No Future Growth Enhancement Expected at the Northern Edge for European Beech due to Continued Water Limitation.

With ongoing global warming, increasing water deficits promote physiological stress on forest ecosystems with negative impacts on tree growth, vitality, and survival. How individual tree species will react to increased drought stress is therefore a key research question to address for carbon accounting and the development of climate change mitigation strategies. Recent tree-ring studies have shown that trees at higher latitudes will benefit from warmer temperatures, yet this is likely highly species-dependent and less well-known for more temperate tree species. Using a unique pan-European tree-ring network of 26,430 European beech (Fagus sylvatica L.) trees from 2118 sites, we applied a linear mixed-effects modeling framework to (i) explain variation in climate-dependent growth and (ii) project growth for the near future (2021-2050) across the entire distribution of beech. We modeled the spatial pattern of radial growth responses to annually varying climate as a function of mean climate conditions (mean annual temperature, mean annual climatic water balance, and continentality). Over the calibration period (1952-2011), the model yielded high regional explanatory power (R2 = 0.38-0.72). Considering a moderate climate change scenario (CMIP6 SSP2-4.5), beech growth is projected to decrease in the future across most of its distribution range. In particular, projected growth decreases by 12%-18% (interquartile range) in northwestern Central Europe and by 11%-21% in the Mediterranean region. In contrast, climate-driven growth increases are limited to around 13% of the current occurrence, where the historical mean annual temperature was below ~6°C. More specifically, the model predicts a 3%-24% growth increase in the high-elevation clusters of the Alps and Carpathian Arc. Notably, we find little potential for future growth increases (-10 to +2%) at the poleward leading edge in southern Scandinavia. Because in this region beech growth is found to be primarily water-limited, a northward shift in its distributional range will be constrained by water availability.

Partial asynchrony of coniferous forest carbon sources and sinks at the intra-annual time scale.

As major terrestrial carbon sinks, forests play an important role in mitigating climate change. The relationship between the seasonal uptake of carbon and its allocation to woody biomass remains poorly understood, leaving a significant gap in our capacity to predict carbon sequestration by forests. Here, we compare the intra-annual dynamics of carbon fluxes and wood formation across the Northern hemisphere, from carbon assimilation and the formation of non-structural carbon compounds to their incorporation in woody tissues. We show temporally coupled seasonal peaks of carbon assimilation (GPP) and wood cell differentiation, while the two processes are substantially decoupled during off-peak periods. Peaks of cambial activity occur substantially earlier compared to GPP, suggesting the buffer role of non-structural carbohydrates between the processes of carbon assimilation and allocation to wood. Our findings suggest that high-resolution seasonal data of ecosystem carbon fluxes, wood formation and the associated physiological processes may reduce uncertainties in carbon source-sink relationships at different spatial scales, from stand to ecosystem levels.

Identifying drivers of non-stationary climate-growth relationships of European beech.

The future performance of the widely abundant European beech (Fagus sylvatica L.) across its ecological amplitude is uncertain. Although beech is considered drought-sensitive and thus negatively affected by drought events, scientific evidence indicating increasing drought vulnerability under climate change on a cross-regional scale remains elusive. While evaluating changes in climate sensitivity of secondary growth offers a promising avenue, studies from productive, closed-canopy forests suffer from knowledge gaps, especially regarding the natural variability of climate sensitivity and how it relates to radial growth as an indicator of tree vitality. Since beech is sensitive to drought, we in this study use a drought index as a climate variable to account for the combined effects of temperature and water availability and explore how the drought sensitivity of secondary growth varies temporally in dependence on growth variability, growth trends, and climatic water availability across the species' ecological amplitude. Our results show that drought sensitivity is highly variable and non-stationary, though consistently higher at dry sites compared to moist sites. Increasing drought sensitivity can largely be explained by increasing climatic aridity, especially as it is exacerbated by climate change and trees' rank progression within forest communities, as (co-)dominant trees are more sensitive to extra-canopy climatic conditions than trees embedded in understories. However, during the driest periods of the 20th century, growth showed clear signs of being decoupled from climate. This may indicate fundamental changes in system behavior and be early-warning signals of decreasing drought tolerance. The multiple significant interaction terms in our model elucidate the complexity of European beech's drought sensitivity, which needs to be taken into consideration when assessing this species' response to climate change.

Stomatal regulation and xylem hydraulics of limber pine and Engelmann spruce in Great Basin sky-island ecosystems.

Integration of whole-plant stomatal regulation and xylem hydraulics is of critical importance for predicting species response to drought stress. Yet intraspecific variability of stomatal and hydraulic traits, and how these variabilities interact, remain largely unknown. We hypothesized that drought can drive less stomatal regulation but increase xylem hydraulic safety, resulting in stomatal-hydraulic coordination within a species. We estimated sensitivity of whole-tree canopy conductance to soil drying together with xylem hydraulic traits of two dominant conifers, i.e. limber pine (Pinus flexilis) and Engelmann spruce (Picea engelmannii). Our study was conducted using sub-hourly measurements over five consecutive years (2013-2017) at three instrumented sites with different elevations within the Nevada Eco-hydrological Assessment Network (NevCAN) in Great Basin sky-island ecosystems. Both conifers showed a reduction of stomatal sensitivity to soil drying at lower elevations, indicating an active stomatal acclimation to drought. While limber pine increased xylem embolism resistance in parallel with reduced stomatal sensitivity to soil drying, an opposite hydraulic adjustment was detected in Engelmann spruce. Our results provide evidence that mature trees can respond to climatic changes using coordinated shifts in stomatal regulation and xylem hydraulics, but such changes can differ within and between species in ways that need to be examined using in situ data. Deciphering intraspecific variability in whole-plant stomatal and hydraulic traits ultimately contributes to defining drought tolerance and vulnerability, particularly for tree species that inhabit a wide range of landscapes.

Bell-shaped tree-ring responses to air temperature drive productivity trends in long-lived mountain Mediterranean pines.

We investigated the dendroclimatic response of a Pinus heldreichii metapopulation distributed over a wide elevation interval (from 882 to 2143 m a.s.l.), spanning from low mountain to upper subalpine vegetation belts in the southern Italian Apennines. The tested hypothesis is that wood growth along an elevational gradient is non-linearly related to air temperature. During three years of fieldwork (2012-2015) at 24 sites, we collected wood cores from a total of 214 pine trees with diameter at breast height from 19 to 180 cm (average 82.7 ± 32.9 cm). We used a combination of tree-ring and genetic methods to reveal factors involved in growth acclimation using a space-for-time approach. Scores from canonical correspondence analysis were used to combine individual tree-ring series into four composite chronologies related to air temperature along the elevation gradient. Overall, the June dendroclimatic response followed a bell-shaped thermal niche curve, increasing until a peak around 13-14 °C. A similarly bell-shaped response was found with previous autumn air temperature, and both dendroclimatic signals interacted with stem size and growth rates, generating a divergent growth response between the top and the bottom of the elevation gradient. Increased tree growth in the upper subalpine belt was consistent with the consequences of increasing air temperature under no drought stress. A positive link was uncovered between pine growth at all elevations and April mean temperature, with trees growing at the lowest elevations showing the strongest growth response. No elevational genetic differences were found, hence long-lived tree species with small geographical ranges may reverse their climatic response between the lower and upper bioclimatic zones of their environmental niche. Our study revealed a high resistance and acclimation capability of Mediterranean forest stands, and such low vulnerability to changing climatic conditions highlights the potential to store carbon in these ecosystems for the coming decades.

Maximum tree lifespans derived from public-domain dendrochronological data.

The public-domain International Tree-Ring Data Bank (ITRDB) is an under-utilized dataset to improve existing estimates of global tree longevity. We used the longest continuous ring-width series of existing ITRDB collections as an index of maximum tree age for that species and site. Using a total of 3,689 collections, we obtained longevity estimates for 237 unique tree species, 157 conifers and 80 angiosperms, distributed all over the world. More than half of the species (167) were represented by no more than 10 collections, and a similar number of species (144) reached longevity greater than 300 years. Maximum tree ages exceeded 1,000 years for several species (22), all of them conifers, whereas angiosperm longevity peaked around 500 years. Given the current emphasis on identifying human-induced impacts on global systems, detailed analyses of ITRDB holdings provide one of the most reliable sources of information for tree longevity as an ecological trait.

Longevity Estimates of Canary Palms and Dragon Trees via Radiocarbon Dating: Initial Results.

Correctly estimating the maximum lifespan of plant species is a necessary component of demographic and life-history studies, which, in turn, are needed for understanding climatic impacts. Arboreal monocotyledons, which can grow to >30 m in height and >5 m in trunk perimeter, are difficult to age because they do not undergo seasonal dormancy; hence, their longevity has been estimated using various size-related methods. In this study, we tested radiocarbon (14C) dating with Accelerator Mass Spectrometry (AMS) as an additional tool for determining the age of two iconic monocotyledons: the Canary Island palm and the dragon tree. A total of 25 samples were collected from the basal stem of four palms and five dragon trees on Gran Canaria and Tenerife and then processed using the most advanced 14C-AMS analysis available. Calibration curves provided by the "IntCal group" were used to determine the oldest possible age of each sample, and 16 of them were found to be "modern", i.e., formed after the 1950s. Nine samples that were either collected from exterior, but lignified, palm tissues or from interior, and lignified, dragon tree tissues suggested ages > 300 years. Given the constant improvement of 14C-AMS tools, they can contribute to the further refinement of existing scientific knowledge on Macaronesian charismatic megaflora.

Water-Use Efficiency of Co-occurring Sky-Island Pine Species in the North American Great Basin.

Water-use efficiency (WUE), weighing the balance between plant transpiration and growth, is a key characteristic of ecosystem functioning and a component of tree drought resistance. Seasonal dynamics of tree-level WUE and its connections with drought variability have not been previously explored in sky-island montane forests. We investigated whole-tree transpiration and stem growth of bristlecone (Pinus longaeva) and limber pine (Pinus flexilis) within a high-elevation stand in central-eastern Nevada, United States, using sub-hourly measurements over 5 years (2013-2017). A moderate drought was generally observed early in the growing season, whereas interannual variability of summer rains determined drought levels between years, i.e., reducing drought stress in 2013-2014 while enhancing it in 2015-2017. Transpiration and basal area increment (BAI) of both pines were coupled throughout June-July, resulting in a high but relatively constant early season WUE. In contrast, both pines showed high interannual plasticity in late-season WUE, with a predominant role of stem growth in driving WUE. Overall, bristlecone pine was characterized by a lower WUE compared to limber pine. Dry or wet episodes in the late growing season overrode species differences. Our results suggested thresholds of vapor pressure deficit and soil moisture that would lead to opposite responses of WUE to late-season dry or wet conditions. These findings provide novel insights and clarify potential mechanisms modulating tree-level WUE in sky-island ecosystems of semi-arid regions, thereby helping land managers to design appropriate science-based strategies and reduce uncertainties associated with the impact of future climatic changes.

Wood Anatomy of Douglas-Fir in Eastern Arizona and Its Relationship With Pacific Basin Climate.

Dendroclimatic reconstructions, which are a well-known tool for extending records of climatic variability, have recently been expanded by using wood anatomical parameters. However, the relationships between wood cellular structures and large-scale climatic patterns, such as El Niño-Southern Oscillation (ENSO) and the Pacific Decadal Oscillation (PDO), are still not completely understood, hindering the potential for wood anatomy as a paleoclimatic proxy. To better understand the teleconnection between regional and local climate processes in the western United States, our main objective was to assess the value of these emerging tree-ring parameters for reconstructing climate dynamics. Using Confocal Laser Scanning Microscopy, we measured cell lumen diameter and cell wall thickness (CWT) for the period 1966 to 2015 in five Douglas-firs [Pseudotsuga menziesii (Mirb.) Franco] from two sites in eastern Arizona (United States). Dendroclimatic analysis was performed using chronologies developed for 10 equally distributed sectors of the ring and daily climatic records to identify the strongest climatic signal for each sector. We found that lumen diameter in the first ring sector was sensitive to previous fall-winter temperature (September 25th to January 23rd), while a precipitation signal (October 27th to February 13th) persisted for the entire first half of the ring. The lack of synchronous patterns between trees for CWT prevented conducting meaningful climate-response analysis for that anatomical parameter. Time series of lumen diameter showed an anti-phase relationship with the Southern Oscillation Index (a proxy for ENSO) at 10 to 14year periodicity and particularly in 1980-2005, suggesting that chronologies of wood anatomical parameters respond to multidecadal variability of regional climatic modes. Our findings demonstrate the potential of cell structural characteristics of southwestern United States conifers for reconstructing past climatic variability, while also improving our understanding of how large-scale ocean-atmosphere interactions impact local hydroclimatic patterns.

On tree longevity.

Large, majestic trees are iconic symbols of great age among living organisms. Published evidence suggests that trees do not die because of genetically programmed senescence in their meristems, but rather are killed by an external agent or a disturbance event. Long tree lifespans are therefore allowed by specific combinations of life history traits within realized niches that support resistance to, or avoidance of, extrinsic mortality. Another requirement for trees to achieve their maximum longevity is either sustained growth over extended periods of time or at least the capacity to increase their growth rates when conditions allow it. The growth plasticity and modularity of trees can then be viewed as an evolutionary advantage that allows them to survive and reproduce for centuries and millennia. As more and more scientific information is systematically collected on tree ages under various ecological settings, it is becoming clear that tree longevity is a key trait for global syntheses of life history strategies, especially in connection with disturbance regimes and their possible future modifications. In addition, we challenge the long-held notion that shade-tolerant, late-successional species have longer lifespans than early-successional species by pointing out that tree species with extreme longevity do not fit this paradigm. Identifying extremely old trees is therefore the groundwork not only for protecting and/or restoring entire landscapes, but also to revisit and update classic ecological theories that shape our understanding of environmental change.

Photoperiod and temperature as dominant environmental drivers triggering secondary growth resumption in Northern Hemisphere conifers.

Wood formation consumes around 15% of the anthropogenic CO2 emissions per year and plays a critical role in long-term sequestration of carbon on Earth. However, the exogenous factors driving wood formation onset and the underlying cellular mechanisms are still poorly understood and quantified, and this hampers an effective assessment of terrestrial forest productivity and carbon budget under global warming. Here, we used an extensive collection of unique datasets of weekly xylem tissue formation (wood formation) from 21 coniferous species across the Northern Hemisphere (latitudes 23 to 67°N) to present a quantitative demonstration that the onset of wood formation in Northern Hemisphere conifers is primarily driven by photoperiod and mean annual temperature (MAT), and only secondarily by spring forcing, winter chilling, and moisture availability. Photoperiod interacts with MAT and plays the dominant role in regulating the onset of secondary meristem growth, contrary to its as-yet-unquantified role in affecting the springtime phenology of primary meristems. The unique relationships between exogenous factors and wood formation could help to predict how forest ecosystems respond and adapt to climate warming and could provide a better understanding of the feedback occurring between vegetation and climate that is mediated by phenology. Our study quantifies the role of major environmental drivers for incorporation into state-of-the-art Earth system models (ESMs), thereby providing an improved assessment of long-term and high-resolution observations of biogeochemical cycles across terrestrial biomes.

Transpiration drivers of high-elevation five-needle pines (Pinus longaeva and Pinus flexilis) in sky-island ecosystems of the North American Great Basin.

We investigated the interaction between soil water supply and atmospheric evaporative demand for driving the seasonal pattern of transpiration in sky-island high-elevation forest ecosystems. Sap flow measurements were collected at 10-minute intervals for five consecutive years (2013-2017) on two co-occurring subalpine conifers, i.e. limber pine (Pinus flexilis) and bristlecone pine (Pinus longaeva). Our study site is part of the Nevada Climate-ecohydrological Assessment Network (NevCAN), and is located at 3355 m a.s.l. within an undisturbed mixed-conifer stand. We found that seasonal changes in soil moisture regulated transpiration sensitivity to atmospheric conditions. Sap flow density was mainly limited by evaporative demands under non-water limiting conditions, but was influenced only by soil moisture when water availability decreased. Daily sap flow density increased with radiation and soil moisture in June and July when soil moisture was generally above 10%, but correlated only with soil moisture in August and September when soil drought occurred. Sap flow sensitivity to vapor pressure deficit and solar radiation was therefore reduced under decreasing soil moisture conditions. Transpiration peaked in mid-to-late June during both dry and wet years, with a lower peak in late summer during wet years. Normalized mean daily canopy conductance of both species declined with decreasing soil moisture (i.e., increasing soil drought). Severe soil drying (i.e., soil moisture <7% at 20 cm depth), which was rarely detected in wet summers (2013-2014) but occurred more frequently in dry summers (2015-2017), induced a minimum in crown conductance with unchanged low-level sap flow, which might potentially trigger hydraulic failure. The minimum sap flow level under severe soil drought was higher for limber pine than bristlecone pine, possibly because of wider tracheids in limber compared to bristlecone pine. Our findings provide insights into physiological mechanisms of drought-induced stress for iconic sky-island five-needle pines located at high elevation in xeric environments.

Climatically controlled reproduction drives interannual growth variability in a temperate tree species.

Climatically controlled allocation to reproduction is a key mechanism by which climate influences tree growth and may explain lagged correlations between climate and growth. We used continent-wide datasets of tree-ring chronologies and annual reproductive effort in Fagus sylvatica from 1901 to 2015 to characterise relationships between climate, reproduction and growth. Results highlight that variable allocation to reproduction is a key factor for growth in this species, and that high reproductive effort ('mast years') is associated with stem growth reduction. Additionally, high reproductive effort is associated with previous summer temperature, creating lagged climate effects on growth. Consequently, understanding growth variability in forest ecosystems requires the incorporation of reproduction, which can be highly variable. Our results suggest that future response of growth dynamics to climate change in this species will be strongly influenced by the response of reproduction.

Moisture-driven xylogenesis in Pinus ponderosa from a Mojave Desert mountain reveals high phenological plasticity.

Future seasonal dynamics of wood formation in hyperarid environments are still unclear. Although temperature-driven extension of the growing season and increased forest productivity are expected for boreal and temperate biomes under global warming, a similar trend remains questionable in water-limited regions. We monitored cambial activity in a montane stand of ponderosa pine (Pinus ponderosa) from the Mojave Desert for 2 consecutive years (2015-2016) showing opposite-sign anomalies between warm- and cold-season precipitation. After the wet winter/spring of 2016, xylogenesis started 2 months earlier compared to 2015, characterized by abundant monsoonal (July-August) rainfall and hyperarid spring. Tree size did not influence the onset and ending of wood formation, highlighting a predominant climatic control over xylem phenological processes. Moisture conditions in the previous month, in particular soil water content and dew point, were the main drivers of cambial phenology. Latewood formation started roughly at the same time in both years; however, monsoonal precipitation triggered the formation of more false rings and density fluctuations in 2015. Because of uncertainties in future precipitation patterns simulated by global change models for the Southwestern United States, the dependency of P. ponderosa on seasonal moisture implies a greater conservation challenge than for species that respond mostly to temperature conditions.

Dating old hollow trees by applying a multistep tree-ring and radiocarbon procedure to trunk and exposed roots.

In the process of dating the oldest trees, which are often hollow, we developed a new method that combines tree-ring cross dating and wiggle matching radiocarbon techniques on wood samples extracted from the stem and from exposed roots. The method can be illustrated by the following steps: •crossdated tree-ring series from trunk cores reveal a multi-century tree age, and the hollow section is large enough to contain several more years (decades to centuries)•exposed roots can be cored for acquiring wood samples older than the stem cores and for construction of a floating root average tree-ring series•if synchronization between stem and exposed roots is unclear, proceed to date the root wood samples by radiocarbon wiggle matching; match root and stem tree-ring series within the radiocarbon-dated period to more accurately date the tree. This new multistep dating method allowed for refining the age estimation of the oldest Pinus heldreichii tree in Pollino National Park by 166 years, to 789 CE. This tree, which we named Italus, was 1229 years old in 2017, making it the oldest, scientifically dated, living tree in Europe. Any study that relies on tree age determination for paleo-reconstructions, for biological and genetic research on what controls longevity, or for understanding structural dynamics and succession in old-growth forests, would potentially benefit from the multistep dating method we tested.

Global patterns of drought recovery.

Drought, a recurring phenomenon with major impacts on both human and natural systems, is the most widespread climatic extreme that negatively affects the land carbon sink. Although twentieth-century trends in drought regimes are ambiguous, across many regions more frequent and severe droughts are expected in the twenty-first century. Recovery time-how long an ecosystem requires to revert to its pre-drought functional state-is a critical metric of drought impact. Yet the factors influencing drought recovery and its spatiotemporal patterns at the global scale are largely unknown. Here we analyse three independent datasets of gross primary productivity and show that, across diverse ecosystems, drought recovery times are strongly associated with climate and carbon cycle dynamics, with biodiversity and CO2 fertilization as secondary factors. Our analysis also provides two key insights into the spatiotemporal patterns of drought recovery time: first, that recovery is longest in the tropics and high northern latitudes (both vulnerable areas of Earth's climate system) and second, that drought impacts (assessed using the area of ecosystems actively recovering and time to recovery) have increased over the twentieth century. If droughts become more frequent, as expected, the time between droughts may become shorter than drought recovery time, leading to permanently damaged ecosystems and widespread degradation of the land carbon sink.

Wood Cellular Dendroclimatology: Testing New Proxies in Great Basin Bristlecone Pine.

Dendroclimatic proxies can be generated from the analysis of wood cellular structures, allowing for a more complete understanding of the physiological mechanisms that control the climatic response of tree species. Century-long (1870-2013) time series of anatomical parameters were developed for Great Basin bristlecone pine (Pinus longaeva D.K. Bailey) by capturing strongly contrasted microscopic images through a Confocal Laser Scanning Microscope. Environmental information embedded in wood anatomical series was analyzed in comparison with ring-width series using measures of empirical signal strength. Response functions were calculated against monthly climatic variables to evaluate climate sensitivity of cellular features (e.g., lumen area; lumen diameter) for the period 1950-2013. Calibration-verification tests were used to determine the potential to generate long climate reconstructions from these anatomical proxies. A total of eight tree-ring parameters (two ring-width and six chronologies of xylem anatomical parameters) were analyzed. Synchronous variability among samples varied among tree-ring parameters, usually decreasing from ring-width to anatomical features. Cellular parameters linked to plant hydraulic performance (e.g., tracheid lumen area and radial lumen diameter) showed empirical signal strength similar to ring-width series, while noise was predominant in chronologies of lumen tangential width and cell wall thickness. Climatic signals were different between anatomical and ring-width chronologies, revealing a positive and temporally stable correlation of tracheid size (i.e., lumen and cell diameter) with monthly (i.e., March) and seasonal precipitation. In particular, tracheid lumen diameter emerged as a reliable moisture indicator and was then used to reconstruct total March-August precipitation from 1870 to 2013. Wood anatomy holds great potential to refine and expand dendroclimatic records by allowing estimates of plant physiological adaptations to external stressors. Integrating xylem cellular features with ring-width chronologies can widen our understanding of past climatic variability (including annual extreme events) and improve the evaluation of long-term plant response to drought, especially in connection with future warming scenarios.

Environmental drivers of cambial phenology in Great Basin bristlecone pine.

The timing of wood formation is crucial to determine how environmental factors affect tree growth. The long-lived bristlecone pine (Pinus longaeva D. K. Bailey) is a foundation treeline species in the Great Basin of North America reaching stem ages of about 5000 years. We investigated stem cambial phenology and radial size variability to quantify the relative influence of environmental variables on bristlecone pine growth. Repeated cellular measurements and half-hourly dendrometer records were obtained during 2013 and 2014 for two high-elevation stands included in the Nevada Climate-ecohydrological Assessment Network. Daily time series of stem radial variations showed rehydration and expansion starting in late April-early May, prior to the onset of wood formation at breast height. Formation of new xylem started in June and lasted until mid-September. There were no differences in phenological timing between the two stands, or in the air and soil temperature thresholds for the onset of xylogenesis. A multiple logistic regression model highlighted a separate effect of air and soil temperature on xylogenesis, the relevance of which was modulated by the interaction with vapor pressure and soil water content. While air temperature plays a key role in cambial resumption after winter dormancy, soil thermal conditions coupled with snowpack dynamics also influence the onset of wood formation by regulating plant-soil water exchanges. Our results help build a physiological understanding of climate-growth relationships in P. longaeva, the importance of which for dendroclimatic reconstructions can hardly be overstated. In addition, environmental drivers of xylogenesis at the treeline ecotone, by controlling the growth of dominant species, ultimately determine ecosystem responses to climatic change.