A critical thermal transition driving spring phenology of Northern Hemisphere conifers.

Despite growing interest in predicting plant phenological shifts, advanced spring phenology by global climate change remains debated. Evidence documenting either small or large advancement of spring phenology to rising temperature over the spatio-temporal scales implies a potential existence of a thermal threshold in the responses of forests to global warming. We collected a unique data set of xylem cell-wall-thickening onset dates in 20 coniferous species covering a broad mean annual temperature (MAT) gradient (-3.05 to 22.9°C) across the Northern Hemisphere (latitudes 23°-66° N). Along the MAT gradient, we identified a threshold temperature (using segmented regression) of 4.9 ± 1.1°C, above which the response of xylem phenology to rising temperatures significantly decline. This threshold separates the Northern Hemisphere conifers into cold and warm thermal niches, with MAT and spring forcing being the primary drivers for the onset dates (estimated by linear and Bayesian mixed-effect models), respectively. The identified thermal threshold should be integrated into the Earth-System-Models for a better understanding of spring phenology in response to global warming and an improved prediction of global climate-carbon feedbacks.

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.

Different growth sensitivity to climate of the conifer Juniperus thurifera on both sides of the Mediterranean Sea.

Mediterranean plants cope with cold wet winters and dry hot summers, with a drought gradient from northwest to southeast. Limiting climatic conditions have become more pronounced in the last decades due to the warming trend and rainfall decrease. Juniperus thurifera L., a long-lived conifer tree endemic to the western Mediterranean region, has a disjunct distribution in Europe and Africa, making it a suitable species to study sensitivity to climate in both sides of the Mediterranean Basin. Tree-ring width chronologies were built for three J. thurifera stands at Spain (Europe) and three in Morocco (Africa) and correlated with monthly temperature and precipitation. The temporal stability of climate-growth relationships was assessed using moving correlations; the drought effect on growth was calculated using the monthly standardized precipitation-evapotranspiration index (SPEI) at different temporal scales. In the wettest stands, increasing spring temperature and summer precipitation enhanced growth, while in the driest stands, growth was enhanced by higher spring precipitation and lower summer temperature. The climate-growth correlations shifted during the twentieth century, especially since the 1970s. Particularly noticeable is the recent negative correlation with previous autumn and winter precipitation in the wettest stands of J. thurifera, probably related with an effect of cloud cover or flooding on carbon storage depletion for next year growth. The driest stands were affected by drought at long time scales, while the wettest stands respond to drought at short time scales. This reveals a different strategy to cope with drought conditions, with populations from drier sites able to cope with short periods of water deficit.

High preseason temperature variability drives convergence of xylem phenology in the Northern Hemisphere conifers.

Wood growth is key to understanding the feedback of forest ecosystems to the ongoing climate warming. An increase in spatial synchrony (i.e., coincident changes in distant populations) of spring phenology is one of the most prominent climate responses of forest trees. However, whether temperature variability contributes to an increase in the spatial synchrony of spring phenology and its underlying mechanisms remains largely unknown. Here, we analyzed an extensive dataset of xylem phenology observations of 20 conifer species from 75 sites over the Northern Hemisphere. Along the gradient of increase in temperature variability in the 75 sites, we observed a convergence in the onset of cell enlargement roughly toward the 5th of June, with a convergence in the onset of cell wall thickening toward the summer solstice. The increase in rainfall since the 5th of June is favorable for cell division and expansion, and as the most hours of sunlight are received around the summer solstice, it allows the optimization of carbon assimilation for cell wall thickening. Hence, the convergences can be considered as the result of matching xylem phenological activities to favorable conditions in regions with high temperature variability. Yet, forest trees relying on such consistent seasonal cues for xylem growth could constrain their ability to respond to climate warming, with consequences for the potential growing season length and, ultimately, forest productivity and survival in the future.

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.

Extreme Growth Increments Reveal Local and Regional Climatic Signals in Two Pinus pinaster Populations.

Tree rings are valuable proxies of past climate that allow inferring past growth responses to climate variability and extreme events, which is only possible considering that the relationship between tree growth and environmental conditions is linear and stable over time. However, in the last decades, divergent growth patterns have been observed in trees from the same forest stand, while unprecedented growth convergence was observed between trees from distant locations. Here, we use a new approach that considers convergent and divergent event years in two populations of Pinus pinaster Aiton in an altitudinal and oceanic-continental gradient to investigate what is triggering divergence and convergence in tree growth. The two study sites are Tocha (TCH), a plantation on sand dunes at low altitude near the ocean, and Serra da Estrela (SdE), a mountain plantation located at 1,100 m altitude, 100 km away from the ocean. The analysis of the climatic conditions in convergent growth years revealed that positive convergent growth was related to above average precipitation in previous winter and that negative convergent growth was related to below average precipitation during the growing season. Divergent growth revealed a temperature signal with warmer temperatures in spring promoting growth in SdE and growth reduction in TCH. Convergent growth was associated with a regional climatic signal, reinforcing the importance of precipitation in the Mediterranean region, and divergent growth to site conditions, revealing local adaptation. The information gathered in this study gives valuable insights on the response of P. pinaster to extreme climatic events, allowing for more adjusted management strategies of Mediterranean pine forests.

Tree Growth Under Climate Change: Evidence From Xylogenesis Timings and Kinetics.

Tree growth is one of the most studied aspects of tree biology, particularly secondary growth. In the Mediterranean region, cambial activity is mostly determined by water availability. Climatic projections for the Mediterranean region predict more frequent and intense droughts, and longer periods without precipitation. To investigate tree growth under the predicted scenarios of climate change, a water manipulation experiment was conducted in a maritime pine stand (Pinus pinaster Aiton). In 2017, fifteen trees were divided into three groups: control, rain exclusion, and irrigation. Drought conditions were simulated by installing a continuous plastic sheet on the forest floor from March to September. Trees under irrigation treatment were watered twice a week in September. Cambial activity and xylem formation was monitored every 10 days from February 2017 until March 2018. Cell production was maximal around the spring equinox in all treatments. Trees under rain exclusion decreased cell production rates, xylogenesis duration, and latewood cell wall thickness. The extra irrigation in September did not produce noticeable differences in xylogenesis compared to trees in the control treatment. The synchronization of maximum cambial division rates around the vernal equinox (spring) could allow Mediterranean trees to mitigate the impact of summer drought. With the predicted increase in drought intensity and frequency, lower tree productivity, carbon sequestration, and wood biomass are expected.

Climatic and physiological regulation of the bimodal xylem formation pattern in Pinus pinaster saplings.

Seasonality in tree cambial activity and xylem formation encompass large variation in environmental conditions. Abiotic stressors such as warming or drought also modulate plant behavior at species and individual level. Despite xylem formation susceptibility to carbon (C) and water availability, it is still unknown which are the key physiological variables that regulate xylogenesis, and to what extent plant performance contributes to further explain the number of cells in the different phases of xylem development. Xylogenesis and physiological behavior was monitored in saplings of Pinus pinaster Aiton, a bimodal growth pattern species, distributed in different irrigation regimes. Xylogenesis and plant physiological behavior were compared between treatments and the relationship between climate, physiology and the number of cells in the cambium, enlargement and cell-wall thickening phases was evaluated. Xylogenesis regulation shifted from physiological to climatic control as cell differentiation advanced to mature tracheids. The number of cells in the cambium increased with assimilation rates and decreased with the water potential gradient through the plant. Enlargement was the most susceptible phase to plant relative water content, whereas no physiological variable contributed to explain the number of cells in the wall thickening phase, which declined as temperatures increased. All treatments showed a bimodal growth pattern with a second growth period starting when primary growth was completed and after plants had experienced the highest summer hydraulic losses. Our study demonstrates the importance of including physiological responses and not only climate to fully understand xylogenesis, with special attention to the enlargement phase. This is critical when studying species with a bimodal growth pattern because the second growth peak responds to internal shifts of C allocation and may strongly depend on plant hydraulic responses and not on a fine tuning of cambial activity with soil water availability.

Intra-specific variation in growth and wood density traits under water-limited conditions: Long-term-, short-term-, and sudden responses of four conifer tree species.

Consequences of climate change will severely affect forest ecosystems in the near future, yet our understanding of how and why trees are responding to their abiotic environment is still limited. Intra-specific variation (ITV) in the growth response of trees to warming and drought has been widely neglected so far, but could play a key role for adapting forests to future climate conditions. We analyzed tree rings from four conifers (Picea abies, Abies alba, Larix decidua, Pseudotsuga menziesii) regarding their intra-specific adaptation potential when trees are growing at the warm and dry margins of species distributions. Our study comprises data from four common garden experiments (45 provenances and a total of 743 trees) and assessed growth response at different temporal scales from decades (long-term) to only a few event years (short-term) and finally for density fluctuations within one year (sudden response). We observed significant variation among provenances at all time-scales, but with varying degree among species. However, variation in short-term response (drought years) was remarkably unstable across all species, when the seasonal variation of drought occurrence was considered. Silver-fir and Douglas-fir showed significant associations between seed-source climate and growth response as well as trade-offs between early- and latewood growth reaction which strongly suggests that growth responses are adaptive. Intra-specific variation in conifers in response to drought will probably be sufficient to mitigate climate change consequences on forest growth, but growth-environment interactions as well as dependencies between temporal scales could create major pitfalls for adaptive forest management in the future.

Climatic Signals from Intra-annual Density Fluctuation Frequency in Mediterranean Pines at a Regional Scale.

Tree rings provide information about the climatic conditions during the growing season by recording them in different anatomical features, such as intra-annual density fluctuations (IADFs). IADFs are intra-annual changes of wood density appearing as latewood-like cells within earlywood, or earlywood-like cells within latewood. The occurrence of IADFs is dependent on the age and size of the tree, and it is triggered by climatic drivers. The variations of IADF frequency of different species and their dependence on climate across a wide geographical range have still to be explored. The objective of this study is to investigate the effect of age, tree-ring width and climate on IADF formation and frequency at a regional scale across the Mediterranean Basin in Pinus halepensis Mill., Pinus pinaster Ait., and Pinus pinea L. The analyzed tree-ring network was composed of P. pinea trees growing at 10 sites (2 in Italy, 4 in Spain, and 4 in Portugal), P. pinaster from 19 sites (2 in Italy, 13 in Spain, and 4 in Portugal), and P. halepensis from 38 sites in Spain. The correlations between IADF frequency and monthly minimum, mean and maximum temperatures, as well as between IADF frequency and total precipitation, were analyzed. A significant negative relationship between IADF frequency and tree-ring age was found for the three Mediterranean pines. Moreover, IADFs were more frequent in wider rings than in narrower ones, although the widest rings showed a reduced IADF frequency. Wet conditions during late summer/early autumn triggered the formation of IADFs in the three species. Our results suggest the existence of a common climatic driver for the formation of IADFs in Mediterranean pines, highlighting the potential use of IADF frequency as a proxy for climate reconstructions with geographical resolution.

Structure and Function of Intra-Annual Density Fluctuations: Mind the Gaps.

Tree rings are natural archives of climate and environmental information with a yearly resolution. Indeed, wood anatomical, chemical, and other properties of tree rings are a synthesis of several intrinsic and external factors, and their interaction during tree growth. In particular, Intra-Annual Density Fluctuations (IADFs) can be considered as tree-ring anomalies that can be used to better understand tree growth and to reconstruct past climate conditions with intra-annual resolution. However, the ecophysiological processes behind IADF formation, as well as their functional impact, remain unclear. Are IADFs resulting from a prompt adjustment to fluctuations in environmental conditions to avoid stressful conditions and/or to take advantage from favorable conditions? In this paper we discuss: (1) the influence of climatic factors on the formation of IADFs; (2) the occurrence of IADFs in different species and environments; (3) the potential of new approaches to study IADFs and identify their triggering factors. Our final aim is to underscore the advantages offered by network analyses of data and the importance of high-resolution measurements to gain insight into IADFs formation processes and their relations with climatic conditions, including extreme weather events.

Plastic Response of Tracheids in Pinus pinaster in a Water-Limited Environment: Adjusting Lumen Size instead of Wall Thickness.

The formation of wood results from cambial activity and its anatomical properties reflect the variability of environmental conditions during the growing season. Recently, it was found that wood density variations in conifers growing under cold-limited environment result from the adjustment of cell wall thickness (CWT) to temperature. Additionally, it is known that intra-annual density fluctuations (IADFs) are formed in response to precipitation after the summer drought. Although IADFs are frequent in Mediterranean conifers no study has yet been conducted to determine if these structures result from the adjustment of lumen diameter (LD) or CWT to soil water availability. Our main objective is to investigate the intra-ring variation of wood anatomical features (LD and CWT) in Pinus pinaster Ait. growing under a water-limited environment. We compared the tracheidograms of LD and CWT for the years 2010-2013 in P. pinaster growing in the west coast of Portugal. Our results suggest a close association between LD and soil moisture content along the growing season, reinforcing the role of water availability in determining tracheid size. Compared with CWT, LD showed a higher intra- and inter-annual variability suggesting its strong adjustment value to variations in water availability. The formation of a latewood IADF appears to be predisposed by higher rates of cell production in spring and triggered by early autumn precipitation. Our findings reinforce the crucial role of water availability on cambial activity and wood formation in Mediterranean conifers, and emphasize the high plasticity of wood anatomical features under Mediterranean climate.

Adjustment capacity of maritime pine cambial activity in drought-prone environments.

Intra-annual density fluctuations (IADFs) are anatomical features formed in response to changes in the environmental conditions within the growing season. These anatomical features are commonly observed in Mediterranean pines, being more frequent in younger and wider tree rings. However, the process behind IADF formation is still unknown. Weekly monitoring of cambial activity and wood formation would fill this void. Although studies describing cambial activity and wood formation have become frequent, this knowledge is still fragmentary in the Mediterranean region. Here we present data from the monitoring of cambial activity and wood formation in two diameter classes of maritime pine (Pinus pinaster Ait.), over two years, in order to test: (i) whether the differences in stem diameter in an even-aged stand were due to timings and/or rates of xylogenesis; (ii) if IADFs were more common in large trees; and (iii) if their formation is triggered by cambial resumption after the summer drought. Larger trees showed higher rates of cell production and longer growing seasons, due to an earlier start and later end of xylogenesis. When a drier winter occurs, larger trees were more affected, probably limiting xylogenesis in the summer months. In both diameter classes a latewood IADF was formed in 2012 in response to late-September precipitation, confirming that the timing of the precipitation event after the summer drought is crucial in determining the resumption of cambial activity and whether or not an IADF is formed. It was the first time that the formation of a latewood IADF was monitored at a weekly time scale in maritime pine. The capacity of maritime pine to adjust cambial activity to the current environmental conditions represents a valuable strategy under the future climate change conditions.

Woody biomass production lags stem-girth increase by over one month in coniferous forests.

Wood is the main terrestrial biotic reservoir for long-term carbon sequestration(1), and its formation in trees consumes around 15% of anthropogenic carbon dioxide emissions each year(2). However, the seasonal dynamics of woody biomass production cannot be quantified from eddy covariance or satellite observations. As such, our understanding of this key carbon cycle component, and its sensitivity to climate, remains limited. Here, we present high-resolution cellular based measurements of wood formation dynamics in three coniferous forest sites in northeastern France, performed over a period of 3 years. We show that stem woody biomass production lags behind stem-girth increase by over 1 month. We also analyse more general phenological observations of xylem tissue formation in Northern Hemisphere forests and find similar time lags in boreal, temperate, subalpine and Mediterranean forests. These time lags question the extension of the equivalence between stem size increase and woody biomass production to intra-annual time scales(3, 4, 5, 6). They also suggest that these two growth processes exhibit differential sensitivities to local environmental conditions. Indeed, in the well-watered French sites the seasonal dynamics of stem-girth increase matched the photoperiod cycle, whereas those of woody biomass production closely followed the seasonal course of temperature. We suggest that forecasted changes in the annual cycle of climatic factors(7) may shift the phase timing of stem size increase and woody biomass production in the future.

Occupational exposure to inhalable wood dust in the member states of the European Union.

The aim of this study was to estimate occupational exposure to inhalable wood dust by country, industry, the level of exposure and type of wood dust in 25 member states of the European Union (EU-25) for the purposes of hazard control, exposure surveillance and assessment of health risks. National labour force statistics, a country questionnaire (in 15 member states, EU-15), a company survey (in Finland, France, Germany and Spain), exposure measurements (from Denmark, Finland, France, Germany, The Netherlands and the United Kingdom) and expert judgements were used to generate preliminary estimates of exposure to different types of wood dust. The estimates were generated according to industrial class (six wood industries, four other sectors) and level of exposure (five classes). These estimates were reviewed and finalized by national experts from 15 member states. Crude estimates were generated also for 10 new member states (EU-10). The basic data and final estimates were included in the WOODEX database. In 2000-2003, about 3.6 million workers (2.0% of the employed EU-25 population) were occupationally exposed to inhalable wood dust. Of those, construction employed 1.2 million exposed workers (33%), mostly construction carpenters. The numbers of exposed workers were 700,000 (20%) in the furniture industry, 300,000 (9%) in the manufacture of builders' carpentry, 200,000 (5%) in sawmilling, 150,000 (4%) in forestry and <100,000 in other wood industries. In addition, there were 700,000 exposed workers (20%) in miscellaneous industries employing carpenters, joiners and other woodworkers. The numbers of exposed workers varied by country ranging from <3,000 in Luxembourg and Malta to 700,000 in Germany. The highest exposure levels were estimated to occur in the construction sector and furniture industry. Due to limited exposure data there was considerable uncertainty in the estimates concerning construction woodworkers. About 560,000 workers (16% of the exposed) may be exposed to a level exceeding 5 mg m(-3). Mixed exposure to more than one species of wood and dust from wooden boards was very common, but reliable data on exposure to different species of wood could not be retrieved. This kind of assessment procedure integrating measurement data, company data, country-specific data and expert judgement could also serve as one model for the assessment of other occupational exposures.