Vapour pressure deficit was not a primary limiting factor for gas exchange in an irrigated, mature dryland Aleppo pine forest.

Climate change is often associated with increasing vapour pressure deficit (VPD) and changes in soil moisture (SM). While atmospheric and soil drying often co-occur, their differential effects on plant functioning and productivity remain uncertain. We investigated the divergent effects and underlying mechanisms of soil and atmospheric drought based on continuous, in situ measurements of branch gas exchange with automated chambers in a mature semiarid Aleppo pine forest. We investigated the response of control trees exposed to combined soil-atmospheric drought (low SM, high VPD) during the rainless Mediterranean summer and that of trees experimentally unconstrained by soil dryness (high SM; using supplementary dry season water supply) but subjected to atmospheric drought (high VPD). During the seasonal dry period, branch conductance (gbr ), transpiration rate (E) and net photosynthesis (Anet ) decreased in low-SM trees but greatly increased in high-SM trees. The response of E and gbr to the massive rise in VPD (to 7 kPa) was negative in low-SM trees and positive in high-SM trees. These observations were consistent with predictions based on a simple plant hydraulic model showing the importance of plant water potential in the gbr and E response to VPD. These results demonstrate that avoiding drought on the supply side (SM) and relying on plant hydraulic regulation constrains the effects of atmospheric drought (VPD) as a stressor on canopy gas exchange in mature pine trees under field conditions.

The grassland carbon cycle: Mechanisms, responses to global changes, and potential contribution to carbon neutrality.

Grassland is one of the largest terrestrial biomes, providing critical ecosystem services such as food production, biodiversity conservation, and climate change mitigation. Global climate change and land-use intensification have been causing grassland degradation and desertification worldwide. As one of the primary medium for ecosystem energy flow and biogeochemical cycling, grassland carbon (C) cycling is the most fundamental process for maintaining ecosystem services. In this review, we first summarize recent advances in our understanding of the mechanisms underpinning spatial and temporal patterns of the grassland C cycle, discuss the importance of grasslands in regulating inter- and intra-annual variations in global C fluxes, and explore the previously unappreciated complexity in abiotic processes controlling the grassland C balance, including soil inorganic C accumulation, photochemical and thermal degradation, and wind erosion. We also discuss how climate and land-use changes could alter the grassland C balance by modifying the water budget, nutrient cycling and additional plant and soil processes. Further, we examine why and how increasing aridity and improper land use may induce significant losses in grassland C stocks. Finally, we identify several priorities for future grassland C research, including improving understanding of abiotic processes in the grassland C cycle, strengthening monitoring of grassland C dynamics by integrating ground inventory, flux monitoring, and modern remote sensing techniques, and selecting appropriate plant species combinations with suitable traits and strong resistance to climate fluctuations, which would help design sustainable grassland restoration strategies in a changing climate.

Dryland mechanisms could widely control ecosystem functioning in a drier and warmer world.

Responses of terrestrial ecosystems to climate change have been explored in many regions worldwide. While continued drying and warming may alter process rates and deteriorate the state and performance of ecosystems, it could also lead to more fundamental changes in the mechanisms governing ecosystem functioning. Here we argue that climate change will induce unprecedented shifts in these mechanisms in historically wetter climatic zones, towards mechanisms currently prevalent in dry regions, which we refer to as 'dryland mechanisms'. We discuss 12 dryland mechanisms affecting multiple processes of ecosystem functioning, including vegetation development, water flow, energy budget, carbon and nutrient cycling, plant production and organic matter decomposition. We then examine mostly rare examples of the operation of these mechanisms in non-dryland regions where they have been considered irrelevant at present. Current and future climate trends could force microclimatic conditions across thresholds and lead to the emergence of dryland mechanisms and their increasing control over ecosystem functioning in many biomes on Earth.

Patterns of total root and shoot carbon dioxide fluxes and their impact on daily tree carbon budget in large tropical tree saplings.

A significant amount of the carbon (C) assimilated in photosynthesis by trees is re-emitted to the atmosphere via the respiratory CO2 flux of roots. Because of technical constraints, we have little understanding of the extent and dynamics of the respiratory CO2 flux of roots at the total root system scale (RCF). This study aimed to fill this gap and to quantify the daily C budget of entire trees. We used aeroponics as a novel approach to measure directly and simultaneously RCF and the net CO2 flux of the entire shoot (SCF), to estimate their night- and day-time contributions to daily tree CO2 budget and to estimate the relative contribution of different root categories to RCF in large saplings of the tropical tree species Ceiba pentandra (L.) Gaertn. By maintaining root temperature within a narrow range (24-27.5 °C), we controlled for its effect on RCF, thus allowing the potential relationship between RCF and SCF to be tested. The carbon gain of the fast-growing saplings was 0.79 ± 0.10 g C sapling-1 day-1, with day-time shoot CO2 uptake outweighing night-time shoot and day- and night-time root CO2 losses by a factor of two. Other than a slight rise in the morning hours, RCF was relatively stable and not coupled to the daily dynamics of SCF. Albeit having lower specific respiration rates compared with fine-roots, the relative contributions of coarse-roots (diameter >2 mm) to RCF were substantial because of their large biomass and were estimated to range from 43 to 63% of RCF at midday of different days during the growing season. The results of this study suggest that (i) the entire root system needs to be monitored for its impact on the tree CO2 budget, (ii) RCF cannot be derived from SCF and (iii) the importance of coarse-root respiration to RCF may be greater than appreciated.

The importance of tree internal water storage under drought conditions.

Global warming and drying trends, as well as the increase in frequency and intensity of droughts, may have unprecedented impacts on various forest ecosystems. We assessed the role of internal water storage (WS) in drought resistance of mature pine trees in the semi-arid Yatir Forest. Transpiration (T), soil moisture and sap flow (SF) were measured continuously, accompanied by periodical measurements of leaf and branch water potential (Ψleaf) and water content (WC). The data were used to parameterize a tree hydraulics model to examine the impact of WS capacitance on the tree water relations. The results of the continuous measurements showed a 5-h time lag between T and SF in the dry season, which peaked in the early morning and early afternoon, respectively. A good fit between model results and observations was only obtained when the empirically estimated WS capacitance was included in the model. Without WS during the dry season, Ψleaf would drop below a threshold known to cause hydraulic failure and cessation of gas exchange in the studied tree species. Our results indicate that tree WS capacitance is a key drought resistance trait that could enhance tree survival in a drying climate, contributing up to 45% of the total daily transpiration during the dry season.

Multi-seasonal water-stress memory versus temperature-driven dynamic structural changes in grapevine.

Perennial plants perpetually adapt to environmental changes in complex and yet insufficiently understood manner. We aimed to separate the intra-seasonal temperature effects on structure and function from perennial and annual water stress effects. This study focused on grapevine (Vitis vinifera L. 'Cabernet Sauvignon') petioles, which being a continuously produced organ, represent the current status of the plant. Field-grown mature plants subjected to multi-annual irrigation treatments (severe water stress, mild water stress and non-stressed) throughout the growing season were compared with greenhouse-grown plants under three temperature regimes (22, 28 and 34 °C). Physiological and functional anatomy parameters were measured. A generalized additive model (GAM) based on meteorological and lysimeter-based field data was applied to determine the relative influence of various meteorological parameters on evapotranspiration (ETc) during the growing season in the field experiment. At the beginning of the growing season, in May, petioles in the severe stress treatment showed a stress-related structure (decreased length, safer hydraulic structure and increased lignification), though having high values of stem water potential (SWP). As the season progressed and temperatures increased, all water availability treatments petioles showed similar changes, and at the end of season, in August, were structurally very similar. Those changes were independent of SWP and were comparable to high temperature-induced changes in the greenhouse. In contrast, stems hydraulic structure was strongly influenced by water availability. Regression analyses indicated a relationship between petioles xylem structure and stomatal conductance (gs), whereas gs (but not SWP) was temperature-dependent. The GAM showed that ETc was mainly dependent on temperature. Our results indicate a perennial water-stress memory response, influencing the petiole structure at the beginning of the following season. Intra-seasonally, the petiole's structure becomes independent of water status, whereas temperature drives the structural changes. Thus, ongoing climate change might disrupt plant performance by purely temperature-induced effects.

Seeking the "point of no return" in the sequence of events leading to mortality of mature trees.

Drought-related tree mortality is increasing globally, but the sequence of events leading to it remains poorly understood. To identify this sequence, we used a 2016 tree mortality event in a semi-arid pine forest where dendrometry and sap flow measurements were carried out in 31 trees, of which seven died. A comparative analysis revealed three stages leading to mortality. First, a decrease in tree diameter in all dying trees, but not in the surviving trees, 8 months "prior to the visual signs of mortality" (PVSM; e.g., near complete canopy browning). Second, a decay to near zero in the diurnal stem swelling/shrinkage dynamics, reflecting the loss of stem radial water flow in the dying trees, 6 months PVSM. Third, cessation of stem sap flow 3 months PVSM. Eventual mortality could therefore be detected long before visual signs were observed, and the three stages identified here demonstrated the differential effects of drought on stem growth, water storage capacity and soil water uptake. The results indicated that breakdown of stem radial water flow and phloem function is a critical element in defining the "point of no return" in the sequence of events leading to mortality of mature trees.

Carbon allocation to the root system of tropical tree Ceiba pentandra using 13C pulse labelling in an aeroponic facility.

Despite the important role of tropical forest ecosystems in the uptake and storage of atmospheric carbon dioxide (CO2), the carbon (C) dynamics of tropical tree species remains poorly understood, especially regarding belowground roots. This study assessed the allocation of newly assimilated C in the fast-growing pioneer tropical tree species Ceiba pentandra (L.), with a special focus on different root categories. During a 5-day pulse-labelling experiment, 9-month-old (~3.5-m-tall) saplings were labelled with 13CO2 in a large-scale aeroponic facility, which allowed tracing the label in bulk biomass and in non-structural carbohydrates (sugars and starch) as well as respiratory CO2 from the canopy to the root system, including both woody and non-woody roots. A combined logistic and exponential model was used to evaluate 13C mean transfer time and mean residence time (MRT) to the root systems. We found 13C in the root phloem as early as 2 h after the labelling, indicating a mean C transfer velocity of 2.4 ± 0.1 m h-1. Five days after pulse labelling, 27% of the tracers taken up by the trees were found in the leaves and 13% were recovered in the woody tissue of the trunk, 6% in the bark and 2% in the root systems, while 52% were lost, most likely by respiration and exudation. Larger amounts of 13C were found in root sugars than in starch, the former also demonstrating shorter MRT than starch. Of all investigated root categories, non-woody white roots (NRW) showed the largest 13C enrichment and peaked in the deepest NRW (2-3.5 m) as early as 24 ± 2 h after labelling. In contrast to coarse woody brown roots, the sink strength of NRW increased with root depth. The findings of this study improve the understanding of C allocation in young tropical trees and provide unique insights into the changing contributions of woody and non-woody roots to C sink strengths with depth.

Patterns and dynamics of canopy-root coupling in tropical tree saplings vary with light intensity but not with root depth.

Carbon (C) dynamics in canopy and roots influence whole-tree carbon fluxes, but little is known about canopy regulation of tree-root activity. Here, the patterns and dynamics of canopy-root C coupling are assessed in tropical trees. Large aeroponics facility was used to study the root systems of Ceiba pentandra and Khaya anthotheca saplings directly at different light intensities. In Ceiba, root respiration (Rr ) co-varied with photosynthesis (An ) in large saplings (3-to-7-m canopy-root axis) at high-light, but showed no consistent pattern at low-light. At medium-light and in small saplings (c. 1-m axis), Rr tended to decrease transiently towards midday. Proximal roots had higher Rr and nonstructural carbohydrate concentrations than distal roots, but canopy-root coupling was unaffected by root location. In medium-sized Khaya, no Rr pattern was observed, and in both species, Rr was unrelated to temperature. The early-afternoon increase in Rr suggests that canopy-root coupling is based on mass flow of newly fixed C in the phloem, whereas the early-morning rise in Rr with An indicates an additional coupling signal that travels faster than the phloem sap. In large saplings and potentially also in higher trees, light and possibly additional environmental factors control the diurnal patterns of canopy-root coupling, irrespective of root location.

Evidence for large carbon sink and long residence time in semiarid forests based on 15 year flux and inventory records.

The rate of change in atmospheric CO2 is significantly affected by the terrestrial carbon sink, but the size and spatial distribution of this sink, and the extent to which it can be enhanced to mitigate climate change are highly uncertain. We combined carbon stock (CS) and eddy covariance (EC) flux measurements that were collected over a period of 15 years (2001-2016) in a 55 year old 30 km2 pine forest growing at the semiarid timberline (with no irrigating or fertilization). The objective was to constrain estimates of the carbon (C) storage potential in forest plantations in such semiarid lands, which cover ~18% of the global land area. The forest accumulated 145-160 g C m-2  year-1 over the study period based on the EC and CS approaches, with a mean value of 152.5 ± 30.1 g C m-2  year-1 indicating 20% uncertainty in carbon uptake estimates. Current total stocks are estimated at 7,943 ± 323 g C/m2 and 372 g N/m2 . Carbon accumulated mostly in the soil (~71% and 29% for soil and standing biomass carbon, respectively) with long soil carbon turnover time (59 years). Regardless of unexpected disturbances beyond those already observed at the study site, the results support a considerable carbon sink potential in semiarid soils and forest plantations, and imply that afforestation of even 10% of semiarid land area under conditions similar to that of the study site, could sequester ~0.4 Pg C/year over several decades.

Differential drought resistance strategies of co-existing woodland species enduring the long rainless Eastern Mediterranean summer.

In anticipation of a drier climate and to project future changes in forest dynamics, it is imperative to understand species-specific differences in drought resistance. The objectives of this study were to form a comprehensive understanding of the drought resistance strategies adopted by Eastern Mediterranean woodland species, and to elaborate specific ecophysiological traits that can explain the observed variation in survival among these species. We examined leaf water potential (𝛹), gas exchange and stem hydraulics during 2-3 years in mature individuals of the key woody species Phillyrea latifolia L., Pistacia lentiscus L. and Quercus calliprinos Webb that co-exist in a dry woodland experiencing ~ 6 rainless summer months. As compared with the other two similarly functioning species, Phillyrea displayed considerably lower 𝛹 (minimum 𝛹 of -8.7 MPa in Phillyrea vs -4.2 MPa in Pistacia and Quercus), lower 𝛹 at stomatal closure and lower leaf turgor loss point (𝛹TLP ), but reduced hydraulic vulnerability and wider safety margins. Notably, Phillyrea allowed 𝛹 to drop below 𝛹TLP under severe drought, whereas the other two species maintained positive turgor. These results indicate that Phillyrea adopted a more anisohydric drought resistance strategy, while Pistacia and Quercus exhibited a more isohydric strategy and probably relied on deeper water reserves. Unlike the two relatively isohydric species, Phillyrea reached complete stomatal closure at the end of the dry summer. Despite assessing a large number of physiological traits, none of them could be directly related to tree mortality. Higher mortality was observed for Quercus than for the other two species, which may result from higher water consumption due to its 2.5-10 times larger crown volume. The observed patterns suggest that similar levels of drought resistance in terms of survival can be achieved via different drought resistance strategies. Conversely, similar resistance strategies in terms of isohydricity can lead to different levels of vulnerability to extreme drought.

Burrowing detritivores regulate nutrient cycling in a desert ecosystem.

Nutrient cycling in most terrestrial ecosystems is controlled by moisture-dependent decomposer activity. In arid ecosystems, plant litter cycling exceeds rates predicted based on precipitation amounts, suggesting that additional factors are involved. Attempts to reveal these factors have focused on abiotic degradation, soil-litter mixing and alternative moisture sources. Our aim was to explore an additional hypothesis that macro-detritivores control litter cycling in deserts. We quantified the role different organisms play in clearing plant detritus from the desert surface, using litter baskets with different mesh sizes that allow selective entry of micro-, meso- or macrofauna. We also measured soil nutrient concentrations in increasing distances from the burrows of a highly abundant macro-detritivore, the desert isopod Hemilepistus reaumuri. Macro-detritivores controlled the clearing of plant litter in our field site. The highest rates of litter removal were measured during the hot and dry summer when isopod activity peaks and microbial activity is minimal. We also found substantial enrichment of inorganic nitrogen and phosphorous near isopod burrows. We conclude that burrowing macro-detritivores are important regulators of litter cycling in this arid ecosystem, providing a plausible general mechanism that explains the unexpectedly high rates of plant litter cycling in deserts.

Size and Reproductive Traits Rather than Leaf Economic Traits Explain Plant-Community Composition in Species-Rich Annual Vegetation along a Gradient of Land Use Intensity.

Agricultural land use imposes a major disturbance on ecosystems worldwide, thus greatly modifying the taxonomic and functional composition of plant communities. However, mechanisms of community assembly, as assessed by plant functional traits, are not well known for dryland ecosystems under agricultural disturbance. Here we investigated trait responses to disturbance intensity and availability of resources to identify the main drivers of changes in composition of semiarid communities under diverging land use intensities. The eastern Mediterranean study region is characterized by an extended rainless season and by very diverse, mostly annual communities. At 24 truly replicated sites, we recorded the frequency of 241 species and the functional traits of the 53 most common species, together with soil resources and disturbance intensity across a land use gradient ranging from ungrazed shrubland to intensively managed cropland (six land use types). Multivariate RLQ analysis (linking functional traits, sites and environmental factors in a three-way ordination) and fourth corner analysis (revealing significant relations between traits and environmental factors) were used in a complementary way to get insights into trait-environment relations. Results revealed that traits related to plant size (reflecting light absorption and competitive ability) increased with resource availability, such as soil phosphorus and water holding capacity. Leaf economic traits, such as specific leaf area (SLA), leaf nitrogen content (LNC), and leaf dry matter content showed low variation across the disturbance gradient and were not related to environmental variables. In these herbaceous annual communities where plants grow and persist for just 3-5 months, SLA and LNC were unrelated, which together with relatively high SLA values might point to strategies of drought escape and grazing avoidance. Seed mass was high both at higher and lower resource availability, whereas seed number increased with the degree of disturbance. The strong response of size and reproduction traits, and the missing response of leaf economic traits reveal light interception and resource competition rather than resource acquisition and litter decomposition as drivers of plant community composition. Deviations from trait relationships observed in commonly studied temperate ecosystems confirm that climatic conditions play a fundamental role by filtering species with particular life forms and ecological strategies.

Biotic degradation at night, abiotic degradation at day: positive feedbacks on litter decomposition in drylands.

The arid and semi-arid drylands of the world are increasingly recognized for their role in the terrestrial net carbon dioxide (CO2 ) uptake, which depends largely on plant litter decomposition and the subsequent release of CO2 back to the atmosphere. Observed decomposition rates in drylands are higher than predictions by biogeochemical models, which are traditionally based on microbial (biotic) degradation enabled by precipitation as the main mechanism of litter decomposition. Consequently, recent research in drylands has focused on abiotic mechanisms, mainly photochemical and thermal degradation, but they only partly explain litter decomposition under dry conditions, suggesting the operation of an additional mechanism. Here we show that in the absence of precipitation, absorption of dew and water vapor by litter in the field enables microbial degradation at night. By experimentally manipulating solar irradiance and nighttime air humidity, we estimated that most of the litter CO2 efflux and decay occurring in the dry season was due to nighttime microbial degradation, with considerable additional contributions from photochemical and thermal degradation during the daytime. In a complementary study, at three sites across the Mediterranean Basin, litter CO2 efflux was largely explained by litter moisture driving microbial degradation and ultraviolet radiation driving photodegradation. We further observed mutual enhancement of microbial activity and photodegradation at a daily scale. Identifying the interplay of decay mechanisms enhances our understanding of carbon turnover in drylands, which should improve the predictions of the long-term trend of global carbon sequestration.

Non-structural carbohydrates in woody plants compared among laboratories.

Non-structural carbohydrates (NSC) in plant tissue are frequently quantified to make inferences about plant responses to environmental conditions. Laboratories publishing estimates of NSC of woody plants use many different methods to evaluate NSC. We asked whether NSC estimates in the recent literature could be quantitatively compared among studies. We also asked whether any differences among laboratories were related to the extraction and quantification methods used to determine starch and sugar concentrations. These questions were addressed by sending sub-samples collected from five woody plant tissues, which varied in NSC content and chemical composition, to 29 laboratories. Each laboratory analyzed the samples with their laboratory-specific protocols, based on recent publications, to determine concentrations of soluble sugars, starch and their sum, total NSC. Laboratory estimates differed substantially for all samples. For example, estimates for Eucalyptus globulus leaves (EGL) varied from 23 to 116 (mean = 56) mg g(-1) for soluble sugars, 6-533 (mean = 94) mg g(-1) for starch and 53-649 (mean = 153) mg g(-1) for total NSC. Mixed model analysis of variance showed that much of the variability among laboratories was unrelated to the categories we used for extraction and quantification methods (method category R(2) = 0.05-0.12 for soluble sugars, 0.10-0.33 for starch and 0.01-0.09 for total NSC). For EGL, the difference between the highest and lowest least squares means for categories in the mixed model analysis was 33 mg g(-1) for total NSC, compared with the range of laboratory estimates of 596 mg g(-1). Laboratories were reasonably consistent in their ranks of estimates among tissues for starch (r = 0.41-0.91), but less so for total NSC (r = 0.45-0.84) and soluble sugars (r = 0.11-0.83). Our results show that NSC estimates for woody plant tissues cannot be compared among laboratories. The relative changes in NSC between treatments measured within a laboratory may be comparable within and between laboratories, especially for starch. To obtain comparable NSC estimates, we suggest that users can either adopt the reference method given in this publication, or report estimates for a portion of samples using the reference method, and report estimates for a standard reference material. Researchers interested in NSC estimates should work to identify and adopt standard methods.

Root-shoot allometry of tropical forest trees determined in a large-scale aeroponic system.

BACKGROUND AND AIMS: This study is a first step in a multi-stage project aimed at determining allometric relationships among the tropical tree organs, and carbon fluxes between the various tree parts and their environment. Information on canopy-root interrelationships is needed to improve understanding of above- and below-ground processes and for modelling of the regional and global carbon cycle. Allometric relationships between the sizes of different plant parts will be determined. METHODS: Two tropical forest species were used in this study: Ceiba pentandra (kapok), a fast-growing tree native to South and Central America and to Western Africa, and Khaya anthotheca (African mahogany), a slower-growing tree native to Central and Eastern Africa. Growth and allometric parameters of 12-month-old saplings grown in a large-scale aeroponic system and in 50-L soil containers were compared. The main advantage of growing plants in aeroponics is that their root systems are fully accessible throughout the plant life, and can be fully recovered for harvesting. KEY RESULTS: The expected differences in shoot and root size between the fast-growing C. pentandra and the slower-growing K. anthotheca were evident in both growth systems. Roots were recovered from the aeroponically grown saplings only, and their distribution among various diameter classes followed the patterns expected from the literature. Stem, branch and leaf allometric parameters were similar for saplings of each species grown in the two systems. CONCLUSIONS: The aeroponic tree growth system can be utilized for determining the basic allometric relationships between root and shoot components of these trees, and hence can be used to study carbon allocation and fluxes of whole above- and below-ground tree parts.

Potential Maternal Effects of Elevated Atmospheric CO(2) on Development and Disease Severity in a Mediterranean Legume.

Global change can greatly affect plant populations both directly by influencing growing conditions and indirectly by maternal effects on development of offspring. More information is needed on transgenerational effects of global change on plants and their interactions with pathogens. The current study assessed potential maternal effects of atmospheric CO(2) enrichment on performance and disease susceptibility of first-generation offspring of the Mediterranean legume Onobrychis crista-galli. Mother plants were grown at three CO(2) concentrations, and the study focused on their offspring that were raised under common ambient climate and CO(2). In addition, progeny were exposed to natural infection by the fungal pathogen powdery mildew. In one out of 3 years, offspring of high-CO(2) treatments (440 and 600 ppm) had lower shoot biomass and reproductive output than offspring of low-CO(2) treatment (280 ppm). Disease severity in a heavy-infection year was higher in high-CO(2) than in low-CO(2) offspring. However, some of the findings on maternal effects changed when the population was divided into two functionally diverging plant types distinguishable by flower color (pink, Type P; white, Type W). Disease severity in a heavy-infection year was higher in high-CO(2) than in low-CO(2) progeny in the more disease-resistant (Type P), but not in the more susceptible plant type (Type W). In a low-infection year, maternal CO(2) treatments did not differ in disease severity. Mother plants of Type P exposed to low CO(2) produced larger seeds than all other combinations of CO(2) and plant type, which might contribute to higher offspring performance. This study showed that elevated CO(2) potentially exerts environmental maternal effects on performance of progeny and, notably, also on their susceptibility to natural infection by a pathogen. Maternal effects of global change might differently affect functionally divergent plant types, which could impact population fitness and alter plant communities.