]) is increasing, which increases leaf-scale photosynthesis and intrinsic water-use efficiency. These direct responses have the potential to increase plant growth, vegetation biomass, and soil organic matter; transferring carbon from the atmosphere into terrestrial ecosystems (a carbon sink). A substantial global terrestrial carbon sink would slow the rate of [CO2 ] increase and thus climate change. However, ecosystem CO2 responses are complex or confounded by concurrent changes in multiple agents of global change and evidence for a [CO2 ]-driven terrestrial carbon sink can appear contradictory. Here we synthesize theory and broad, multidisciplinary evidence for the effects of increasing [CO2 ] (iCO2 ) on the global terrestrial carbon sink. Evidence suggests a substantial increase in global photosynthesis since pre-industrial times. Established theory, supported by experiments, indicates that iCO2 is likely responsible for about half of the increase. Global carbon budgeting, atmospheric data, and forest inventories indicate a historical carbon sink, and these apparent iCO2 responses are high in comparison to experiments and predictions from theory. Plant mortality and soil carbon iCO2 responses are highly uncertain. In conclusion, a range of evidence supports a positive terrestrial carbon sink in response to iCO2 , albeit with uncertain magnitude and strong suggestion of a role for additional agents of global change.

Climate sensitivity of understory trees differs from overstory trees in temperate mesic forests.

The response of understory trees to climate variability is key to understanding current and future forest dynamics. However, analyses of climatic effects on tree growth have primarily focused on the upper canopy, leaving understory dynamics unresolved. We analyzed differences in climate sensitivity based on canopy position of four common tree species (Acer rubrum, Fagus grandifolia, Quercus rubra, and Tsuga canadensis) using growth information from 1,084 trees across eight sites in the northeastern United States. Effects of canopy position on climate response varied, but were significant and often nonlinear, for all four species. Compared to overstory trees, understory trees showed stronger reductions in growth at high temperatures and varied shifts in precipitation response. This contradicts the prevailing assumption that climate responses, particularly to temperature, of understory trees are buffered by the overstory. Forest growth trajectories are uncertain in compositionally and structurally complex forests, and future demography and regeneration dynamics may be misinferred if not all canopy levels are represented in future forecasts.

Topography influences species-specific patterns of seasonal primary productivity in a semiarid montane forest.

Semiarid forests in the southwestern USA are generally restricted to mountain regions where complex terrain adds to the challenge of characterizing stand productivity. Among the heterogeneous features of these ecosystems, topography represents an important control on system-level processes including snow accumulation and melt. This basic relationship between geology and hydrology affects radiation and water balances within the forests, with implications for canopy structure and function across a range of spatial scales. In this study, we quantify the effect of topographic aspect on primary productivity by observing the response of two codominant native tree species to seasonal changes in the timing and magnitude of energy and water inputs throughout a montane headwater catchment in Arizona, USA. On average, soil moisture on north-facing aspects remained higher during the spring and early summer compared with south-facing aspects. Repeated measurements of net carbon assimilation (Anet) showed that Pinus ponderosa C. Lawson was sensitive to this difference, while Pseudotsuga menziesii (Mirb.) Franco was not. Irrespective of aspect, we observed seasonally divergent patterns at the species level where P. ponderosa maintained significantly greater Anet into the fall despite more efficient water use by P. menziesii individuals during that time. As a result, this study at the southern extent of the geographical P. menziesii distribution suggests that this species could increase water-use efficiency as a response to future warming and/or drying, but at lower rates of production relative to the more drought-adapted P. ponderosa. At the sub-landscape scale, opposing aspects served as a mesocosm of current versus anticipated climate conditions. In this way, these results also constrain the potential for changing carbon sequestration patterns from Pinus-dominated landscapes due to forecasted changes in seasonal moisture availability.

High productivity in hybrid-poplar plantations without isoprene emission to the atmosphere.

Hybrid-poplar tree plantations provide a source for biofuel and biomass, but they also increase forest isoprene emissions. The consequences of increased isoprene emissions include higher rates of tropospheric ozone production, increases in the lifetime of methane, and increases in atmospheric aerosol production, all of which affect the global energy budget and/or lead to the degradation of air quality. Using RNA interference (RNAi) to suppress isoprene emission, we show that this trait, which is thought to be required for the tolerance of abiotic stress, is not required for high rates of photosynthesis and woody biomass production in the agroforest plantation environment, even in areas with high levels of climatic stress. Biomass production over 4 y in plantations in Arizona and Oregon was similar among genetic lines that emitted or did not emit significant amounts of isoprene. Lines that had substantially reduced isoprene emission rates also showed decreases in flavonol pigments, which reduce oxidative damage during extremes of abiotic stress, a pattern that would be expected to amplify metabolic dysfunction in the absence of isoprene production in stress-prone climate regimes. However, compensatory increases in the expression of other proteomic components, especially those associated with the production of protective compounds, such as carotenoids and terpenoids, and the fact that most biomass is produced prior to the hottest and driest part of the growing season explain the observed pattern of high biomass production with low isoprene emission. Our results show that it is possible to reduce the deleterious influences of isoprene on the atmosphere, while sustaining woody biomass production in temperate agroforest plantations.

Constraining estimates of terrestrial carbon uptake: new opportunities using long-term satellite observations and data assimilation.

The response of terrestrial carbon uptake to increasing atmospheric [CO2 ], that is the CO2 fertilization effect (CFE), remains a key area of uncertainty in carbon cycle science. Here we provide a perspective on how satellite observations could be better used to understand and constrain CFE. We then highlight data assimilation (DA) as an effective way to reconcile different satellite datasets and systematically constrain carbon uptake trends in Earth System Models. As a proof-of-concept, we show that joint DA of multiple independent satellite datasets reduced model ensemble error by better constraining unobservable processes and variables, including those directly impacted by CFE. DA of multiple satellite datasets offers a powerful technique that could improve understanding of CFE and enable more accurate forecasts of terrestrial carbon uptake.

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.

Beyond greenness: Detecting temporal changes in photosynthetic capacity with hyperspectral reflectance data.

Earth's future carbon balance and regional carbon exchange dynamics are inextricably linked to plant photosynthesis. Spectral vegetation indices are widely used as proxies for vegetation greenness and to estimate state variables such as vegetation cover and leaf area index. However, the capacity of green leaves to take up carbon can change throughout the season. We quantify photosynthetic capacity as the maximum rate of RuBP carboxylation (Vcmax) and regeneration (Jmax). Vcmax and Jmax vary within-season due to interactions between ontogenetic processes and meteorological variables. Remote sensing-based estimation of Vcmax and Jmax using leaf reflectance spectra is promising, but temporal variation in relationships between these key determinants of photosynthetic capacity, leaf reflectance spectra, and the models that link these variables has not been evaluated. To address this issue, we studied hybrid poplar (Populus spp.) during a 7-week mid-summer period to quantify seasonally-dynamic relationships between Vcmax, Jmax, and leaf spectra. We compared in situ estimates of Vcmax and Jmax from gas exchange measurements to estimates of Vcmax and Jmax derived from partial least squares regression (PLSR) and fresh-leaf reflectance spectroscopy. PLSR models were robust despite dynamic temporal variation in Vcmax and Jmax throughout the study period. Within-population variation in plant stress modestly reduced PLSR model predictive capacity. Hyperspectral vegetation indices were well-correlated to Vcmax and Jmax, including the widely-used Normalized Difference Vegetation Index. Our results show that hyperspectral estimation of plant physiological traits using PLSR may be robust to temporal variation. Additionally, hyperspectral vegetation indices may be sufficient to detect temporal changes in photosynthetic capacity in contexts similar to those studied here. Overall, our results highlight the potential for hyperspectral remote sensing to estimate determinants of photosynthetic capacity during periods with dynamic temporal variations related to seasonality and plant stress, thereby improving estimates of plant productivity and characterization of the associated carbon budget.

Emergent climate and CO2 sensitivities of net primary productivity in ecosystem models do not agree with empirical data in temperate forests of eastern North America.

Ecosystem models show divergent responses of the terrestrial carbon cycle to global change over the next century. Individual model evaluation and multimodel comparisons with data have largely focused on individual processes at subannual to decadal scales. Thus far, data-based evaluations of emergent ecosystem responses to climate and CO2 at multidecadal and centennial timescales have been rare. We compared the sensitivity of net primary productivity (NPP) to temperature, precipitation, and CO2 in ten ecosystem models with the sensitivities found in tree-ring reconstructions of NPP and raw ring-width series at six temperate forest sites. These model-data comparisons were evaluated at three temporal extents to determine whether the rapid, directional changes in temperature and CO2 in the recent past skew our observed responses to multiple drivers of change. All models tested here were more sensitive to low growing season precipitation than tree-ring NPP and ring widths in the past 30 years, although some model precipitation responses were more consistent with tree rings when evaluated over a full century. Similarly, all models had negative or no response to warm-growing season temperatures, while tree-ring data showed consistently positive effects of temperature. Although precipitation responses were least consistent among models, differences among models to CO2 drive divergence and ensemble uncertainty in relative change in NPP over the past century. Changes in forest composition within models had no effect on climate or CO2 sensitivity. Fire in model simulations reduced model sensitivity to climate and CO2 , but only over the course of multiple centuries. Formal evaluation of emergent model behavior at multidecadal and multicentennial timescales is essential to reconciling model projections with observed ecosystem responses to past climate change. Future evaluation should focus on improved representation of disturbance and biomass change as well as the feedbacks with moisture balance and CO2 in individual models.

Interactions between temperature and intercellular CO2 concentration in controlling leaf isoprene emission rates.

Plant isoprene emissions have been linked to several reaction pathways involved in atmospheric photochemistry. Evidence exists from a limited set of past observations that isoprene emission rate (Is ) decreases as a function of increasing atmospheric CO2 concentration, and that increased temperature suppresses the CO2 effect. We studied interactions between intercellular CO2 concentration (Ci ) and temperature as they affect Is in field-grown hybrid poplar trees in one of the warmest climates on earth - the Sonoran Desert of the southwestern United States. We observed an unexpected midsummer downregulation of Is despite the persistence of relatively high temperatures. High temperature suppression of the Is :Ci relation occurred at all times during the growing season, but sensitivity of Is to increased Ci was greatest during the midsummer period when Is was lowest. We interpret the seasonal downregulation of Is and increased sensitivity of Is to Ci as being caused by weather changes associated with the onset of a regional monsoon system. Our observations on the temperature suppression of the Is :Ci relation are best explained by the existence of a small pool of chloroplastic inorganic phosphate, balanced by several large, connected metabolic fluxes, which together, determine the Ci and temperature dependencies of phosphoenolpyruvate import into the chloroplast.

Carbon isotopic composition of forest soil respiration in the decade following bark beetle and stem girdling disturbances in the Rocky Mountains.

Bark beetle outbreaks are widespread in western North American forests, reducing primary productivity and transpiration, leading to forest mortality across large areas and altering ecosystem carbon cycling. Here the carbon isotope composition (δ(13) C) of soil respiration (δJ ) was monitored in the decade after disturbance for forests affected naturally by mountain pine beetle infestation and artificially by stem girdling. The seasonal mean δJ changed along both chronosequences. We found (a) enrichment of δJ relative to controls (<1 ‰) in near-surface soils in the first 2 years after disturbance; (b) depletion (1‰ or no change) during years 3-7; and (c) a second period of enrichment (1-2‰) in years 8-10. Results were consistent with isotopic patterns associated with the gradual death and decomposition of rhizosphere organisms, fine roots, conifer needles and woody roots and debris over the course of a decade after mortality. Finally, δJ was progressively more (13) C-depleted deeper in the soil than near the surface, while the bulk soil followed the well-established pattern of (13) C-enrichment at depth. Overall, differences in δJ between mortality classes (<1‰) and soil depths (<3‰) were smaller than variability within a class or depth over a season (up to 6‰).

Changes in soil biogeochemistry following disturbance by girdling and mountain pine beetles in subalpine forests.

A recent unprecedented epidemic of beetle-induced tree mortality has occurred in the lodgepole pine forests of Western North America. Here, we present the results of studies in two subalpine forests in the Rocky Mountains, one that experienced natural pine beetle disturbance and one that experienced simulated disturbance imposed through bole girdling. We assessed changes to soil microclimate and biogeochemical pools in plots representing different post-disturbance chronosequences. High plot tree mortality, whether due to girdling or beetle infestation, caused similar alterations in soil nutrient pools. During the first 4 years after disturbance, sharp declines were observed in the soil dissolved organic carbon (DOC) concentration (45-51 %), microbial biomass carbon concentration (33-39 %), dissolved organic nitrogen (DON) concentration (31-42%), and inorganic phosphorus (PO4(3-)) concentration (53-55%). Five to six years after disturbance, concentrations of DOC, DON, and PO4(3-) recovered to 71-140 % of those measured in undisturbed plots. Recovery was coincident with observed increases in litter depth and the sublitter, soil O-horizon. During the 4 years following disturbance, soil ammonium, but not nitrate, increased to 2-3 times the levels measured in undisturbed plots. Microbial biomass N increased in plots where increased ammonium was available. Our results show that previously observed declines in soil respiration following beetle-induced disturbance are accompanied by losses in key soil nutrients. Recovery of the soil nutrient pool occurs only after several years following disturbance, and is correlated with progressive mineralization of dead tree litter.

A tree-ring perspective on the terrestrial carbon cycle.

Tree-ring records can provide valuable information to advance our understanding of contemporary terrestrial carbon cycling and to reconstruct key metrics in the decades preceding monitoring data. The growing use of tree rings in carbon-cycle research is being facilitated by increasing recognition of reciprocal benefits among research communities. Yet, basic questions persist regarding what tree rings represent at the ecosystem level, how to optimally integrate them with other data streams, and what related challenges need to be overcome. It is also apparent that considerable unexplored potential exists for tree rings to refine assessments of terrestrial carbon cycling across a range of temporal and spatial domains. Here, we summarize recent advances and highlight promising paths of investigation with respect to (1) growth phenology, (2) forest productivity trends and variability, (3) CO2 fertilization and water-use efficiency, (4) forest disturbances, and (5) comparisons between observational and computational forest productivity estimates. We encourage the integration of tree-ring data: with eddy-covariance measurements to investigate carbon allocation patterns and water-use efficiency; with remotely sensed observations to distinguish the timing of cambial growth and leaf phenology; and with forest inventories to develop continuous, annually-resolved and long-term carbon budgets. In addition, we note the potential of tree-ring records and derivatives thereof to help evaluate the performance of earth system models regarding the simulated magnitude and dynamics of forest carbon uptake, and inform these models about growth responses to (non-)climatic drivers. Such efforts are expected to improve our understanding of forest carbon cycling and place current developments into a long-term perspective.

Persistent reduced ecosystem respiration after insect disturbance in high elevation forests.

Amid a worldwide increase in tree mortality, mountain pine beetles (Dendroctonus ponderosae Hopkins) have led to the death of billions of trees from Mexico to Alaska since 2000. This is predicted to have important carbon, water and energy balance feedbacks on the Earth system. Counter to current projections, we show that on a decadal scale, tree mortality causes no increase in ecosystem respiration from scales of several square metres up to an 84 km(2) valley. Rather, we found comparable declines in both gross primary productivity and respiration suggesting little change in net flux, with a transitory recovery of respiration 6-7 years after mortality associated with increased incorporation of leaf litter C into soil organic matter, followed by further decline in years 8-10. The mechanism of the impact of tree mortality caused by these biotic disturbances is consistent with reduced input rather than increased output of carbon.

Increases in the flux of carbon belowground stimulate nitrogen uptake and sustain the long-term enhancement of forest productivity under elevated CO2.

The earth's future climate state is highly dependent upon changes in terrestrial C storage in response to rising concentrations of atmospheric CO2. Here we show that consistently enhanced rates of net primary production (NPP) are sustained by a C-cascade through the root-microbe-soil system; increases in the flux of C belowground under elevated CO2 stimulated microbial activity, accelerated the rate of soil organic matter decomposition and stimulated tree uptake of N bound to this SOM. This process set into motion a positive feedback maintaining greater C gain under elevated CO2 as a result of increases in canopy N content and higher photosynthetic N-use efficiency. The ecosystem-level consequence of the enhanced requirement for N and the exchange of plant C for N belowground is the dominance of C storage in tree biomass but the preclusion of a large C sink in the soil.