Papers by Cyrille Rathgeber
Impact des changements climatiques et de l'augmentation du taux de CO2 atmosphérique sur la productivité des écosystèmes forestiers : exemple du pin d'Alep (Pinus halepensis Mill.) en Provence calcaire (France)
Les donnees provenant de 21 peuplements de pin d'Alep ont permis de calculer un indice synthe... more Les donnees provenant de 21 peuplements de pin d'Alep ont permis de calculer un indice synthetique de croissance qui exprime les variations inter-annuelles de productivite. Pour chaque peuplement, trois types de modeles de croissance (climatique, bioclimatique et biogeochimique) ont ete confrontes aux observations et valides. Le modele biogeochimique n'est pas sensible aux changements climatiques mais simule une tres forte augmentation de la productivite liee a l'augmentation du taux de CO2. Le modele climatique simule une forte augmentation de productivite liee a l'augmentation des temperatures printanieres. Le modele bioclimatique simule une diminution significative de la productivite liee a une augmentation de la secheresse estivale. La reaction d'un peuplement depend des conditions stationnelles. L'exposition determine le bilan thermique alors que la pente, la capacite hydrique du sol et la permeabilite du sous-sol contraignent le bilan hydrique.
Annals of Forest Science
Key message The emergence of the characteristic treering pattern during xylogenesis is commonly t... more Key message The emergence of the characteristic treering pattern during xylogenesis is commonly thought to be controlled by a gradient of morphogen (auxin, TDIF peptide...). We show that this hypothesis accounts for Handling Editor: Erwin DREYER Contribution of the co-authors F.P. Hartmann, C.B.K. Rathgeber. M. Fournier and B. Moulia conceived and designed the model and the numerical experiments. F. Hartmann developed and ran the model and analyzed the data. F. Hartmann, C. Rathgeber and B. Moulia wrote the paper. M. Fournier proofread the paper.
Annals of Forest Science, 2013
& Context Modification of stand density by thinning may buffer the response of tree growth and vi... more & Context Modification of stand density by thinning may buffer the response of tree growth and vigor to changes in climate by enhancing soil water availability. & Aims We tested the impact of thinning intensity on cambial growth of Aleppo pine (Pinus halepensis L.) under semi-arid, Mediterranean conditions. & Methods A multiple thinning experiment was established on an Aleppo pine plantation in Spain. We analysed the stem growth dynamics of two different crown classes under four different thinning intensities (15 %, 30 %, and 45 % removal of the basal area) for 2 years, based on biweekly band dendrometer recordings. Local relative extractable soil water was derived from the use of a water balance model Biljou© (available at ) and used as an explanatory variable. & Results Radial growth was mainly controlled by soil water availability during the growing season, and differed by crown class. The growth rates of dominant trees were significantly higher than the growth rates of suppressed trees. Removal of 30 % and 45 % of the initial basal area produced a growth release in both dominant and suppressed trees that did not occur under less intense thinning treatments. & Conclusions Soil water availability was the main driver of radial growth during the growing season. Forest management confirmed its value for ameliorating the effects of water limitations on individual tree growth. These results may help managers understand how altering stand density will differentially affect diameter growth responses of Aleppo pine to short-term climatic fluctuations, promoting forests that are resilient to future climatic conditions.
Annals of Botany, 2013
† Background and Aims Ongoing global warming has been implicated in shifting phenological pattern... more † 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.
PLoS ONE, 2013
We investigated the variability of the climate-growth relationship of Aleppo pine across its dist... more We investigated the variability of the climate-growth relationship of Aleppo pine across its distribution range in the Mediterranean Basin. We constructed a network of tree-ring index chronologies from 63 sites across the region. Correlation function analysis identified the relationships of tree-ring index to climate factors for each site. We also estimated the dominant climatic gradients of the region using principal component analysis of monthly, seasonal, and annual mean temperature and total precipitation from 1,068 climatic gridpoints. Variation in ring width index was primarily related to precipitation and secondarily to temperature. However, we found that the dendroclimatic relationship depended on the position of the site along the climatic gradient. In the southern part of the distribution range, where temperature was generally higher and precipitation lower than the regional average, reduced growth was also associated with warm and dry conditions. In the northern part, where the average temperature was lower and the precipitation more abundant than the regional average, reduced growth was associated with cool conditions. Thus, our study highlights the substantial plasticity of Aleppo pine in response to different climatic conditions. These results do not resolve the source of response variability as being due to either genetic variation in provenance, to phenotypic plasticity, or a combination of factors. However, as current growth responses to inter-annual climate variability vary spatially across existing climate gradients, future climategrowth relationships will also likely be determined by differential adaptation and/or acclimation responses to spatial climatic variation. The contribution of local adaptation and/or phenotypic plasticity across populations to the persistence of species under global warming could be decisive for prediction of climate change impacts across populations. In this sense, a more complex forest dynamics modeling approach that includes the contribution of genetic variation and phenotypic plasticity can improve the reliability of the ecological inferences derived from the climate-growth relationships.
Journal of Experimental Botany, 2013
The intra-annual dynamics of wood formation, which involves the passage of newly produced cells t... more 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.
Annals of Forest Science
& Key message Spring temperature increase is the main driver of larch tree wood formation onset a... more & Key message Spring temperature increase is the main driver of larch tree wood formation onset along a 1000-m elevation gradient in the Southern Alps, while its cessation is more probably controlled by water stress at the lowest elevation and photoperiod at higher ones. & Context The survival of perennial plants depends on their adaptation to changing environment and specially temperature, which in trees is notably implemented through wood formation process. & Aims Our main objective is to understand how the phenology of wood formation is related to environmental factors and to temperature in particular. & Methods We monitored the xylogenesis of 60 larch trees, distributed in four stands along an elevation gradient of 1000 m in the French Southern Alps. & Results Cambial activity started around mid-May at the lowest site (1350 m) and around mid-June at the highest one (2300 m), showing a delay of 5.4 days per°C. The onset of wall-thickening and mature phenophases followed the same linear trend with a delay of 5.2 and 3 days per°C, respectively. Phenophase cessations followed a parabolic trend with trees from the lowest site finishing their growth the first, while those from 1700 m finished the last. Our results show that the onset of xylem formation is mainly driven by spring temperature increase, while its cessation is more related to photoperiod, with water shortage being able to hasten it. & Conclusion Future climatic changes will most probably increase growing season length (but not necessarily wood production) and shift upwards the optimal elevation for larch growth in the Southern Alps.
Annals of Forest Science
& Key message This study presents a novel histologic approach to quantify the intra-annual dynami... more & Key message This study presents a novel histologic approach to quantify the intra-annual dynamics of carbon sequestration in forming wood. This innovative approach, based on repeated measurements of xylem apparent density, is more direct, and more accurate than the previously published cellular-based approach. Moreover, this new approach, which was tested here on softwoods, is also applicable to hardwoods without any modification. & Context Forest ecosystems are key players of the terrestrial carbon cycle. Indeed, wood represents the principal carbon pool of terrestrial biomass, accumulated in trees through cambial activity. & Aims Here, we present a novel, simple, and fast approach to accurately estimate the intra-annual dynamics of aboveground woody biomass production based on image analysis of forming xylem sections. & Methods During the 2015 growing season, we weekly collected wood samples (microcores) containing the forming xylem on seven Norway spruces (Picea abies (L.) Karst), grown in Hesse forest (North-East France). The microcores were prepared to allow the observation of the forming tissues with an optical microscope. Xylem apparent density and radial increment were then measured directly on images of the histological sections. In order to compare our Bhistologic approach^with the previously published Bcellular approach,^we also counted the number of tracheids in each differentiation zones, and measured the tracheid dimensions all along the last-formed tree ring. & Results The two approaches yielded comparable meaningful results, describing xylem size increase and aboveground woody biomass production as bell-shaped curves culminating in May and June respectively. However, the histologic approach provided a shorter time lag between xylem size increase and biomass production than the cellular one. & Conclusion Better quantification of the shift between stem growth in size and in biomass will require addressing the knowledge gap regarding lignin deposition kinetics. Nevertheless, our novel histologic approach is simpler and more direct than the cellular one, and may open the way to a first quantification of intra-annual dynamics of woody biomass production in angiosperms, where the cellular approach is hardly applicable.
Ecologia mediterranea
Les changements planétaires (changements climatiques, augmentation du taux de CO 2 atmosphérique ... more Les changements planétaires (changements climatiques, augmentation du taux de CO 2 atmosphérique et augmentation des dépôts azotés) sont susceptibles d'avoir un effet sur la production des écosystèmes forestiers. La dendrochronologie offre un moyen de vérifier cette hypothèse en milieu naturel, car les données de croissance radiale peuvent être interprétées comme des indicateurs de la productivité des écosystèmes forestiers. Les données dendrochronologiques utilisées dans cette étude proviennent de 21 peuplements de pin d'Alep localisés en Provence calcaire, dans le sud-est de la France. Les variables analysées sont : la densité minimale, la densité du bois initial, la largeur du bois initial, la densité maximale, la densité du bois final, la largeur du bois final, ainsi qu'un indice synthétique de croissance. Les tendances sont détectées sur la période . Cette étude n'a pas permis de mettre en évidence de tendances générales positives et significatives concernant les variables relatives à la largeur des cernes, contrairement à ce que laissait prévoir la littérature scientifique. Ce travail a cependant permis de mettre en évidence une augmentation de la densité moyenne du bois initial et une diminution de la densité moyenne du bois final ainsi que de la densité maximale. Ces résultats montrent que la baisse de densité du bois final observée par différents auteurs pour le nord et le centre de l'Europe semble également être valide pour le sud de l'Europe. Cela suggère l'influence d'un facteur commun à toutes ces régions qui pourrait être l'augmentation des dépôts azotés.
Cutting time slices of tree rings —How intra-annual dynamics of wood formation help to decipher space for time conversion in tree-ring sciences
&... more <p>Despite a long-standing interest in retrieving intra-annual environmental information from tree-ring features, none of the approaches developed so far for accurately dating intra-ring sector has been validated on observations. Here, we investigated space-for-time association across regular intra-ring sectors for which we estimated the timing of formation. For this purpose, a unique dataset containing quantitative wood anatomy measurements and kinetics of tracheid differentiation was compiled for 45 trees grown in North-East France (three years of wood formation monitoring, for five trees, from three different conifer species). Tracheid dimensions were measured directly on the best anatomical sections at the end of the growing season, while the kinetics of xylem cell differentiation were provided at tree-level by an empirical model of wood formation dynamics. Our results confirmed that the time taken to form sectors of the same width increased from earlywood (composed of wide thin-walled tracheids) to latewood (composed of narrow thick-walled tracheids). This mainly reflected the increase of the duration of cell wall deposition through the growing season, and, to a lesser extent, the augmentation of the number of tracheids per sectors. However, our results also show that regular intra-ring sectors, which were well separated in space, overlapped in time. The overlapping culminated during the summer period, reaching 40 % for 10 sectors. It could be reduced to approx. 30 % by increasing the number of sectors (from 10 to 25, for example), but it cannot be removed. Therefore, successive intra-ring sectors could not be attributed to a succession of separated time intervals by simply using their relative position along the ring. However, the formation of sectors of equivalent ranks were noticeably synchronous between the different trees and years, reaching 80 % of synchronicity for the process of wall thickening. This suggest that data from regular intra-ring sectors could be reliably used to build mean chronologies expressing the common signal of tree populations. Our results show the limits that the xylogenesis process itself imposes on the dating of intra-ring features. They also argue for an in-depth understanding of the association between cell differentiation processes (enlargement, wall thickening and lignification) and wood characteristics (density, anatomy, stable isotope composition).</p>
Global ecological trends in wood cell production of coniferous trees
&... more <p>As a consequence of recent climatic changes, many studies have reported an increase in tree growth, forest ecosystem net primary productivity, and terrestrial biosphere carbon up-take, making forests one of the largest carbon sink on Earth. Direct and remote observations, as well as eco-physiological models, have suggested that it is mainly the rise in temperature and the resulting extended period of growth that is responsible for forest enhanced productivity. However, up to now, there is no comprehensive observation-based study deciphering the respective roles of the length of the growing season versus its intensity, to confirm this interpretation. Based on a large wood-formation-monitoring dataset, encompassing numerous sites from Mediterranean to Boreal conifer forests, we tested the hypothesis that the length of the growing period is more important than the rate of growth to explain tree-ring width. Moreover, we explored the influence of the environmental conditions on the variation in both timings and rates of xylem cell production.</p><p>We collected data from more than 50 sites spread at various altitudes and latitudes, on three continents (America, Europe, Asia), in the extra tropical parts of the Northern Hemisphere (Boreal, Temperate and Mediterranean bioclimatic zones). Wood formation was monitored at a weekly time-step using histological sections of forming xylem collected from the stems of more than 15 conifer species. The critical dates of xylem phenology were assessed at tree level using logistic regressions, while the rates of cell production were computed using Gompertz models. A basic physical model was developed relating the total number of xylem cells with the rate and duration of its production. A sensitivity analyses was performed to reveal the global ecological patterns of tree-ring formation, while mixed effect models were used to quantify the influences of the environmental factors.</p><p>The basic physical model of xylem cell production was applied successfully to the whole dataset (including Mediterranean sites) explaining more than 80 % of the observed variability. The sensitivity analysis showed that the rate of xylem cell production contributed a bit more than the duration to the variation in the final number of cells. Trees presented contrasted strategies according to the bioclimatic zone they belong to: while Boreal trees grew at a high speed during a short time; Mediterranean trees proceeded slowly, but for an extended period of time. Nevertheless, even for Mediterranean trees, the rate of growth remained the first driver of the final number of cells. Moreover, we showed that xylem phenology was consistently explained by the change in thermal conditions occurring with altitude or latitude, while growth rate was more related to species effect and site…
Annals of Forest Science
& Key message This special issue of Annals of Forest Science compiles ten papers on "Wood formati... more & Key message This special issue of Annals of Forest Science compiles ten papers on "Wood formation and tree adaptation to climate", which were presented at "Le Studium" International Conference in May 2018 in Orléans (France). These papers present observational, experimental and modelling studies investigating the influence of climatic changes on tree growth from the hour to the century, and from the cell to the landscape.
Influence du statut social des arbres sur la dynamique intra-annuelle de la formation du bois
Collection EDYTEM. Cahiers de géographie
Dynamique intra-annuelle de la formation du bois de trois espèces de conifères (Épicéa commun, Pin sylvestre et Sapin pectiné) dans les Vosges
Collection EDYTEM. Cahiers de géographie
Annals of Forest Science
& Key message In order to record the seasonal changes in aboveground biomass production (trunk an... more & Key message In order to record the seasonal changes in aboveground biomass production (trunk and branches) in a forest, changes in wood density must be taken into account. A 60-year-old beech forest displayed a large intra-annual variability in its aboveground woody biomass production efficiency. This variation followed a seasonal trend with a maximum during the summer while gross primary production was rather low. & Context In the current context of land use and climate change, there is a need to precisely quantify the carbon (C) balance of forest ecosystems, and more specifically, of C allocation to tree compartments. & Aims We quantified the seasonal changes in the aboveground biomass production (aBP) of a beech forest growing on two different soils: an alocrisol and a calci-brunisol. In addition, for the alocrisol ecosystem, we assessed the existence and degree of intra-annual variability in the ratio of wood aBP to gross primary production (GPP), i.e., the wood aBP efficiency. & Methods The study site is a 60-year-old beech forest in northeastern France. An eddy covariance tower records continuously net ecosystem exchange. To investigate the temporal changes in aBP, mini-cores were drilled and diameter at breast height measurements were taken on a monthly basis from 45 trees for both stands studied over 2014. & Results A clear difference in aBP was observed between the two soils with the alocrisol being more productive than the calcibrunisol. For the alocrisol, both woody aBP and GPP changed over the course of the year, reaching peak values during June (6 and 12.5 gC m −2 day −1 , respectively). Wood applied bias photon-to-current efficiency aboveground Biomass Production Efficiency (aBPE) also showed important intra-annual variations, ranging from 0.09 in September to 0.58 in July. Wood density varied throughout the year, and not taking it into account would have led to an overestimation of aBP by as much as 20% in April and May. & Conclusion Our study highlights the importance of taking wood density into account for intra-annual studies of aBP. Wood aBPE cannot be considered as constant as it fluctuated from 0.09 to 0.58 throughout the year for an annual value of 0.34. The potential error in wood aBPE stemming from not taking these changes into account amounts to 15%.
Global Change Biology
The phenology of wood formation is a critical process to consider for predicting how trees from t... more The phenology of wood formation is a critical process to consider for predicting how trees from the temperate and boreal zones may react to climate change. Compared to leaf phenology, however, the determinism of wood phenology is still poorly known. Here, we compared for the first time three alternative ecophysiological model classes (threshold models, heat-sum models and chillinginfluenced heat-sum models) and an empirical model in their ability to predict the starting date of xylem cell enlargement in spring, for four major Northern Hemisphere conifers (Larix decidua, Pinus sylvestris, Picea abies and Picea mariana). We fitted models with Bayesian inference to wood phenological data collected for 220 site-years over Europe and Canada. The chilling-influenced heatsum model received most support for all the four studied species, predicting validation data with a 7.7-day error, which is within one-day of the observed data resolution. We conclude that both chilling and forcing temperatures determine the onset of wood formation in Northern Hemisphere conifers. Importantly, the chilling-influenced heat-sum model showed virtually no spatial bias whichever the species, despite the large environmental gradients considered. This suggests that the spring onset of wood formation is far less affected by local adaptation than by environmentallydriven plasticity. In a context of climate change, we therefore expect rising winter-spring temperature to exert ambivalent effects on the spring onset of wood formation, tending to hasten it through the accumulation of forcing temperature, but imposing a higher forcing-temperature requirement through the lower accumulation of chilling.
Tree Physiology
In the last decade, the pervasive question of climate change impacts on forests has revived inves... more 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-formationmonitoring 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.
Couplings in cell differentiation kinetics mitigate air temperature influence on conifer wood anatomy
Plant, cell & environment, Jan 16, 2018
Conifer trees possess a typical anatomical tree-ring structure characterized by a transition from... more 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 seven 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 2200 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 miti...
Trees
Data presented in this figure are correct, however, the LAI at site O1 was determined in a differ... more Data presented in this figure are correct, however, the LAI at site O1 was determined in a different way as described in the methods section for LAI of T1-T4:
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Papers by Cyrille Rathgeber