(2021) Perspectives in Plant Ecology, Evolution and Systematics. 48, 125586. Abstract
The high-mountain ecosystems of Central Asia are a biodiversity hotspot with unique plant communities and many endemic species. Intense human pressure and global warming have caused habitat destruction in these areas and a parallel increase in the number of endangered species. Lagochilus species are key medicinal herbaceous plants native to Central Asia, many of which have been recently added to the endangered of species in Uzbekistan. To assess the climate sensitivity of Lagochilus species, we (1) located populations of six species in their native sites across Uzbekistan, and assessed their health by partitioning to ontogenetic stages along five consecutive years; (2) collected plant materials from these species, as well as from old herbarium samples (1918–1964); and (3) analyzed the carbon-13 composition in those samples, as an indicator for drouht stress. Over the course of five years (2014–2018) of continuous monitoring, fluctuations in annual precipitation in the region indicated a decrease by ∼20 %, and the fraction of young plants in each population decreased from 20–50% to 0–5 %, depending on the species. Comparing the carbon-13 composition in current and historical leaf samples showed an increase of 1.5–3.5‰ associated with a decrease in precipitation of 2–30 %, depending on the site and species. Our results show the high sensitivity of Lagochilus populations’ regeneration to drying, among six species and in sites across Uzbekistan. On a multi-decadal temporal scale, the dramatic changes in carbon-13 indicate that the response to precipitation reduction is related with drought stress. Considering the expectation for drier and hotter climate in Uzbekistan in the coming decades, conservation of Lagochilus populations should become a priority in Central Asia.
Physiological effects of mature tree transplanting characterize the roles of the soil-root interface in the field(2020) Agricultural and Forest Meteorology. 295, 108192. Abstract
The intimate connection between roots and soil particles is a prerequisite for the continuous flow of water and nutrients from soil to trees, and carbon flow from roots to the rhizosphere. The soil-root interface has been studied in multiple laboratory and greenhouse experiments. Yet its multiple roles and their differential contributions to tree health have rarely been experimentally studied on mature trees in the field. We took advantage of mature olive tree transplanting to test the physiological effects of breakage of the soil-root interface in situ. Eight olive trees were monitored following transplantation into a site located 4 km from their native site, along two years. Additional eight trees were monitored simultaneously at the native site, as control. To decrease mortality risk, transplanted trees were heavily pruned before transplanting, and were irrigated and fertilized in their new site. Transplanted trees had ~50% lower rates of leaf photosynthesis and transpiration; ~80% lower root starch content; and ~30% higher loss of xylem conductivity, than native trees. Leaf water potential (LWP) was similar across trees, becoming more negative in the transplanted trees only in the second year following transplanting. While starch content and xylem conductivity recovered in the second year, leaf gas exchange and LWP remained significantly lower than in native trees. Soil P and K were higher under transplanted trees that remained stressed than under trees that recovered. Breakage of the soil-root interface caused a multi-system stress to trees. The lack of persistent LWP response might indicate that loss of hydraulic conductivity was driven by root, rather than aboveground, embolisms. Degradation of starch in the roots indicates an increase in belowground sinks. In the long run, recovery of starch content means no carbon limitation; yet the prevailing effects on leaf activities suggest a long-term stress unrelated with water or carbon supply.
Enhanced root exudation of mature broadleaf and conifer trees in a Mediterranean forest during the dry season(2020) Tree Physiology. 40, 11, p. 1595-1605 Abstract
Root exudates are part of the rhizodeposition process, which is the major source of soil organic carbon (C) released by plant roots. This flux of C is believed to have profound effects on C and nutrient cycling in ecosystems. The quantity of root exudates depends on the plant species, the period throughout the year, and external biotic and abiotic factors. Since root exudates of mature trees are difficult to collect in field conditions, very little is known about their flux, especially in water-limited ecosystems, such as the seasonally hot and dry Mediterranean maquis. Here, we collected exudates from DNA-identified roots in the forest from the gymnosperm Cupressus sempervirens L. and the evergreen angiosperm Pistacia lentiscus L. by 48-h incubations on a monthly temporal resolution throughout the year. We examined relationships of the root exudate C flux to abiotic parameters of the soil (water content, water potential, temperature) and atmosphere (vapor pressure deficit, temperature). We also studied relationships to C fluxes through the leaves as indicators of tree C balance. Root exudation rates varied significantly along the year, increasing from 6 μg C cm -2 root day-1 in both species in the wet season to 4- and 11-fold rates in Pistacia and Cupressus, respectively, in the dry season. A stepwise linear mixed-effects model showed that the three soil parameters were the most influential on exudation rates. Among biotic factors, there was a significant negative correlation of exudation rate with leaf assimilation in Cupressus and a significant negative correlation with leaf respiration in Pistacia. Our observation of enhanced exudation flux during the dry season indicates that exudation dynamics in the field are less sensitive to the low tree C availability in the dry season. The two key Mediterranean forest species seem to respond to seasonal changes in the rhizosphere such as drying and warming, and therefore invest C in the rhizosphere under seasonal drought.
Tree Forensics: Modern DNA barcoding and traditional anatomy identify roots threatening an ancient necropolis(2020) Plants, People, Planet. Abstract
Tree roots have penetrated the ceiling of burial caves in a ~1,800‐years‐old necropolis in the Galilee, Israel, damaging the antiquities and risking the catacombs with collapse. Root identification was needed to enable selective cutting (at the species level), facilitating the conservation of the world heritage site, while maintaining the majority of trees growing on top of the burial caves. Samples of roots penetrating the cave ceilings were collected and identified both by using DNA barcoding, which has become a standard method for the reliable identification of organisms in their natural environment, and also by traditional morpho‐anatomical methods. However, woody plant species of the Mediterranean region are under‐represented in DNA databases. Therefore, we added relevant species to the ITS2 database by sequencing the internal transcribed spacer (ITS)2 of the 18S‐26S rDNA from sampled leaves of 19 woody species of the Mediterranean maquis. The identification of these tree species facilitated their selective removal, balancing antiquities, and nature conservation needs.
Rapid starch degradation in the wood of olive trees under heat and drought is permitted by three stress-specific beta amylases(2020) New Phytologist. Abstract
Carbon reserve use is a major drought response in trees, enabling tree survival in conditions prohibiting photosynthesis. However, regulation of starch metabolism under drought at the whole-tree scale is still poorly understood. To this end, we combined measurements of nonstructural carbohydrates (NSCs), tree physiology and gene expression. The experiment was conducted outside on olive trees in pots under 90 d of seasonal spring to summer warming. Half of the trees were also subjected to limited water conditions for 28 d. Photosynthesis decreased in dehydrating trees from 19 to 0.5 µmol m−2 s−1 during the drought period. Starch degradation and mannitol production were a major drought response, with mannitol increasing to 71% and 41% out of total NSCs in shoots and roots, respectively. We identified the gene family members potentially relevant either to long-term or stress-induced carbon storage. Partitioning of expression patterns among β amylase and starch synthase family members was observed, with three β amylases possibly facilitating the rapid starch degradation under heat and drought. Our results suggest a group of stress-related, starch metabolism genes, correlated with NSC fluctuations during drought and recovery. The daily starch metabolism gene expression was different from the stress-mode starch metabolism pattern, where some genes are uniquely expressed during the stress-mode response.
Intraspecific responses to climate reveal nonintuitive warming impacts on a widespread thermophilic conifer(2020) New Phytologist. 2, p. 525-540 Abstract
Many ecologically important forest trees from dry areas have been insufficiently investigated for their ability to adapt to the challenges posed by climate change, which hampers the implementation of mitigation policies. We analyzed 14 common-garden experiments across the Mediterranean which studied the widespread thermophilic conifer Pinus halepensis and involved 157 populations categorized into five ecotypes.Ecotype-specific tree height responses to climate were applied to projected climate change (2071-2100 ad), to project potential growth patterns both locally and across the species' range.We found contrasting ecotypic sensitivities to annual precipitation but comparatively uniform responses to mean temperature, while evidence of local adaptation for tree height was limited to mesic ecotypes. We projected intriguing patterns of response range-wide, implying either height inhibition or stimulation of up to 75%, and deduced that the ecotype currently experiencing more favorable (wetter) conditions will show the largest inhibition. Extensive height reductions can be expected for coastal areas of France, Greece, Spain and northern Africa.Our findings underline the fact that intraspecific variations in sensitivity to precipitation must be considered when projecting tree height responses of dry forests to future climate. The ecotype-specific projected performances call for management activities to ensure forest resilience in the Mediterranean through, for example, tailored deployment strategies.
(2020) Tree Physiology. 40, 4, p. 454-466 Abstract
Trees of the genus Prunus produce some of the most widely consumed fruits globally. The combination of climate change-related warming and increased drought stress, scarcity of freshwater resources for irrigation, and increasing demands due to population growth creates a need for increased drought tolerance in these tree species. Recently, we have shown in the field that a native wild pear species performs better under drought than two cultivated pear species. Here, a comparative field study was conducted in Israel to investigate traits associated with drought tolerance in almond (cultivated Prunus dulcis (Mill.) D. A. Webb vs wild Prunus ramonensis Danin) and plum (cultivated Prunus domestica L. vs wild Prunus ursina Kotschy). Measurements of xylem embolism and shoot and root carbon reserves were done along a year, including seasonal drought in the wild and a 35-day drought experiment in the orchards. Synchronous measurements of native xylem embolism and shoot water potential showed that cultivated and wild almond trees lost similar to 50% of hydraulic conductivity at -2.3 and -3.2 MPa, respectively. Micro-CT images confirmed the higher embolism ratio in cultivated versus wild almond, whereas the two plum species were similar. Dynamics of tissue concentrations of nonstructural carbohydrates were mostly similar across species, with higher levels in cultivated versus wild plum. Our results indicate an advantage for the wild almond over its cultivated relative in terms of xylem resistance to embolism, a major risk factor for trees under drought stress. This result is in line with our previous experiment on pear species. However, the opposite trends observed among the studied plum species mean that these trends cannot be generalized. It is possible that the potential for superior drought tolerance in wild tree species, relative to their cultivated relatives, is limited to wild species from dry and hot habitats.
Tree rings reveal the adverse effect of water pumping on protected riparian Platanus orientalis tree growth(2020) Forest Ecology and Management. 458, 117784. Abstract
The ongoing increase in human population and the subsequent freshwater demands raise conflicts regarding conservation of riparian ecosystems. Identifying anthropogenic effects on these vulnerable nature resources is crucial for preventing future damages. Here we measured tree-ring width and isotopic carbon composition (delta C-13) in stem wood of protected Platanus orientalis trees at the Kziv Nature Reserve, a Mediterranean riparian ecosystem in northern Israel. In this reserve, water was pumped for human needs during 1976-2006 from the major spring feeding the stream. We show a negative exponential correlation between stem growth and pumped water amounts. Spring drawdown had a significant negative effect on growth even in years when amounts were reduced to similar to 2.10(6)m(3) year(-1), leveling off at around 5.10(6) m(3) year(-1). Precipitation and spring volume effects on growth were exposed only after pumping stopped, further indicating its role in inhibiting tree growth. During the pumping years, stem wood delta C-13 was up to 1.8%0 higher than after pumping cessation, indicating the drought stress imposed on trees. Our results provide an unequivocal evidence for the adverse effect of water pumping on riparian Platanus orientalis tree growth. Such effects, and their related tree mortality risk, must be considered in sustainable water management planning.
Correction: Exposing the hidden half: root research at the forefront of science (vol 41, pg 235, 2019)(2020) Plant and Soil. 447, 1-2, p. 7-8 Abstract
In the published version of this editorial paper, the sentence in the first paragraph should be corrected as shown below: This special section of Plant and Soil contains 13 contributions based on presentations at the 10th Symposium of the International Society of Root Research (ISRR10), which took place in Israel from 8 to 12 July, 2018.
(2020) Plant and Soil. 447, 1-2, p. 1-5 Abstract
This special section of Plant and Soil contains 12 contributions based on presentations at the 10th Symposium of the International Society of Root Research (ISRR10), which took place in Israel from 8 to 12 July, 2018 (https://www.ortra.com/events/isrr10/Home.aspx). The symposium promoted fundamental understanding of the diverse aspects of root biology. The symposium, titled: “Exposing the Hidden Half - Root Research at the Forefront of Science”, assembled multiple disciplines in order to facilitate exploration of novel approaches and investigation of complex processes and mechanisms. The intersections of root physiology, root development, root architecture and root interactions with the environment were tackled by researchers from around the globe through oral presentations, poster sessions and discussions. Basic research at multiple scales (proteins, cells, tissues and the root system as a whole) and cutting-edge methodologies were highlighted as important means to advance plant health and growth, thereby supporting sustainable and nutritious food production.
Stomatal optimization based on xylem hydraulics (SOX) improves land surface model simulation of vegetation responses to climate(2020) New Phytologist. 6, p. 1622-1637 Abstract[All authors]
Land surface models (LSMs) typically use empirical functions to represent vegetation responses to soil drought. These functions largely neglect recent advances in plant ecophysiology that link xylem hydraulic functioning with stomatal responses to climate.We developed an analytical stomatal optimization model based on xylem hydraulics (SOX) to predict plant responses to drought. Coupling SOX to the Joint UK Land Environment Simulator (JULES) LSM, we conducted a global evaluation of SOX against leaf- and ecosystem-level observations.SOX simulates leaf stomatal conductance responses to climate for woody plants more accurately and parsimoniously than the existing JULES stomatal conductance model. An ecosystem-level evaluation at 70 eddy flux sites shows that SOX decreases the sensitivity of gross primary productivity (GPP) to soil moisture, which improves the model agreement with observations and increases the predicted annual GPP by 30% in relation to JULES. SOX decreases JULES root-mean-square error in GPP by up to 45% in evergreen tropical forests, and can simulate realistic patterns of canopy water potential and soil water dynamics at the studied sites.SOX provides a parsimonious way to incorporate recent advances in plant hydraulics and optimality theory into LSMs, and an alternative to empirical stress factors.
(2020) Nature Communications. 11, 1, 545. Abstract[All authors]
Severe droughts have the potential to reduce forest productivity and trigger tree mortality. Most trees face several drought events during their life and therefore resilience to dry conditions may be crucial to long-term survival. We assessed how growth resilience to severe droughts, including its components resistance and recovery, is related to the ability to survive future droughts by using a tree-ring database of surviving and now-dead trees from 118 sites (22 species, >3,500 trees). We found that, across the variety of regions and species sampled, trees that died during water shortages were less resilient to previous non-lethal droughts, relative to coexisting surviving trees of the same species. In angiosperms, drought-related mortality risk is associated with lower resistance (low capacity to reduce impact of the initial drought), while it is related to reduced recovery (low capacity to attain pre-drought growth rates) in gymnosperms. The different resilience strategies in these two taxonomic groups open new avenues to improve our understanding and prediction of drought-induced mortality.
A race to the unknown: Contemporary research on tree and forest drought resistance, an Israeli perspective(2020) Journal of Arid Environments. 172, 104045. Abstract
Forestry at the dry edge of forest existence has been a long-lasting interest to arid land residents. Current land-use and climate changes have broaden this interest to the global society, seeking for improved tree and forest drought resistance across biomes. Within this transition, Israel is a hub for scientific research and testing ground alike. Israel is a small country, spanning over arid, semi-arid, and thermo-Mediterranean environments, with relatively little forest. Nevertheless afforestation efforts have been unprecedented (by percent change in land cover), and many of these forests serve today as a 'living lab' for forest and tree drought resistance research. Considering the ongoing warming and drying, tree physiologists, forest ecologists, and forest managers in Israel are running a race to the unknown. To ensure local forest sustainability for future generations, the gap between the increased drought risk on the one hand, and the rather stationary forest drought resistance on the other hand, must be closed. The aim of this review is to highlight the findings and achievements, as well as challenges, of this contemporary research. Examples from Israel are given at the Middle East, and the wider, global arid land, contexts. In particular, important progress has been made in the following aspects: (1) the physiology of tree drought resistance, including water-use traits and phenology; (2) the genetic approach, advancing from provenance trials, to the application of molecular tools in the identification of tree drought resistance mechanisms; (3) the canopy flux measurement approach, e.g. monitoring the exchange of carbon, water, and energy in water-limited forests; (4) the application of remote sensing tools, such as satellite-based vegetation indices; and (5) the application of adaptive management practices in increasing forest resilience under drought. Taken together, these advances represent a way forward, while indicating important gaps, and open questions to future research. Lessons learnt in forests in Israel should be useful and transferable to other forest ecosystems in the Middle East, the Mediterranean, and additional water-limited regions.
(2020) Global Change Biology. 26, 1, p. 119-188 Abstract
Plant traits-the morphological, anatomical, physiological, biochemical and phenological characteristics of plants-determine how plants respond to environmental factors, affect other trophic levels, and influence ecosystem properties and their benefits and detriments to people. Plant trait data thus represent the basis for a vast area of research spanning from evolutionary biology, community and functional ecology, to biodiversity conservation, ecosystem and landscape management, restoration, biogeography and earth system modelling. Since its foundation in 2007, the TRY database of plant traits has grown continuously. It now provides unprecedented data coverage under an open access data policy and is the main plant trait database used by the research community worldwide. Increasingly, the TRY database also supports new frontiers of trait-based plant research, including the identification of data gaps and the subsequent mobilization or measurement of new data. To support this development, in this article we evaluate the extent of the trait data compiled in TRY and analyse emerging patterns of data coverage and representativeness. Best species coverage is achieved for categorical traits-almost complete coverage for 'plant growth form'. However, most traits relevant for ecology and vegetation modelling are characterized by continuous intraspecific variation and trait-environmental relationships. These traits have to be measured on individual plants in their respective environment. Despite unprecedented data coverage, we observe a humbling lack of completeness and representativeness of these continuous traits in many aspects. We, therefore, conclude that reducing data gaps and biases in the TRY database remains a key challenge and requires a coordinated approach to data mobilization and trait measurements. This can only be achieved in collaboration with other initiatives.
(2020) Molecular Ecology. 13, p. 2321-2333 Abstract
The mutualistic symbiosis between forest trees and ectomycorrhizal fungi (EMF) is among the most ubiquitous and successful interactions in terrestrial ecosystems. Specific species of EMF are known to colonize specific tree species, benefitting from their carbon source, and in turn, improving their access to soil water and nutrients. EMF also form extensive mycelial networks that can link multiple root-tips of different trees. Yet the number of tree species connected by such mycelial networks, and the traffic of material across them, are just now under study. Recently we reported substantial belowground carbon transfer between Picea, Pinus, Larix and Fagus trees in a mature forest. Here, we analyze the EMF community of these same individual trees and identify the most likely taxa responsible for the observed carbon transfer. Among the nearly 1,200 EMF root-tips examined, 50%-70% belong to operational taxonomic units (OTUs) that were associated with three or four tree host species, and 90% of all OTUs were associated with at least two tree species. Sporocarp C-13 signals indicated that carbon originating from labelled Picea trees was transferred among trees through EMF networks. Interestingly, phylogenetically more closely related tree species exhibited more similar EMF communities and exchanged more carbon. Our results show that belowground carbon transfer is well orchestrated by the evolution of EMFs and tree symbiosis.
(2019) Forest Ecology and Management. 453, 117573. Abstract
Drought-induced productivity reductions and tree mortality have been increasing in recent decades in forests around the globe. Prescribed reduction in stand density, i.e. thinning, has been proposed as a management tool to improve forest sustainability in face of a warmer, drier future. Thinning should potentially reduce net stand water use and improve water-availability for remaining trees, thus reducing their subsequent drought vulnerability. However, few studies have directly measured these effects.In 2009 we established a large-scale thinning experiment in a semi-arid, 40-years-old pine afforestation. Study plots (70 x 70 m) were thinned to 100,200, and 300 trees ha(-1), and compared with unthinned control plots (210-400 trees ha(-1)), each at five replications. Stem and needle growth, and needle gas exchange were measured along 3-9 consecutive years at seasonal to annual temporal resolution. Measurements at the tree-scale were further up-scaled using both simple upscaling relationships and using an ecosystem model of coupled carbon, energy and hydrology (Regional Hydro Ecologic Simulation System, RHESSys).At the needle scale, photosynthesis was 70% higher at the 100 trees ha(-1) than at 300 trees ha(-1), whereas transpiration was merely 10% higher. Consequently, stem and needle growth increased by 100% and 20%, respectively. For most parameters, there was little change between 200 and 100 trees ha(-1). Applying RHESSys at the stand-scale, these effects on tree physiology translated into 35% reduction in CO2 uptake and a 47% reduction in tree water-use, which was compensated for by increased evaporation from exposed soil.Our long-term measurements at the dry timberline highlight the role of thinning in enhancing the activity and growth of remaining trees, with increased water-use efficiency. Unexpectedly, this density reduction was associated with a relatively small decrease in forest carbon uptake. Light availability was a limiting factor in the higher density plots, even in our light-abundant forest.
Drought tolerance mechanisms and aquaporin expression of wild vs. cultivated pear tree species in the field(2019) Environmental and Experimental Botany. 167, 103832. Abstract
Water availability is becoming a limiting factor with increasing world population that challenges global food security. Thus, we need to enhance cultivation in increasingly drier and hotter climate and prepare fruit trees for the ongoing climate change. Wild tree species might offer vital information and plant material in face of these challenges.A year-long comparative field study was conducted to investigate the mechanisms underlying drought tolerance in pear species (cultivated Pyrus communis and Pyrus pyrifolia vs. the wild Pyrus syriaca).We confirmed the hypothesis of higher drought tolerance in wild pear compared to its cultivated relative. P. syriaca xylem had fewer, narrower vessels, and lower vulnerability to embolism. It showed higher intrinsic water-sue efficiency and more robust seasonal patterns of photosynthesis, hydraulic conductivity, and PIP (plasma intrinsic protein) aquaporin expression. Across species, we identified a ubiquitous gene (PIP1:5/1:6), nine drought-inhibited genes, and two drought-induced genes (PIP1:4 and 2:6/2:7, confirming previous studies).Our study highlights the potential of using wild relatives of fruit tree species to prepare key crops to a drier and hotter future. The study of PIPS leads the way to a more focused research of the role of these cellular water channels in minimizing tree water loss under drought, while ensuring hydration of specific tissues.
Increased Nitrogen Availability in the Soil Under Mature Picea abies Trees Exposed to Elevated CO2 Concentrations(2019) Frontiers in forests and global change. 2, 59. Abstract
The response of trees to increasing atmospheric CO2 concentrations is often mediated by the availability of nutrients. However, little is known about the influence of CO2 enrichment on nutrient availability in forests with mature trees. We studied processes in the soil under five 35-m-tall Norway spruce trees (Picea abies) in NW Switzerland that were exposed to a mean CO2 concentration of 550 ppm for 5 growing seasons using free air CO2 enrichment (FACE). We compared them with values from the soil under five control trees. Ceramic suction cups were installed in the soil under each tree to collect soil solution, and ion-exchange resin bags were buried in the soil to absorb ammonium and nitrate. Soil cores taken at the end of the experiment were used to measure the gross production of ammonium and nitrate by the 15N dilution technique. Although temporally and spatially variable, the nitrate concentration was higher in the soil solution under CO2-enriched trees. This effect was reflected in the resin bag extracts, which additionally indicated a trend of increased ammonium availability. Dissolved reduced N concentration (mainly dissolved organic N), however, was lower in the soil solution under CO2-enriched trees. K and Mg, and to a lesser extent Na and sulfate concentrations increased in the soil solution. P concentrations mostly remained below the detection limit. In spite of the higher concentrations of nitrate in soil extracts, gross N mineralization and nitrification rates were not affected by FACE. Needles from CO2-enriched trees contained slightly more N. No difference was observed for other nutrients. Overall, these results support the hypothesis of a priming effect, i.e., that FACE led to the production of more root exudates, which in turn stimulated soil biological activity, including mineralization, over a time-span of at least several years. However, these tall trees showed no growth response to elevated CO2; hence, they gained no advantage from increased nitrate in the soil solution, presumably owing to other growth constraints including P and Mg availability.
(2019) Functional Ecology. 33, 8, p. 1411-1424 Abstract
The response of tree leaf gas exchange to elevated CO2 concentrations has been investigated in numerous experiments along the past 30 years. Stomatal regulation is a major plant control over leaf gas exchange, and the response to the increasing CO2 will shape the biological activity of forests in the future. Here, we collected 144 records from 57 species on stomatal conductance in CO2 manipulation experiments on trees (340-980 ppm CO2). CO2-induced stomatal downregulation was calculated as the slope of the linear regression between stomatal conductance and [CO2]. Among tree species, the slope (a) of change in stomatal conductance per 100 ppm CO(2 )increase ranged between 0 and -151, indicating stomatal downregulation, and only four species showed upregulation. There was a significant divergence between evergreen gymnosperms (a = -3.6 +/- 1.0), deciduous angiosperms (a = -16.3 +/- 3.1) and evergreen angiosperms (a = -32.8 +/- 7.1). Gymnosperms were less sensitive to CO2 changes than deciduous angiosperms even when considering only field experiments. The significant role of tree functional group in predicting CO2-induced stomatal downregulation was detected in multiple mixed-effect models, with p values ranging between 0.0002 and 0.0295. The significantly higher stomatal sensitivity to CO2 of angiosperms versus gymnosperms might be related to the overall higher stomatal conductance of angiosperms; their thinner leaves, in turn losing water faster; and the decreasing atmospheric [CO2] at the time of their taxa diversification. We conclude that species differences must be taken into account in forecasting future forest fluxes. A plain language summary is available for this article.
Use of thermal imaging to detect evaporative cooling in coniferous and broadleaved tree species of the Mediterranean maquis(2019) Agricultural and Forest Meteorology. 271, p. 285-294 Abstract
Among forest types, the Mediterranean maquis is specifically exposed to fluctuations in water availability. Therefore, monitoring the water-use patterns of its major tree species is key in quantifying the local and regional water balance. However, the traditional measurement methods of tree water-use at high spatial scales are difficult and labor-intensive, thus indirect methods become useful. Evaporation of water from the stomatal pores on the leaf surface involves evaporative cooling, and hence the differences between the leaf temperature and its surrounding air temperature (ΔT
leaf-air ) can serve as a reliable estimator for tree water-use. Here, we used direct measurement of transpiration rate (E) with a gas exchange system, simultaneously with ground Thermal Infra-Red (TIR) imaging to study the relationship between ΔT
leaf-air and E in dominant tree species of the Mediterranean maquis. Controlled experiments were conducted in parallel with measurements in the forest, on five tree species of contrasting leaf shapes (Conifers: Pinus halepensis; Cupressus sempervirens; Broadleaf: simple: Quercus calliprinos; Ceratonia siliqua; compound: Pistacia lentiscus). Next, we used a quantitative approach, applying a leaf energy balance model to estimate E from the TIR images and compared it to the direct measurement of the gas exchange system. We report evaporative cooling across the five species, replicated in tree saplings and in mature trees in the forest. The conifers were significantly cooler than broadleaves by up to ∼4 °C and produced narrower ΔT
leaf-air ranges. Estimations of E from ΔT
leaf-air were relatively close to the observed E, with some overestimations. Our observations show that TIR imaging can detect transpiration-related differences in ΔT
leaf-air among species and can be used to estimate E in natural environments. Yet, the dependence of ΔT
leaf-air on E is species-specific and thus, empirical associations must be developed separately for each of the species.
Mortality versus survival in drought-affected Aleppo pine forest depends on the extent of rock cover and soil stoniness(2019) Functional Ecology. 33, 5, p. 901-912 Abstract
Drought-related tree mortality had become a widespread phenomenon in forests around the globe. This process leading to these events and its complexity is not fully understood. Trees in the dry timberline are exposed to ongoing drought, and the available water for transpiration in the soil can determine their survival chances. Recent drought years led to 5%–10% mortality in the semi-arid pine forest of Yatir (Israel). The distribution of dead trees was, however, highly heterogeneous with parts of the forest showing >80% dead trees (D plots) and others with mostly live trees (L plots). At the tree level, visible stress was associated with low pre-dawn leaf water potential at the dry season (−2.8 MPa vs. −2.3 MPa in non-stressed trees), shorter needles (5.5 vs. 7.7 mm) and lower chlorophyll content (0.6 vs. 1 mg/g dw). Trends in tree-ring widths reflected differences in stress intensity (30% narrower rings in stressed compared with unstressed trees), which could be identified 15–20 years prior to mortality. At the plot scale, no differences in topography, soil type, tree age or stand density could explain the mortality difference between the D and L plots. It could only be explained by the higher surface rock cover and in stoniness across the soil profile in the L plots. Simple bucket model simulations using the site’s long-term hydrological data supported the idea that these differences could result in higher soil water concentration (m 3 /m 3 ) in the L plots and extend the time above wilting point by several months across the long dry season. Accounting for subsurface heterogeneity may therefore critical to assessing stand-level response to drought and projecting tree survival, and can be used in management strategies in regions undergoing drying climate trends.[All authors]
A nation-wide analysis of tree mortality under climate change: Forest loss and its causes in Israel 1948-2017(2019) Forest Ecology and Management. 432, p. 840-849 Abstract
Is tree mortality increasing? Are recent mortality events related to climate change? Which tree species are the most affected? Many case studies have been published in the last decade, but the necessary large-scale and long-term knowledge is still missing.Here we combined data from forest surveys and satellite imagery, to create the first spatial tree mortality history at the national scale. Israel is a small country with only 7% forest cover, but its large environmental diversity and mosaic of many, small, forest areas makes it a good 'miniature model' for the task.Tree mortality events have been increasing significantly since 1991 and correlated well with drought. Among mortality events, 24% of the loss was directly related to drought, and 58% to fire, with 69% of fires occurring over a drought background. Conifers were disproportionally more affected than native broadleaved trees.This is the first national-scale study of tree mortality dynamics, and it confirms the suspected increase in this phenomenon in recent decades, and the dominant role of drought. Our study opens a way to a better, multi-source monitoring future for forest management and ensuring forest sustainability under climate change.
(2019) Frontiers in Plant Science. 9, 1964. Abstract
Tree mortality is a key driver of forest dynamics and its occurrence is projected to increase in the future due to climate change. Despite recent advances in our understanding of the physiological mechanisms leading to death, we still lack robust indicators of mortality risk that could be applied at the individual tree scale. Here, we build on a previous contribution exploring the differences in growth level between trees that died and survived a given mortality event to assess whether changes in temporal autocorrelation, variance, and synchrony in time-series of annual radial growth data can be used as early warning signals of mortality risk. Taking advantage of a unique global ring-width database of 3065 dead trees and 4389 living trees growing together at 198 sites (belonging to 36 gymnosperm and angiosperm species), we analyzed temporal changes in autocorrelation, variance, and synchrony before tree death (diachronic analysis), and also compared these metrics between trees that died and trees that survived a given mortality event (synchronic analysis). Changes in autocorrelation were a poor indicator of mortality risk. However, we found a gradual increase in inter- annual growth variability and a decrease in growth synchrony in the last similar to 20 years before mortality of gymnosperms, irrespective of the cause of mortality. These changes could be associated with drought-induced alterations in carbon economy and allocation patterns. In angiosperms, we did not find any consistent changes in any metric. Such lack of any signal might be explained by the relatively high capacity of angiosperms to recover after a stress-induced growth decline. Our analysis provides a robust method for estimating early-warning signals of tree mortality based on annual growth data. In addition to the frequently reported decrease in growth rates, an increase in inter-annual growth variability and a decrease in growth synchrony may be powerful predictors of gymnosperm mortality risk, but not necessarily so for angiosperms.[All authors]
(2018) Oecologia. 188, 3, p. 695-705 Abstract
Drought-induced tree mortality has been recently increasing and is expected to increase further under warming climate. Conversely, tree species that survive under arid conditions might provide vital information on successful drought resistance strategies. Although Acacia (Vachellia) species dominate many of the globe's deserts, little is known about their growth dynamics and water-use in situ. Stem diameter dynamics, leaf phenology, and sap flow were monitored during 3 consecutive years in five Acacia raddiana trees and five Acacia tortilis trees in the Arid Arava Valley, southern Israel (annual precipitation 20-70mm, restricted to October-May). We hypothesized that stem growth and other tree activities are synchronized with, and limited to single rainfall or flashflood events. Unexpectedly, cambial growth of both Acacia species was arrested during the wet season, and occurred during most of the dry season, coinciding with maximum daily temperatures as high as 45 degrees C and vapor pressure deficit of up to 9kPa. Summer growth was correlated with peak sap flow in June, with almost year-round activity and foliage cover. To the best of our knowledge, these are the harshest drought conditions ever documented permitting cambial growth. These findings point to the possibility that summer cambial growth in Acacia under hyper-arid conditions relies on concurrent leaf gas exchange, which is in turn permitted by access to deep soil water. Soil water can support low-density tree populations despite heat and drought, as long as recharge is kept above a minimum threshold.
Ecotypic variation and stability in growth performance of the thermophilic conifer Pinus halepensis across the Mediterranean basin(2018) Forest Ecology and Management. 424, p. 205-215 Abstract
The combined effects of local adaptation and phenotypic plasticity influencing plant performance are relevant to understand the capacity for genetic responses to climate change. Pima halepensis is a native species of low- to mid-elevation Mediterranean forests with a high ecological value in drought-prone areas. Thus, it is of utmost importance to determine its adaptive structure for key traits such as growth or survival. Here, we analyse a highly unbalanced dataset collated from different common-garden networks that cover the distribution range of the species. A total of 82 range-wide populations were evaluated in nine Mediterranean trials located in Israel, Italy and Spain. A climate classification of populations allowed for the definition of six different groups, or ecotypes, which showed contrasting performances for tree height and survival at age 15. The effects of ecotypic differentiation and among-ecotypes genetic variation in plasticity were disentangled by fitting stability models accounting for interaction and heteroscedasticity in genotype-by-environment tables. For growth, a Finlay-Wilkinson model suggested high predictability of ecotypic plastic responses in P. halepensis, as described by different linear reaction norms. However, differences in mean height of ca. 15% among ecotypes dominated infra-specific patterns of tree growth across trials, pointing to preponderance of genotypic adaptation over differential ecotypic plasticity in this species. For survival, ecotypic differences were approximately constant across trials, suggesting lack of genotype-by-environment effects. Sub-humid cool climate populations from the eastern Mediterranean (e.g., Greek populations) showed general adaptation and high sensitivity to improved growing conditions, as opposed to populations from the driest ecological extreme of the species (e.g., south Spain and Maghreb populations), which exhibited specific adaptation to harsh environments. Altogether, our results indicate a general adaptive syndrome by which less reactive ecotypes to ameliorated conditions (e.g., non-water-limited) would be associated with high survival rates and low growth. The reported ecotypic differentiation constitutes the basis for tailoring infra-specific responses to climate and disentangling the relationship between adaptive variation and resilience towards climatic warming for this exemplary Mediterranean pine.
Xylem embolism refilling and resilience against drought-induced mortality in woody plants: processes and trade-offs(2018) Ecological Research. 33, 5, p. 839-855 Abstract
Understanding which species are able to recover from drought, under what conditions, and the mechanistic processes involved, will facilitate predictions of plant mortality in response to global change. In response to drought, some species die because of embolism-induced hydraulic failure, whilst others are able to avoid mortality and recover, following rehydration. Several tree species have evolved strategies to avoid embolism, whereas others tolerate high embolism rates but can recover their hydraulic functioning upon drought relief. Here, we focus on structures and processes that might allow some plants to recover from drought stress via embolism reversal. We provide insights into how embolism repair may have evolved, anatomical and physiological features that facilitate this process, and describe possible trade-offs and related costs. Recent controversies on methods used for estimating embolism formation/repair are also discussed, providing some methodological suggestions. Although controversial, embolism repair processes are apparently based on the activity of phloem and ray/axial parenchyma. The mechanism is energetically demanding, and the costs to plants include metabolism and transport of soluble sugars, water and inorganic ions. We propose that embolism repair should be considered as a possible component of a hydraulic efficiency-safety' spectrum. We also advance a framework for vegetation models, describing how vulnerability curves may change in hydrodynamic model formulations for plants that recover from embolism.[All authors]
Elevated CO2 compensates for drought effects in lemon saplings via stomatal downregulation, increased soil moisture, and increased wood carbon storage(2018) Environmental and Experimental Botany. 148, p. 117-127 Abstract
Tree growth enhancement under elevated [CO2] is much smaller than originally anticipated; yet carbon overabundance can lead to increased wood carbon storage and to stomata] downregulation and hence reduced water use. Notably, all three outcomes increase tree drought resistance. Here we studied growth, water relations, and nonstructural carbohydrates of 60 lemon saplings growing in CO2-controlled rooms at the same greenhouse, under 400, 650, and 850 ppm (CO2]. At each [CO2] level, 10 saplings were exposed to 1-month dry-down after 2 months of standard irrigation, followed by re-watering for another month. The other 10 saplings served as controls. Under drought, tree growth was maintained at elevated, but not ambient, CO2, linked with mild vs. severe tree water stress (leaf water potential of 3.5 at elevated and 5.5 MPa at ambient [CO2]). Stomatal downregulation with increasing [CO2] meant that leaf transpiration and diurnal plant water-use were 13-46% lower at elevated vs. ambient [CO2] but photosynthesis was still 15-25% higher. CO2-induced increases in root and shoot starch were transient but significant. Our results suggest that when predicting tree growth in a warmer and drier future, concomitant atmospheric CO2 concentration must be considered. In young lemon trees, elevated CO2 partially compensated for drought effects on tree growth and water status, and might delay some of the effects of the anthropogenic climate change.
Ecosystem dynamics and management after forest die-off: a global synthesis with conceptual state-and-transition models(2017) Ecosphere. 8, 12, 02034. Abstract
Broad-scale forest die-off associated with drought and heat has now been reported from every forested continent, posing a global-scale challenge to forest management. Climate-driven die-off is frequently compounded with other drivers of tree mortality, such as altered land use, wildfire, and invasive species, making forest management increasingly complex. Facing similar challenges, rangeland managers have widely adopted the approach of developing conceptual models that identify key ecosystem states and major types of transitions between those states, known as "state-and-transition models" (S&T models). Using expert opinion and available research, the development of such conceptual S&T models has proven useful in anticipating ecosystem changes and identifying management actions to undertake or to avoid. In cases where detailed data are available, S&T models can be developed into probabilistic predictions, but even where data are insufficient to predict transition probabilities, conceptual S&T models can provide valuable insights for managing a given ecosystem and for comparing and contrasting different ecosystem dynamics. We assembled a synthesis of 14 forest die-off case studies from around the globe, each with sufficient information to infer impacts on forest dynamics and to inform management options following a forest die-off event. For each, we developed a conceptual S&T model to identify alternative ecosystem states, pathways of ecosystem change, and points where management interventions have been, or may be, successful in arresting or reversing undesirable changes. We found that our diverse set of mortality case studies fit into three broad classes of ecosystem trajectories: (1) single-state transition shifts, (2) ecological cascading responses and feedbacks, and (3) complex dynamics where multiple interactions, mortality drivers, and impacts create a range of possible state transition responses. We integrate monitoring and management goals in a framework aimed to facilitate development of conceptual S&T models for other forest die-off events. Our results highlight that although forest die-off events across the globe encompass many different underlying drivers and pathways of ecosystem change, there are commonalities in opportunities for successful management intervention.[All authors]
(2017) URBAN FORESTRY & URBAN GREENING. 24, p. 1-4 Abstract
Green roofs provide many ecosystem services such as regulation of building temperatures, reducing urban heat-island effects and draining rainwater. In addition, they are expected to reduce the high levels of CO2 concentrations in big cities. Previous CO2 fixation studies on green roofs were done by taking long-timeperiod samples using expensive equipment and with limited replication. To plan green roofs for optimal CO2 reduction, a simple method to quantify CO2 fixation rate in relation to plant species-composition is required. The method we tested is direct measurement of CO2 concentrations with a portable air-quality meter, which allows a large number of samples. Here we focus on differences in the photosynthetic effect between plots containing the local Mediterranean succulent, Sedum sediforme and plots containing various annuals. In a factorial design (presence or absence of Sedum crossed with presence or absence of annuals), we tested the effect of sedum and annual treatments on CO2 concentrations. To compare our results with a commonly used method, and to evaluate the role of the different species, we examined the photosynthetic activity at the single plant level under these treatments by using a portable gas-exchange measuring system. We found that our method can detect the effect of different green roof plots and can be used as a simple and reliable tool for green-roof planers. We found that annuals reduced CO2 concentrations, but only in the absence of Sedum. Sedum alone had no effect on CO2 concentrations. This emphasizes the importance of integrating plots with annual plants in Sedum-based green roofs. (C) 2017 Elsevier GmbH. All rights reserved.
(2017) Science of the Total Environment. 584, p. 1147-1151 Abstract
Green roofs are expected to absorb and store carbon in plants and soils and thereby reduce the high CO2 concentration levels in big cities. Sedum species, which are succulent perennials, are commonly used in extensive green roofs due to their shallow root system and ability to withstand long water deficiencies. Here we examined CO2 fixation and emission rates for Mediterranean Sedum sediforme on green-roof experimental plots. During late winter to early spring, we monitored CO2 concentrations inside transparent tents placed over 1 m(2) plots and followed gas exchange at the leaf level using a portable gas-exchange system. We found high rates of CO2 emission at daytime, which is when CO2 concentration in the city is the highest Both plot- and leaf-scale measurements showed that these CO2 emissions were not fully compensated by the nighttime uptake. We conclude that although carbon sequestration may only be a secondary benefit of green roofs, for improving this ecosystem service, other plant species than Sedum should also be considered for use in green roofs, especially in Mediterranean and other semi-arid climates. (C) 2017 Elsevier B.V. All rights reserved.
(2016) Proceedings of the National Academy of Sciences of the United States of America. 113, 46, p. 13098-13103 Abstract
Climate change is expected to exacerbate drought for many plants, making drought tolerance a key driver of species and ecosystem responses. Plant drought tolerance is determined by multiple traits, but the relationships among traits, either within individual plants or across species, have not been evaluated for general patterns across plant diversity. We synthesized the published data for stomatal closure, wilting, declines in hydraulic conductivity in the leaves, stems, and roots, and plant mortality for 262 woody angiosperm and 48 gymnosperm species. We evaluated the correlations among the drought tolerance traits across species, and the general sequence of water potential thresholds for these traits within individual plants. The trait correlations across species provide a framework for predicting plant responses to a wide range of water stress from one or two sampled traits, increasing the ability to rapidly characterize drought tolerance across diverse species. Analyzing these correlations also identified correlations among the leaf and stem hydraulic traits and the wilting point, or turgor loss point, beyond those expected from shared ancestry or independent associations with water stress alone. Further, on average, the angiosperm species generally exhibited a sequence of drought tolerance traits that is expected to limit severe tissue damage during drought, such as wilting and substantial stem embolism. This synthesis of the relationships among the drought tolerance traits provides crucial, empirically supported insight into representing variation in multiple traits in models of plant and ecosystem responses to drought.
(2016) Journal of Ecology. 104, 6, p. 1720-1733 Abstract
Are mature forests carbon limited? To explore this question, we exposed ca. 110-year-old, 40-m tall Picea abies trees to a 550-ppm CO2 concentration in a mixed lowland forest in NW Switzerland. The site receives substantial soluble nitrogen (N) via atmospheric deposition, and thus, trees are unlikely N-limited. We used a construction crane to operate the free-air CO2 release system and for canopy access. Here, we summarize the major results for growth and carbon (C) fluxes. Tissue C-13 signals confirmed the effectiveness of the CO2 enrichment system and permitted tracing the continuous flow of new C in trees. Tree responses were individually standardized by pre-treatment signals. Over the five experimental years, needles retained their photosynthetic capacity and absorbed up to 37% more CO2 under elevated (E) compared to ambient (A) conditions. However, we did not detect an effect on stem radial growth, branch apical growth and needle litter production. Neither stem nor soil CO2 efflux was stimulated under elevated CO2. The rate at which fine roots filled soil ingrowth cores did not significantly differ between A- and E-trees. Since trees showed no stomatal responses to elevated CO2, sap flow remained unresponsive, both in the long run as well as during short-term CO2 on-off experiments. As a consequence, soil moisture remained unaffected. We trapped significantly more nitrate in the root sphere of E-trees suggesting a CO2-stimulated breakdown of soil organic matter, presumably induced by extra carbohydrate exudation (priming').Synthesis. The lack of a single enhanced C sink to match the increased C uptake meant a missing C sink. Increased C transport to below-ground sinks was indicated by C transfer to ectomycorrhiza and on to neighbouring trees and by increased C export to soil. We conclude that these tall Picea abies trees are not C limited at current CO2 concentrations and further atmospheric CO2 enrichment will have at most subtle effects on growth, despite
Diurnal dynamics of water transport, storage and hydraulic conductivity in pine trees under seasonal drought(2016) IFOREST-BIOGEOSCIENCES AND FORESTRY. 9, p. 710-719 Abstract
The temporal dynamics of water transport and storage in plants have major implications for plant functioning and survival. In trees, stress on the conductive tissue can be moderated by water storage. Yet, trees can survive high percent loss of conductivity (PLC, up to 80%), suggesting efficient recovery. We assess the role of tree water storage and PLC recovery based on simultaneous measurements of leaf transpiration, branch hydraulic conductivity, and stem sap-flow from different seasons in three study years in mature Pinus halepensis (Miller) trees in a semi-arid forest. During the wet season the rates of transpiration (T) and sap flow (SF) peaked at high morning and through the midday. During the dry season T peaked at similar to 9: 00 and then decreased, whereas SF lagged T and fully compensated for it only in the evening, resulting in a midday water deficit of similar to 5 kg tree(-1), and with up to 33% of daily T derived from storage. PLC of 30-40% developed during mid-day and subsequently recovered to near zero within 2-3 hr in the dry season (May, June, and September), but not in the wet season (January). The observed temporal decoupling between leaf water loss and soil water recharge is consistent with optimization of the trees' water and gas exchange economy, while apparently facilitating their survival in the semi-arid conditions.
Coordination between growth, phenology and carbon storage in three coexisting deciduous tree species in a temperate forest(2016) Tree Physiology. 36, 7, p. 847-855 Abstract
In deciduous trees growing in temperate forests, bud break and growth in spring must rely on intrinsic carbon (C) reserves. Yet it is unclear whether growth and C storage occur simultaneously, and whether starch C in branches is sufficient for refoliation. To test in situ the relationships between growth, phenology and C utilization, we monitored stem growth, leaf phenology and stem and branch nonstructural carbohydrate (NSC) dynamics in three deciduous species: Carpinus betulus L., Fagus sylvatica L. and Quercus petraea (Matt.) Liebl. To quantify the role of NSC in C investment into growth, a C balance approach was applied. Across the three species, >95% of branchlet starch was consumed during bud break, confirming the importance of C reserves for refoliation in spring. The C balance calculation showed that 90% of the C investment in foliage (7.0-10.5 kg tree(-1) and 5-17 times the C needed for annual stem growth) was explained by simultaneous branchlet starch degradation. Carbon reserves were recovered sooner than expected, after leaf expansion, in parallel with stem growth. Carpinus had earlier leaf phenology (by similar to 25 days) but delayed cambial growth (by similar to 15 days) than Fagus and Quercus, the result of a competitive strategy to flush early, while having lower NSC levels.
Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe(2016) Proceedings of the National Academy of Sciences of the United States of America. 113, 18, p. 5024-5029 Abstract
Drought-induced tree mortality has been observed globally and is expected to increase under climate change scenarios, with large potential consequences for the terrestrial carbon sink. Predicting mortality across species is crucial for assessing the effects of climate extremes on forest community biodiversity, composition, and carbon sequestration. However, the physiological traits associated with elevated risk of mortality in diverse ecosystems remain unknown, although these traits could greatly improve understanding and prediction of tree mortality in forests. We performed a meta-analysis on species' mortality rates across 475 species from 33 studies around the globe to assess which traits determine a species' mortality risk. We found that species-specific mortality anomalies from community mortality rate in a given drought were associated with plant hydraulic traits. Across all species, mortality was best predicted by a low hydraulic safety margin-the difference between typical minimum xylem water potential and that causing xylem dysfunction-and xylem vulnerability to embolism. Angiosperms and gymnosperms experienced roughly equal mortality risks. Our results provide broad support for the hypothesis that hydraulic traits capture key mechanisms determining tree death and highlight that physiological traits can improve vegetation model prediction of tree mortality during climate extremes.
(2016) The New Phytologist. 210, 2, p. 485-496 Abstract
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 1-7d was studied using 10yr 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.
(2016) Science. 352, 6283, p. 342-344 Abstract
Forest trees compete for light and soil resources, but photoassimilates, once produced in the foliage, are not considered to be exchanged between individuals. Applying stable carbon isotope labeling at the canopy scale, we show that carbon assimilated by 40-meter-tall spruce is traded over to neighboring beech, larch, and pine via overlapping root spheres. Isotope mixing signals indicate that the interspecific, bidirectional transfer, assisted by common ectomycorrhiza networks, accounted for 40% of the fine root carbon ( about 280 kilograms per hectare per year tree-to-tree transfer). Although competition for resources is commonly considered as the dominant tree-to-tree interaction in forests, trees may interact in more complex ways, including substantial carbon exchange.
Association between sap flow-derived and eddy covariance-derived measurements of forest canopy CO uptake.(2015) The New Phytologist. Abstract
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 x GPPEC , r2 = 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.
(2014) Tree Physiology. 34, 9, p. 981-992 Abstract
In trees exposed to prolonged drought, both carbon uptake (C source) and growth (C sink) typically decrease. This correlation raises two important questions: (i) to what degree is tree growth limited by C availability; and (ii) is growth limited by concurrent C storage (e.g., as nonstructural carbohydrates, NSC)? To test the relationships between drought, growth and C reserves, we monitored the changes in NSC levels and constructed stem growth chronologies of mature Pinus halepensis Miller trees of three drought stress levels growing in Yatir forest, Israel, at the dry distribution limit of forests. Moderately stressed and stressed trees showed 34 and 14% of the stem growth, 71 and 31% of the sap flux density, and 79 and 66% of the final needle length of healthy trees in 2012. In spite of these large reductions in growth and sap flow, both starch and soluble sugar concentrations in the branches of these trees were similar in all trees throughout the dry season (2-4% dry mass). At the same time, the root starch concentrations of moderately stressed and stressed trees were 47 and 58% of those of healthy trees, but never
Knockdown of the Arabidopsis thaliana chloroplast protein disulfide isomerase 6 results in reduced levels of photoinhibition and increased D1 synthesis in high light(2014) Plant Journal. 78, 6, p. 1003-1013 Abstract
A chloroplast protein disulfide isomerase (PDI) was previously proposed to regulate translation of the unicellular green alga Chlamydomonas reinhardtii chloroplast psbA mRNA, encoding the D1 protein, in response to light. Here we show that AtPDI6, one of 13 Arabidopsis thalianaPDI genes, also plays a role in the chloroplast. We found that AtPDI6 is targeted and localized to the chloroplast. Interestingly, AtPDI6 knockdown plants displayed higher resistance to photoinhibition than wild-type plants when exposed to a tenfold increase in light intensity. The AtPDI6 knockdown plants also displayed a higher rate of D1 synthesis under a similar light intensity. The increased resistance to photoinhibition may not be rationalized by changes in antenna or non-photochemical quenching. Thus, the increased D1 synthesis rate, which may result in a larger proportion of active D1 under light stress, may led to the decrease in photoinhibition. These results suggest that, although the D1 synthesis rates observed in wild-type plants under high light intensities are elevated, repair can potentially occur faster. The findings implicate AtPDI6 as an attenuator of D1 synthesis, modulating photoinhibition in a light-regulated manner.
Quantifying transpirable soil water and its relations to tree water use dynamics in a water- limited pine forest(2014) Ecohydrology. 7, 2, p. 409-419 Abstract
Knowledge of the relationship between soil water dynamics and tree water use is critical to understanding forest response to environmental change in water-limited ecosystems. However, the dynamics in soil water availability for tree transpiration (T-t) cannot be easily deduced from conventional measurements of soil water content (SWC), notably because T-t is influenced by soil water potential ((s)) that, in turn, depends on soil characteristics. Using tree sap flow and water potential and deriving depth-dependent soil water retention curves, we quantified the transpirable soil water content' (tSWC) and its seasonal and inter-annual variations in a semi-arid Pinus halepensis forest. The results indicated that tSWC varied in time and with soil depth. Over one growing season T-t was 57% of rain and 72% of the infiltrated SWC. In early winter, T-t was exclusively supported by soil moisture at the top 10cm (tSWC=11mm), whereas in spring (tSWC>18mm) and throughout the dry season, source water for T-t shifted to 20-40cm, where the maximum fine root density occurs. Simulation with the soil-plant-atmosphere water and energy transport model MuSICA supported the idea that consistent tSWC at the 20-40cm soil layer critically depended on limited water infiltration below 40cm, because of high water retention below this depth. Quantifying tSWC is critical to the precise estimation of the onset and termination of the growing season (when tSWC>0) in this semi-arid ecosystem. Copyright (c) 2013 John Wiley & Sons, Ltd.
Relationships between stomatal regulation, water-use, and water-use efficiency of two coexisting key Mediterranean tree species(2013) Forest Ecology and Management. 302, p. 34-42 Abstract
This study aims to test the hypothesis that as leaf water potential decreases, stomata! conductance (g(s)) and total water use decrease faster in trees tending toward isohydric behavior than in coexisting anisohydric trees. We measured leaf gas exchange rates in two key Mediterranean species: Pious halepensis (isohydric) and Quercus calliprinos (anisohydric) growing together in two different sites during seven field campaigns over 14 months. Intrinsic water-use efficiency (WUEi) was calculated from gas exchange ratios, and independently from carbon isotopic composition, delta C-13, of annual tree-ring sub-sections in four representative growth years. As expected, g(s) was greatly restricted already at VPD 5 kPa. Consequently, mean transpiration rates were 0.2-2.2 and 0.5-3.9 mmol m(2) s(-1) in coexisting pines and oaks, respectively. Mean delta C-13 values were 1.5 parts per thousand higher in tree- rings of the pine compared to the oak trees, consistent with the differences in WOE; between 75 and 64 mu mol CO2 mol(-1) H2O in pines and oaks, respectively, based on the short-term gas exchange measurements. A preliminary attempt to upscale the results to typical forest stands of the two species, on annual time-scales, demonstrated that the differences in stomatal regulation and water-use could imply similar to 30% higher water-use (or similar to 70% lower water yield) in oak stand compared to pine stand, related to its tendency toward anisohydric behavior. This sets the limit for typical 300 trees ha(-1) oak and pine stands at the 460 and 360 mm iso-precipitation lines, respectively, consistent with their current distribution along the precipitation gradient in our region. The results can help predict or manage changes in species composition in the face of increasing water limitations in Mediterranean regions. (C) 2013 Elsevier B.V. All rights reserved.
(2013) Global Change Biology. 19, 1, p. 75-89 Abstract
We review observational, experimental, and model results on how plants respond to extreme climatic conditions induced by changing climatic variability. Distinguishing between impacts of changing mean climatic conditions and changing climatic variability on terrestrial ecosystems is generally underrated in current studies. The goals of our review are thus (1) to identify plant processes that are vulnerable to changes in the variability of climatic variables rather than to changes in their mean, and (2) to depict/evaluate available study designs to quantify responses of plants to changing climatic variability. We find that phenology is largely affected by changing mean climate but also that impacts of climatic variability are much less studied, although potentially damaging. We note that plant water relations seem to be very vulnerable to extremes driven by changes in temperature and precipitation and that heatwaves and flooding have stronger impacts on physiological processes than changing mean climate. Moreover, interacting phenological and physiological processes are likely to further complicate plant responses to changing climatic variability. Phenological and physiological processes and their interactions culminate in even more sophisticated responses to changing mean climate and climatic variability at the species and community level. Generally, observational studies are well suited to study plant responses to changing mean climate, but less suitable to gain a mechanistic understanding of plant responses to climatic variability. Experiments seem best suited to simulate extreme events. In models, temporal resolution and model structure are crucial to capture plant responses to changing climatic variability. We highlight that a combination of experimental, observational, and/or modeling studies have the potential to overcome important caveats of the respective individual approaches.[All authors]
Differential ecophysiological response of a major Mediterranean pine species across a climatic gradient(2013) Tree Physiology. 33, 1, p. 26-36 Abstract
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 mu mol CO2 mol(-1) H2O 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.
(2011) Tree Physiology. 31, 6, p. 637-648 Abstract
Drought-induced tree mortality has increased over the last decades in forests around the globe. Our objective was to investigate under controlled conditions the hydraulic adjustments underlying the observed ability of Pinus halepensis to survive seasonal drought under semi-arid conditions. One hundred 18-month saplings were exposed in the greenhouse to 10 different drought treatments, simulating combinations of intensities (fraction of water supply relative to control) and durations (period with no water supply) for 30 weeks. Stomata closed at a leaf water potential (psi(l)) of -2.8 MPa, suggesting isohydric stomatal regulation. In trees under extreme drought treatments, stomatal closure reduced CO(2) uptake to -1 mu mol m(-2) s(-1), indicating the development of carbon starvation. A narrow hydraulic safety margin of 0.3 MPa (from stomatal closure to 50% loss of hydraulic conductivity) was observed, indicating a strategy of maximization of CO(2) uptake in trees otherwise adapted to water stress. A differential effect of drought intensity and duration was observed, and was explained by a strong dependence of the water stress effect on the ratio of transpiration to evapotranspiration T/ET and the larger partitioning to transpiration associated with larger irrigation doses. Under intense or prolonged drought, the root system became the main target for biomass accumulation, taking up to 100% of the added biomass, while the stem tissue biomass decreased, associated with up to 60% reduction in xylem volume.