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 longer wood growing season does not lead to higher carbon sequestration.

A reliable assessment of forest carbon sequestration depends on our understanding of wood ecophysiology. Within a forest, trees exhibit different timings and rates of growth during wood formation. However, their relationships with wood anatomical traits remain partially unresolved. This study evaluated the intra-annual individual variability in growth traits in balsam fir [Abies balsamea (L.) Mill.]. We collected wood microcores weekly from April to October 2018 from 27 individuals in Quebec (Canada) and prepared anatomical sections to assess wood formation dynamics and their relationships with the anatomical traits of the wood cells. Xylem developed in a time window ranging from 44 to 118 days, producing between 8 and 79 cells. Trees with larger cell production experienced a longer growing season, with an earlier onset and later ending of wood formation. On average, each additional xylem cell lengthened the growing season by 1 day. Earlywood production explained 95% of the variability in xylem production. More productive individuals generated a higher proportion of earlywood and cells with larger sizes. Trees with a longer growing season produced more cells but not more biomass in the wood. Lengthening the growing season driven by climate change may not lead to enhanced carbon sequestration from wood production.

Spatial patterns and climatic drivers of leaf spring phenology of maple in eastern North America.

The resurgent frequency of extreme weather events and their strongly distinctive spatial patterns lead to a growing interest in phenology as an indicator of tree susceptibility. Using a long-term chronology of observations collected in situ, we predicted and investigated the spatial patterns and environmental drivers of spring leaf phenology across maple stand polygons dominated by Acer saccharum Marsh. and/or Acer rubra L. in eastern North America for 2000-2018. Model' calibration was based on Bayesian ordinal regressions relating the timing of the phenological events' observations to the MODIS vegetation indices EVI, NDVI and LAI. DAYMET data have been extracted to compute temperature and precipitation during spring phenology. Model accuracy increased as the season progressed, with prediction uncertainty spanning from 9 days for bud swelling to 4 days for leaf unfolding. NDVI and LAI were the best predictors for the onset and ending of spring phenology, respectively. Bud swelling occurred at the end of March in the early stands and at the onset of May in the late stands, while leaf unfolding was completed at the beginning of April for the early and in mid-June for the late stands. Early and late stands polarized towards a south-west-north-east gradient. In the south-western regions, which are also the driest, total precipitation and minimum temperature explained respectively 73 % and 25 % of the duration of spring phenology. In the north-eastern regions, precipitation and minimum temperature explained 62 % and 26 % of the duration of spring phenology. Our results suggest high vulnerability to extreme weather events in stands located in the south-west of the species distribution. The increasing incidence of drought in these locations might affect spring phenology, decreasing net primary production in these stands. Warmer nights might expose the buds to late frosts, events that are expected to become more frequent in the coming years.

The early bud gets the cold: Diverging spring phenology drives exposure to late frost in a Picea mariana [(Mill.) BSP] common garden.

Under climate change, the increasing occurrence of late frost combined with advancing spring phenology can increase the risk of frost damage in trees. In this study, we tested the link between intra-specific variability in bud phenology and frost exposure and damages. We analysed the effects of the 2021 late frost event in a black spruce (Picea mariana (Mill.) BSP) common garden in Québec, Canada. We hypothesised that the timing of budbreak drives the exposure of vulnerable tissues and explains differences in frost damage. Budbreak was monitored from 2015 to 2021 in 371 trees from five provenances originating between 48° and 53° N and planted in a common garden at 48° N. Frost damages were assessed on the same trees through the proportion of damaged buds per tree and related to the phenological phases by ordinal regressions. After an unusually warm spring, minimum temperatures fell to -1.9°C on May 28 and 29, 2021. At this moment, trees from the northern provenances were more advanced in their phenology and showed more frost damage. Provenances with earlier budbreak had a higher probability of damage occurrence according to ordinal regression. Our study highlights the importance of intra-specific variability of phenological traits on the risk of frost exposure. We provide evidence that the timings of bud phenology affect sensitivity to frost, leading to damages at temperatures of -1.9°C. Under the same conditions, the earlier growth reactivation observed in the northern provenances increases the risks of late frost damage on the developing buds.

Upscaling xylem phenology: sample size matters.

BACKGROUND AND AIMS: Upscaling carbon allocation requires knowledge of the variability at the scales at which data are collected and applied. Trees exhibit different growth rates and timings of wood formation. However, the factors explaining these differences remain undetermined, making samplings and estimations of the growth dynamics a complicated task, habitually based on technical rather than statistical reasons. This study explored the variability in xylem phenology among 159 balsam firs [Abies balsamea (L.) Mill.]. METHODS: Wood microcores were collected weekly from April to October 2018 in a natural stand in Quebec, Canada, to detect cambial activity and wood formation timings. We tested spatial autocorrelation, tree size and cell production rates as explanatory variables of xylem phenology. We assessed sample size and margin of error for wood phenology assessment at different confidence levels. KEY RESULTS: Xylem formation lasted between 40 and 110 d, producing between 12 and 93 cells. No effect of spatial proximity or size of individuals was detected on the timings of xylem phenology. Trees with larger cell production rates showed a longer growing season, starting xylem differentiation earlier and ending later. A sample size of 23 trees produced estimates of xylem phenology at a confidence level of 95 % with a margin of error of 1 week. CONCLUSIONS: This study highlighted the high variability in the timings of wood formation among trees within an area of 1 km2. The correlation between the number of new xylem cells and the growing season length suggests a close connection between the processes of wood formation and carbon sequestration. However, the causes of the observed differences in xylem phenology remain partially unresolved. We point out the need to carefully consider sample size when assessing xylem phenology to explore the reasons underlying this variability and to allow reliable upscaling of carbon allocation in forests.

Auxin concentration and xylem production of Pinus massoniana in a subtropical forest in south China.

Auxin is involved in various developmental processes of plants, including cell division in cambium and xylem differentiation. However, most studies linking auxin and xylem cell production are performed in environments with a strong seasonality (i.e., temperate and boreal climates). The temporal dynamics of auxin and cambial activity of subtropical trees remain basically unknown. In this study, we sampled four microcores weekly in three individuals of Chinese red pine (Pinus massoniana Lamb.) from February to December 2015-16 to compare xylem formation with auxin concentration in subtropical China. During the entire period of sampling, the number of cambial cells varied from 2 to 7, while the number of cells in the enlarging zone ranged from 1 to 4 and from 1 to 5 in the wall-thickening zone. In 2015, the average auxin concentration was 3.46 ng g-1, with 33 xylem cells being produced at the end of the year. In 2016, a lower auxin concentration (2.59 ng g-1) corresponded to a reduced annual xylem production (13.7 cells). No significant relationship between auxin concentration and number of xylem cells in differentiation was found at the weekly scale. Unlike in boreal and temperate forests, the lack of wood formation seasonality in subtropical forests makes it more difficult to reveal the relationship between auxin concentration and number of xylem cells in differentiation at the intra-annual scale. The frequent and repeated samplings might have reduced auxin concentration in the developing cambium and xylem, resulting in a lower xylem cell production.

Environmental and developmental factors driving xylem anatomy and micro-density in black spruce.

Wood density is the product of carbon allocation for structural growth and reflects the trade-off between mechanical support and water conductivity. We tested a conceptual framework based on the assumption that micro-density depends on direct and indirect relationships with endogenous and exogenous factors. The dynamics of wood formation, including timings and rates of cell division, cell enlargement, and secondary wall deposition, were assessed from microcores collected weekly between 2002 and 2016 from five black spruce stands located along a latitudinal gradient in Quebec, Canada. Cell anatomy and micro-density were recorded by anatomical analyses and X-ray measurements. Our structural equation model explained 80% of micro-density variation within the tree-ring with direct effects of wall thickness (σ = 0.61), cell diameter (σ = -0.51), and photoperiod (σ = -0.26). Wood formation dynamics had an indirect effect on micro-density. Micro-density increased under longer periods of cell-wall deposition and shorter durations of enlargement. Our results fill a critical gap in understanding the relationships underlying micro-density variation in conifers. We demonstrated that short-term responses to environmental variations could be overridden by plastic responses that modulate cell differentiation. Our results point to wood formation dynamics as a reliable predictor of carbon allocation in trees.

Contrasting Carbon Allocation Strategies of Ring-Porous and Diffuse-Porous Species Converge Toward Similar Growth Responses to Drought.

Extreme climatic events that are expected under global warming expose forest ecosystems to drought stress, which may affect the growth and productivity. We assessed intra-annual growth responses of trees to soil water content in species belonging to different functional groups of tree-ring porosity. We pose the hypothesis that species with contrasting carbon allocation strategies, which emerge from different relationships between wood traits and canopy architecture, display divergent growth responses to drought. We selected two diffuse-porous species (Acer saccharum and Betula alleghaniensis) and two ring-porous species (Quercus rubra and Fraxinus americana) from the mixed forest of Quebec (Canada). We measured anatomical wood traits and canopy architecture in eight individuals per species and assessed tree growth sensitivity to water balance during 2008-2017 using the standardized precipitation evapotranspiration index (SPEI). Stem elongation in diffuse-porous species mainly depended upon the total number of ramifications and hydraulic diameter of the tree-ring vessels. In ring-porous species, stem elongation mainly depended upon the productivity of the current year, i.e., number of vessels and basal area increment. Diffuse-porous and ring-porous species had similar responses to soil water balance. The effect of soil water balance on tree growth changed during the growing season. In April, decreasing soil temperature linked to wet conditions could explain the negative relationship between SPEI and tree growth. In late spring, greater water availability affected carbon partitioning, by promoting the formation of larger xylem vessels in both functional groups. Results suggest that timings and duration of drought events affect meristem growth and carbon allocation in both functional groups. Drought induces the formation of fewer xylem vessels in ring-porous species, and smaller xylem vessels in diffuse-porous species, the latter being also prone to a decline in stem elongation due to a reduced number of ramifications. Indeed, stem elongation of diffuse-porous species is influenced by environmental conditions of the previous year, which determine the total number of ramifications during the current year. Drought responses in different functional groups are thus characterized by different drivers, express contrasting levels of resistance or resilience, but finally result in an overall similar loss of productivity.

Comparing the Cell Dynamics of Tree-Ring Formation Observed in Microcores and as Predicted by the Vaganov-Shashkin Model.

New insights into the intra-annual dynamics of tree-ring formation can improve our understanding of tree-growth response to environmental conditions at high-resolution time scales. Obtaining this information requires, however, a weekly monitoring of wood formation, sampling that is extremely time-intensive and scarcely feasible over vast areas. Estimating the timing of cambial and xylem differentiation by modeling thus represents an interesting alternative for obtaining this important information by other means. Temporal dynamics of cambial divisions can be extracted from the daily tree-ring growth rate computed by the Vaganov-Shashkin (VS) simulation model, assuming that cell production is tightly linked to tree-ring growth. Nonetheless, these predictions have yet to be compared with direct observations of wood development, i.e., via microcoring, over a long time span. We tested the performance of the VS model by comparing the observed and predicted timing of wood formation in black spruce [Picea mariana (Mill.)]. We obtained microcores over 15 years at 5 sites along a latitudinal gradient in Quebec (Canada). The measured variables included cell size and the timing of cell production and differentiation. We calibrated the VS model using daily temperature and precipitation recorded by weather stations located on each site. The predicted and observed timing of cambial and enlarging cells were highly correlated (R 2 = 0.8); nonetheless, we detected a systematic overestimation in the predicted timing of cambial cells, with predictions delayed by 1-20 days compared with observations. The growth rate of cell diameter was correlated with the predicted growth rate assigned to each cambial cell, confirming that cell diameter developmental dynamics have the potential to be inferred by the tree-ring growth curve of the VS model. Model performances decrease substantially in estimating the end of wood formation. The systematic errors suggest that the actual relationships implemented in the model are unable to explain the phenological events in autumn. The mismatch between the observed and predicted timing of wood formation in black spruce within our study area can be reduced by better adapting the VS model to wet sites, a context for which this model has been rarely used.

How plant allometry influences bud phenology and fruit yield in two Vaccinium species.

BACKGROUND AND AIMS: Understanding how plant allometry, plant architecture and phenology contribute to fruit production can identify those plant traits that maximize fruit yield. In this study, we compared these variables and fruit yield for two shrub species, Vaccinium angustifolium and Vaccinium myrtilloides, to test the hypothesis that phenology is linked to the plants' allometric traits, which are predictors of fruit production. METHODS: We measured leaf and flower phenology and the above-ground biomass of both Vaccinium species in a commercial wild lowbush blueberry field (Quebec, Canada) over a 2-year crop cycle; 1 year of pruning followed by 1 year of harvest. Leaf and flower phenology were measured, and the allometric traits of shoots and buds were monitored over the crop cycle. We hand-collected the fruits of each plant to determine fruit attributes and biomass. KEY RESULTS: During the harvesting year, the leafing and flowering of V. angustifolium occurred earlier than that of V. myrtilloides. This difference was related to the allometric characteristics of the buds due to differences in carbon partitioning by the plants during the pruning year. Through structural equation modelling, we identified that the earlier leafing in V. angustifolium was related to a lower leaf bud number, while earlier flowering was linked to a lower number of flowers per bud. Despite differences in reproductive allometric traits, vegetative biomass still determined reproductive biomass in a log-log scale model. CONCLUSIONS: Growing buds are competing sinks for non-structural carbohydrates. Their differences in both number and characteristics (e.g. number of flowers per bud) influence levels of fruit production and explain some of the phenological differences observed between the two Vaccinium species. For similar above-ground biomass, both Vaccinium species had similar reproductive outputs in terms of fruit biomass, despite differences in reproductive traits such as fruit size and number.

Is size an issue of time? Relationship between the duration of xylem development and cell traits.

BACKGROUND AND AIMS: Secondary growth is a process related to the formation of new cells that increase in size and wall thickness during xylogenesis. Temporal dynamics of wood formation influence cell traits, in turn affecting cell patterns across the tree ring. We verified the hypothesis that cell diameter and cell wall thickness are positively correlated with the duration of their differentiation phases. METHODS: Histological sections were produced by microcores to assess the periods of cell differentiation in black spruce [Picea mariana (Mill.) B.S.P.]. Samples were collected weekly between 2002 and 2016 from a total of 50 trees in five sites along a latitudinal gradient in Quebec (Canada). The intra-annual temporal dynamics of cell differentiation were estimated at a daily scale, and the relationships between cell traits and duration of differentiation were fitted using a modified von Bertalanffy growth equation. KEY RESULTS: At all sites, larger cell diameters and cell wall thicknesses were observed in cells that experienced a longer period of differentiation. The relationship was a non-linear, decreasing trend that occasionally resulted in a clear asymptote. Overall, secondary wall deposition lasted longer than cell enlargement. Earlywood cells underwent an enlargement phase that lasted for 12 d on average, while secondary wall thickness lasted 15 d. Enlargement in latewood cells averaged 7 d and secondary wall deposition occurred over an average of 27 d. CONCLUSIONS: Cell size across the tree ring is closely connected to the temporal dynamics of cell formation. Similar relationships were observed among the five study sites, indicating shared xylem formation dynamics across the entire latitudinal distribution of the species.The duration of cell differentiation is a key factor involved in cell growth and wall thickening of xylem, thereby determining the spatial variation of cell traits across the tree ring.