Controls and relationships of soil organic carbon abundance and persistence vary across pedo-climatic regions.

One of the largest uncertainties in the terrestrial carbon cycle is the timing and magnitude of soil organic carbon (SOC) response to climate and vegetation change. This uncertainty prevents models from adequately capturing SOC dynamics and challenges the assessment of management and climate change effects on soils. Reducing these uncertainties requires simultaneous investigation of factors controlling the amount (SOC abundance) and duration (SOC persistence) of stored C. We present a global synthesis of SOC and radiocarbon profiles (nProfile = 597) to assess the timescales of SOC storage. We use a combination of statistical and depth-resolved compartment models to explore key factors controlling the relationships between SOC abundance and persistence across pedo-climatic regions and with soil depth. This allows us to better understand (i) how SOC abundance and persistence covary across pedo-climatic regions and (ii) how the depth dependence of SOC dynamics relates to climatic and mineralogical controls on SOC abundance and persistence. We show that SOC abundance and persistence are differently related; the controls on these relationships differ substantially between major pedo-climatic regions and soil depth. For example, large amounts of persistent SOC can reflect climatic constraints on soils (e.g., in tundra/polar regions) or mineral absorption, reflected in slower decomposition and vertical transport rates. In contrast, lower SOC abundance can be found with lower SOC persistence (e.g., in highly weathered tropical soils) or higher SOC persistence (e.g., in drier and less productive regions). We relate variable patterns of SOC abundance and persistence to differences in the processes constraining plant C input, microbial decomposition, vertical C transport and mineral SOC stabilization potential. This process-oriented grouping of SOC abundance and persistence provides a valuable benchmark for global C models, highlighting that pedo-climatic boundary conditions are crucial for predicting the effects of climate change and soil management on future C abundance and persistence.

The mobilization and transport of newly fixed carbon are driven by plant water use in an experimental rainforest under drought.

Non-structural carbohydrates (NSCs) are building blocks for biomass and fuel metabolic processes. However, it remains unclear how tropical forests mobilize, export, and transport NSCs to cope with extreme droughts. We combined drought manipulation and ecosystem 13CO2 pulse-labeling in an enclosed rainforest at Biosphere 2, assessed changes in NSCs, and traced newly assimilated carbohydrates in plant species with diverse hydraulic traits and canopy positions. We show that drought caused a depletion of leaf starch reserves and slowed export and transport of newly assimilated carbohydrates below ground. Drought effects were more pronounced in conservative canopy trees with limited supply of new photosynthates and relatively constant water status than in those with continual photosynthetic supply and deteriorated water status. We provide experimental evidence that local utilization, export, and transport of newly assimilated carbon are closely coupled with plant water use in canopy trees. We highlight that these processes are critical for understanding and predicting tree resistance and ecosystem fluxes in tropical forest under drought.

Controls on timescales of soil organic carbon persistence across sub-Saharan Africa.

Given the importance of soil for the global carbon cycle, it is essential to understand not only how much carbon soil stores but also how long this carbon persists. Previous studies have shown that the amount and age of soil carbon are strongly affected by the interaction of climate, vegetation, and mineralogy. However, these findings are primarily based on studies from temperate regions and from fine-scale studies, leaving large knowledge gaps for soils from understudied regions such as sub-Saharan Africa. In addition, there is a lack of data to validate modeled soil C dynamics at broad scales. Here, we present insights into organic carbon cycling, based on a new broad-scale radiocarbon and mineral dataset for sub-Saharan Africa. We found that in moderately weathered soils in seasonal climate zones with poorly crystalline and reactive clay minerals, organic carbon persists longer on average (topsoil: 201 ± 130 years; subsoil: 645 ± 385 years) than in highly weathered soils in humid regions (topsoil: 140 ± 46 years; subsoil: 454 ± 247 years) with less reactive minerals. Soils in arid climate zones (topsoil: 396 ± 339 years; subsoil: 963 ± 669 years) store organic carbon for periods more similar to those in seasonal climate zones, likely reflecting climatic constraints on weathering, carbon inputs and microbial decomposition. These insights into the timescales of organic carbon persistence in soils of sub-Saharan Africa suggest that a process-oriented grouping of soils based on pedo-climatic conditions may be useful to improve predictions of soil responses to climate change at broader scales.

Carbon dynamics during long-term starving poplar trees-the importance of older carbohydrates and a shift to lipids during survival.

Carbon (C) assimilation can be severely impaired during periods of environmental stress like drought or defoliation, making trees heavily dependent on the use of C reserve pools for survival; yet, dynamics of reserve use during periods of reduced C supply are still poorly understood. We used stem girdling in mature poplar trees (Populus tremula L. hybrids), a lipid-storing species, to permanently interrupt phloem C transport and induced C shortage in the isolated stem section below the girdle and monitored metabolic activity during three campaigns in the growing seasons of 2018, 2019, and 2021. We measured respiratory fluxes (CO2 and O2), NSC concentration, the respiratory substrate (based on isotopic analysis and CO2/O2 ratio) and the age of the respiratory substrate (based on radiocarbon analysis). Our study shows that poplar trees can survive long periods of reduced C supply from the canopy by switching in metabolism from recent carbohydrates to older storage pools with a potential mixture of respiratory substrates, including lipids. This mechanism of stress resilience can explain why tree decline may take many years until death occurs.

Microbial degradation and assimilation of veratric acid in oxic and anoxic groundwaters.

Microbial communities are key players in groundwater ecosystems. In this dark environment, heterotrophic microbes rely on biomass produced by the activity of lithoautotrophs or on the degradation of organic matter seeping from the surface. Most studies on bacterial diversity in groundwater habitats are based on 16S gene sequencing and full genome reconstructions showing potential metabolic pathways used in these habitats. However, molecular-based studies do not allow for the assessment of population dynamics over time or the assimilation of specific compounds and their biochemical transformation by microbial communities. Therefore, in this study, we combined DNA-, phospholipid fatty acid-, and metabolomic-stable isotope probing to target and identify heterotrophic bacteria in the groundwater setting of the Hainich Critical Zone Exploratory (CZE), focusing on 2 aquifers with different physico-chemical conditions (oxic and anoxic). We incubated groundwater from 4 different wells using either 13C-labeled veratric acid (a lignin-derived compound) (single labeling) or a combination of 13CO2 and D-labeled veratric acid (dual labeling). Our results show that heterotrophic activities dominate all groundwater sites. We identified bacteria with the potential to break down veratric acid (Sphingobium or Microbacterium). We observed differences in heterotrophic activities between the oxic and anoxic aquifers, indicating local adaptations of bacterial populations. The dual labeling experiments suggested that the serine pathway is an important carbon assimilation pathway and that organic matter was an important source of hydrogen in the newly produced lipids. These experiments also yielded different labeled taxa compared to the single labeling experiments, showing that there exists a complex interaction network in the groundwater habitats.

A special issue preface: Radiocarbon in the Anthropocene.

The Anthropocene is defined by marked acceleration in human-induced perturbations to the Earth system. Anthropogenic emissions of CO2 and other greenhouse gases to the atmosphere and attendant changes to the global carbon cycle are among the most profound and pervasive of these perturbations. Determining the magnitude, nature and pace of these carbon cycle changes is crucial for understanding the future climate that ecosystems and humanity will experience and need to respond to. This special issue illustrates the value of radiocarbon as a tool to shed important light on the nature, magnitude and pace of carbon cycle change. This article is part of the Theo Murphy meeting issue 'Radiocarbon in the Anthropocene'.

Making the case for an International Decade of Radiocarbon.

Radiocarbon (14C) is a critical tool for understanding the global carbon cycle. During the Anthropocene, two new processes influenced 14C in atmospheric, land and ocean carbon reservoirs. First, 14C-free carbon derived from fossil fuel burning has diluted 14C, at rates that have accelerated with time. Second, 'bomb' 14C produced by atmospheric nuclear weapon tests in the mid-twentieth century provided a global isotope tracer that is used to constrain rates of air-sea gas exchange, carbon turnover, large-scale atmospheric and ocean transport, and other key C cycle processes. As we write, the 14C/12C ratio of atmospheric CO2 is dropping below pre-industrial levels, and the rate of decline in the future will depend on global fossil fuel use and net exchange of bomb 14C between the atmosphere, ocean and land. This milestone coincides with a rapid increase in 14C measurement capacity worldwide. Leveraging future 14C measurements to understand processes and test models requires coordinated international effort-a 'decade of radiocarbon' with multiple goals: (i) filling observational gaps using archives, (ii) building and sustaining observation networks to increase measurement density across carbon reservoirs, (iii) developing databases, synthesis and modelling tools and (iv) establishing metrics for identifying and verifying changes in carbon sources and sinks. This article is part of the Theo Murphy meeting issue 'Radiocarbon in the Anthropocene'.

Relating mineral-organic matter stabilization mechanisms to carbon quality and age distributions using ramped thermal analysis.

Organic carbon (OC) association with soil minerals stabilizes OC on timescales reflecting the strength of mineral-C interactions. We applied ramped thermal oxidation to subsoil B horizons with different mineral-C associations to separate OC according to increasing temperature of oxidation, i.e. thermal activation energy. Generally, OC released at lower temperatures was richer in bioavailable forms like polysaccharides, while OC released at higher temperatures was more aromatic. Organic carbon associated with pedogenic oxides was released at lower temperatures and had a narrow range of 14C content. By contrast, N-rich compounds were released at higher temperatures from samples with 2 : 1 clays and short-range ordered (SRO) amorphous minerals. Temperatures of release overlapped for SRO minerals and crystalline oxides, although the mean age of OC released was older for the SRO. In soils with more mixed mineralogy, the added presence of older OC released at temperatures greater than 450°C from clays resulted in a broader distribution of OC ages within the sample, especially for soils rich in 2 : 1 layer expandable clays such as smectite. While pedogenic setting affects mineral stability and absolute OC age, mineralogy controls the structure of OC age distribution within a sample, which may provide insight into model structures and OC dynamics under changing conditions. This article is part of the Theo Murphy meeting issue 'Radiocarbon in the Anthropocene'.

Soil carbon stocks in stable tropical landforms are dominated by geochemical controls and not by land use.

Soil organic carbon (SOC) dynamics depend on soil properties derived from the geoclimatic conditions under which soils develop and are in many cases modified by land conversion. However, SOC stabilization and the responses of SOC to land use change are not well constrained in deeply weathered tropical soils, which are dominated by less reactive minerals than those in temperate regions. Along a gradient of geochemically distinct soil parent materials, we investigated differences in SOC stocks and SOC (Δ14 C) turnover time across soil profile depth between montane tropical forest and cropland situated on flat, non-erosive plateau landforms. We show that SOC stocks and soil Δ14 C patterns do not differ significantly with land use, but that differences in SOC can be explained by the physicochemical properties of soils. More specifically, labile organo-mineral associations in combination with exchangeable base cations were identified as the dominating controls over soil C stocks and turnover. We argue that due to their long weathering history, the investigated tropical soils do not provide enough reactive minerals for the stabilization of C input in either high input (tropical forest) or low-input (cropland) systems. Since these soils exceeded their maximum potential for the mineral related stabilization of SOC, potential positive effects of reforestation on tropical SOC storage are most likely limited to minor differences in topsoil without major impacts on subsoil C stocks. Hence, in deeply weathered soils, increasing C inputs may lead to the accumulation of a larger readily available SOC pool, but does not contribute to long-term SOC stabilization.

Soil organic matter turnover rates increase to match increased inputs in grazed grasslands.

Managed grasslands have the potential to store carbon (C) and partially mitigate climate change. However, it remains difficult to predict potential C storage under a given soil or management practice. To study C storage dynamics due to long-term (1952-2009) phosphorus (P) fertilizer and irrigation treatments in New Zealand grasslands, we measured radiocarbon (14C) in archived soil along with observed changes in C stocks to constrain a compartmental soil model. Productivity increases from P application and irrigation in these trials resulted in very similar C accumulation rates between 1959 and 2009. The ∆14C changes over the same time period were similar in plots that were both irrigated and fertilized, and only differed in a non-irrigated fertilized plot. Model results indicated that decomposition rates of fast cycling C (0.1 to 0.2 year-1) increased to nearly offset increases in inputs. With increasing P fertilization, decomposition rates also increased in the slow pool (0.005 to 0.008 year-1). Our findings show sustained, significant (i.e. greater than 4 per mille) increases in C stocks regardless of treatment or inputs. As the majority of fresh inputs remain in the soil for less than 10 years, these long term increases reflect dynamics of the slow pool. Additionally, frequent irrigation was associated with reduced stocks and increased decomposition of fresh plant material. Rates of C gain and decay highlight trade-offs between productivity, nutrient availability, and soil C sequestration as a climate change mitigation strategy. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s10533-021-00838-z.

Storage of carbon reserves in spruce trees is prioritized over growth in the face of carbon limitation.

Climate change is expected to pose a global threat to forest health by intensifying extreme events like drought and insect attacks. Carbon allocation is a fundamental process that determines the adaptive responses of long-lived late-maturing organisms like trees to such stresses. However, our mechanistic understanding of how trees coordinate and set allocation priorities among different sinks (e.g., growth and storage) under severe source limitation remains limited. Using flux measurements, isotopic tracing, targeted metabolomics, and transcriptomics, we investigated how limitation of source supply influences sink activity, particularly growth and carbon storage, and their relative regulation in Norway spruce (Picea abies) clones. During photosynthetic deprivation, absolute rates of respiration, growth, and allocation to storage all decline. When trees approach neutral carbon balance, i.e., daytime net carbon gain equals nighttime carbon loss, genes encoding major enzymes of metabolic pathways remain relatively unaffected. However, under negative carbon balance, photosynthesis and growth are down-regulated while sucrose and starch biosynthesis pathways are up-regulated, indicating that trees prioritize carbon allocation to storage over growth. Moreover, trees under negative carbon balance actively increase the turnover rate of starch, lipids, and amino acids, most likely to support respiration and mitigate stress. Our study provides molecular evidence that trees faced with severe photosynthetic limitation strategically regulate storage allocation and consumption at the expense of growth. Understanding such allocation strategies is crucial for predicting how trees may respond to extreme events involving steep declines in photosynthesis, like severe drought, or defoliation by heat waves, late frost, or insect attack.

The size and the age of the metabolically active carbon in tree roots.

Little is known about the sources and age of C respired by tree roots. Previous research in stems identified two functional pools of non-structural carbohydrates (NSC): an "active" pool supplied directly from canopy photo-assimilates supporting metabolism and a "stored" pool used when fresh C supplies are limited. We compared the C isotope composition of water-soluble NSC and respired CO2 for aspen roots (Populus tremula hybrids) cut off from fresh C supply after stem-girdling or prolonged incubation of excised roots. We used bomb radiocarbon to estimate the time elapsed since C fixation for respired CO2 , water-soluble NSC and structural α-cellulose. While freshly excised roots (mostly <2.9 mm in diameter) respired CO2 fixed <1 year previously, the age increased to 1.6-2.9 year within a week after root excision. Freshly excised roots from trees girdled ~3 months ago had respiration rates and NSC stocks similar to un-girdled trees but respired older C (~1.2 year). We estimate that over 3 months NSC in girdled roots must be replaced 5-7 times by reserves remobilized from root-external sources. Using a mixing model and observed correlations between Δ14 C of water-soluble C and α-cellulose, we estimate ~30% of C is "active" (~5 mg C g-1 ).

Starch and lipid storage strategies in tropical trees relate to growth and mortality.

Non-structural carbon (NSC) storage (i.e. starch, soluble sugras and lipids) in tree stems play important roles in metabolism and growth. Their spatial distribution in wood may explain species-specific differences in carbon storage dynamics, growth and survival. However, quantitative information on the spatial distribution of starch and lipids in wood is sparse due to methodological limitations. Here we assessed differences in wood NSC and lipid storage between tropical tree species with different growth and mortality rates and contrasting functional types. We measured starch and soluble sugars in wood cores up to 4 cm deep into the stem using standard chemical quantification methods and histological slices stained with Lugol's iodine. We also detected neutral lipids using histological slices stained with Oil-Red-O. The histological method allowed us to group individuals into two categories according to their starch storage strategy: fiber-storing trees and parenchyma-storing trees. The first group had a bigger starch pool, slower growth and lower mortality rates than the second group. Lipid storage was found in wood parenchyma in five species and was related to low mortality rates. The quantification of the spatial distribution of starch and lipids in wood improves our understanding of NSC dynamics in trees and reveals additional dimensions of tree growth and survival strategies.

Simultaneous Real-Time Measurement of Isoprene and 2-Methyl-3-Buten-2-ol Emissions From Trees Using SIFT-MS.

The C5 hemiterpenes isoprene and 2-methyl-3-buten-2-ol (MBO) are important biogenic volatiles emitted from terrestrial vegetation. Isoprene is emitted from many plant groups, especially trees such as Populus, while emission of MBO is restricted to certain North American conifers, including species of Pinus. MBO is also a pheromone emitted by several conifer bark beetles. Both isoprene and MBO have typically been measured by proton-transfer reaction mass spectrometry (PTR-MS), but this method cannot accurately distinguish between them because of their signal overlap. Our study developed a method for using selective ion flow tube mass spectrometry (SIFT-MS) that allows simultaneous on-line measurement of isoprene and MBO by employing different reagent ions. The use of m/z(NO+) = 68 u for isoprene and m/z(O2 +) = 71 u for MBO gave minimal interference between the compounds. We tested the suitability of the method by measuring the emission of young trees of Populus, Picea, and Pinus. Our results largely confirm previous findings that Populus nigra, Picea glauca, and Picea abies emit isoprene and Pinus ponderosa emits MBO, but we also found MBO to be emitted by Picea abies. Thus SIFT-MS provides a reliable, easy to use, on-line measuring tool to distinguish between isoprene and MBO. The method should be of use to atmospheric chemists, tree physiologists and forest entomologists, among others.

Impacts of Degradation on Water, Energy, and Carbon Cycling of the Amazon Tropical Forests.

Selective logging, fragmentation, and understory fires directly degrade forest structure and composition. However, studies addressing the effects of forest degradation on carbon, water, and energy cycles are scarce. Here, we integrate field observations and high-resolution remote sensing from airborne lidar to provide realistic initial conditions to the Ecosystem Demography Model (ED-2.2) and investigate how disturbances from forest degradation affect gross primary production (GPP), evapotranspiration (ET), and sensible heat flux (H). We used forest structural information retrieved from airborne lidar samples (13,500 ha) and calibrated with 817 inventory plots (0.25 ha) across precipitation and degradation gradients in the eastern Amazon as initial conditions to ED-2.2 model. Our results show that the magnitude and seasonality of fluxes were modulated by changes in forest structure caused by degradation. During the dry season and under typical conditions, severely degraded forests (biomass loss ≥66%) experienced water stress with declines in ET (up to 34%) and GPP (up to 35%) and increases of H (up to 43%) and daily mean ground temperatures (up to 6.5°C) relative to intact forests. In contrast, the relative impact of forest degradation on energy, water, and carbon cycles markedly diminishes under extreme, multiyear droughts, as a consequence of severe stress experienced by intact forests. Our results highlight that the water and energy cycles in the Amazon are driven by not only climate and deforestation but also the past disturbance and changes of forest structure from degradation, suggesting a much broader influence of human land use activities on the tropical ecosystems.

Agricultural acceleration of soil carbonate weathering.

Soil carbonates (i.e., soil inorganic carbon or SIC) represent more than a quarter of the terrestrial carbon pool and are often considered to be relatively stable, with fluxes significant only on geologic timescales. However, given the importance of climatic water balance on SIC accumulation, we tested the hypothesis that increased soil water storage and transport resulting from cultivation may enhance dissolution of SIC, altering their local stock at decadal timescales. We compared SIC storage to 7.3 m depth in eight sites, each having paired plots of native vegetation and rain-fed croplands, and half the sites having additional irrigated cropland plots. Rain-fed and irrigated croplands had 328 and 730 Mg C/ha less SIC storage, respectively, compared to their native vegetation (grassland or woodland) pairs, and irrigated croplands had 402 Mg C/ha less than their rain-fed pairs (p < .0001). SIC contents were negatively correlated with estimated groundwater recharge, suggesting that dissolution and leaching may be responsible for SIC losses observed. Under croplands, the remaining SIC had more modern radiocarbon and a δ13 C composition that was closer to crop inputs than under native vegetation, suggesting that cultivation has led to faster turnover and incorporation of recent crop carbon into the SIC pool (p < .0001). The losses occurred just 30-100 years after land-use changes, indicating SIC stocks that were stable for millennia can rapidly adjust to increased soil water flows. Large SIC losses (194-242 Mg C/ha) also occurred below 4.9 m deep under irrigated croplands, with SIC losses lagging behind the downward-advancing wetting front by ~30 years, suggesting that even deep SIC were affected. These observations suggest that the vertical distribution of SIC in dry ecosystems is dynamic on decadal timescales, highlighting its potential role as a carbon sink or source to be examined in the context of land use and climate change.

Flood-pulse disturbances as a threat for long-living Amazonian trees.

The long-lived tree species Eschweilera tenuifolia (O. Berg) Miers is characteristic of oligotrophic Amazonian black-water floodplain forests (igapó), seasonally inundated up to 10 months per year, often forming monodominant stands. We investigated E. tenuifolia' growth and mortality patterns in undisturbed (Jaú National Park - JNP) and disturbed igapós (Uatumã Sustainable Development Reserve - USDR, downstream of the Balbina hydroelectric dam). We analysed age-diameter relationships, basal area increment (BAI) through 5-cm diameter classes, growth changes and growth ratios preceding death, BAI clustering, BAI ratio, and dated the individual year of death (14 C). Growth and mortality patterns were then related to climatic or anthropogenic disturbances. Results were similar for both populations for estimated maximum ages (JNP, 466 yr; USDR, 498 yr, except for one USDR tree with an estimated age of 820 yr) and slightly different for mean diameter increment (JNP: 2.04 mm; USDR: 2.28 mm). Living trees from JNP showed altered growth post-1975 and sparse tree mortality occurred at various times, possibly induced by extreme hydroclimatic events. In contrast with the JNP, abrupt growth changes and massive mortality occurred in the USDR after the dam construction began (1983). Even more than 30 yr after dam construction, flood-pulse alteration continues to affect both growth and mortality of E. tenuifolia. Besides its vulnerability to anthropogenic disturbances, this species is also susceptible to long-lasting dry and wet periods induced by climatic events, the combination of both processes may cause its local and regional extinction.

Production of constitutive and induced secondary metabolites is coordinated with growth and storage in Norway spruce saplings.

A mechanistic understanding of how trees balance the trade-offs between growth, storage and defense is limited but crucial for predicting tree responses to abiotic and biotic stresses. Here we investigated how trees allocate storage of non-structural carbohydrates (NSC) to growth and constitutive and induced secondary metabolites (SM). We exposed Norway spruce (Picea abies) saplings to 5 weeks of complete darkness to induce light and/or carbon limitation and then applied methyl jasmonate (MeJA) to simulate biotic attack. We measured changes in biomass, NSC (sum of soluble sugars and starches), and constitutive and induced SM (sum of phenolic compounds and terpenoids) in current-year developing and previous-year mature needles and branches, as well as volatiles emitted from the canopy. Under darkness, NSC storage was preferentially used for constitutive biosynthesis of monoterpenes rather than biosynthesis of stilbenes and growth of developing organs, while SM stored in mature organs cannot be remobilized and recycled. Furthermore, MeJA-induced production of SM was constrained by low NSC availability in developing organs but not in mature organs grown in the dark. Emissions of volatiles were suppressed in the dark but after 1 h of re-illumination, emissions of both constitutive and induced monoterpene hydrocarbons recovered rapidly, whereas emissions of linalool and sesquiterpene produced via de novo synthesis did not recover. Our results highlight that light and/or carbon limitation may constrain constitutive and JA-induced biosynthesis of SM in coordination with growth, NSC storage and mobilization.

Tropical Trees as Time Capsules of Anthropogenic Activity.

After the ice caps, tropical forests are globally the most threatened terrestrial environments. Modern trees are not just witnesses to growing contemporary threats but also legacies of past human activity. Here, we review the use of dendrochronology, radiocarbon analysis, stable isotope analysis, and DNA analysis to examine ancient tree management. These methods exploit the fact that living trees record information on environmental and anthropogenic selective forces during their own and past generations of growth, making trees living archaeological 'sites'. The applicability of these methods across prehistoric, historic, and industrial periods means they have the potential to detect evolving anthropogenic threats and can be used to set conservation priorities in rapidly vanishing environments.