Henri E. Cuny

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.

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.

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!"

In conifers, interactions between the rates and the durations of wood formation prevent the recording of climatic influences in tree-ring structure, except in the last formed cells. 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.

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.

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.

On Modeling Wood Formation Using Parametric and Semiparametric Regressions for Count Data

Understanding how wood develops has become an important problematic of plant sciences. However, studying wood formation requires the acquisition of count data difficult to interpret. Here, the annual wood formation dynamics of a conifer tree species were modeled using generalized linear and additive models (GLM and GAM); GAM for location, scale, and shape (GAMLSS); a discrete semiparametric kernel regression for count data. The performance of models is evaluated using bootstrap methods. GLM was useful to describe the wood formation general pattern but had a lack of fitting, while GAM, GAMLSS, and kernel regression had a higher sensibility to short-term variations.

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.

Discrete triangular associated kernel and bandwidth choices in semiparametric estimation for count data

This work deals with semiparametric kernel estimator of probability mass functions which are assumed to be modified Poisson distributions. This semiparametric approach is based on discrete associated kernel method appropriated for modelling count data; in particular, the famous discrete symmetric triangular kernels are used. Two data-driven bandwidth selection procedures are investigated and an explicit expression of optimal bandwidth not available until now is provided. Moreover, some asymptotic properties of the cross-validation criterion adapted for discrete semiparametric kernel estimation are studied. Finally, to measure the performance of semiparametric estimator according to each type of bandwidth parameter, some applications are realized on three real count data-sets from sociology and biology.