Timing Of Bud Burst Research Articles

Evolution, plasticity and evolving plasticity of phenology in the tree species Alnus glutinosa.

Both traits and the plasticity of these traits are subject to evolutionary change and therefore affect the long-term persistence of populations and their role in local communities. We subjected clones from 12 different populations of Alnus glutinosa, located along a latitudinal gradient, to two different temperature treatments, to disentangle the distribution of genetic variation in timing of bud burst and bud burst plasticity within and among genotypes, populations, and regions. We calculated heritability and evolvability estimates for bud burst and bud burst plasticity and assessed the influence of divergent selection relative to neutral drift. We observed higher levels of heritability and evolvability for bud burst than for its plasticity, whereas the total phenological heritability and evolvability (i.e. combining timing of bud burst and bud burst plasticity) suggest substantial evolutionary potential with respect to phenology. Earlier bud burst was observed for the low-latitudinal populations than for the populations from higher latitudes, whereas the high-latitudinal populations did not show the expected delayed bud burst. This countergradient variation can be due to evolution towards increased phenological plasticity at higher latitudes. However, because we found little evidence for adaptive differences in phenological plasticity across the latitudinal gradient, we suggest differential frost tolerance as the most likely explanation for the observed phenological patterns in A. glutinosa.

Population differentiation and phenotypic plasticity in temperature response of bud burst in Frangula alnus provenances of different latitude

Flushing in spring marks an important adaptive process in a tree’s growth cycle. We studied bud burst in three provenances of a common small tree Frangula alnus Mill., originating from Italy, Belgium and Sweden. We observed timing of bud burst and leaf senescence in a common garden, and timing and duration of bud burst in greenhouse conditions (cuttings) with different temperature regimes, all located in Belgium. The early bud burst response of the southern European provenance together with the later leaf senescence compared to the local provenance indicated population differentiation that may, at least partly, be driven by local adaptation to a longer growing season. The duration of the process was longer in the cold greenhouse compared to the local provenance, whereas it responded similar as the local provenance in the warm greenhouse, suggesting adaptation to warmer conditions. Unexpectedly, the northern European provenance expressed a plastic reaction to warmer temperatures in the field trial and in the greenhouse conditions flushing in both cases earlier than the local provenance. The duration of the process in the warm greenhouse compared to the local provenance was shorter, whereas in the cold greenhouse it was similar. This result again suggested that not only the onset, but also the duration of the bud burst process was a plastic reaction to the warmer conditions compared to its site of origin. Together, our results suggest two mechanisms driving bud burst in F. alnus provenances, a co-gradient and a counter-gradient variation depending on the latitude of origin.

Chilling temperature and photoperiod influence the timing of bud burst in juvenile Betula pubescens Ehrh. and Populus tremulaL. trees

This research demonstrates that inadequate chilling has the potential to slow both the rate and speed of bud burst of two important European forest species; Betula pubescens and Populus tremula. The timing of bud burst in deciduous trees has been widely used as an indicator of spring warming. However, winter chilling conditions can have a significant impact on the timing of bud burst. If trees receive insufficient chilling, there may be a delay in bud burst even if spring temperatures rise. Therefore, it is important to understand the effect of chilling on spring phenology of trees. Here, we exposed juvenile (3–6-year old) birch (B. pubescens Ehrh.) and aspen (P. tremula L.) trees to a range of photoperiods, chilling durations and forcing temperatures in controlled environment chambers to assess the impact on the timing of bud burst. Analysis of variance demonstrated that longer chilling duration resulted in earlier bud burst in both species, and less thermal time was needed to reach maximum bud burst. Therefore, in warmer winters bud burst in spring may be expected to be delayed if insufficient chilling is received. However, longer photoperiod may, at least in part, compensate for shorter chilling duration. These results suggest that models predicting climate warming impacts on phenology should take winter chilling into account when considering the timing of bud burst in deciduous species.

Differentiation in phenological and physiological traits in European beech (Fagus sylvatica L.)

The knowledge of the extent of local adaptation is essential for forest reproductive material transfer, designing gene conservation programs and measures for mitigation of the ongoing climate change. A common methodology for assessing selection underlying local adaptation is the comparison of differentiation at neutral markers (measured by F ST) against quantitative traits (measured by Q ST). We investigated differentiation in phenology, height and diameter growth, and parameters of photosynthesis and water regime in a widespread European broadleaved tree, European beech (Fagus sylvatica L.). As the assessment of Q ST requires known pedigree structure of the tested populations, it was approximated by the coefficient of phenotypic differentiation P ST. For all phenology traits, especially budburst timing, there is a strong and reliable evidence of local adaptation as indicated by P ST > F ST. On the other hand, P ST was generally smaller than F ST for most growth and physiological traits, but the evidence for uniform selection or canalization acting at genes underlying these traits is generally absent or weak. Possible heritable basis of phenological differentiation is discussed, and implications for the current EU legislation on forest reproductive material are drawn.

Limited effective gene flow between two interfertile red oak species

Key message Highly elevated differentiation in differ- ent life stages between two interfertile oak species at a CONSTANS-like gene suggests a role of this gene in pre- zygotic isolation and adaptive divergence between species. Abstract Genome-wide differentiation patterns among oak species suggest that divergent selection can maintain species-specific adaptations and morphological integrity by reducing effective interspecific gene flow. While there is evidence for both pre- and post-zygotic isolation mechan- isms in oaks (e.g., differences in flowering time, selection against hybrids), these mechanisms are rarely studied at each life stage from acorns to adult trees within the same forest. To assess the reproductive isolation mechanisms between two ecologically divergent species, we (1) quan- tified the number of hybrids in different life stages in Quercus rubra and Quercus ellipsoidalis, two interfertile red oaks with different adaptations to drought, and (2) assessed the timing of bud burst in both natural populations and in a seedling common garden trial. The low number of hybrids in all life stages suggested pre-zygotic isolation between species or selection in very early life stages that have not been sampled (e.g., early seed abortion). Sig- nificant differences in bud burst were found in two con- secutive years between species in a common garden seedling trial but not in natural populations of the same provenance. In addition, we found evidence for divergent selection on several gene loci between species in each life stage. In particular, an SSR repeat located within the coding sequence of a CONSTANS-like gene, a locus in- volved in the photoperiodic regulation of flowering time and development, showed very high interspecific differ- entiation between species in all life stages (mean FST = 0.83), compared to the average neutral differen- tiation of 3.7 %.

OBJECTIVE PHENOTYPING THE TIME OF BUD BURST BY ANALYZING GRAPEVINE FIELD IMAGES

In grapevine breeding programs and other studies, the acquisition of phenology is usually performed directly in the vineyard, mainly by visual estimation. In order to acquire the time of bud burst, the BBCH scale is applied so that the person in charge estimates the BBCH stage for each genotype over a time period of at least two weeks. Phenotyping is thus strongly limited by time, cost, and the subjectivity of records. In the present study an efficient image based phenotyping method was developed and validated. Based on the sum of degree-day, image acquisition was carried out at only one single time point directly in the vineyard, and image analysis was conducted by using Matlab®. For each grapevine image a weighted length Lw (ratio of counted buds, number of shoots and average shoot length) was calculated. Lw was compared with reference evaluation data and significant correlations of r=-0.87 and r=0.76 were obtained. The range of Lw was used for classifying the trait ?time of bud burst? into an objective five-class system from very early to very late genotypes. The classification method was applied in order to rate the trait within a mapping population in comparison to traditional cultivars used as references. It was observed that the time of bud burst distributed into all five classes.

Introducing a sensor to measure budburst and its environmental drivers.

Budburst is a key adaptive trait that can help us understand how plants respond to a changing climate from the molecular to landscape scale. Despite this, acquisition of budburst data is constrained by a lack of information at the plant scale on the environmental stimuli associated with the release of bud dormancy. Additionally, to date, little effort has been devoted to phenotyping plants in natural populations due to the challenge of accounting for the effect of environmental variation. Nonetheless, natural selection operates on natural populations, and investigation of adaptive phenotypes in situ is warranted and can validate results from controlled laboratory experiments. To identify genomic effects on individual plant phenotypes in nature, environmental drivers must be concurrently measured, and characterized. Here, we designed and evaluated a sensor to meet these requirements for temperate woody plants. It was designed for use on a tree branch to measure the timing of budburst together with its key environmental drivers; temperature, and photoperiod. Specifically, we evaluated the sensor through independent corroboration with time-lapse photography and a suite of environmental sampling instruments. We also tested whether the presence of the device on a branch influenced the timing of budburst. Our results indicated the following: the temperatures measured by the budburst sensor’s digital thermometer closely approximated the temperatures measured using a thermocouple touching plant tissue; the photoperiod detector measured ambient light with the same accuracy as did time lapse photography; the budburst sensor accurately detected the timing of budburst; and the sensor itself did not influence the budburst timing of Populus clones. Among other potential applications, future use of the sensor may provide plant phenotyping at the landscape level for integration with landscape genomics.

Frost hardiness of tree species is independent of phenology and macroclimatic niche.

The differences in timing in bud burst between species have been interpreted as an adaptation to late frost events in spring. Thus, it has been suggested that the degree of frost susceptibility of leaves is species-specific and depends on the species' phenology and geographic distribution range. To test for relationships between frost tolerance and phenology as well as between frost tolerance and distribution range across Central European tree species, we studied the frost hardiness of closed buds before bud burst and of freshly opened buds at the time of bud burst. We hypothesized that species with early bud burst and species distributed in eastern and northern areas were more frost tolerant than species with late bud burst and species distributed in western and southern areas. Frost hardiness was estimated by exposing twigs to 11 frost temperatures between -4 °C and -80 °C and by assessing tissue damage by the electrolyte leakage method. In contrast to our hypotheses, neither frost hardiness of closed buds nor frost hardiness of freshly opened buds were related to any variable describing species' macroclimatic niche. Furthermore, frost hardiness of freshly opened buds did not differ among species. Thus, the investigated species with early bud burst take higher risks of frost damage than the species with late bud bursts. These findings indicate that frost hardiness might not play the key role in limiting the geographic distribution ranges previously anticipated.

Towards more ecologically realistic scenarios of plant uptake modelling for chemicals: PAHs in a small forest

The importance of plants in the accumulation of organic contaminants from air and soil was recognized to the point that even regulatory predictive approaches now include a vegetation compartment or sub-compartment. However, it has recently been shown that many of such approaches lack ecological realism to properly evaluate the dynamic of air/plant/soil exchange, especially when environmental conditions are subject to sudden variations of meteorological or ecological parameters. This paper focuses on the development of a fully dynamic scenario in which the variability of concentrations of selected chemicals in air and plant leaves was studied weekly and related to the corresponding meteorological and ecological parameters, to the evaluate their influence. To develop scenarios for modelling purposes, two different sampling campaigns were performed to measure temporal variability of: 1) polycyclic aromatic hydrocarbon (PAH) concentrations in air of a clearing and a forest site, as well as in leaves of two broadleaf species and 2) two important leaf and canopy traits, specific leaf area (SLA) and leaf area index (LAI). The aim was to evaluate in detail how the variability of meteorological and ecological parameters (SLA and LAI) can influence the uptake/release of organic contaminants by plants and therefore air concentrations. A principal component analysis demonstrated how both meteorological and ecological parameters jointly influence PAH air concentrations. SLA, LAI, as well as leaf density were showed to change over time and among species and to be directly proportional to leaf/canopy uptake rate. While hazelnut had the higher leaf uptake rate, maple became the most important species when considering the canopy uptake rate due to its higher LAI. Other species specific traits, such as the seasonal variation in production of new leaves and the timing of bud burst, were also shown to influence the uptake rate of PAHs by vegetation.

Within-stand variation in silver birch (Betula pendula Roth) phenology

Within a local population genotypes differ in the timing of bud burst, but genotypes with early bud burst unfold their leaves slower, resulting in an equal period of carbon gain. The ability of local populations to cope with disturbances like adverse weather events or a changing climate depends on the genotypic richness of such populations, emphasising the importance of differences between genotypes in traits related to growth and survival at this scale. Due to their longevity, these differences are of special importance in trees, yet for trees, differences between genotypes within local populations remain unexplored. The phenological cycle is important in this respect, since a correct timing of phenological events is critical for growth and survival of trees, especially in environments with strong seasonality and changes in the timing of phenological events has consequences for, among others, net ecosystem productivity and the climate system as a whole. In this light accounting for differences in the timing of phenological events within species is currently identified as a research challenge. This study contributes to the knowledge of differences between genotypes on the small spatial scale of a local population. We examined the timing of phenological events of 15 micropropagated silver birch (Betula pendula Roth) genotypes representing a natural population. Measurements covered bud burst (7 years) and leaf unfolding in spring and chlorophyll degradation in autumn (2 years for both). These data were used to estimate the period of carbon gain. Differences between genotypes in the temperature sum required for bud burst were present, with genotypes showing ‘early’ (i.e. a low temperature sum requirement for bud burst) and ‘late’ bud burst across the 7-year study period. Differences were small in most years (i.e. 3 days), but differences of 16 days were recorded within the 7-year study period as well. Genotypes with ‘early’ bud burst were less sensitive to variations in environmental conditions in spring compared to genotypes with ‘late’ bud burst. Differences in bud burst were not carried over to the estimated period of carbon gain. Due to faster leaf expansion in genotypes with ‘late’ bud burst and the lack of differences between genotypes in autumn senescence the estimated period of carbon gain was similar among genotypes.

Genetic diversity, population structure and phenotypic variation in European Salix viminalis L. (Salicaceae)

To investigate the potential of association genetics for willow breeding, Salix viminalis germplasm was assembled from UK and Swedish collections (comprising accessions from several European countries) and new samples collected from nature. A subset of the germplasm was planted at two sites (UK and Sweden), genotyped using 38 SSR markers and assessed for phenological and biomass traits. Population structure, genetic differentiation (F ST ) and quantitative trait differentiation (Q ST ) were investigated. The extent and patterns of trait adaptation were assessed by comparing F ST and Q ST parameters. Of the 505 genotyped diploid accessions, 27 % were not unique. Genetic diversity was high: 471 alleles was amplified; the mean number of alleles per locus was 13.46, mean observed heterozygosity was 0.55 and mean expected heterozygosity was 0.62. Bayesian clustering identified four subpopulations which generally corresponded to Western Russia, Western Europe, Eastern Europe and Sweden. All pairwise F ST values were highly significant (p < 0.001) with the greatest genetic differentiation detected between the Western Russian and the Western European subpopulations (F ST = 0.12), and the smallest between the Swedish and Eastern European populations (F ST = 0.04). The Swedish population also had the highest number of identical accessions, supporting the view that S. viminalis was introduced into this country and has been heavily influenced by humans. Q ST values were high for growth cessation and leaf senescence, and to some extent stem diameter, but low for bud burst time and shoot number. Overall negative clines between longitudinal coordinates and leaf senescence, bud burst and stem diameter were also found.

Tall Deciduous Shrubs Offset Delayed Start of Growing Season Through Rapid Leaf Development in the Alaskan Arctic Tundra

Increasing temperatures in arctic regions are causing earlier spring snowmelt, leading to earlier plant emergence, which could lengthen the period of carbon uptake. Warming is also leading to a shift from graminoid to deciduous shrub-dominated tundra, and in many areas deciduous shrubs are becoming taller. As taller shrubs become increasingly dominant, arctic landscapes may retain more snow, which could lengthen spring snow cover duration and offset advances in the start of the growing season that are expected as a result of earlier spring snowmelt. As a consequence, deeper snow and later snowmelt in taller shrub tundra could delay plant emergence and shorten the period of carbon uptake. This study tracked leaf development of two abundant deciduous shrubs, Betula nana and Salix pulchra, and compared individuals along a natural shrub height gradient on the North Slope of Alaska. We measured spring snow depth and snow cover duration, bud and developing leaf nitrogen content, as well as the timing of budburst and leaf expansion. Taller deciduous shrubs in shrub-dominated communities had deeper snow surrounding them, and became snow-free 1 to 6 days later, delaying budburst by 2 to 12 days relative to shorter deciduous shrubs in graminoid-dominated communities. However, leaf development of tall shrubs caught up to that of short shrubs; occasionally, tall shrubs reached full leaf expansion 1 to 4 days before short shrubs, indicating more rapid leaf development. This convergence in the timing of later leaf development stages is potentially enabled by approximately 16% to 25% greater nitrogen in buds and developing leaves of taller shrubs compared with shorter shrubs. Our findings suggest that delayed snowmelt in areas dominated by taller shrubs may have a short-lived impact on the timing of leaf development, likely resulting in no difference in duration of peak photosynthetic period between tall and short stature shrubs.

Sugars take a central position in plant growth, development and, stress responses. A focus on apical dominance.

Sugars take a central position in plant growth, development and, stress responses. A focus on apical dominance.

Evolutionary responses of tree phenology to the combined effects of assortative mating, gene flow and divergent selection.

The timing of bud burst (TBB) in temperate trees is a key adaptive trait, the expression of which is triggered by temperature gradients across the landscape. TBB is strongly correlated with flowering time and is therefore probably mediated by assortative mating. We derived theoretical predictions and realized numerical simulations of evolutionary changes in TBB in response to divergent selection and gene flow in a metapopulation. We showed that the combination of the environmental gradient of TBB and assortative mating creates contrasting genetic clines, depending on the direction of divergent selection. If divergent selection acts in the same direction as the environmental gradient (cogradient settings), genetic clines are established and inflated by assortative mating. Conversely, under divergent selection of the same strength but acting in the opposite direction (countergradient selection), genetic clines are slightly constrained. We explored the consequences of these dynamics for population maladaptation, by monitoring pollen swamping. Depending on the direction of divergent selection with respect to the environmental gradient, pollen filtering owing to assortative mating either facilitates or impedes adaptation in peripheral populations.

Process‐based models not always better than empirical models for simulating budburst of Norway spruce and birch in Europe

Budburst models have mainly been developed to capture the processes of individual trees, and vary in their complexity and plant physiological realism. We evaluated how well eleven models capture the variation in budburst of birch and Norway spruce in Germany, Austria, the United Kingdom and Finland. The comparison was based on the models performance in relation to their underlying physiological assumptions with four different calibration schemes. The models were not able to accurately simulate the timing of budburst. In general the models overestimated the temperature effect, thereby the timing of budburst was simulated too early in the United Kingdom and too late in Finland. Among the better performing models were three models based on the growing degree day concept, with or without day length or chilling, and an empirical model based on spring temperatures. These models were also the models least influenced by the calibration data. For birch the best calibration scheme was based on multiple sites in either Germany or Europe, and for Norway spruce the best scheme included multiple sites in Germany or cold years of all sites. Most model and calibration combinations indicated greater bias with higher spring temperatures, mostly simulating earlier than observed budburst.

Does the prediction of the time of egg hatch of Thaumetopoea processionea (Lepidoptera: Notodontidae) using a frost day/temperature sum model provide evidence of an increasing temporal mismatch between the time of egg hatch and that of budburst of Quercus robur due to recent global warming?

Thaumetopoea processionea is a serious defoliator of oak and of medical concern whose abundance has consistently in- creased throughout Europe during the past two decades. This study validates a previously published frost day/temperature sum model for predicting time of egg hatch of this species using five years of recent field data from South-West Germany. This model proved satisfactory for predicting the time of egg hatch of T. processionea. Hence, the model was used to retrospectively predict the time of egg hatch of T. processionea in the Karlsruhe area, which indicates that the time of egg hatch has fluctuated over the past 130 years. In the last two decades, however, predicted time of egg hatch is much earlier than the long-term average due to the increase in winter and early spring temperatures. Comparison of predicted time of egg hatch of T. processionea and long-term records of the time of foliation of its common host Quercus robur revealed that in the study area the temporal advance in the timing of both events was similar. This is not in accordance with recently published research on spring-feeding folivores, which report a diverging trend in the timing of egg hatch and budburst of their host plants as a consequence of human-induced climate change.

Internal development of vegetative buds of Norway spruce trees in relation to accumulated chilling and forcing temperatures.

The timing of budburst of temperate trees is known to be controlled by complicated interactions of temperature and photoperiod. To improve the phenological models of budburst, better knowledge of the internal bud development preceding budburst in relation to environmental cues is needed. We studied the effect of accumulated chilling and forcing temperatures on the internal development of vegetative buds preceding budburst in Norway spruce [Picea abies (L.) Karst.]. Branches from 17-year-old trees of southern Finnish origin were transferred eight times at 1- to 2-week intervals from October to December 2007 from the field at Punkaharju (61°48'N, 29°20'E) to the greenhouse with forcing conditions (day length 12 h, +20 °C). After seven different durations of forcing, the developmental phase and primordial shoot growth of the buds were analysed at the stereomicroscopic level. Air temperature was recorded hourly throughout the study period. The accumulated chilling unit sum had a significant effect on the temperature sum that was required to attain a certain developmental phase; a higher amount of chilling required a lower amount of forcing. The variation in the rate of development of different buds within each sample branch in relation to the chilling unit and forcing temperature sum was low. Regarding primordial shoot growth, there was also an inverse relation between accumulated chilling and forcing, i.e., a higher accumulated chilling unit sum before forcing required a lower temperature sum to initiate primordial shoot growth and resulted in a stronger effect of accumulated forcing. A second-order regression model with an interaction of chilling and forcing explained the variation of primordial shoot growth with high precision (R(2) = 0.88). However, further studies are required to determine the final parameter values to be used in phenological modelling.

Simulating local adaptation to climate of forest trees with a Physio‐Demo‐Genetics model

One challenge of evolutionary ecology is to predict the rate and mechanisms of population adaptation to environmental variations. The variations in most life history traits are shaped both by individual genotypic and by environmental variation. Forest trees exhibit high levels of genetic diversity, large population sizes, and gene flow, and they also show a high level of plasticity for life history traits. We developed a new Physio-Demo-Genetics model (denoted PDG) coupling (i) a physiological module simulating individual tree responses to the environment; (ii) a demographic module simulating tree survival, reproduction, and pollen and seed dispersal; and (iii) a quantitative genetics module controlling the heritability of key life history traits. We used this model to investigate the plastic and genetic components of the variations in the timing of budburst (TBB) along an elevational gradient of Fagus sylvatica (the European beech). We used a repeated 5 years climatic sequence to show that five generations of natural selection were sufficient to develop nonmonotonic genetic differentiation in the TBB along the local climatic gradient but also that plastic variation among different elevations and years was higher than genetic variation. PDG complements theoretical models and provides testable predictions to understand the adaptive potential of tree populations.

Ornamental Willow Growth Response Across Five Concentrations of Controlled-Release Fertilizer

Growth response of five ornamental willows (Salix), with sales potential for the cut-stem industry, was assessed in a 1-year container trial studying various concentrations of fertilizer. Plants were grown in 3-gal nursery containers fertilized with five concentrations of 18N–2.6P–6.6K controlled-release fertilizer (100-day release period) with micronutrients, applied as top dressings at 0, 10, 20, 40, and 60 g/container. Yield data were collected on the commercially important parameters including total stem length, stem quantity, and fresh weight of stems. Additional effects of fertilization on the timing of tip abscission and floral bud burst were also evaluated. Total stem length and fresh weight increased for all willows in the fertilized treatments compared with control; however, treatments above 40 g/container did not result in an increase of these parameters. Kori-yanagi willow (S. koriyanagi) had the highest yields across all treatments of fertilization. Fertilizer applications extended the period of stem elongation by delaying tip abscission for all willows, and for ‘The Hague’ willow (S. gracilistyla × S. caprea) tip abscission was delayed by 44.0 days at 40 g/container treatment compared with control. Floral bud burst dates, which differed greatly among willows, were unaffected by applications of controlled-release fertilizer.

Is the use of cuttings a good proxy to explore phenological responses of temperate forests in warming and photoperiod experiments?

For obvious practical reasons, tree phenological data obtained in warming and photoperiod experiments are generally conducted on juvenile trees (saplings and seedlings) or on watered or rooted cuttings collected from adult trees. As juvenile trees differ from adult trees in their phenological response to environmental conditions, they represent inappropriate plant material to experimentally assess the phenological responses of forests to seasonality. Cuttings are physiologically closer to adult trees, but cutting itself and the disruption of hormonal signals may create artefacts. This study aimed to investigate the potential deviation between phenological responses of cuttings vs donor trees. We hypothesized that, once dormant, buds may respond autonomously to environmental influences such as chilling, photoperiod and warming, and, thus, cuttings may exhibit similar phenological responses to mature trees. We compared bud development of seedlings, saplings and mature trees of three deciduous tree species with bud development of cuttings that were excised from both saplings and adults and positioned in situ in the vicinity of adult trees within a mature mixed forest in the foothills of the Swiss Jura Mountains. No significant difference was detected in the timing of bud burst between cuttings and donor trees for the three studied tree species when the vertical thermal profile was accounted for. However, a significant difference in the timing of flushing was found between seedlings, saplings and adults, with earlier flushing during the juvenile stage. At least for the three studied species, this study clearly demonstrates that cuttings are better surrogates than juvenile trees to assess potential phenological responses of temperate forests to climate change in warming and photoperiod experiments.