Tamir Klein

A plant’s perspective of extremes: Terrestrial plant responses to changing climatic variability

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 heat-waves 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.

The variability of stomatal sensitivity to leaf water potential across tree species indicates a continuum between isohydric and anisohydric behaviours

Summary The relationship between stomatal conductance (gs) and leaf water potential (Ψl) is key to the understanding of plant function under changing climate. The variability among tree species gave rise to selection towards either of two contrasting water management types: isohydric or anisohydric. This study explores the variability of gs to Ψl across tree species. Curves of gs(Ψl) were collected from the scientific literature for 70 woody plant species. The data set is comprised of angiosperm and gymnosperm species from all major forest biomes. The hypothesis that curves from different tree species diverge between isohydric and anisohydric behaviours was tested. Species-specific curves formed a continuum, rather than dichotomy between isohydric and anisohydric, as confirmed by distribution models. Alternatively, the water potential at 50% of the maximum gs (Ψgs50) was used to quantitatively compare between species. A major difference emerged among xylem anatomy classes whereby ring-porous species had higher absolute gs at Ψl < −2 MPa than diffuse-porous and coniferous species. A positive, linear correlation was shown between Ψgs50 and Ψl at 50% loss of xylem conductivity. The results suggest that stomatal sensitivity to leaf water potential strongly relates to xylem characteristics. The use of Ψgs50 offers a quantitative alternative to the current, yet biased, distinction between isohydric and anisohydric species.

Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe

Significance Predicting the impacts of climate extremes on plant communities is a central challenge in ecology. Physiological traits may improve prediction of drought impacts on forests globally. We perform a meta-analysis across 33 studies that span all forested biomes and find that, among the examined traits, hydraulic traits explain cross-species patterns in mortality from drought. Gymnosperm and angiosperm mortality was associated with different hydraulic traits, giving insight into the relative weights of different traits and mechanisms in mortality prediction. Our results provide a foundation for more mechanistic predictions of drought-induced tree mortality across Earth’s diverse forests. 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.

Hydraulic adjustments underlying drought resistance of Pinus halepensis

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 (Ψ(l)) of -2.8 MPa, suggesting isohydric stomatal regulation. In trees under extreme drought treatments, stomatal closure reduced CO(2) uptake to -1 µmol 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 CO2 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.

Belowground carbon trade among tall trees in a temperate forest

Carbon trading between adult trees Competition between individual plants for resources is well known, but sharing of resources may also occur. Klein et al. observed tree-to-tree carbon shuttling between roots of tall trees in a mixed temperate forest in Switzerland (see the Perspective by van der Heijden). By applying stable carbon isotope labeling to individual tree canopies, they show that up to 40% of the carbon in the fine roots of one individual may be derived from photosynthetic products of a neighbor. Carbon transfer of this kind, mediated by plant-associated fungi, or mycorrhizae, in the soil, has been reported on a smaller scale in seedlings, but not before in trees. Science, this issue p. 342; see also p. 290 Isotopic analysis shows that up to 40% of carbon in fine roots of temperate forest trees may be derived from neighbors. [Also see Perspective by van der Heijden] 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.

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.

The correlations and sequence of plant stomatal, hydraulic, and wilting responses to drought

Significance Many plant species face increasing drought under climate change, making plant drought tolerance integral to predicting species and ecosystem responses. Many physiology traits interact to determine overall drought tolerance, but trait relationships have not been assessed for general patterns across global plant diversity. We analyzed stomatal, hydraulic, and mesophyll drought tolerance traits for 310 species from ecosystems worldwide. We evaluated the sequence of drought responses for plants under increasing water stress, and showed that coselection with environmental water stress drives most trait correlations across species, with functional coordination additionally important for some relationships. These results provide insight into how variation in multiple traits should be represented within plants and across species in models of plant responses to drought. 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.

Drought stress, growth and nonstructural carbohydrate dynamics of pine trees in a semi-arid forest

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 <2% dry mass. Our results show that all the studied trees maintain a fairly good coordination between C supply and demand, and even during prolonged drought there is more than one way for a tree to maintain a positive C balance.

Allocation, stress tolerance and carbon transport in plants: how does phloem physiology affect plant ecology?

Despite the crucial role of carbon transport in whole plant physiology and its impact on plant-environment interactions and ecosystem function, relatively little research has tried to examine how phloem physiology impacts plant ecology. In this review, we highlight several areas of active research where inquiry into phloem physiology has increased our understanding of whole plant function and ecological processes. We consider how xylem-phloem interactions impact plant drought tolerance and reproduction, how phloem transport influences carbon allocation in trees and carbon cycling in ecosystems and how phloem function mediates plant relations with insects, pests, microbes and symbiotes. We argue that in spite of challenges that exist in studying phloem physiology, it is critical that we consider the role of this dynamic vascular system when examining the relationship between plants and their biotic and abiotic environment.

Towards an advanced assessment of the hydrological vulnerability of forests to climate change-induced drought

Preserving the integrity of the hydraulic system is crucial for survival of trees under dry conditions (Br eda et al., 2006). Maintaining a hydraulic safety margin (HSM) between the water potential (WP) associated with stomatal closure and the WP associated with cavitation can therefore be an important drought resistance trait in many tree species. Based on a broad survey of HSMs across tree species, it was recently concluded that all forest biomes are similarly and strongly threatened by climate changeinduced drought (Choat et al., 2012). We submit that while the prevalence of narrow HSMs across tree species and climates is remarkable, additional factors must be considered to assess vulnerability of trees and forests to drought, that is, the degree to which they are susceptible to, and unable to cope with, adverse impacts of drought (IPCC, 2007). In fact, such prevalence of narrowHSM is likely a basis, and a trigger, for the development of a range of strategies to cope with this situation in light of the everimminent drought stress. Furthermore, settling for an apparently small HSM alone may slow down research into critical aspects of water-use strategies in trees. For example, the accumulating evidence in recent years for rapid recovery from loss of hydraulic conductivity (Brodersen & McElrone, 2013, and references cited therein) indicates a lesser importance of the HSM and any temporary loss of conductivity than suggested. Here, we briefly review key issues in tree strategies to cope with drought that are critical to consider in addition to HSM, if we are to improve predictions of drought related vulnerability of forests.