Physiological and phenological adjustments in water and carbon fluxes of Aleppo pine forests under contrasting climates in the Eastern Mediterranean.

The ability of plants to adjust to the adverse effects of climate change is important for their survival and for their contribution to the global carbon cycle. This is particularly true in the Mediterranean region, which is among the regions that are most vulnerable to climate change. Here, we carried out a 2-year comparative ecophysiological study of ecosystem function in two similar Eastern Mediterranean forests of the same tree species (Pinus halepensis Mill.) under mild (Sani, Greece) and extreme (Yatir, Israel) climatic conditions. The partial effects of key environmental variables, including radiation, vapor pressure deficit, air temperature and soil moisture (Rg, D, T and soil water content (SWC), respectively), on the ecosystems' CO2 and water vapor fluxes were estimated using generalized additive models (GAMs). The results showed a large adjustment between sites in the seasonal patterns of both carbon and water fluxes and in the time and duration of the optimal period (defined here as the time when fluxes were within 85% of the seasonal maximum). The GAM analysis indicated that the main factor influencing the seasonal patterns was SWC, while T and D had significant but milder effects. During the respective optimal periods, the two ecosystems showed strong similarities in the fluxes' responses to the measured environmental variables, indicating similarity in their underlying physiological characteristics. The results indicate that Aleppo pine forests have a strong phenotypic adjustment potential to cope with increasing environmental stresses. This, in turn, will help their survival and their continued contribution to the terrestrial carbon sink in the face of climate change in this region.

Photovoltaic fields largely outperform afforestation efficiency in global climate change mitigation strategies.

Suppression of carbon emissions through photovoltaic (PV) energy and carbon sequestration through afforestation provides complementary climate change mitigation (CCM) strategies. However, a quantification of the "break-even time" (BET) required to offset the warming impacts of the reduced surface reflectivity of incoming solar radiation (albedo effect) is needed, though seldom accounted for in CCM strategies. Here, we quantify the CCM potential of PV fields and afforestation, considering atmospheric carbon reductions, solar panel life cycle analysis (LCA), surface energy balance, and land area required across different climatic zones, with a focus on drylands, which offer the main remaining land area reserves for forestation aiming climate change mitigation (Rohatyn S, Yakir D, Rotenberg E, Carmel Y. Limited climate change mitigation potential through forestation of the vast dryland regions. 2022. Science 377:1436-1439). Results indicate a BET of PV fields of ∼2.5 years but >50× longer for dryland afforestation, even though the latter is more efficient at surface heat dissipation and local surface cooling. Furthermore, PV is ∼100× more efficient in atmospheric carbon mitigation. While the relative efficiency of afforestation compared with PV fields significantly increases in more mesic climates, PV field BET is still ∼20× faster than in afforestation, and land area required greatly exceeds availability for tree planting in a sufficient scale. Although this analysis focusing purely on the climatic radiative forcing perspective quantified an unambiguous advantage for the PV strategy over afforestation, both approaches must be combined and complementary, depending on climate zone, since forests provide crucial ecosystem, climate regulation, and even social services.

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.

Detailed in situ leaf energy budget permits the assessment of leaf aerodynamic resistance as a key to enhance non-evaporative cooling under drought.

The modulation of the leaf energy budget components to maintain optimal leaf temperature are fundamental aspects of plant functioning and survival. Better understanding these aspects becomes increasingly important under a drying and warming climate when cooling through evapotranspiration (E) is suppressed. Combining novel measurements and theoretical estimates, we obtained unusually comprehensive twig-scale leaf energy budgets under extreme field conditions in droughted (suppressed E) and non-droughted (enhanced E) plots of a semi-arid pine forest. Under the same high mid-summer radiative load, leaf cooling shifted from relying on nearly equal contributions of sensible (H) and latent (LE) energy fluxes in non-droughted trees to relying almost exclusively on H in droughted ones, with no change in leaf temperature. Relying on our detailed leaf energy budget, we could demonstrate that this is due to a 2× reduction in leaf aerodynamic resistance. This capability for LE-to-H shift in leaves of mature Aleppo pine trees under droughted field conditions without increasing leaf temperature is likely a critical factor in the resilience and relatively high productivity of this important Mediterranean tree species under drying conditions.

Limited climate change mitigation potential through forestation of the vast dryland regions.

Forestation of the vast global drylands has been considered a promising climate change mitigation strategy. However, its actual climatic benefits are uncertain because the forests' reduced albedo can produce large warming effects. Using high-resolution spatial analysis of global drylands, we found 448 million hectares suitable for afforestation. This area's carbon sequestration potential until 2100 is 32.3 billion tons of carbon (Gt C), but 22.6 Gt C of that is required to balance albedo effects. The net carbon equivalent would offset ~1% of projected medium-emissions and business-as-usual scenarios over the same period. Focusing forestation only on areas with net cooling effects would use half the area and double the emissions offset. Although such smart forestation is clearly important, its limited climatic benefits reinforce the need to reduce emissions rapidly.

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.

'Dual-reference' method for high-precision infrared measurement of leaf surface temperature under field conditions.

Temperature is a key control over biological activities from the cellular to the ecosystem scales. However, direct, high-precision measurements of surface temperature of small objects, such as leaves, under field conditions with large variations in ambient conditions remain rare. Contact methods, such as thermocouples, are prone to large errors. The use of noncontact remote-sensing methods, such as thermal infrared measurements, provides an ideal solution, but their accuracy has been low (c. 2°C) owing to the necessity for corrections for material emissivity and fluctuations in background radiation Lbg . A novel 'dual-reference' method was developed to increase the accuracy of infrared needle-leaf surface temperature measurements in the field. It accounts for variations in Lbg and corrects for the systematic camera offset using two reference plates. We accurately captured surface temperature and leaf-to-air temperature differences of needle-leaves in a forest ecosystem with large diurnal and seasonal temperature fluctuations with an uncertainty of ± 0.23°C and ± 0.28°C, respectively. Routine high-precision leaf temperature measurements even under harsh field conditions, such as demonstrated here, opens the way for investigating a wide range of leaf-scale processes and their dynamics.

Evidence for efficient nonevaporative leaf-to-air heat dissipation in a pine forest under drought conditions.

The drier climates predicted for many regions will result in reduced evaporative cooling, leading to leaf heat stress and enhanced mortality. The extent to which nonevaporative cooling can contribute to plant resilience under these increasingly stressful conditions is not well known at present. Using a novel, high accuracy infrared system for the continuous measurement of leaf temperature in mature trees under field conditions, we assessed leaf-to-air temperature differences (ΔTleaf-air ) of pine needles during drought. On mid-summer days, ΔTleaf-air remained < 3°C, both in trees exposed to summer drought and in those provided with supplemental irrigation, which had a more than 10-fold higher transpiration rate. The nonevaporative cooling in the drought-exposed trees must be facilitated by low resistance to heat transfer, generating a large sensible heat flux, H. ΔTleaf-air was weakly related to variations in the radiation load and mean wind speed in the lower part of the canopy, but was dependent on canopy structure and within-canopy turbulence that enhanced the H. Nonevaporative cooling is demonstrated as an effective cooling mechanism in needle-leaf trees which can be a critical factor in forest resistance to drying climates. The generation of a large H at the leaf scale provides a basis for the development of the previously identified canopy-scale 'convector effect'.

Assessing model performance via the most limiting environmental driver in two differently stressed pine stands.

Climate change will impact forest productivity worldwide. Forecasting the magnitude of such impact, with multiple environmental stressors changing simultaneously, is only possible with the help of process-based models. In order to assess their performance, such models require careful evaluation against measurements. However, direct comparison of model outputs against observational data is often not reliable, as models may provide the right answers due to the wrong reasons. This would severely hinder forecasting abilities under unprecedented climate conditions. Here, we present a methodology for model assessment, which supplements the traditional output-to-observation model validation. It evaluates model performance through its ability to reproduce observed seasonal changes of the most limiting environmental driver (MLED) for a given process, here daily gross primary productivity (GPP). We analyzed seasonal changes of the MLED for GPP in two contrasting pine forests, the Mediterranean Pinus halepensis Mill. Yatir (Israel) and the boreal Pinus sylvestris L. Hyytiälä (Finland) from three years of eddy-covariance flux data. Then, we simulated the same period with a state-of-the-art process-based simulation model (LandscapeDNDC). Finally, we assessed if the model was able to reproduce both GPP observations and MLED seasonality. We found that the model reproduced the seasonality of GPP in both stands, but it was slightly overestimated without site-specific fine-tuning. Interestingly, although LandscapeDNDC properly captured the main MLED in Hyytiälä (temperature) and in Yatir (soil water availability), it failed to reproduce high-temperature and high-vapor pressure limitations of GPP in Yatir during spring and summer. We deduced that the most likely reason for this divergence is an incomplete description of stomatal behavior. In summary, this study validates the MLED approach as a model evaluation tool, and opens up new possibilities for model improvement.

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.

Method for accurate measurement of infrared emissivity for opaque low-reflectance materials.

Accurate determination of infrared (IR) emissivity is important for non-contact temperature measurement and for energy balance evaluation in systems that exchange radiation. A method for accurate measurement is proposed based on active modulation of the background radiation. The hemispherical directional reflectance is measured as a proxy for directional emissivity using an IR camera and an integrating sphere, while the background radiation is modulated using an IR emitter and a mechanical shutter. Measurement of the apparent temperature observed by the camera under two different illumination conditions allows the extraction of reflectance and emissivity. The accuracy of the measurement and its sensitivity to surface properties are analyzed, showing uncertainty values as low as 0.004 in some cases. Example measurements of natural and artificial surfaces are presented.

Investigation of ozone deposition to vegetation under warm and dry conditions near the Eastern Mediterranean coast.

Dry deposition of ozone (O3) to vegetation is an important removal pathway for tropospheric O3, while O3 uptake through plant stomata negatively affects vegetation and leads to climate change. Both processes are controlled by vegetation characteristics and ambient conditions via complex mechanisms. Recent studies have revealed that these processes can be fundamentally impacted by coastal effects, and by dry and warm conditions in ways that have not been fully characterized, largely due to lack of measurements under such conditions. Hence, we hypothesized that measuring dry deposition of O3 to vegetation along a sharp spatial climate gradient, and at different distances from the coast, can offer new insights into the characterization of these effects on O3 deposition to vegetation and stomatal uptake, providing important information for afforestation management and for climate and air-quality model improvement. To address these hypotheses, several measurement campaigns were performed at different sites, including pine, oak, and mixed Mediterranean forests, at distances of 20-59 km from the Eastern Mediterranean coast, under semiarid, Mediterranean and humid Mediterranean climate conditions. The eddy covariance technique was used to quantify vertical O3 flux (Ftot) and its partitioning to stomatal flux (Fst) and non-stomatal flux (Fns). Whereas Fst tended to peak around noon under humid Mediterranean and Mediterranean conditions in summer, it was strongly limited by drought under semiarid conditions from spring to early winter, with minimum average Fst/Ftot of 8-11% during the summer. Fns in the area was predominantly controlled by relative humidity (RH), whereas increasing Fns with RH for RH < 70% indicated enhancement of Fns by aerosols, via surface wetness stimulation. At night, efficient turbulence due to sea and land breezes, together with increased RH, resulted in strong enhancement of Ftot. Extreme dry surface events, some induced by dry intrusion from the upper troposphere, resulted in positive Fns events.

Assessing canopy performance using carbonyl sulfide measurements.

Carbonyl sulfide (COS) is a tracer of ecosystem photosynthesis that can advance carbon cycle research from leaf to global scales; however, a range of newly reported caveats related to sink/source strength of various ecosystem components hinder its application. Using comprehensive eddy-covariance and chamber measurements, we systematically measure ecosystem contributions from leaf, stem, soil, and litter and were able to close the ecosystem COS budget. The relative contributions of nonphotosynthetic components to the overall canopy-scale flux are relatively small (~4% during peak activity season) and can be independently estimated based on their responses to temperature and humidity. Converting COS to photosynthetic CO2 fluxes based on the leaf relative uptake of COS/CO2 , faces challenges due to observed daily and seasonal changes. Yet, this ratio converges around a constant value (~1.6), and the variations, dominated by light intensity, were found unimportant on a flux-weighted daily time-scale, indicating a mean ratio of daytime gross-to-net primary productivity of ~2 in our ecosystem. The seasonal changes in the leaf relative uptake ratio may indicate a reduction in mesophyll conductance in winter, and COS-derived canopy conductance permitted canopy temperature estimate consistent with radiative skin temperature. These results support the feasibility of using COS as a powerful and much-needed means of assessing ecosystem function and its response to change.

Large-scale semi-arid afforestation can enhance precipitation and carbon sequestration potential.

Afforestation is an important approach to mitigate global warming. Its complex interactions with the climate system, however, makes it controversial. Afforestation is expected to be effective in the tropics where biogeochemical and biogeophysical effects act in concert; however, its potential in the large semi-arid regions remains insufficiently explored. Here, we use a Global Climate Model to provide a process-based demonstration that implementing measured characteristics of a successful semi-arid afforestation system (2000 ha, ~300 mm mean annual precipitation) over large areas (~200 million ha) of similar precipitation levels in the Sahel and North Australia leads to the weakening and shifting of regional low-level jets, enhancing moisture penetration and precipitation (+0.8 ± 0.1 mm d-1 over the Sahel and +0.4 ± 0.1 mm d-1 over North Australia), influencing areas larger than the original afforestation. These effects are associated with increasing root depth and surface roughness and with decreasing albedo. This results in enhanced evapotranspiration, surface cooling and the modification of the latitudinal temperature gradient. It is estimated that the carbon sequestration potential of such large-scale semi-arid afforestation can be on the order of ~10% of the global carbon sink of the land biosphere and would overwhelm any biogeophysical warming effects within ~6 years.

Forest GPP Calculation Using Sap Flow and Water Use Efficiency Measurements.

This is a protocol to evaluate gross primary productivity (GPP) of a forest stand based on the measurements of tree's sap flow (SF), 13C derived water use efficiency (WUE), and meteorological (met) data. GPP was calculated from WUE and stomatal conductance (gs), the later obtained from SF up-scaled from sampled trees to stand level on a daily time-scale and met data. WUE is obtained from 13C measurements in dated tree-ring wood and/or foliage samples. This protocol is based on the recently published study of Klein et al., 2016 .

Resilience to seasonal heat wave episodes in a Mediterranean pine forest.

Short-term, intense heat waves (hamsins) are common in the eastern Mediterranean region and provide an opportunity to study the resilience of forests to such events that are predicted to increase in frequency and intensity. The response of a 50-yr-old Aleppo pine (Pinus halepensis) forest to hamsin events lasting 1-7 d was studied using 10 yr of eddy covariance and sap flow measurements. The highest frequency of heat waves was c. four per month, coinciding with the peak productivity period (March-April). During these events, net ecosystem carbon exchange (NEE) and canopy conductance (gc ) decreased by c. 60%, but evapotranspiration (ET) showed little change. Fast recovery was also observed with fluxes reaching pre-stress values within a day following the event. NEE and gc showed a strong response to vapor pressure deficit that weakened as soil moisture decreased, while sap flow was primarily responding to changes in soil moisture. On an annual scale, heat waves reduced NEE and gross primary productivity by c. 15% and 4%, respectively. Forest resilience to short-term extreme events such as heat waves is probably a key to its survival and must be accounted for to better predict the increasing impact on productivity and survival of such events in future climates.

Potential and limitations of inferring ecosystem photosynthetic capacity from leaf functional traits.

The aim of this study was to systematically analyze the potential and limitations of using plant functional trait observations from global databases versus in situ data to improve our understanding of vegetation impacts on ecosystem functional properties (EFPs). Using ecosystem photosynthetic capacity as an example, we first provide an objective approach to derive robust EFP estimates from gross primary productivity (GPP) obtained from eddy covariance flux measurements. Second, we investigate the impact of synchronizing EFPs and plant functional traits in time and space to evaluate their relationships, and the extent to which we can benefit from global plant trait databases to explain the variability of ecosystem photosynthetic capacity. Finally, we identify a set of plant functional traits controlling ecosystem photosynthetic capacity at selected sites. Suitable estimates of the ecosystem photosynthetic capacity can be derived from light response curve of GPP responding to radiation (photosynthetically active radiation or absorbed photosynthetically active radiation). Although the effect of climate is minimized in these calculations, the estimates indicate substantial interannual variation of the photosynthetic capacity, even after removing site-years with confounding factors like disturbance such as fire events. The relationships between foliar nitrogen concentration and ecosystem photosynthetic capacity are tighter when both of the measurements are synchronized in space and time. When using multiple plant traits simultaneously as predictors for ecosystem photosynthetic capacity variation, the combination of leaf carbon to nitrogen ratio with leaf phosphorus content explains the variance of ecosystem photosynthetic capacity best (adjusted R2 = 0.55). Overall, this study provides an objective approach to identify links between leaf level traits and canopy level processes and highlights the relevance of the dynamic nature of ecosystems. Synchronizing measurements of eddy covariance fluxes and plant traits in time and space is shown to be highly relevant to better understand the importance of intra- and interspecific trait variation on ecosystem functioning.

Association between sap flow-derived and eddy covariance-derived measurements of forest canopy CO2 uptake.

The carbon sink intensity of the biosphere depends on the balance between gross primary productivity (GPP) of forest canopies and ecosystem respiration. GPP, however, cannot be directly measured and estimates are not well constrained. A new approach relying on canopy transpiration flux measured as sap flow, and water-use efficiency inferred from carbon isotope analysis (GPPSF ) has been proposed, but not tested against eddy covariance-based estimates (GPPEC ). Here we take advantage of parallel measurements using the two approaches at a semi-arid pine forest site to compare the GPPSF and GPPEC estimates on diurnal to annual timescales. GPPSF captured the seasonal dynamics of GPPEC (GPPSF  = 0.99 × GPPEC , r(2)  = 0.78, RMSE = 0.82, n = 457 d) with good agreement at the annual timescale (653 vs 670 g C m(-2)  yr(-1) ). Both methods showed that GPP ranged between 1 and 8 g C m(-2)  d(-1) , and the GPPSF /GPPEC ratio was between 0.5 and 2.0 during 82% of the days. Carbon uptake dynamics at the individual tree scale conformed with leaf scale rates of net assimilation. GPPSF can produce robust estimations of tree- and canopy-scale rates of CO2 uptake, providing constraints and greatly extending current GPPEC estimations.

Differential ecophysiological response of a major Mediterranean pine species across a climatic gradient.

The rate of migration and in situ genetic variation in forest trees may not be sufficient to compete with the current rapid rate of climate change. Ecophysiological adjustments of key traits, however, could complement these processes and allow sustained survival and growth across a wide range of climatic conditions. This was tested in Pinus halepensis Miller by examining seven physiological and phenological parameters in five provenances growing in three common garden plots along a climatic transect from meso-Mediterranean (MM) to thermo-Mediterranean (TM) and semi-arid (SA) climates. Differential responses to variations in ambient climatic conditions were observed in three key traits: (i) growing season length decreased with drying in all provenances examined (from 165 under TM climate to 100 days under SA climate, on average); (ii) water use efficiency (WUE) increased with drying, but to a different extent in different provenances, and on average from 80, to 95, to 110 µmol CO(2) mol(-1) H(2)O under MM, TM and SA climates, respectively; (iii) xylem native embolism was stable across climates, but varied markedly among different provenances (percent loss of conductivity, was below 5% in two provenances and above 35% in others). The results indicated that changes in growing season length and WUE were important contributors to tree growth across climates, whereas xylem native embolism negatively correlated with tree survival. The results indicated that irrespective of slow processes (e.g., migration, genetic adaptation), the capacity for ecophysiological adjustments combined with existing variations among provenances could help sustain P. halepensis, a major Mediterranean tree species, under relatively extreme warming and drying climatic trends.

Contribution of semi-arid forests to the climate system.

Forests both take up CO2 and enhance absorption of solar radiation, with contrasting effects on global temperature. Based on a 9-year study in the forests' dry timberline, we show that substantial carbon sequestration (cooling effect) is maintained in the large dry transition zone (precipitation from 200 to 600 millimeters) by shifts in peak photosynthetic activities from summer to early spring, and this is counteracted by longwave radiation (L) suppression (warming effect), doubling the forestation shortwave (S) albedo effect. Several decades of carbon accumulation are required to balance the twofold S + L effect. Desertification over the past several decades, however, contributed negative forcing at Earth's surface equivalent to approximately 20% of the global anthropogenic CO2 effect over the same period, moderating warming trends.