Carbon starvation following a decade of experimental drought consumes old reserves in Pinus edulis.

Shifts in the age or turnover time of non-structural carbohydrates (NSC) may underlie changes in tree growth under long-term increases in drought stress associated with climate change. But NSC responses to drought are challenging to quantify, due in part to large NSC stores in trees and subsequently long response times of NSC to climate variation. We measured NSC age (Δ14 C) along with a suite of ecophysiological metrics in Pinus edulis trees experiencing either extreme short-term drought (-90% ambient precipitation plot, 2020-2021) or a decade of severe drought (-45% plot, 2010-2021). We tested the hypothesis that carbon starvation - consumption exceeding synthesis and storage - increases the age of sapwood NSC. One year of extreme drought had no impact on NSC pool size or age, despite significant reductions in predawn water potential, photosynthetic rates/capacity, and twig and needle growth. By contrast, long-term drought halved the age of the sapwood NSC pool, coupled with reductions in sapwood starch concentrations (-75%), basal area increment (-39%), and bole respiration rates (-28%). Our results suggest carbon starvation takes time, as tree carbon reserves appear resilient to extreme disturbance in the short term. However, after a decade of drought, trees apparently consumed old stored NSC to support metabolism.

COSORE: A community database for continuous soil respiration and other soil-atmosphere greenhouse gas flux data.

Globally, soils store two to three times as much carbon as currently resides in the atmosphere, and it is critical to understand how soil greenhouse gas (GHG) emissions and uptake will respond to ongoing climate change. In particular, the soil-to-atmosphere CO2 flux, commonly though imprecisely termed soil respiration (RS ), is one of the largest carbon fluxes in the Earth system. An increasing number of high-frequency RS measurements (typically, from an automated system with hourly sampling) have been made over the last two decades; an increasing number of methane measurements are being made with such systems as well. Such high frequency data are an invaluable resource for understanding GHG fluxes, but lack a central database or repository. Here we describe the lightweight, open-source COSORE (COntinuous SOil REspiration) database and software, that focuses on automated, continuous and long-term GHG flux datasets, and is intended to serve as a community resource for earth sciences, climate change syntheses and model evaluation. Contributed datasets are mapped to a single, consistent standard, with metadata on contributors, geographic location, measurement conditions and ancillary data. The design emphasizes the importance of reproducibility, scientific transparency and open access to data. While being oriented towards continuously measured RS , the database design accommodates other soil-atmosphere measurements (e.g. ecosystem respiration, chamber-measured net ecosystem exchange, methane fluxes) as well as experimental treatments (heterotrophic only, etc.). We give brief examples of the types of analyses possible using this new community resource and describe its accompanying R software package.

Whole-tree nonstructural carbohydrate storage and seasonal dynamics in five temperate species.

Despite the importance of nonstructural carbohydrates (NSC) for growth and survival in woody plants, we know little about whole-tree NSC storage. The conventional theory suggests that NSC reserves will increase over the growing season and decrease over the dormant season. Here, we compare storage in five temperate tree species to determine the size and seasonal fluctuation of whole-tree total NSC pools as well as the contribution of individual organs. NSC concentrations in the branches, stemwood, and roots of 24 trees were measured across 12 months. We then scaled up concentrations to the whole-tree and ecosystem levels using allometric equations and forest stand inventory data. While whole-tree total NSC pools followed the conventional theory, sugar pools peaked in the dormant season and starch pools in the growing season. Seasonal depletion of total NSCs was minimal at the whole-tree level, but substantial at the organ level, particularly in branches. Surprisingly, roots were not the major storage organ as branches stored comparable amounts of starch throughout the year, and root reserves were not used to support springtime growth. Scaling up NSC concentrations to the ecosystem level, we find that commonly used, process-based ecosystem and land surface models all overpredict NSC storage.

Distribution and mixing of old and new nonstructural carbon in two temperate trees.

We know surprisingly little about whole-tree nonstructural carbon (NSC; primarily sugars and starch) budgets. Even less well understood is the mixing between recent photosynthetic assimilates (new NSC) and previously stored reserves. And, NSC turnover times are poorly constrained. We characterized the distribution of NSC in the stemwood, branches, and roots of two temperate trees, and we used the continuous label offered by the radiocarbon (carbon-14, (14) C) bomb spike to estimate the mean age of NSC in different tissues. NSC in branches and the outermost stemwood growth rings had the (14) C signature of the current growing season. However, NSC in older aboveground and belowground tissues was enriched in (14) C, indicating that it was produced from older assimilates. Radial patterns of (14) C in stemwood NSC showed strong mixing of NSC across the youngest growth rings, with limited 'mixing in' of younger NSC to older rings. Sugars in the outermost five growth rings, accounting for two-thirds of the stemwood pool, had a mean age < 1 yr, whereas sugars in older growth rings had a mean age > 5 yr. Our results are thus consistent with a previously-hypothesized two-pool ('fast' and 'slow' cycling NSC) model structure. These pools appear to be physically distinct.

Seasonal dynamics and age of stemwood nonstructural carbohydrates in temperate forest trees.

Nonstructural carbohydrate reserves support tree metabolism and growth when current photosynthates are insufficient, offering resilience in times of stress. We monitored stemwood nonstructural carbohydrate (starch and sugars) concentrations of the dominant tree species at three sites in the northeastern United States. We estimated the mean age of the starch and sugars in a subset of trees using the radiocarbon ((14) C) bomb spike. With these data, we then tested different carbon (C) allocation schemes in a process-based model of forest C cycling. We found that the nonstructural carbohydrates are both highly dynamic and about a decade old. Seasonal dynamics in starch (two to four times higher in the growing season, lower in the dormant season) mirrored those of sugars. Radiocarbon-based estimates indicated that the mean age of the starch and sugars in red maple (Acer rubrum) was 7-14 yr. A two-pool (fast and slow cycling reserves) model structure gave reasonable estimates of the size and mean residence time of the total NSC pool, and greatly improved model predictions of interannual variability in woody biomass increment, compared with zero- or one-pool structures used in the majority of existing models. This highlights the importance of nonstructural carbohydrates in the context of forest ecosystem carbon cycling.

Age, allocation and availability of nonstructural carbon in mature red maple trees.

The allocation of nonstructural carbon (NSC) to growth, metabolism and storage remains poorly understood, but is critical for the prediction of stress tolerance and mortality. We used the radiocarbon ((14) C) 'bomb spike' as a tracer of substrate and age of carbon in stemwood NSC, CO2 emitted by stems, tree ring cellulose and stump sprouts regenerated following harvesting in mature red maple trees. We addressed the following questions: which factors influence the age of stemwood NSC?; to what extent is stored vs new NSC used for metabolism and growth?; and, is older, stored NSC available for use? The mean age of extracted stemwood NSC was 10 yr. More vigorous trees had both larger and younger stemwood NSC pools. NSC used to support metabolism (stem CO2 ) was 1-2 yr old in spring before leaves emerged, but reflected current-year photosynthetic products in late summer. The tree ring cellulose (14) C age was 0.9 yr older than direct ring counts. Stump sprouts were formed from NSC up to 17 yr old. Thus, younger NSC is preferentially used for growth and day-to-day metabolic demands. More recently stored NSC contributes to annual ring growth and metabolism in the dormant season, yet decade-old and older NSC is accessible for regrowth.

An incubation method to determine the age of available nonstructural carbon in woody plant tissues.

Radiocarbon (∆14C) measurements of nonstructural carbon enable inference on the age and turnover time of stored photosynthate (e.g., sugars, starch), of which the largest pool in trees resides in the main bole. Because of potential issues with extraction-based methods, we introduce an incubation method to capture the ∆14C of nonstructural carbon via respired CO2. In this study, we compared the ∆14C obtained from these incubations with ∆14C from a well-established extraction method, using increment cores from a mature trembling aspen (Populus tremuloides). To understand any potential ∆14C disagreement, the yields from both methods were also benchmarked against the phenol-sulfuric acid concentration assay. We found incubations captured less than 100% of measured sugar and starch carbon, with recovery ranging from ~ 3% in heartwood to 85% in shallow sapwood. However, extractions universally over-yielded (mean 273 ± 101% expected sugar carbon; as high as 480%), where sugars represented less than half of extracted soluble carbon, indicating very poor specificity. While separation of soluble and insoluble nonstructural carbon is ostensibly a strength of extraction based methods, there was also evidence of poor separation of these two fractions in extractions. The ∆14C of respired CO2 and ∆14C from extractions were similar in the sapwood, while extractions resulted in comparatively higher ∆14C (older carbon) in heartwood and bark. Because yield and ∆14C discrepancies were largest in old tissues, incubations may better capture the ∆14C of nonstructural carbon that is actually metabolically available. That is, we suggest extractions include metabolically irrelevant carbon from dead tissues or cells, as well as carbon that is neither sugar nor starch. In contrast, nonstructural carbon captured by extractions must be respired to be measured. We thus suggest incubations of live tissues are a potentially viable, inexpensive, and versatile method to study the ∆14C of metabolically relevant (available) nonstructural carbon.

Old reserves and ancient buds fuel regrowth of coast redwood after catastrophic fire.

For long-lived organisms, investment in insurance strategies such as reserve energy storage can enable resilience to resource deficits, stress or catastrophic disturbance. Recent fire in California damaged coast redwood (Sequoia sempervirens) groves, consuming all foliage on some of the tallest and oldest trees on Earth. Burned trees recovered through resprouting from roots, trunk and branches, necessarily supported by nonstructural carbon reserves. Nonstructural carbon reserves can be many years old, but direct use of old carbon has rarely been documented and never in such large, old trees. We found some sprouts contained the oldest carbon ever observed to be remobilized for growth. For certain trees, simulations estimate up to half of sprout carbon was acquired in photosynthesis more than 57 years prior, and direct observations in sapwood show trees can access reserves at least as old. Sprouts also emerged from ancient buds-dormant under bark for centuries. For organisms with millennial lifespans, traits enabling survival of infrequent but catastrophic events may represent an important energy sink. Remobilization of decades-old photosynthate after disturbance demonstrates substantial amounts of nonstructural carbon within ancient trees cycles on slow, multidecadal timescales.

Soil-atmosphere fluxes of CO2, CH4, and N2O across an experimentally-grown, successional gradient of biocrust community types.

Biological soil crusts (biocrusts) are critical components of dryland and other ecosystems worldwide, and are increasingly recognized as novel model ecosystems from which more general principles of ecology can be elucidated. Biocrusts are often diverse communities, comprised of both eukaryotic and prokaryotic organisms with a range of metabolic lifestyles that enable the fixation of atmospheric carbon and nitrogen. However, how the function of these biocrust communities varies with succession is incompletely characterized, especially in comparison to more familiar terrestrial ecosystem types such as forests. We conducted a greenhouse experiment to investigate how community composition and soil-atmosphere trace gas fluxes of CO2, CH4, and N2O varied from early-successional light cyanobacterial biocrusts to mid-successional dark cyanobacteria biocrusts and late-successional moss-lichen biocrusts and as biocrusts of each successional stage matured. Cover type richness increased as biocrusts developed, and richness was generally highest in the late-successional moss-lichen biocrusts. Microbial community composition varied in relation to successional stage, but microbial diversity did not differ significantly among stages. Net photosynthetic uptake of CO2 by each biocrust type also increased as biocrusts developed but tended to be moderately greater (by up to ≈25%) for the mid-successional dark cyanobacteria biocrusts than the light cyanobacterial biocrusts or the moss-lichen biocrusts. Rates of soil C accumulation were highest for the dark cyanobacteria biocrusts and light cyanobacteria biocrusts, and lowest for the moss-lichen biocrusts and bare soil controls. Biocrust CH4 and N2O fluxes were not consistently distinguishable from the same fluxes measured from bare soil controls; the measured rates were also substantially lower than have been reported in previous biocrust studies. Our experiment, which uniquely used greenhouse-grown biocrusts to manipulate community composition and accelerate biocrust development, shows how biocrust function varies along a dynamic gradient of biocrust successional stages.

The model-data fusion pitfall: assuming certainty in an uncertain world.

Model-data fusion is a powerful framework by which to combine models with various data streams (including observations at different spatial or temporal scales), and account for associated uncertainties. The approach can be used to constrain estimates of model states, rate constants, and driver sensitivities. The number of applications of model-data fusion in environmental biology and ecology has been rising steadily, offering insights into both model and data strengths and limitations. For reliable model-data fusion-based results, however, the approach taken must fully account for both model and data uncertainties in a statistically rigorous and transparent manner. Here we review and outline the cornerstones of a rigorous model-data fusion approach, highlighting the importance of properly accounting for uncertainty. We conclude by suggesting a code of best practices, which should serve to guide future efforts.

Seasonal and episodic moisture controls on plant and microbial contributions to soil respiration.

Moisture inputs drive soil respiration (SR) dynamics in semi-arid and arid ecosystems. However, determining the contributions of root and microbial respiration to SR, and their separate temporal responses to periodic drought and water pulses, remains poorly understood. This study was conducted in a pine forest ecosystem with a Mediterranean-type climate that receives seasonally varying precipitation inputs from both rainfall (in the winter) and fog-drip (primarily in the summer). We used automated SR measurements, radiocarbon SR source partitioning, and a water addition experiment to understand how SR, and its separate root and microbial sources, respond to seasonal and episodic changes in moisture. Seasonal changes in SR were driven by surface soil water content and large changes in root respiration contributions. Superimposed on these seasonal patterns were episodic pulses of precipitation that determined the short-term SR patterns. Warm season precipitation pulses derived from fog-drip, and rainfall following extended dry periods, stimulated the largest SR responses. Microbial respiration dominated these SR responses, increasing within hours, whereas root respiration responded more slowly over days. We conclude that root and microbial respiration sources respond differently in timing and magnitude to both seasonal and episodic moisture inputs. These findings have important implications for the mechanistic representation of SR in models and the response of dry ecosystems to changes in precipitation patterns.

Seasonal fluctuation of nonstructural carbohydrates reveals the metabolic availability of stemwood reserves in temperate trees with contrasting wood anatomy.

Nonstructural carbohydrates (NSCs) play a critical role in plant physiology and metabolism, yet we know little about their distribution within individual organs such as the stem. This leaves many open questions about whether reserves deep in the stem are metabolically active and available to support functional processes. To gain insight into the availability of reserves, we measured radial patterns of NSCs over the course of a year in the stemwood of temperate trees with contrasting wood anatomy (ring porous vs diffuse porous). In a subset of trees, we estimated the mean age of soluble sugars within and between different organs using the radiocarbon (14C) bomb spike approach. First, we found that NSC concentrations were the highest and most seasonally dynamic in the outermost stemwood segments for both ring-porous and diffuse-porous trees. However, while the seasonal fluctuation of NSCs was dampened in deeper stemwood segments for ring-porous trees, it remained high for diffuse-porous trees. These NSC dynamics align with differences in the proportion of functional sapwood and the arrangement of vessels between ring-porous and diffuse-porous trees. Second, radial patterns of 14C in the stemwood showed that sugars became older when moving toward the pith. The same pattern was found in the coarse roots. Finally, when taken together, our results highlight how the radial distribution and age of NSCs relate to wood anatomy and suggest that while deeper, and likely older, reserves in the stemwood fluctuated across the seasons, the deepest reserves at the center of the stem were not used to support tree metabolism under usual environmental conditions.

Nonstructural carbon in woody plants.

Nonstructural carbon (NSC) provides the carbon and energy for plant growth and survival. In woody plants, fundamental questions about NSC remain unresolved: Is NSC storage an active or passive process? Do older NSC reserves remain accessible to the plant? How is NSC depletion related to mortality risk? Herein we review conceptual and mathematical models of NSC dynamics, recent observations and experiments at the organismal scale, and advances in plant physiology that have provided a better understanding of the dynamics of woody plant NSC. Plants preferentially use new carbon but can access decade-old carbon when the plant is stressed or physically damaged. In addition to serving as a carbon and energy source, NSC plays important roles in phloem transport, osmoregulation, and cold tolerance, but how plants regulate these competing roles and NSC depletion remains elusive. Moving forward requires greater synthesis of models and data and integration across scales from -omics to ecology.

Cloud shading and fog drip influence the metabolism of a coastal pine ecosystem.

Assessing the ecological importance of clouds has substantial implications for our basic understanding of ecosystems and for predicting how they will respond to a changing climate. This study was conducted in a coastal Bishop pine forest ecosystem that experiences regular cycles of stratus cloud cover and inundation in summer. Our objective was to understand how these clouds impact ecosystem metabolism by contrasting two sites along a gradient of summer stratus cover. The site that was under cloud cover ~15% more of the summer daytime hours had lower air temperatures and evaporation rates, higher soil moisture content, and received more frequent fog drip inputs than the site with less cloud cover. These cloud-driven differences in environmental conditions translated into large differences in plant and microbial activity. Pine trees at the site with greater cloud cover exhibited less water stress in summer, larger basal area growth, and greater rates of sap velocity. The difference in basal area growth between the two sites was largely due to summer growth. Microbial metabolism was highly responsive to fog drip, illustrated by an observed ~3-fold increase in microbial biomass C with increasing summer fog drip. In addition, the site with more cloud cover had greater total soil respiration and a larger fractional contribution from heterotrophic sources. We conclude that clouds are important to the ecological functioning of these coastal forests, providing summer shading and cooling that relieve pine and microbial drought stress as well as regular moisture inputs that elevate plant and microbial metabolism. These findings are important for understanding how these and other seasonally dry coastal ecosystems will respond to predicted changes in stratus cover, rainfall, and temperature.

Contribution of new photosynthetic assimilates to respiration by perennial grasses and shrubs: residence times and allocation patterns.

Quantification of the fate of carbon (C) used by plant metabolism is necessary to improve predictions of terrestrial ecosystem respiration and its sources. Here, a dual isotope ((13)C and (14)C) pulse-label was used to determine the allocation of new C to different respiratory pathways in the early and late growing seasons for two plant functional types, perennial grasses and shrubs, in the Owens Valley, CA, USA. Allocation differences between plant types exceeded seasonal allocation variation. Grasses respired 71 and 64% and shrubs respired 22 and 17% of the label below-ground in the early and late growing seasons, respectively. Across seasons and plant types, approximately 48-61% of the label recovered was respired in 24 h, approximately 68-84% in 6 d, and approximately 16-33% in 6-36 d after labeling. Three C pools were identified for plant metabolism: a fast pool with mean residence times (MRTs) of approximately 0.5 and approximately 1 d below- and above-ground, respectively; an intermediate pool with MRTs of 19.9 and 18.9 d; and a storage pool detected in new leaf early growing season respiration > 9 months after assimilation. Differences in allocation to fast vs intermediate C pools resulted in the mean age of C respired by shrubs being shorter (3.8-4.5 d) than that of the grasses (4.8-8.2 d).

Radiocarbon--a low-impact tool to study nutrient transport by soil fungi under field conditions.

Here, we present a new in-situ method to study the uptake of amino acids by soil fungi. We injected 14C-labeled glycine into a marshland soil and measured the rate and the 14C signature of CO2 respired from sporocarps of Pholiota terrestris over 53.5 h and 2 m. We also determined the incorporation of glycine-C into sporocarp tissue. The 14C signature of the CO2 and tissue was quantified by accelerator mass spectrometry. After the label application, the rate of CO2 flux and its 14C signature from chambers with sporocarps were significantly higher than from chambers without sporocarps, and then declined with time. Postlabel, the 14C signature of the sporocarp tissue increased by 35 per thousand. We show that this approach can be used to study below-ground food webs on an hourly time-scale while minimizing the perturbation of competitive relationships among soil microorganisms and between plants and soil microorganisms. Additionally we show that care must be taken to avoid confounding effects of sporocarp senescence on rates and radiocarbon signatures of respired CO2.