Global patterns of tree wood density.

Wood density is a fundamental property related to tree biomechanics and hydraulic function while playing a crucial role in assessing vegetation carbon stocks by linking volumetric retrieval and a mass estimate. This study provides a high-resolution map of the global distribution of tree wood density at the 0.01° (~1 km) spatial resolution, derived from four decision trees machine learning models using a global database of 28,822 tree-level wood density measurements. An ensemble of four top-performing models combined with eight cross-validation strategies shows great consistency, providing wood density patterns with pronounced spatial heterogeneity. The global pattern shows lower wood density values in northern and northwestern Europe, Canadian forest regions and slightly higher values in Siberia forests, western United States, and southern China. In contrast, tropical regions, especially wet tropical areas, exhibit high wood density. Climatic predictors explain 49%-63% of spatial variations, followed by vegetation characteristics (25%-31%) and edaphic properties (11%-16%). Notably, leaf type (evergreen vs. deciduous) and leaf habit type (broadleaved vs. needleleaved) are the most dominant individual features among all selected predictive covariates. Wood density tends to be higher for angiosperm broadleaf trees compared to gymnosperm needleleaf trees, particularly for evergreen species. The distributions of wood density categorized by leaf types and leaf habit types have good agreement with the features observed in wood density measurements. This global map quantifying wood density distribution can help improve accurate predictions of forest carbon stocks, providing deeper insights into ecosystem functioning and carbon cycling such as forest vulnerability to hydraulic and thermal stresses in the context of future climate change.

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.

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.

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.

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.

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.

Does the Genotype Have a Significant Effect on the Formation of Intra-Annual Density Fluctuations? A Case Study Using Larix decidua from Northern Poland.

Intra-annual density fluctuations (IADFs) can imprint environmental conditions within the growing season and most of the research on IADFs has been focused on their climatic signal. However, to our knowledge, the genetic influence on the frequency and type of IADFs has not been evaluated. To understand if the genotype can affect the formation of IADFs we have used a common garden experiment using eight families of Larix decidua established in two neighboring forest stands in northern Poland. Four types of IADFs were identified using X-ray density profiles: latewood-like cells within earlywood (IADF-type E), latewood-like cells in the transition from early- to latewood (IADF type E+), earlywood-like cells within latewood (IADF-type L), and earlywood-like cells in the border zone between the previous and present annual ring (IADF-type L+). The influence of explanatory variables i.e., families, sites, and years on identified density fluctuations was analyzed using generalized estimating equations (GEE). We hypothesized that trees from different families will differ in terms of frequency and type of IADFs because each family will react to precipitation and temperature in a different way, depending on the origin of those trees. The most frequent fluctuation was E+ and L types on both sites. The most important factors in the formation of IADFs were the site and year, the last one reflecting the variable climatic conditions, with no significant effect of the family. However, the relation between the formation of IADFs and selected climate parameters was different between families. Although, our results did not give a significant effect of the genotype on the formation of IADFs, the different sensitivity to climatic parameters among different families indicate that there is a genetic influence.

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.

Pre-dispersal predation effect on seed packaging strategies and seed viability.

An increased understanding of intraspecific seed packaging (i.e. seed size/number strategy) variation across different environments may improve current knowledge of the ecological forces that drive seed evolution in plants. In particular, pre-dispersal seed predation may influence seed packaging strategies, triggering a reduction of the resources allocated to undamaged seeds within the preyed fruits. Assessing plant reactions to pre-dispersal seed predation is crucial to a better understanding of predation effects, but the response of plants to arthropod attacks remains unexplored. We have assessed the effect of cone predation on the size and viability of undamaged seeds in populations of Juniperus thurifera with contrasting seed packaging strategies, namely, North African populations with single-large-seeded cones and South European populations with multi-small-seeded cones. Our results show that the incidence of predation was lower on the single-large-seeded African cones than on the multi-small-seeded European ones. Seeds from non-preyed cones were also larger and had a higher germination success than uneaten seeds from preyed cones, but only in populations with multi-seeded cones and in cones attacked by Trisetacus sp., suggesting a differential plastic response to predation. It is possible that pre-dispersal seed predation has been a strong selective pressure in European populations with high cone predation rates, being a process which maintains multi-small-seeded cones and empty seeds as a strategy to save some seeds from predation. Conversely, pre-dispersal predation might not have a strong effect in the African populations with single-large-seeded cones characterized by seed germination and filling rates higher than those in the European populations. Our results indicate that differences in pre-dispersal seed predators and predation levels may affect both selection on and intraspecific variation in seed packaging.

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.

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.

Genetic diversity and differentiation of Juniperus thurifera in Spain and Morocco as determined by SSR.

Juniperus thurifera L. is an important tree endemic to the western Mediterranean basin that it is able to grow in semi-arid climates. It nowadays exhibits a disjunct distribution pattern, occurring in North Africa, Spain, France and the Italian Alps. The Strait of Gibraltar has acted as an efficient barrier against gene flow between African and European populations, which are considered different subspecies by some authors. We aimed at describing the intraspecific genetic diversity of J. thurifera in populations from the Iberian Peninsula and Morocco and the phylogeographical relationships among these populations. The ploidy level of J. thurifera was examined and eleven nuclear microsatellites (nSSRs) developed for J. thurifera were assessed for genotyping this species. Six nSSRs were polymorphic and subsequently used to assess the genetic diversity and structure of the studied populations. Genotyping of the tetraploid J. thurifera using nuclear microsatellites supports the separation of Moroccan and Spanish populations into two genetically differentiated groups that correspond to the proposed subspecies africana and thurifera. High values of within population genetic diversity were found, that accounted for 90% of the total genetic variance, while population structure was weak. The estimators of genetic diversity were higher in populations of Spain than in populations of Morocco pointing for a possible loss of genetic diversity during the spread of this species to Africa from Europe.

Effect of root age on the allocation of metals, amino acids and sugars in different cell fractions of the perennial grass Paspalum notatum (bahiagrass).

This work aimed to compare the allocation of Al, Fe, Cu, Ni, amino acids and sugars in different fractions of root cells of Paspalum notatum with 21 and 120 days old grown in quartz sand. In general younger roots showed a higher content of Al, Fe, Cu Ni, amino acids and sugars, compared to older roots. This can be due to a higher metabolic activity of younger roots and/or to structural changes that can occur with cell ageing. Al and Fe were mainly allocated to fractions with pectin, hemicellulose and cellulose, both in younger and older roots. However, older roots also showed a significant fraction of Al allocated to the intracellular fraction. It seems that older roots were less able to prevent the entry of Al in the cytoplasm. The proportion of Cu was higher in intracellular components, both in younger and older roots, as expected from an essential nutrient. Ni content was very low in older roots and in younger roots it was mainly allocated to the intracellular fraction and to the cell wall polysaccharides fraction. The amino acids were mainly allocated to the cytoplasm and polysaccharide fraction. Although younger roots showed a higher total amount of amino acids compared to older roots, the amino acids profile and allocation, mainly in the cytoplasm polysaccharides, was quite similar. Arabinose, a major component of structural glycoproteins of the primary cell wall matrix, was only detected in younger roots. Thus, it seems that root cells of P. notatum suffered changes in the composition of the cell wall components with ageing. To further understand the structural changes of root cells with ageing and its effect on metal allocation, it is important to quantify several components of the cell wall matrix, namely pectins and glycoproteins.

Nickel speciation in the xylem sap of the hyperaccumulator Alyssum serpyllifolium ssp. lusitanicum growing on serpentine soils of northeast Portugal.

Nickel speciation was studied in the xylem sap of Alyssum serpyllifolium ssp. lusitanicum, a Ni-hyperaccumulator endemic to the serpentine soils of northeast Portugal. The xylem sap was collected from plants growing in its native habitat and characterized in terms of carboxylic and amino acids content. The speciation of nickel was studied in model and real solutions of xylem sap by voltammetric titrations using Square Wave Voltammetry (SWV). The results showed that Ni transport in the xylem sap occurs mainly as a free hydrated cation (about 70%) and complexed with carboxylic acids, mainly citric acid (18%). Altogether, oxalic acid, malic acid, malonic acid and aspartic acid complexed less than 13% of total Ni. A negligible amount bounded to the amino acids, like glutamic acid and glutamine (<1%). Histidine did not play a role in Ni translocation in the xylem sap of A. serpyllifolium under field conditions. Amino acids are one of the main forms of N transport in the xylem sap, and under field conditions, N is usually a limited nutrient. We hypothesize that the translocation of Ni in the xylem sap as a free ion or chelated with carboxylic acids is 'cheaper' in terms of N resources.