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.

Turgor - a limiting factor for radial growth in mature conifers along an elevational gradient.

A valid representation of intra-annual wood formation processes in global vegetation models is vital for assessing climate change impacts on the forest carbon stock. Yet, wood formation is generally modelled with photosynthesis, despite mounting evidence that cambial activity is rather directly constrained by limiting environmental factors. Here, we apply a state-of-the-art turgor-driven growth model to simulate 4 yr of hourly stem radial increment from Picea abies (L.) Karst. and Larix decidua Mill. growing along an elevational gradient. For the first time, wood formation observations were used to validate weekly to annual stem radial increment simulations, while environmental measurements were used to assess the climatic constraints on turgor-driven growth. Model simulations matched the observed timing and dynamics of wood formation. Using the detailed model outputs, we identified a strict environmental regulation on stem growth (air temperature > 2°C and soil water potential > -0.6 MPa). Warmer and drier summers reduced the growth rate as a result of turgor limitation despite warmer temperatures being favourable for cambial activity. These findings suggest that turgor is a central driver of the forest carbon sink and should be considered in next-generation vegetation models, particularly in the context of global warming and increasing frequency of droughts.

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.

Couplings in cell differentiation kinetics mitigate air temperature influence on conifer wood anatomy.

Conifer trees possess a typical anatomical tree-ring structure characterized by a transition from large and thin-walled earlywood tracheids to narrow and thick-walled latewood tracheids. However, little is known on how this characteristic structure is maintained across contrasting environmental conditions, due to its crucial role to ensure sap ascent and mechanical support. In this study, we monitored weekly wood cell formation for up to 7 years in two temperate conifer species (i.e., Picea abies (L.) Karst and Larix decidua Mill.) across an 8°C thermal gradient from 800 to 2,200 m a.s.l. in central Europe to investigate the impact of air temperature on rate and duration of wood cell formation. Results indicated that towards colder sites, forming tracheids compensate a decreased rate of differentiation (cell enlarging and wall thickening) by an extended duration, except for the last cells of the latewood in the wall-thickening phase. This compensation allows conifer trees to mitigate the influence of air temperature on the final tree-ring structure, with important implications for the functioning and resilience of the xylem to varying environmental conditions. The disappearing compensation in the thickening latewood cells might also explain the higher climatic sensitivity usually found in maximum latewood density.

CAVIAR: an R package for checking, displaying and processing wood-formation-monitoring data.

In the last decade, the pervasive question of climate change impacts on forests has revived investigations on intra-annual dynamics of wood formation, involving disciplines such as plant ecology, tree physiology and dendrochronology. This resulted in the creation of many research groups working on this topic worldwide and a rapid increase in the number of studies and publications. Wood-formation-monitoring studies are generally based on a common conceptual model describing xylem cell formation as the succession of four differentiation phases (cell division, cell enlargement, cell wall thickening and mature cells). They generally use the same sampling techniques, sample preparation methods and anatomical criteria to separate between differentiation zones and discriminate and count forming xylem cells, resulting in very similar raw data. However, the way these raw data are then processed, producing the elaborated data on which statistical analyses are performed, still remains quite specific to each individual study. Thereby, despite very similar raw data, wood-formation-monitoring studies yield results that are still quite difficult to compare. CAVIAR-an R package specifically dedicated to the verification, visualization and manipulation of wood-formation-monitoring data-can help to improve this situation. Initially, CAVIAR was built to provide efficient algorithms to compute critical dates of wood formation phenology for conifers growing in temperate and cold environments. Recently, we developed it further to check, display and process wood-formation-monitoring data. Thanks to new and upgraded functions, raw data can now be consistently verified, standardized and modelled (using logistic regressions and Gompertz functions), in order to describe wood phenology and intra-annual dynamics of tree-ring formation. We believe that CAVIAR will help strengthening the science of wood formation dynamics by effectively contributing to the standardization of its concepts and methods, making thereby possible the comparison between data and results from different studies.

Cell size and wall dimensions drive distinct variability of earlywood and latewood density in Northern Hemisphere conifers.

Interannual variability of wood density - an important plant functional trait and environmental proxy - in conifers is poorly understood. We therefore explored the anatomical basis of density. We hypothesized that earlywood density is determined by tracheid size and latewood density by wall dimensions, reflecting their different functional tasks. To determine general patterns of variability, density parameters from 27 species and 349 sites across the Northern Hemisphere were correlated to tree-ring width parameters and local climate. We performed the same analyses with density and width derived from anatomical data comprising two species and eight sites. The contributions of tracheid size and wall dimensions to density were disentangled with sensitivity analyses. Notably, correlations between density and width shifted from negative to positive moving from earlywood to latewood. Temperature responses of density varied intraseasonally in strength and sign. The sensitivity analyses revealed tracheid size as the main determinant of earlywood density, while wall dimensions become more influential for latewood density. Our novel approach of integrating detailed anatomical data with large-scale tree-ring data allowed us to contribute to an improved understanding of interannual variations of conifer growth and to illustrate how conifers balance investments in the competing xylem functions of hydraulics and mechanical support.

Biological Basis of Tree-Ring Formation: A Crash Course.

Wood is of crucial importance for man and biosphere. In this mini review, we present the fundamental processes involved in tree-ring formation and intra-annual dynamics of cambial activity, along with the influences of the environmental factors. During wood formation, new xylem cells produced by the cambium are undergoing profound transformations, passing through successive differentiation stages, which enable them to perform their functions in trees. Xylem cell formation can be divided in five major phases: (1) the division of a cambial mother cell that creates a new cell; (2) the enlargement of this newly formed cell; (3) the deposition of its secondary wall; (4) the lignification of its cell wall; and finally, (5) its programmed cell death. In most regions of the world cambial activity follows a seasonal cycle. At the beginning of the growing season, when temperature increases, the cambium resumes activity, producing new xylem cells. These cells are disposed along radial files, and start their differentiation program according to their birth date, creating typical developmental strips in the forming xylem. The width of these strips smoothly changes along the growing season. Finally, when climatic conditions deteriorate (temperature or water availability in particular), cambial activity stops, soon followed by cell enlargement, and later on by secondary wall deposition. Without a clear understanding of the xylem formation process, it is not possible to comprehend how annual growth rings and typical wood structures are formed, recording normal seasonal variations of the environment as well as extreme climatic events.

Xylogenesis: Coniferous Trees of Temperate Forests Are Listening to the Climate Tale during the Growing Season But Only Remember the Last Words!

The complex inner mechanisms that create typical conifer tree-ring structure (i.e. the transition from large, thin-walled earlywood cells to narrow, thick-walled latewood cells) were recently unraveled. However, what physiological or environmental factors drive xylogenesis key processes remain unclear. Here, we aim to quantify the influence of seasonal variations in climatic factors on the spectacular changes in the kinetics of wood cell differentiation and in the resulting tree-ring structure. Wood formation was monitored in three sites over 3 years for three coniferous species (Norway spruce [Picea abies], Scots pine [Pinus sylvestris], and silver fir [Abies alba]). Cell differentiation rates and durations were calculated and related to tracheid final dimensions and corresponding climatic conditions. On the one hand, we found that the kinetics of cell enlargement and the final size of the tracheids were not explained by the seasonal changes in climatic factors. On the other hand, decreasing temperatures strongly constrained cell wall deposition rates during latewood formation. However, the influence of temperature was permanently written into tree-ring structure only for the very last latewood cells, when the collapse of the rate of wall deposition was no longer counterbalanced by the increase of its duration. Our results show that the formation of the typical conifer tree-ring structure, in normal climatic conditions, is only marginally driven by climate, suggesting strong developmental control of xylogenesis. The late breakage of the compensatory mechanism at work in the wall deposition process appears as a clue to understand the capacity of the maximum latewood density to record past temperature conditions.

Pattern of xylem phenology in conifers of cold ecosystems at the Northern Hemisphere.

The interaction between xylem phenology and climate assesses forest growth and productivity and carbon storage across biomes under changing environmental conditions. We tested the hypothesis that patterns of wood formation are maintained unaltered despite the temperature changes across cold ecosystems. Wood microcores were collected weekly or biweekly throughout the growing season for periods varying between 1 and 13 years during 1998-2014 and cut in transverse sections for assessing the onset and ending of the phases of xylem differentiation. The data set represented 1321 trees belonging to 10 conifer species from 39 sites in the Northern Hemisphere and covering an interval of mean annual temperature exceeding 14 K. The phenological events and mean annual temperature of the sites were related linearly, with spring and autumnal events being separated by constant intervals across the range of temperature analysed. At increasing temperature, first enlarging, wall-thickening and mature tracheids appeared earlier, and last enlarging and wall-thickening tracheids occurred later. Overall, the period of wood formation lengthened linearly with the mean annual temperature, from 83.7 days at -2 °C to 178.1 days at 12 °C, at a rate of 6.5 days °C-1 . April-May temperatures produced the best models predicting the dates of wood formation. Our findings demonstrated the uniformity of the process of wood formation and the importance of the environmental conditions occurring at the time of growth resumption. Under warming scenarios, the period of wood formation might lengthen synchronously in the cold biomes of the Northern Hemisphere.

Compensatory mechanisms mitigate the effect of warming and drought on wood formation.

Because of global warming, high-latitude ecosystems are expected to experience increases in temperature and drought events. Wood formation will have to adjust to these new climatic constraints to maintain tree mechanical stability and long-distance water transport. The aim of this study is to understand the dynamic processes involved in wood formation under warming and drought. Xylogenesis, gas exchange, water relations and wood anatomy of black spruce [Picea mariana (Mill.) B.S.P.] saplings were monitored during a greenhouse experiment where temperature was increased during daytime or night-time (+6 °C) combined with a drought period. The kinetics of tracheid development expressed as rate and duration of the xylogenesis sub-processes were quantified using generalized additive models. Drought and warming had a strong influence on cell production, but little effect on wood anatomy. The increase in cell production rate under warmer temperatures, and especially during the night-time warming at the end of the growing season, resulted in wider tree-rings. However, the strong compensation between rates and durations of cell differentiation processes mitigates warming and drought effects on tree-ring structure. Our results allowed quantification of how wood formation kinetics is regulated when water and heat stress increase, allowing trees to adapt to future environmental 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.

Kinetics of tracheid development explain conifer tree-ring structure.

Conifer tree rings are generally composed of large, thin-walled cells of light earlywood followed by narrow, thick-walled cells of dense latewood. Yet, how wood formation processes and the associated kinetics create this typical pattern remains poorly understood. We monitored tree-ring formation weekly over 3 yr in 45 trees of three conifer species in France. Data were used to model cell development kinetics, and to attribute the relative importance of the duration and rate of cell enlargement and cell wall deposition on tree-ring structure. Cell enlargement duration contributed to 75% of changes in cell diameter along the tree rings. Remarkably, the amount of wall material per cell was quite constant along the rings. Consequently, and in contrast with widespread belief, changes in cell wall thickness were not principally attributed to the duration and rate of wall deposition (33%), but rather to the changes in cell size (67%). Cell enlargement duration, as the main driver of cell size and wall thickness, contributed to 56% of wood density variation along the rings. This mechanistic framework now forms the basis for unraveling how environmental stresses trigger deviations (e.g. false rings) from the normal tree-ring structure.

A meta-analysis of cambium phenology and growth: linear and non-linear patterns in conifers of the northern hemisphere.

BACKGROUND AND AIMS: Ongoing global warming has been implicated in shifting phenological patterns such as the timing and duration of the growing season across a wide variety of ecosystems. Linear models are routinely used to extrapolate these observed shifts in phenology into the future and to estimate changes in associated ecosystem properties such as net primary productivity. Yet, in nature, linear relationships may be special cases. Biological processes frequently follow more complex, non-linear patterns according to limiting factors that generate shifts and discontinuities, or contain thresholds beyond which responses change abruptly. This study investigates to what extent cambium phenology is associated with xylem growth and differentiation across conifer species of the northern hemisphere. METHODS: Xylem cell production is compared with the periods of cambial activity and cell differentiation assessed on a weekly time scale on histological sections of cambium and wood tissue collected from the stems of nine species in Canada and Europe over 1-9 years per site from 1998 to 2011. KEY RESULTS: The dynamics of xylogenesis were surprisingly homogeneous among conifer species, although dispersions from the average were obviously observed. Within the range analysed, the relationships between the phenological timings were linear, with several slopes showing values close to or not statistically different from 1. The relationships between the phenological timings and cell production were distinctly non-linear, and involved an exponential pattern. CONCLUSIONS: The trees adjust their phenological timings according to linear patterns. Thus, shifts of one phenological phase are associated with synchronous and comparable shifts of the successive phases. However, small increases in the duration of xylogenesis could correspond to a substantial increase in cell production. The findings suggest that the length of the growing season and the resulting amount of growth could respond differently to changes in environmental conditions.

Generalized additive models reveal the intrinsic complexity of wood formation dynamics.

The intra-annual dynamics of wood formation, which involves the passage of newly produced cells through three successive differentiation phases (division, enlargement, and wall thickening) to reach the final functional mature state, has traditionally been described in conifers as three delayed bell-shaped curves followed by an S-shaped curve. Here the classical view represented by the 'Gompertz function (GF) approach' was challenged using two novel approaches based on parametric generalized linear models (GLMs) and 'data-driven' generalized additive models (GAMs). These three approaches (GFs, GLMs, and GAMs) were used to describe seasonal changes in cell numbers in each of the xylem differentiation phases and to calculate the timing of cell development in three conifer species [Picea abies (L.), Pinus sylvestris L., and Abies alba Mill.]. GAMs outperformed GFs and GLMs in describing intra-annual wood formation dynamics, showing two left-skewed bell-shaped curves for division and enlargement, and a right-skewed bimodal curve for thickening. Cell residence times progressively decreased through the season for enlargement, whilst increasing late but rapidly for thickening. These patterns match changes in cell anatomical features within a tree ring, which allows the separation of earlywood and latewood into two distinct cell populations. A novel statistical approach is presented which renews our understanding of xylogenesis, a dynamic biological process in which the rate of cell production interplays with cell residence times in each developmental phase to create complex seasonal patterns.

Life strategies in intra-annual dynamics of wood formation: example of three conifer species in a temperate forest in north-east France.

We investigated whether timing and rate of growth are related to the life strategies and fitness of three conifer species. Intra-annual dynamics of wood formation, shoot elongation and needle phenology were monitored over 3 years in five Norway spruces (Picea abies (L.) Karst.), five Scots pines (Pinus sylvestris L.) and five silver firs (Abies alba Mill.) grown intermixed. For the three species, the growing season (delimited by cambial activity onset and cessation) lasted about 4 months, while the whole process of wood formation lasted 5-6 months. Needle unfolding and shoot elongation followed the onset of cambial activity and lasted only one-third of the season. Pines exhibited an 'extensive strategy' of cambial activity, with long durations but low growth rates, while firs and spruces adopted an 'intensive strategy' with shorter durations but higher growth rates. We estimated that about 75% of the annual radial increment variability was attributable to the rate of cell production, and only 25% to its duration. Cambial activity rates culminated at the same time for the three species, whereas shoot elongation reached its maximal rate earlier in pines. Results show that species-specific life strategies are recognizable through functional traits of intra-annual growth dynamics. The opposition between Scots pine extensive strategy and silver fir and Norway spruce intensive strategy supports the theory that pioneer species are greater resource expenders and develop riskier life strategies to capture resources, while shade-tolerant species utilize resources more efficiently and develop safer life strategies. Despite different strategies, synchronicity of the maximal rates of cambial activity suggests a strong functional convergence between co-existing conifer species, resulting in head-on competition for resources.