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Day length unlikely to constrain climate-driven shifts in leaf-out times of northern woody plants
Abstract
The relative roles of temperature and day length in driving spring leaf unfolding are known for few species, limiting our ability to predict phenology under climate warming. Using experimental data, we assess the importance of photoperiod as a leaf-out regulator in 173 woody species from throughout the Northern Hemisphere, and we also infer the influence of winter duration, temperature seasonality, and inter-annual temperature variability. We combine results from climate- and light-controlled chambers with species’ native climate niches inferred from georeferenced occurrences and range maps. Of the 173 species, only 35% relied on spring photoperiod as a leaf-out signal. Contrary to previous suggestions, these species come from lower latitudes, whereas species from high latitudes with long winters leafed out independent of photoperiod. The strong effect of species’ geographic–climatic history on phenological strategies complicates the prediction of community-wide phenological change.
Supplementary resource (1)
... Photoperiod can additionally modulate the forcing requirements of trees, with longer days reducing the time to leaf-out (Way & Montgomery, 2015;Zohner & Renner, 2015;Fu et al., 2019). Photoperiod limitation on spring leaf-out time is often more pronounced when buds receive insufficient chilling (Laube et al., 2014;Zohner et al., 2016). Despite a robust understanding of these overarching mechanisms that collectively determine leaf emergence in spring, it remains unclear whether, and how, the relative importance of each driver differs across broad spatial scales, which limits our capacity to predict regional variation in spring phenology. ...
... To address this gap, we conducted a full-factorial climate-manipulation experiment on Ginkgo biloba L., a deciduous dioecious tree species, across a wide environmental gradient from subtropical to temperate regions (ranging from 24°to 44°latitude). We tested three main scenarios for how temperature RSP shifts along temperature gradients ( Fig. 1): If chilling and/or photoperiod limitations increase linearly with temperature (Weinberger, 1950;Cannell & Smith, 1983;Zohner et al., 2016), RSP will linearly decrease along temperature gradients (Linear response scenario; Fig. 1a). If there is an upper threshold for chilling accumulation, RSP will decline once temperatures become too warm to induce chilling responses (One-sided response scenario; Fig. 1b). ...
... Each chamber was split into two parts using shade cloth, allowing us to apply two photoperiod treatments: daylengths of 10 and 14 h (Wu et al., 2022a). Two chilling treatments were applied by collecting twigs early (19 December 19; Low chilling) and late (1 March 2022; High chilling) in winter to cause different exposure of twigs to outdoor winter conditions (Zohner et al., 2016;Wang et al., 2022). This setup had 16 treatment combinations (2 chilling × 4 temperature × 2 photoperiod treatments). ...
Global warming is advancing the timing of spring leaf‐out in temperate and boreal plants, affecting biological interactions and global biogeochemical cycles. However, spatial variation in spring phenological responsiveness to climate change within species remains poorly understood.
Here, we investigated variation in the responsiveness of spring phenology to temperature (RSP; days to leaf‐out at a given temperature) in 2754 Ginkgo biloba twigs of trees distributed across subtropical and temperate regions in China from 24°N to 44°N.
We found a nonlinear effect of mean annual temperature on spatial variation in RSP, with the highest response rate at c . 12°C and lower response rates at warmer or colder temperatures due to declines in winter chilling accumulation. We then predicted the spatial maxima in RSP under current and future climate scenarios, and found that trees are currently most responsive in central China, which corresponds to the species' main distribution area. Under a high‐emission scenario, we predict a 4‐degree latitude shift in the responsiveness maximum toward higher latitudes over the rest of the century.
The identification of the nonlinear responsiveness of spring phenology to climate gradients and the spatial shifts in phenological responsiveness expected under climate change represent new mechanistic insights that can inform models of spring phenology and ecosystem functioning.
... Several studies have demonstrated that different functional groups of plants have different environmental triggers for bud break (i.e. the timing of bud unfolding and start of leaf emergence), with temperate-zone woody species responding mainly to air temperature (Laube et al., 2014;Thomas et al., 2003;Zohner et al., 2016;Zohner & Renner, 2014), while perennial herbs appear to respond primarily to soil temperature and snow depth (Jánosi et al., 2020). ...
... The main trigger for tree leaf-out is thought to be the accumulation of warm air temperatures (forcing), but tree phenology also responds to photoperiod and chilling (Basler & Korner, 2014;Laube et al., 2014;Zohner et al., 2016Zohner et al., , 2017Zohner & Renner, 2015), while spring-flowering herbs respond largely to soil temperature and snow depth (Jánosi et al., 2020;Pardee et al., 2019). However, the relationship between air temperatures, soil temperature, and snow depth is not straightforward because higher air temperatures are linked to decreased snow depth, and snow acts to insulate soil from temperature oscillations during winter. ...
... As discussed, reduced snow cover when the soil is still frozen could allow spring-flowering forest herbs to fulfil their chilling requirements and respond rapidly to forcing, perhaps explaining the stronger response of spring-flowering forest herbs at these locations. As for trees, their response to warming temperatures is mediated by interactions with chilling and photoperiod (Basler & Korner, 2014;Laube et al., 2014;Zohner et al., 2016;Zohner & Renner, 2015). In particular, the shorter day lengths in late winter may prevent leafing out in response to warmer temperatures, and this photoperiodic constraint may be particularly acute at high latitudes (Flynn & Wolkovich, 2018;Fu et al., 2012Fu et al., , 2015Fu et al., , 2019Zohner et al., 2017;Zohner & Renner, 2014. ...
The phenologies of co‐occurring trees and spring‐blooming understory herbs in northeastern North American hardwood forests appear to be regulated by different environmental drivers – air temperature and soil temperature/snowpack, respectively. Accordingly, it has been hypothesized that climate change–driven asymmetry in the advancement of canopy leaf‐out relative to the timing of understory growth could reduce photosynthetic rates and reproductive success of understory herbs through greater early‐season shading.
To determine whether trees and spring‐flowering forest herbs are advancing their phenologies at different rates with respect to increasing global temperatures, we examined the phenological responses to warming of 10 species of trees and 11 species of spring‐flowering forest herbs (8045 observations from 965 sites) in northeastern North America using 13 years of data collected by citizen scientists under the auspices of the USA‐National Phenology Network.
Contrary to expectation, the degree of advancement of leaf‐out as a function of temperature was greater in spring‐flowering forest herbs than in trees, with a mean response rate of −4.9 days/°C (95% BCI [−5.2, −4.6]) for spring‐flowering forest herbs vs. −3.3 days/°C (95% BCI [−3.5, −3.1]) for trees. However, the response to temperature was not consistent across the latitudinal range, with spring‐flowering forest herbs responding more strongly to warming than trees at middle (40–44°N) and higher (45–48°N) latitudes but not at lower latitudes (35–39°N).
Synthesis . In contrast to previous suggestions, our study shows spring‐flowering forest herbs advancing their phenology at a higher rate than trees with respect to warming through most of the latitudinal range investigated, which could translate into a longer growing season and increased carbon uptake for spring‐flowering forest herbs as spring temperatures rise.
... Recent evidence, though, suggests that the sensitivity of spring phenology to warming is decreasing in northern forests 15 and that the rate of change in plant productivity does not match that of air temperature 16 . Indeed, plant phenology may be acclimated to long-term biogeographical constraints [17][18][19] and may be co-limited by several other factors, such as light 20 , water [21][22][23] and nutrients 24 . These observations suggests that warming does not have the same effect everywhere 25 , which has increased interest in other environmental drivers in recent decades, especially illustrated by multiple debates about the specific role of light (and photoperiodism) in spring phenology 20,[26][27][28][29][30][31][32][33] . ...
... Indeed, plant phenology may be acclimated to long-term biogeographical constraints [17][18][19] and may be co-limited by several other factors, such as light 20 , water [21][22][23] and nutrients 24 . These observations suggests that warming does not have the same effect everywhere 25 , which has increased interest in other environmental drivers in recent decades, especially illustrated by multiple debates about the specific role of light (and photoperiodism) in spring phenology 20,[26][27][28][29][30][31][32][33] . ...
... The quantity and quality of light depend on plant location, which is the main reason why a response to daylength has often been proposed as a safety mechanism against frost at high latitudes and elevations. Only 35% of the woody species in the Northern Hemisphere, however, depend on daylength as a direct signal for leaf-out 20 , and these species are mainly at mid-to low latitudes. ...
Spring phenology is mainly driven by temperature in extratropical ecosystems. Recent evidence highlighted the key role of micrometeorology and bud temperature on delaying or advancing leaf unfolding. Yet, phenology studies, either using ground-based or remote sensing observations, always substitute plant tissue temperature by air temperature. In fact, temperatures differ substantially between plant tissues and the air because plants absorb and lose energy. Here, we build on recent observations and well-established energy balance theories to discuss how solar radiation, wind and bud traits might affect our interpretation of spring phenology sensitivity to warming. We show that air temperature might be an imprecise and biased predictor of bud temperature. Better characterizing the plants’ phenological response to warming will require new observations of bud traits and temperature for accurately quantifying their energy budget. As consistent micrometeorology datasets are still scarce, new approaches coupling energy budget modelling and plant traits could help to improve phenology analyses across scales. Phenology studies tend to use air temperature instead of plant tissue temperature. This study provides evidence that air and plant temperatures differ to such an extent as to make us reconsider our current interpretation of phenology.
... In recent years, many scholars have also conducted research on the effect of low temperatures on breaking the dormancy of deciduous fruit trees. Zohner et al. (2016) Horticulturae 2023, 9, 628 2 of 9 believed that temperature mainly controls the duration of dormancy; only a small number of woody species are sensitive to photoperiod [11]. According to the recent work of Li et al. (2020), regardless of the photoperiodic conditions, low temperature can induce growth cessation and control dormancy induction during artificial low-temperature induction of Chimonanthus praecox [12]. ...
... In recent years, many scholars have also conducted research on the effect of low temperatures on breaking the dormancy of deciduous fruit trees. Zohner et al. (2016) Horticulturae 2023, 9, 628 2 of 9 believed that temperature mainly controls the duration of dormancy; only a small number of woody species are sensitive to photoperiod [11]. According to the recent work of Li et al. (2020), regardless of the photoperiodic conditions, low temperature can induce growth cessation and control dormancy induction during artificial low-temperature induction of Chimonanthus praecox [12]. ...
Low-temperature accumulation is one of the essential stages in the growth process of woody ornamental plants. In this study, two different low-temperature treatments, 6 °C and 10 °C, were used to analyze the effects of different low-temperature treatments on dormancy release and flowering of the ‘Gulihong’ plant using artificial low temperatures. Based on the experimental results, four typical early-blooming Prunus mume cultivars widely planted in Yangling area of Henan Province, China, including ‘Zaoyudie’, ‘Zaohualve’, ‘Nanjing gongfen’, and ‘Gulihong’, were selected as the experimental materials. The effects of low-temperature accumulation on the flowering characteristics of different cultivars were analyzed using a 6 °C artificial low-temperature treatment. The suitable cultivation temperature for early-blooming cultivars was screened to provide a theoretical basis for further exploration of P. mume bonsai cultivation techniques. The results showed that the flowering rate, flower diameter, flowering quantity, flowering uniformity, and bud development in the 6 °C treatment were significantly better than those in the 10 °C treatment. Furthermore, under 6 °C low-temperature treatment, the flowering rate and quality of different cultivars showed an increasing trend with the accumulation of low temperature, with ‘Gulihong’ exhibiting the highest flowering rate. Therefore, chill accumulation plays a significant role in promoting flowering quality.
... In temperate ecosystems, plant phenological events are found to be sensitive to environmental factors such as photoperiod, temperature, and winter chilling [15]. For example, temperature and day length together affect tree leafing pattern [16], spring temperature (forcing temperature) and late frost affect rate of bud burst [15] and spring temperature variability affects the phenological patterns of the plant [17]. ...
... In temperate ecosystems, plant phenological events are found to be sensitive to environmental factors such as photoperiod, temperature, and winter chilling [15]. For example, temperature and day length together affect tree leafing pattern [16], spring temperature (forcing temperature) and late frost affect rate of bud burst [15] and spring temperature variability affects the phenological patterns of the plant [17]. Thus, changes in environmental factors are critical in determining the response of tree phenological events such as the onset, peak, and end of the phenological events as well as their durations [18]. ...
Phenology, an important ecological attribute, deals with the development of vegetative and reproductive parts of trees called "phenophases", which are important determinants of primary productivity and sensitive to climate change. The present study recorded various phenophases of major tree species (i.e., Quercus leucotrichophora, Rhododendron arboreum, and Myrica esculenta) as per the two-digit numerical system of Biologische Bundesanstalt, Bundessortenamt, Chemische Industrie (BBCH) scale. A total of 72 individual trees, twenty-four from each species, distributed between 1400 and 1980 m. a.s.l elevations were tagged and measured fortnightly for two consecutive years (2019-2021) in the moist temperate forest of Western Himalaya and compared with earlier existing records. Various phenophases were correlated with climatic factors along with duration and thermal time for each phenological growth stage. We found 24 growth stages for Q. leucotrichophora and M. esculenta and 28 for R. arboreum distributed across seven principal growth stages (e.g. bud development, 0; leaf development, 1; shoot development, 3; inflorescence development, 5; flower development, 6; fruit development, 7; and fruit maturation, 8) of trees as per BBCH scale. Maximum growing degree was 748.87 and 627.95 days recorded for R. arboreum and M. esculenta during leaf development, and 796.17 days for Q. leucotrichophora during fruit development. Flower emergence was observed pre, during, and post-emergence of new leaves for R. arboreum, M. esculenta, and Q. leucotrichophora, respectively, which varied at spatial scale with previous findings. Longevity of fruit development to ripening took 17, 4, and 2 months, respectively in Q. leucotrichophora, R. arboreum and M. esculenta. Duration of leaf initiation and flowering was positively correlated with climatic variables, whereas, the reverse was observed for fruiting in the studied tree species. The study concludes that the variations in phenophases of the three species were strongly influenced by climatic variations, especially minimum temperature. The result of the present study would be important in enabling us to formulate efficient forest management strategies by understanding the short-term adaptation of the climate-sensitive important tree species in the western Himalaya.
... Many studies have confirmed this [2,6,[21][22][23]. Photoperiodic monitoring and its interaction with temperature [24] also have a significant influence on the growing time of some genotypes, which may account for about 30% of plant species [25]. ...
... According to the trends observed, for the scenarios RCP2.6 and RCP4.5 in the middle of the 21st century, the culture will bloom, on average, 4-5 days earlier (23)(24)(25), and by the end of the century, 7-9 days earlier (18)(19)(20)(21). Based on the analysis of two climate scenarios, it can be seen that the expected temperature changes will not have a strong impact on the average dates of flowering in the apricot crop. ...
This study presents the results of the development of numerical models for predicting the timing of apricot flowering, including using experimental data on the emergence of plants from a state of deep dormancy. The best results of approximation of the process of accumulation of the necessary cooling in the autumn–winter period were obtained using the sigmoidal function. Models that take into account the combined effect of temperature and photoperiod on the processes of spring development showed a high accuracy of the process of accumulation of thermal units. Based on the results of testing, two models were selected with an accuracy of 3.0 days for the start of flowering and the absence of a systematic bias, which can be considered a good quality assessment These models describe well the interannual variability of apricot flowering dates and can be used to predict these dates. The discrepancy is no more than 2–4 days in 87–89% of cases. Estimates of the timing of flowering and the end of deep dormancy are very important for increasing the profitability of fruit production in the South of Russia without incurring additional costs, by minimizing the risks associated with irrational crop placement and the selection of varieties without taking into account the specifics of climate change. When constructing a system of protective measures and dates of treatments, it is also necessary to take into account the calendar dates of the shift in the development of plants.
... Hence, photoperiodic sensitive species are likely to be more constraint in their adaptation to rising spring temperatures compared to photoperiodic insensitive species in order to benefit from a longer favorable window for their development. However, the photoperiodic sensitivity of species is difficult to quantify and seems to be more prevalent for species growing in ecosystems with shorter winters (Zohner et al., 2016(Zohner et al., , 2017Geng et al., 2022) 2). Consequently, further warming, could result in contrasting effects within and between ecosystems depending on species specific chilling, forcing and photoperiod requirements and the ability to compensate deficient drivers, which might also change the susceptibility of late-spring frost damages in a given ecosystem. ...
... An important future contribution to the field would be to examine species of the Fagaceae family, which includes the genera oak, beech and chestnut that have colonized large parts of the northern hemisphere. Combined with genetic analyses, it would help to understand how species have developed temperature and photoperiod sensitivity to avoid damaging spring frosts once they colonizing new areas (Zohner et al., 2016;Wu et al., 2022b). ...
Winter chilling, spring forcing temperature and photoperiod are the most important drivers explaining the spatial and temporal variability of spring phenology in temperate trees. However, how these factors interact with each other on dormancy release and spring budburst date remains unclear and varies greatly depending on species. Our knowledge is also limited as to whether heat accumulation of forcing temperatures that trigger bud break in spring is a linear or non-linear process. Here, we aimed at experimentally quantifying the effect of chilling, forcing, photoperiod and their interactions on the budburst dates of nine different temperate tree species from East Asia (near Beijing, China) and Central Europe (near Zurich, Switzerland), including six phylogenetically related species (same genus). We conducted a full factorial experiment in climate chambers using two chilling (low and high, i.e., 0 vs. 56 days at 2°C after sampling at the end of December), four forcing (5, 10, 15, and 20°C), and two photoperiod (8 vs. 16 h) treatments simultaneously in Beijing and Zurich. We found that species growing near Beijing responded more readily to forcing conditions than species of the same genus growing near Zurich regardless of chilling treatment. Budburst timing of most species but European beech was marginally, if at all, affected by photoperiod. Furthermore, our results suggest that linear heat accumulation, as commonly used with the growing degree hours (GDH) model, could result in accurate prediction of budburst date depending on the temperature threshold used as a basis for heat accumulation. Our results also demonstrate the important role of chilling in shaping the sensitivity and rate of forcing accumulation to trigger budburst and suggest that species-specific sigmoid relationship for accumulating heat that accounts for prior chilling exposure may yield better predictions of budburst dates. Our results suggest that deciduous trees may have adapted their chilling and forcing requirements in regards to the predictability of winter-spring transition and late spring frosts. A less predictable winter-spring transition, as observed in Central Europe, could have driven species evolution towards higher chilling and forcing requirements compared to species growing in a more predictable climate of Northeastern Asia. Our cross-continental experiment therefore suggests that the spring phenology of East Asian species is tighter coupled to spring forcing temperature than Central European forests.
... of temperate trees were constrained by day length (Rossi, 2015;Zohner et al., 2016). Our results illustrated how the environmental factors interact in space and result in the divergent advancing rates of forest spring phenology , thus providing a new perspective for understanding the potential trajectories of forest growth dynamics under global changes. ...
... (Basler & Körner, 2012;Richardson et al., 2018;Zohner et al., 2016). The importance of the photoperiod was relatively low compared with forcing accumulation, in line with other studies showing that only a minor group (mainly from lower latitudes)F I G U R E 3 (a) Geographical distributions of global conifer cover (data from Global Forest Age Dataset (GFAD) ...
Despite growing interest in predicting plant phenological shifts, advanced spring phenology by global climate change remains debated. Evidence documenting either small or large advancement of spring phenology to rising temperature over the spatio-temporal scales implies a potential existence of a thermal threshold in the responses of forests to global warming. We collected a unique dataset of xylem cell-wall-thickening onset dates in 20 coniferous species covering a broad mean annual temperature (MAT) gradient (-3.05 to 22.9°C) across the Northern Hemisphere (latitudes 23-66°N). Along the MAT gradient, we identified a threshold temperature (using segmented regression) of 4.9±1.1°C, above which the response of xylem phenology to rising temperatures significantly decline. This threshold separates the Northern Hemisphere conifers into cold and warm thermal niches, with MAT and spring forcing being the primary drivers for the onset dates (estimated by linear and Bayesian mixed-effect models), respectively. The identified thermal threshold should be integrated into the Earth-System-Models for a better understanding of spring phenology in response to global warming and an improved prediction of global climate-carbon feedbacks.
... However, there is also increasing evidence for an independent role of photoperiod in regulating the endodormancy release and leaf-out in many temperate (Zohner and Renner, 2015;Singh et al., 2016;Fu et al., 2019a;Meng et al., 2021) and subtropical (Zhang et al., 2021b) tree species. In most boreal trees, leaf-out seems to show little sensitivity to photoperiod (Zohner et al., 2016;Richardson et al., 2018). ...
... The twigs were detached with scissors from the trees and disinfected with a hypochlorite solution (200 ppm active chlorine). The cut end of each twig was then cut once more in tap water and put in test tubes (3 cm in diameter and 20 cm in height), one twig per tube, with 40 μg L − 1 of the broad-spectrum antibiotic gentamicin sulfate added (Zohner et al., 2016). ...
Climatic warming is currently changing the spring phenology of extratropical trees, and this has several important effects on the trees and ecosystems. The major climatic cues regulating the spring phenology are winter chilling, spring forcing, and photoperiod. The interactions between these three remain largely unstudied because most studies concentrate on the effects of one cue, or maximally two, at a time. We studied the effects and interactions of chilling duration, forcing temperature, and forcing photoperiod simultaneously in four subtropical tree species. The main emphasis in our experiments was on the interaction of chilling duration and forcing temperature. The existence of this interaction was suggested in the ‘Vegis theory’, put forward decades ago but largely forgotten since. We also introduced a novel method for testing the theory experimentally. We found support for the Vegis theory in two of the four species examined. In the other two species the leaf-out timing was largely controlled by spring forcing. The effects of photoperiod were generally minor. Our results show that there are major differences between sympatric subtropical tree species in their phenological responses to environmental cues. These differences need to be addressed in the development of process-based tree phenology models. Our results further suggest that different subtropical trees respond differently to climatic warming because of differences related to the Vegis theory. This hypothesis remains to be tested in further studies.
... In addition to phylogeny, plant phenology is strongly influenced by native climate (i.e., the climate in native range of species) of plant species. Several studies have elucidated the patterns and underlying mechanisms of adaptation to native climate of plant species in different regions (Zohner and Renner, 2014;Zohner et al., 2016). It has been demonstrated that species originating from higher latitudes leaf out earlier than contemporaries from lower latitudes under the same conditions (Zohner and Renner, 2014;Zohner et al., 2016). ...
... Several studies have elucidated the patterns and underlying mechanisms of adaptation to native climate of plant species in different regions (Zohner and Renner, 2014;Zohner et al., 2016). It has been demonstrated that species originating from higher latitudes leaf out earlier than contemporaries from lower latitudes under the same conditions (Zohner and Renner, 2014;Zohner et al., 2016). Unfortunately, only a few studies have attempted to quantify the relative contributions of phylogeny and native climate in determining the phenological traits among plant species. ...
The effects of climate change on plant phenology have been widely recognized around the world. However, the effect of plant internal factors (such as phylogeny) on the variations in phenology among plant species remains unclear. In this study, we investigated the phylogenetic conservatism in spring phenological traits using phylogenetic signal and evolutionary models, including Brownian motion (BM) model, Ornstein–Uhlenbeck (OU) model and white noise (WN) model, based on the phenological data of 48 temperate plant species in Northeast China. We also explored the relative contributions of phylogeny and adaptation to native climate (i.e., the climate in native range of species) to the variations in the phenological traits among species using phylogenetic eigenvector regression and variance partitioning analysis. The results showed thatspring phenological traits conformed to the OU model, indicating thatspring traits were phylogenetically conserved. The effect of phylogeny on flowering traits was stronger than that on leaf-out traits. Additionally, the adaptation to native climate contributed more to the variations in spring phenological traits among species than phylogeny, and adaptation to native climate explained more variations in leaf-out traits than in flowering traits. Our results suggested that the spring phenological traits were constrained by both phylogeny and adaptation to native climate. However, the adaptation to native climate had a stronger effect on the variations in phenological traits than phylogeny. Therefore, the degree of similarity in spring phenological traits across closely related species depends on the degree of similarity in the environmental conditions where these close relatives are distributed.
... These findings indicate stronger photoperiodic control in areas where daylength at D LCO is longer (i.e., shorter nights), possibly because plants respond to the duration of uninterrupted darkness rather than daylength (Borthwick & Hendricks, 1960;Hamner, 1940;Howe et al., 1995;Paus et al., 1986). Interestingly, for vegetation with a daylength at D LCO of >13.5 h, D LCO was more positively correlated with pre-D LCO T min in colder areas (Figure 5d-f), indicating a stronger effect of temperature in areas with harsh temperature conditions, consistent with experimental studies (Ford et al., 2017;Zohner et al., 2016). Therefore, although for these types of vegetation the correlation between D LCO and temperature is weak, probably because of stronger photoperiodic control, there is still a signal of temperature influence on D LCO , reflecting a stronger selection pressure in harsher temperature environments. ...
... tween D LCO and T min and in temporal changes in D LCO against the spatial gradient of daylength to explore the dependence of D LCO on daylength. Meanwhile, the spatial variations in the response of autumn leaf phenology to temperature might be associated with local background temperature conditions(Ford et al., 2017;Zohner et al., 2016). Hence, the spatial variations in background temperature should be minimized when assessing the dependence of D LCO on daylength. ...
Aim
Initiation of autumnal leaf senescence is crucial for plant overwintering and ecosystem dynamics. Previous studies have focused on the advanced stages of autumnal leaf senescence and reported that climatic warming delayed senescence, despite the fundamental differences among the stages of senescence. However, the timing of onset of leaf coloration ( D LCO ), the earliest visual sign of senescence, has rarely been studied. Here, we assessed the response of D LCO to temperature.
Location
30–75° N in the Northern Hemisphere.
Time period
2000–2018.
Major taxa studied
Deciduous vegetation.
Methods
We retrieved D LCO from high‐temporal‐resolution satellite data, which were then validated by PhenoCam observations. We investigated the temporal changes in D LCO and the relationship between D LCO and temperature by using satellite and ground observations.
Results
D LCO was not significantly ( p > .05) delayed between 2000 and 2018 in 94% of the area. D LCO was positively ( p < .05) correlated with pre‐ D LCO mean daily minimum temperature ( T min ) in only 9% of the area, whereas the end of leaf coloration ( D LCE ) was positively correlated with pre‐ D LCE mean T min over a larger area (34%). Further analyses showed that warming slowed the progress of leaf coloration. Interestingly, D LCO was less responsive to pre‐ D LCO mean T min in areas where daylength was longer across the Northern Hemisphere, particularly for woody vegetation.
Main conclusions
The rate of progress of coloration is more sensitive to temperature than its start date, resulting in an extension of the duration of leaf senescence under warming. The dependence of D LCO response to temperature on daylength indicates stronger photoperiodic control on initiation of leaf senescence in areas with longer daylength (i.e., shorter nights), possibly because plants respond to the length of uninterrupted darkness rather than daylength. This study indicates that the onset of leaf coloration was not responsive to climate warming and provides observational evidence of photoperiod control of autumnal leaf senescence at biome and continental scales.
... The effect of photoperiod on the leaf-out date is hard to be detected in observational data, because forcing and photoperiod are inherently correlated in spring (Elmendorf & Ettinger, 2020;Wolkovich et al., 2021). A controlled experiment showed that only 2% of the 173 species are photoperiod-sensitive in high chilling conditions (Zohner et al., 2016). Thus, this study mainly focused on the effects of chilling and forcing on the leaf-out date, but only quantified the effect of photoperiod for Fagus sylvatica, a species known to be highly sensitive to photoperiod (Basler & Körner, 2012;Zohner & Renner, 2015). ...
... Besides forcing and chilling, photoperiod has been reported to be a notable factor affecting spring phenology (Way & Montgomery, 2015), although only 35% of species relied on spring photoperiod as a leafout signal in low chilling conditions (Zohner et al., 2016). We selected F. sylvatica, a well-known photoperiod-sensitive species (Basler & Körner, 2012;Zohner & Renner, 2015), to investigate the relative contribution of chilling and photoperiod on phenological change. ...
Winter temperature‐related chilling and spring temperature‐related forcing are two major environmental cues shaping the leaf‐out date of temperate species. To what degree insufficient chilling caused by winter warming would slow phenological responses to spring warming remains unclear. Using 27,071 time series of leaf‐out dates for 16 tree species in Europe, we constructed a phenological model based on the linear or exponential function between the chilling accumulation (CA) and forcing requirements (FR) of leaf‐out. We further used the phenological model to quantify the relative contributions of chilling and forcing on past and future spring phenological change. The results showed that the delaying effect of decreased chilling on the leaf‐out date was prevalent in natural conditions, as more than 99% of time series exhibited a negative relationship between CA and FR. The reduction in chilling linked to winter warming from 1951‐2014 could offset about one half of the spring phenological advance caused by the increase in forcing. In future warming scenarios, if the same model is used and a linear, stable correlation between CA and FR is assumed, declining chilling will continuously offset the advance of leaf‐out to a similar degree. Our study stresses the importance of assessing the antagonistic effects of winter and spring warming on leaf‐out phenology.
... Thus the major difference between the endo-and ecodormant bud is related to the competence to grow, which is lacking in endodormant but present in ecodormant buds. As a rule, the growth-arresting conditions are removed by prolonged exposure to low chilling temperatures, although other drivers, most importantly photoperiod, may also have an effect (Basler and Körner, 2012;Cooke et al., 2012;Vitasse and Basler, 2013;Singh et al., 2017; but see also Zohner et al., 2016). ...
In autumn, the buds of extratropical trees are in a state of endodormancy, since regardless of the prevailing environmental conditions, growth cannot be activated in these buds because the dormancy is caused by physiological factors in the buds. In natural conditions the growth-arresting physiological factors are removed by prolonged exposure to low chilling temperatures. This phenomenon is a key adaptive trait, for it prevents ‘false spring’, i.e., untimely bud burst during mild spells in autumn and winter, which would lead to cold damage during subsequent cold periods. Traditionally, endodormancy and the chilling requirement have been important in practical horticulture, as cultivars with low and high chilling requirements have been bred for locations in warm and cool climates, respectively. More recently, endodormancy and the chilling requirement have become major research themes in climate change studies where climatic change impacts are assessed by means of process-based tree phenology models. The dormancy phenomenon has been studied thoroughly at the whole-tree level for a hundred years, and several genes and genetic pathways involved have recently been identified in tree species such as hybrid aspen, apple, and pear. There is an urgent need, however, to integrate molecular physiological studies with modelling studies so as to understand the impact of climate change on the regulation of dormancy. To that end, we shall provide an overview of bud endodormancy research.
... The timing of bud burst in woody species is more genetically controlled than the timing of leaf senescence and is wellknown to react to temperature (Zohner et al., 2016). The environmental drivers for the timing of autumnal leaf senescence in woody species are not that clear (Delpierre et al., 2009;Gallinat et al., 2015), and most studies have focused on economically important species, neglecting less known shrub species. ...
... Interest in the influence of photoperiod on spring phenology is increasing (Körner and Basler, 2010). However, critical photoperiods have not been found, other than weak and variable compensation of insufficient chilling effects by longer photoperiod (Körner and Basler, 2010;Way and Montgomery, 2015;Zohner et al., 2016). The photoperiod effects reported in the literature are often concluded from growth timing differences, with differences in forcing temperatures ignored (Chu et al., 2021). ...
... The photoperiod may play a role in explaining divergent phenological shifts between trees and shrubs because different species have specific adaptations to the photoperiod [ 38 ]. However, experimental and observational evidence has revealed that trees tend to rely on temperature (spring warming and winter chi l ling) in regions with long and cold winters, whereas the photoperiod mainly regulates spring phenology in species growing at lower latitudes [ 39 ]. The divergent phenological response to warming between trees and shrubs therefore could be largely induced by different effects of chi l ling accumulation on the heat requirement for cambial reactivation between two woody species. ...
Despite the importance of species interactions in modulating plant range shifts, little is known on the responses of coexisting life forms to a warmer climate. Here, we combine a long-term monitoring of cambial phenology in sympatric trees and shrubs at two treelines of the Tibetan Plateau, with a meta-analysis of ring-width series from 344 shrubs and 575 trees paired across 11 alpine treelines in the Northern Hemisphere. Under a spring warming of +1°C, xylem resumption advances by 2-4 days in trees, but delays by 3-8 days in shrubs. The divergent phenological response to warming was due to shrubs being 3.2 times more sensitive than trees to chilling accumulation. Warmer winters increased thermal requirement for cambial reactivation in shrubs, leading to a delayed response to warmer springs. Our meta-analysis confirmed such a mechanism across continental scales. The warming-induced phenological mismatch may give a competitive advantage to trees over shrubs, which provide a new interpretation to explain further alpine treeline shifts under the context of climate change.
... SEQ was developed because the temperature effect on spring phenology could be further divided into winter chilling and spring forcing (Cannell and Smith, 1983;Hänninen et al., 2019;Körner and Basler, 2010), which are respectively connected to endodormancy and ecodormancy periods (Chuine et al., 2016). Meanwhile, daylength (or photoperiod), a proxy of accumulated sunlight over the full day and showing direct link with the plant's active growth rates once leaf onset occurs, is another important environmental trigger for spring phenology (Meng et al., 2021b;Way and Montgomery, 2015;Zohner et al., 2016). Based on these, SEQ was proposed, in which both dormancy periods (endodormancy and ecodormancy) were considered, respectively captured by chilling and forcing, along with subsequent active growth period, captured by daylength. ...
Spring phenology of temperate ecosystems is highly sensitive to climate change, generating various impacts on many important terrestrial surface biophysical processes. Although various prognostic models relying on environmental variables of temperature and photoperiod have been developed for spring phenology, comprehensive ecosystem-scale evaluations over large landscapes and long-time periods remain lacking. Further, environmental variables other than temperature and photoperiod might also importantly constrain spring phenology modelling but remain under-investigation. To address these issues, we leveraged around 20-years datasets of environmental variables (from Daymet and GLDAS products) and the spring phenology metric (i.e., the greenup date) respectively derived from MODIS and PhenoCams across 108 sites in the Northern and Eastern United States. We firstly cross-compared MODIS-derived greenup date with official PhenoCams product with high accuracy (R2 = 0.70). Then, we evaluated the three prognostic models (i.e., Growing Degree Date (GDD), Sequential (SEQ) and optimality-based (OPT)) with MODIS-derived spring phenology, assessed the model residuals and their associations with soil moisture, rainfall, and solar radiation, and revised the two photoperiod-relevant models (SEQ, OPT) by replacing the daylength variable with solar radiation, which was found to contribute the most to model residuals. We found that 1) all models demonstrated good capability in characterizing spring phenology, with OPT performing the best (RMSE = 8.04 ± 5.05 days), followed by SEQ (RMSE = 10.57 ± 7.77 days) and GDD (RMSE = 10.84 ± 8.42 days), 2) all models displayed high model residuals showing tight correlation with solar radiation (r = 0.45-0.75), and 3) the revised models that included solar radiation significantly performed better with an RMSE reduction by 22.08%. Such results are likely because solar radiation better constrains early growing season plant photosynthesis than photoperiod, supporting the hypothesis of spring phenology as an adaptive strategy to maximize photosynthetic carbon gain (approximated by solar radiation) while minimizing frost damage risk (captured by temperature). Collectively, our study reveals the underappreciated importance of solar radiation in constraining spring phenology of temperate ecosystems, and suggests ways to improve spring phenology modelling and other phenology-related ecological processes.
... Delay or advancement of one phenological event usually leads to delay or advancement in the successive events (Fu et al., 2014;Keenan & Richardson, 2015). However, increasing evidence suggests a complex interconnection between spring and autumn phenology depending on the difference in hydroclimatic conditions and the intertwined seasonal biophysical feedbacks (Fu et al., 2018;Keenan & Richardson, 2015;Liu et al., 2016;Zohner et al., 2016). A variety of hypotheses have been proposed to explain the carryover effects of spring phenology on autumn phenology, including: (1) the biophysical feedbacks of variations in spring phenology could alter the hydrothermal conditions during the growing season and affect the autumn phenology (Lian et al., 2021;Piao et al., 2019); and (2) the close interconnection between spring and autumn phenology could be regulated by the seasonal cycle in non-structural carbohydrates, and these links might be hydroclimate dependent (Fu et al., 2014;Zani et al., 2020). ...
Aims
Shifts in xylem phenology directly determine the forest capacity for carbon sequestration. However, a systematic understanding of the spatial patterns and the underpinning drivers in determining the cessation of wood formation ( C cw ) is lacking at a pan‐continental scale. Here, we addressed this knowledge gap by compiling a new dataset of multiple xylem phenology timings for northern conifers.
Locations
Sixty‐two study sites, Northern Hemisphere (25–55° N).
Time period
2003–2018 (16 years).
Taxa
Thirty‐three conifer species.
Methods
A generalized additive model was fitted to characterize the latitudinal pattern in C cw . Structural equation modelling and a linear mixed‐effects model were applied to determine the main drivers underlying the latitudinal pattern in C cw .
Results
The C cw followed a flat S‐shaped pattern with increasing latitude. Photoperiod was the dominant determinant of the latitudinal pattern of C cw , and a longer photoperiod was associated with an earlier C cw . Both mean growing‐season temperature and total growing‐season precipitation exhibited significantly positive relationships to the cessation of cell elongation and thus the C cw across all study sites. In arid regions, the pre‐growing‐season temperature had a significantly negative effect on C cw . In humid regions, C cw was positively affected by the mean growing‐season temperature. The onset of wood formation showed significantly positive coupling with C cw at arid sites but not at humid sites. Early successional species were sensitive to hydrothermal variations during the pre‐growing season.
Main conclusions
We reveal the dominant role of photoperiod in determining the cessation of wood formation for northern conifers and highlight differentiated interactive effects between photoperiod and seasonal climatic factors and the preceding xylem phenophases in determining C cw among ecoregions and tree species. These insights provide evidence to reduce uncertainty in prediction of the forest carbon uptake potential and the consequent biophysical feedbacks of northern forests.
... Apart from phylogeny, native climate, i.e., the climate in the native range of species, also affects plant phenology. Numerous studies have shown that species originating from higher latitudes leaf out earlier than species from lower latitudes when growing under identical conditions (Zohner and Renner, 2014;Zohner et al., 2016;Desnoues et al., 2017). However, it remains to be tested whether phylogeny affects autumn phenology and the relative importance of phylogeny and native climate on autumn phenology across species needs further investigation. ...
Both biotic and abiotic factors restrict changes in autumn phenology, yet their effects remain ambiguous, which hinders the accurate prediction of phenology under future climate change. In this study, based on the phenological records of 135 tree species at ten sites in China during 1979–2018, we first investigated the effects of climatic factors (temperature, precipitation, insolation and wind speed) and spring phenology on interannual changes in leaf coloring date (LCD) with the partial correlation analysis, and assessed the relative importance of phylogeny and native climate to LCD differences among species by using multivariate regression and phylogenetic eigenvector regression approach. The results showed that the effects of climate factors on interannual changes in LCD were more significant than spring phenology. In general, temperature played a more important role in cold regions (e.g. the northeast region), while the control of insolation on LCD was stronger in the warmer and wetter regions (e.g. the north, east and southwest regions). In addition, the effects of precipitation and wind speed were more evident in arid regions (e.g. the northwest region). We also found considerable effects of both native climate and phylogeny on the LCD differences among species, despite the contribution of native climate being almost 2~5 times greater than that of the phylogeny. Our findings confirmed and quantified the combined effects of climate, spring phenology and phylogeny on the autumn phenology of plants, which could help better understand the driving factors and influencing mechanism of plant phenology and provide a reference for the calibration and optimization of phenological models.
... The effectiveness of the calibration method to reduce the geographic biases and errors of predictions further validated the conceptual hypothesis of varied forcing requirements of populations that are proportional to local climatic conditions (Liang 2016). This primarily thermal forcing-based hypothesis may be refined in future work by including gradient variations in additional environmental drivers, such as reduced chilling (Perry & Wu 1960, McGee 1974 and increased photoperiod effect (Zohner et al. 2016) towards warmer climates. ...
Phenological models are needed for forecasting plant and ecosystem responses to climate change. Due to a lack of considering local adaptation induced variations in climatic requirements of plant species for phenological development, traditional uniform/non-spatial models that cover broad geographic regions are susceptible to systematic prediction biases. This study presents a climate calibration method that incorporates climate adaptation patterns of plant species into a widely used Spring Index (SI) First Leaf (FL) model. Multi-year (2009-2021) phenological observation data for a most frequently observed shrub species(common lilac Syringa vulgaris) and a most frequently observed tree species(red maple Acer rubrum) in the eastern USA from the USA-National Phenology Network (USA-NPN) were used to develop and validate the calibrated models. Climatic gradients defined by latitudinal temperature variations were used to predict varied climatic requirements of the populations of each species. Prior to calibration, SI FL predictions showed consistent geographic biases and yielded large prediction errors (especially for red maple, RMSE = 30 d). Calibrated SI FL predictions yielded reduced errors (e.g. RMSE = 16 d for red maple) and were freed from significant geographic biases (α = 0.05) in all cases. The calibration method accounted for both intraspecific and interspecific variations, leading to more accurate broad-scale first leaf predictions for the species tested. The climate-calibrated SI FL allows for more accurate tracking of the onset of spring over extensive geographic areas and would support spatially explicit natural resource and environmental conservation efforts under climate change.
... In addition, phenological models are usually built at the species level, and the phenological information extracted in this study may be an integrated result from different species. Studies have shown that different tree species have different temperature and photoperiod sensitivities (Körner and Basler, 2010;Zohner et al., 2016;Fu et al., 2019). With the development of remote sensing technology, high-resolution data are increasingly available. ...
Vegetation phenological models play a major role in terrestrial ecosystem modeling. However, substantial uncertainties still occur in phenology models because the mechanisms underlying spring phenological events are unclear. Taking into account the asymmetric effects of daytime and nighttime temperature on spring phenology, we analyzed the performance of 17 spring phenological models by combining the effects of photoperiod and precipitation. The global inventory modeling and mapping study third-generation normalized difference vegetation index data (1982–2014) were used to extract the start of the growing season (SOS) in the North–South Transect of Northeast Asia. The satellite-derived SOS of deciduous needleleaf forest (DNF), mixed forest (MF), open shrublands (OSL), and woody savannas (WS) showed high correlation coefficients (r) with the model-predicted SOS, with most exceeding 0.7. For all vegetation types studied, the models that considered the effect of photoperiod and precipitation did not significantly improve the model performance. For temperature-based models, the model using the growing-degree-day temperature response had a lower root mean square error compared with the models using the sigmoid temperature response Importantly, we found that daily maximum temperature was most suitable for the spring phenology prediction of DNF, OSL, and WS; daily mean temperature for MF; and daily minimum temperature for grasslands. These findings indicate that future spring phenological models should consider the asymmetric effect between daytime and nighttime temperature across different vegetation types.
... Such changes include increased heat absorption (Qiu et al., 2017), night light intensity (Meng et al., 2020b), and pollution . Changes in light intensity (Zohner et al., 2016), moisture availability , and human-induced warming (Jochner et al., 2012;Meng et al., 2020a;Xie et al., 2021;Yang et al., 2020) may affect vegetation phenology, which is important for sustainable urbanization in the context of climate change (Jeong et al., 2019;Zhou et al., 2019;Ding et al., 2020). Phenological shifts, in turn, affect ecosystem functioning by altering plant productivity and species distribution (CaraDonna et al., 2014;Zohner et al., 2020) and then feedback to the land-atmosphere interaction (Richardson et al., 2012;Piao et al., 2019). ...
Being an important theme in global warming, the response of vegetation phenology to urbanization has become an increasing concern at both the local and global levels. Previous studies have focused on spatial or temporal responses across urban-rural gradients; thus, the influence of urbanization on vegetation phenology along the dynamic urbanization gradient has not been well quantified. In this study, we comprehensively analyzed the response of vegetation phenology to urbanization in the Guangdong-Hong Kong-Macao Greater Bay Area (GHM-GBA) from a dynamic urban-rural gradient perspective. The results show that the response of vegetation phenology to urbanization level has a distinct spatiotemporal difference across the urban-rural gradient. Compared to rural areas, the change rate of advancements in the start-of-season (SOS) in urban domains was 1.16 DOY/year and that of the end-of-season (EOS) was 0.63 days/year from 2001 to 2020. In the GHM-GBA region, 61.03 % of the remote sensing pixels showed an advancing trend for SOS and 55.75 % for EOS. Urbanization advanced the SOS and EOS but did not extend the growing season length, and the SOS and EOS were advanced by 7 and 6 days along the urban-to-rural gradient, respectively. For every 10 % increase in urbanization levels, the SOS and EOS advanced by 1.085 and 1.091 days across the urban-rural gradient, respectively; the spring land surface temperature (LST) advanced the SOS at a rate of 1.71 days/°C, while the autumn LST advanced the EOS at a rate of 1.88 days/°C. The phenological shift in the urban-rural gradient was more significant than that over time, which was mainly because of land surface warming under different urbanization levels. These quantitative findings are of great importance for understanding the complicated impacts of urbanization on vegetation phenology and for developing models to predict vegetation phenological changes under future urbanization.
... Shifts in phenology in response to warming have been observed across many tree species, and these responses are hypothesized to improve individual fitness by extending the growing season and increasing productivity (Cleland et al., 2007;Fu et al., 2015;Piao et al., 2019;Polgar & Primack, 2011;Richardson et al., 2010). However, other factors, including photoperiod (day-and night-length cues) and/or chilling requirements (for dormancy release), could limit or confound responses to climate warming (Ford et al., 2017;Harrington & Gould, 2015;Singh et al., 2017;Zohner et al., 2016). In addition, phenological shifts can also strongly influence ecosystem processes including plant-insect synchrony, nutrient and water cycling, and climate-productivity feedbacks, among others, resulting in the alteration of ecosystem functioning and service provision (Cleland et al., 2007;Fu et al., 2015;Pan et al., 2011;Piao et al., 2019). ...
In a changing climate, the future survival and productivity of species relies on individual populations to respond to shifting environmental conditions. Many tree species including northern red oak (Quercus rubra) exhibit phenotypic plasticity, the ability to respond to changes in environmental conditions at within‐generation timescales, through varying traits such as leaf phenology. Phenotypic plasticity of phenology may vary among populations within a species’ range, and it is unclear if the range of plasticity is adequate to promote fitness. Here, we used a 58‐year‐old common garden to test whether northern red oak populations differ in phenological sensitivity to changes in temperature, and whether differences in phenological sensitivity are associated with differences in productivity and survival (proxies of fitness). We recorded eight years of spring leaf emergence and autumn leaf coloration and loss in 28 distinct populations from across the species’ full range. Across the 28 populations, spring leaf out consistently advanced in warmer years, but fall phenology was less responsive to changes in temperature. Southern, warm‐adapted populations had larger shifts in phenology in response to springtime warming but had lower long‐term survival. Moreover, higher phenological sensitivity to spring warming was not strongly linked to increased productivity. Instead, fitness was more closely linked to latitudinal gradients. Although springtime phenological sensitivity to climate change is common across northern red oak populations, responses of productivity and survival, which could determine longer‐term trajectories of species abundance, are more variable across the species’ range.
... Winter chilling, forcing requirements, and photoperiod trigger the start of foliar phenology (Richardson et al., 2013). Previous research suggests that chilling requirements will constrain the advance of leaf unfolding in deciduous forests by reducing temperature sensitivity (Fu et al., 2015), whereas other factors such as precipitation (Peaucelle et al., 2019) and photoperiod (Körner & Basler, 2010;Meng et al., 2021;Zohner et al., 2016) may increase the heat requirements during the ecodormancy stage and, as a result, slow down the warming-induced advance of the leaf unfolding. With regards to leaf senescence, a recent study found that increased productivity during the growing season counteracts the warming-induced delay in leaf senescence (Zani et al., 2020). ...
Climatic warming has lengthened the photosynthetically active season in recent decades, thus affecting the functioning and biogeochemistry of ecosystems, the global carbon cycle and climate. Temperature response of carbon uptake phenology varies spatially and temporally, even within species, and daily total intensity of radiation may play a role. We empirically modelled the thresholds of temperature and radiation under which daily carbon uptake is constrained in the temperate and cold regions of the Northern Hemisphere, which include temperate forests, boreal forests, alpine and tundra biomes. The two‐dimensionality of the temperature‐radiation constraint was reduced to one single variable, θ, which represents the angle in a polar coordinate system for the temperature‐radiation observations during the start and end of the growing season. We found that radiation will constrain the trend towards longer growing seasons with future warming but differently during the start and end of season and depending on the biome type and region. We revealed that radiation is a major factor limiting photosynthetic activity that constrains the phenology response to temperature during the end‐of‐season. In contrast, the start of the carbon uptake is overall highly sensitive to temperature but not constrained by radiation at the hemispheric scale. This study thus revealed that while at the end‐of‐season the phenology response to warming is constrained at the hemispheric scale, at the start‐of‐season the advance of spring onset may continue, even if it is at a slower pace.
... For a wide range of forest tree species, the timing of bud burst exhibits a continuous phenotypic variation typical of a quantitative trait (Derory et al., 2001). According to new research, just a few woody species are photoperiod sensitive Zohner et al., 2016). However, bud development in temperate (Pletsers et al., 2015) and subtropical Jewaria et al., 2021) trees is controlled by a combination of photoperiod, chilling (temperature and duration), and spring or forcing temperatures. ...
Bud dormancy and its release are complex physiological phenomena in plants. The molecular mechanisms of bud dormancy in Liriodendron chinense are mainly unknown. Here, we studied bud dormancy and the related physiological and molecular phenomena in Liriodendron under long-day (LD) and short-day (SD). Bud burst was released faster under LD than under SD. Abscisic acid (ABA), superoxide dismutase (SOD), catalase (CAT), and glutathione reductase (GR) activities were increased significantly under LD in Liriodendron buds. In contrast, the contents of gibberellic acid (GA3), ascorbic acid (AsA), glutathione (GSH), malondialdehyde (MDA), and ascorbate peroxidase (APX) activity decreased under LD but increased under SD. Differentially expressed genes (DEGs) were up-regulated under LD and down-regulated under SD and these changes correspondingly promoted (LD) or repressed (SD) cell division and the number and/or size of cells in the bud. Transcriptomic analysis of Liriodendron buds under different photoperiods identified 187 DEGs enriched in several pathways such as flavonoid biosynthesis and phenylpropanoid biosynthesis, plant hormone and signal transduction, etc. that are associated with antioxidant enzymes, non-enzymatic antioxidants, and subsequently promote the growth of the buds. Our findings provide novel insights into regulating bud dormancy via flavonoid and phenylpropanoid biosynthesis, plant hormone and signal transduction pathways, and ABA content. These physiological and biochemical traits would help detect bud dormancy in plants.
... For example, early flushing of leaves may be advantageous in avoiding competition. However, such plant species face a risk of stress, such as frost damage, if they are in a temperate climate (Zohner et al. 2016). Similarly, in forests where trees with contrasting leaf phenological attributes (i.e., evergreens and deciduous) coexist, evergreens can use resources when deciduous species shed their leaves (Kamiyama et al. 2014 a, b). ...
Synchronisation of the leaf phenological patterns with favourable environmental conditions and the variations in the leaf traits allow tree species to coexist, support biodiversity and maintain forest productivity with a larger implication on the global carbon cycle. However, within a forest whether plants with contrasting phenological attributes follow similar or distinct adaptive strategies for resource gain in response to seasonality and how they avoid niche-overlap to coexist is less clear. Further, whether the trade-offs between faster leaf growth within a shorter duration and vice-versa as proposed in the worldwide leaf economic spectrum (WLES) holds at the local scale remain inconclusive. Here, we aim to (1) describe patterns of temporal variation in leaf exposure (i.e. initiation, the peak of exposure, longevity, and expansion period) and leaf structural properties (i.e. area, dry mass, specific leaf area, dry-mass lost, construction cost, and mass acquired before the rainy season) among 12 coexisting evergreen and deciduous trees; and (2) explore whether the predictions of the WLES framework hold for evergreen and deciduous mid-elevation trees of the central Himalaya range. Results suggest that with an earlier leaf flush/leaf initiation and faster leaf recruitment in deciduous tree species, these plant species may maximize resource gains while investing less in structural parts of the leaves. In contrast, evergreens exhibit a higher investment in structural traits and retain leaves for a longer period and thereby maximizing resource gains from the growing season. The principal component analysis showed that PC-1 and PC-2 cumulatively explained 68.4% of the total variation in leaf traits. There was a distinct grouping of evergreen and deciduous species along the principal axis-1 for trait variation, suggesting a niche separation, which may allow species to coexist. When tested for the significance of differences in the average values of leaf traits, we found that deciduous trees had higher average values for mass before the rainy season (MRS), dry mass-loss (DML), specific leaf area (SLA), and leaf area (LA) than evergreens. The leaf life span of evergreens was significantly higher compared to the deciduous form which may allow evergreens to pay back the leaf construction cost which on average is higher than deciduous tree species. In a way, deciduous may adopt the resource acquisition strategy while evergreen exhibits a resource conservation strategy. The proposed generalized conservative-acquisitive traits axis of the world leaf economic spectrum thereby holds true for mid-elevational tree species in the central Himalayas.
... Decreased flowering synchrony likely results from different sensitivity to warming among species, such as the early-vs midand late-flowering species in our study (Fig. 1b, Fig. 4a). Furthermore, differences in the sensitivity to winter cold and day-length among species also contribute to changes in flowering synchrony under warming (Laube et al. 2014, Zohner et al. 2016. Less synchronized flowering among species may affect the reproductive success of plants by altering competition among species for abiotic resources and pollination services (Ghazoul 2006, Forrest et al. 2010, Bogdziewicz et al. 2020a). ...
The timing of phenological events is highly sensitive to climate change, and may influence ecosystem structure and function. Although changes in flowering phenology among species under climate change have been reported widely, how species‐specific shifts will affect phenological synchrony and community‐level phenology patterns remains unclear. We conducted a manipulative experiment of warming and precipitation addition and reduction to explore how climate change affected flowering phenology at the species‐ and community‐levels in an alpine meadow on the eastern Tibetan Plateau. We found that warming advanced the first and last flowering times differently and with no consistent shifts in flowering duration among species, resulting in the entire flowering period of species emerging earlier in the growing season. Early‐flowering species were more sensitive to warming than mid‐ and late‐flowering species, thereby reducing flowering synchrony among species and extending the community‐level flowering season. However, precipitation and its interactions with warming had no significant effects on flowering phenology. Our results suggest that temperature regulates flowering phenology from the species to community‐level in this alpine meadow community, yet how species shifted their flowering timing and duration in response to warming varied. This species level divergence may reshape flowering phenology in this alpine plant community. Decreasing flowering synchrony among species and the extension of community‐level flowering seasons under warming may alter future trophic interactions, with cascading consequences to community and ecosystem function.
... The timing of bud burst displays a continuous phenotypic variation typical of a quantitative attribute for a variety of forest tree species [9]. According to a recent study, only a few woody species are photoperiod sensitive [8,10]. However, a combination of photoperiod, chilling (temperature and duration), and spring or forcing temperatures regulates bud development in temperate [11] and subtropical [8,12] trees. ...
Protein kinases play an essential role in plants' responses to environmental stress signals. SnRK2 (sucrose non-fermenting 1-related protein kinase 2) is a plant-specific protein kinase that plays a crucial role in abscisic acid and abiotic stress responses in some model plant species. In apple, corn, rice, pepper, grapevine, Arabidopsis thaliana, potato, and tomato, a genome-wide study of the SnRK2 protein family was performed earlier. The genome-wide comprehensive investigation was first revealed to categorize the SnRK2 genes in the Liriodendron chinense (L. chinense). The five SnRK2 genes found in the L. chinense genome were highlighted in this study. The structural gene variants, 3D structure, chromosomal distributions, motif analysis, phylogeny, subcellular localiza-tion, cis-regulatory elements, expression profiles in dormant buds, and photoperiod and chilling responses were all investigated in this research. The five SnRK2 genes from L. chinense were grouped into groups (I-IV) based on phylogeny analysis, with three being closely related to other species. Five hormones-, six stress-, two growths and biological process-, and two metabolic-related responsive elements were discovered by studying the cis-elements in the promoters. According to the expression analyses, all five genes were up-and down-regulated in response to abscisic acid (ABA), photoperiod, chilling, and chilling, as well as photoperiod treatments. Our findings gave insight into the SnRK2 family genes in L. chinense and opened up new study options.
... For several photoperiod-sensitive species, the individuals under long photoperiod conditions leaf out earlier than those under short photoperiod conditions. However, the effect of photoperiod is only significant for a small number of tree species (Vitasse and Basler, 2013;Laube et al., 2014;Zohner et al., 2016). ...
Temperate trees could cope with climate change through phenotypic plasticity of phenological key events or adaptation in situ via selection on genetic variation. However, the relative contribution of local adaptation and phenotypic plasticity to phenological change is unclear for many ecologically important tree species. Here, we analyzed the leaf-out data of European beech (Fagus sylvatica L.) from 50 provenances planted in 7 trial sites. We first constructed a function between chilling accumulation (CA) and photoperiod-associated heat requirement (PHR) of leaf-out date for each provenance and quantified the relationship between parameters of the CA-PHR function and climatic variables at provenance origins by using the random forest model. Furthermore, we used the provenance-specific CA-PHR function to simulate future leaf-out dates under two climate change scenarios (RCP 4.5 and 8.5) and two assumptions (no adaptation and adaptation). The results showed that both CA, provenance, and their interactions affected the PHR of leaf-out. The provenances from southeastern Europe exhibited a stronger response of PHR to CA and thus flushed earlier than northwestern provenances. The parameters of the CA-PHR function were connected with climatic variables (e.g., mean diurnal temperature range, temperature seasonality) at the originating sites of each provenance. If only considering the phenotypic plasticity, the leaf-out date of European beech in 2070–2099 will advance by 6.8 and 9.0 days on average relative to 1951–2020 under RCP 4.5 and RCP 8.5, respectively. However, if F. sylvatica adapts to future climate change by adopting the current strategy, the advance of the leaf-out date will weaken by 1.4 and 3.4 days under RCP 4.5 and RCP 8.5, respectively. Our results suggest that the European beech could slow down its spring phenological advances and reduce its spring frost risk if it adopts the current strategy to adapt to future climate change.
... And different from previous ideas, day length is a less useful signal of the arrival of spring further north than it is in south because at high latitudes, the fastest increase in daylength occurs long before the end of night frosts, which would kill any young leaves. Instead, northern trees rely on air temperature to optimize the timing of bud burst (Zohner et al. 2016. The more Constantin worked on botanical garden phenological data (also using those from gardens in North America and China), the more ideas we had about hypotheses to test. ...
This review describes, in chronological order, the research topics in which I have been involved over the past 40 years, a time during which the study of plant evolution, systematics, and biodiversity has moved from relying solely on morphology to relying mostly on DNA sequences and now partially assembled genomes. When I began to do systematics, traveling to tropical countries for fieldwork was a big draw and probably influenced my initial choice of plant groups to work on. In 1989, I made a conscious decision to shift my focus from monographs, floras, and herbarium-based species discovery to the evolution of plant sexual systems and the functioning of unisexual flowers, selecting first Siparunaceae and then Cucurbitaceae as suitable groups. I also became an early adopter of molecular clock approaches in the study of biogeography and plant/animal mutualisms, and was involved in the discovery of natural horizontal gene transfers in seed plants, which in turn led to an interest in mitochondrial and plastid genomes in parasitic plants. Three topics, bee behaviour on flowers, the evolution of ant/plant interactions, and plant phenology, have accompanied me from my dissertation to the present, while others, such as molecular cytogenetics, grew from the interests and expertise of students. The breadth of topics reflects a great change in systematics since the 1980s, namely the increasing role of collaborations. Monographs, floras, and cladistics (when morphology based) used to be done in isolation. With DNA data came lab work, bioinformatics, and both the need and the possibility to collaborate, which brought systematists out of their niche, gave comparative biology a huge push, and resulted in a better integration of biodiversity studies within biology.
... Generally, the phenological response in a particular region depends upon the regional climate and is expected to be species-specific (Gillooly et al. 2001), as the sensitivity to seasonal warming differs amongst species (Fitter and Fitter 2002;Sherry et al. 2007;Zohner et al. 2017Zohner et al. , 2016Laube et al. 2014a, b). The closely related species show different phenological responses to climate warming, with certain species responding much faster than the others (Miller-Rushing and Inouye 2009). ...
Experimental evidences in support of climate warming–driven phenological shifts are still scarce, particularly from the developing world. Here, we investigated the effect of experimental warming on flowering phenology of selected woody plants in Kashmir Himalaya. We selected the twigs of four congeneric pairs of temperate woody species (Prunus, Populus, Ulmus, Viburnum)—typical spring-flowering plants in the region. Using randomised block design, we monitored these winter dormant twigs in controlled growth chambers to study the effect of different temperature regimes (9, 17, 20 and 23 °C) and species identity on the patterns of phenological shifts. We observed a significant phenological shift in all the species showing preponement in the first flower out and senescence phases ranging from 0.56 to 3.0 and 0.77 to 4.04 days per degree increase in temperature, respectively. The duration of flowering phase in all the species showed a corresponding decrease along the gradient of increasing temperature, which was more driven by preponement of the flower senescence than the start of flower- ing. The patterns of phenological shifts were highly species-specific, and the magnitude of these shifts significantly varied in all the four pairs of congeneric species despite their phylogenetic similarity. Our study provides experimental support to the previous long-term observation and herbarium-based studies showing that the patterns of phenological shifts in response to global climate warming are likely to vary between species, even those belonging to same evolutionary stock. Our findings highlight that a one-size-fits-all strategy to manage the likely impacts of climate warming–induced phenological shifts will seldom succeed, and should instead be designed for the specific phenological responses of species and regions.
... As such, accurate predictions of future carbon uptake require an understanding of major phenological processes like spring leaf out or autumn leaf senescence. While the timing of leaf out is mainly driven by temperature (Zohner et al., 2016(Zohner et al., , 2017, the environmental drivers of autumn leaf senescence are less clear (Gallinat et al., 2015), and predictions of future growing-season length thus remain highly uncertain (Richardson et al., 2012). Autumn senescence has traditionally been thought to be primarily driven by temperature and daylength (Krol et al., 1995;Rosenthal and Camm, 1997), while additional variation can be explained by factors, such as nutrient (Sigurdsson, 2001) and water statuses (Leuzinger et al., 2005), pathogen infections (Mutz et al., 2021), and air pollution (Gielen et al., 2007). ...
The growing-season length of temperate and boreal trees has a strong effect on the global carbon cycle. Yet, a poor understanding of the drivers of phenological processes, such as autumn leaf senescence in deciduous trees, limits our capacity to estimate growing-season lengths under climate change. While temperature has been shown to be an important driver of autumn leaf senescence, carbon source–sink dynamics have been proposed as a mechanism that could help explain variation of this important process. According to the carbon sink limitation hypothesis, senescence is regulated by the interplay between plant carbon source and sink dynamics, so that senescence occurs later upon low carbon inputs (source) and earlier upon low carbon demand (sink). Here, we manipulated carbon source–sink dynamics in birch saplings (Betula pendula) to test the relevance of carbon sink limitation for autumn leaf senescence and photosynthetic decline in a widespread deciduous tree. Specifically, we conducted a gradient of leaf and bud removal treatments and monitored the effects on autumnal declines in net photosynthesis and the timing of leaf senescence. In line with the carbon sink limitation hypothesis, we observed that leaf removal tended to increase total leaf-level autumn photosynthesis and delayed the timing of senescence. Conversely, we did not observe an effect of bud removal on either photosynthesis or senescence, which was likely caused by the fact that our bud removal treatment did not considerably affect the plant carbon sink. While we cannot fully rule out that the observed effect of leaf removal was influenced by possible treatment-level differences in leaf age or soil resource availability, our results provide support for the hypothesis of carbon sink limitation as a driver of growing-season length and move the scientific field closer to narrowing the uncertainty in climate change predictions.
... Hence, understanding how ecological and bioclimatic processes control vegetation phenology is critical to understanding how ecosystems will respond to future climate change (Buermann et al., 2018;Piao et al., 2019;Richardson et al., 2018). However, despite extensive efforts devoted to this topic, mechanistic understanding of what controls plant phenology remains incomplete (Delpierre et al., 2016;Zohner et al., 2016). In this context, a large proportion of phenological research has focused on the mechanisms that control the timing of leaf emergence, while understanding of the ecophysiological processes that control leaf senescence is less welldeveloped (Chen et al., 2020;Vitasse et al., 2021;Zani et al., 2020). ...
Incomplete understanding of the processes controlling senescence limits our ability to forecast how the timing of leaf senescence will change in coming decades. In this study, we use a hierarchical Bayesian model (HBM) in association with a 27+ year record of field observations for 12 temperate deciduous tree species collected at Harvard Forest in central Massachusetts to examine how variability in bioclimatic controls affects the timing of leaf senescence. To test how general and extensible our results are over a broader biogeographic range, we used a multi-year record of land surface phenology derived from remote sensing encompassing all forested lands in New England. Results from the HBM showed that while air temperature is an important factor that influences the timing of leaf senescence, photoperiod uniformly exerts the strongest control across all 12 species. Species exhibiting the strongest dependence on photoperiod, particularly Acer species, showed low inter-annual variation and no long-term trends in the timing of leaf senescence. In contrast, species with greater dependence on air temperature, particularly Quercus species, showed statistically significant trends toward later senescence dates in response to long-term warming. Results from analyses conducted at regional scale across all of New England using data derived from remote sensing corroborated results obtained at Harvard Forest. Specifically, relative to ecoregions dominated by Quercus species, the timing of leaf senescence in ecoregions dominated by Acer species exhibited lower interannual variability and lower correlation with year-to-year variation in pre-senescence period mean air temperatures. These results suggest that forecasting how the timing of leaf senescence in temperate forests will change in the future requires species-specific understanding of how bioclimatic forcing controls the timing of leaf senescence.
... Despite the strong focus on spring temperatures, increasing evidence in climate change studies suggests a more complicated physiology (e.g. Zohner et al., 2016;Gauzere et al., 2019;Ettinger et al., 2020). For decades, studies of agricultural and model species have found that three major cues underlie spring phenology (Maurya & Bhalerao, 2017;Satake et al., 2022): chilling (cool temperatures, generally occurring in the fall and winter), forcing (warm temperatures, generally occurring in the late winter and early spring), and photoperiod (day length). ...
Climate change has advanced plant phenology globally 4‐6 days per °C on average. Such shifts are some of the most reported and predictable biological impacts of rising temperatures. Yet as climate change has marched on, phenological shifts have appeared muted over recent decades—failing to match simple predictions of an advancing spring with continued warming. The main hypothesis for these changing trends is that interactions between spring phenological cues—long‐documented in lab environments—are playing a greater role in natural environments due to climate change. Here we argue that accurately linking shifts observed in long‐term data to underlying phenological cues is slowed by biases in observational studies and limited integration of insights from lab studies. We synthesize seven decades of lab experiments to quantify how phenological cue‐space has been studied and how treatments compare to shifts caused by climate change. Most studies focus on one cue, limiting our ability to make accurate predictions, but some well‐studied forest species offer opportunities to advance forecasting. We outline how greater integration of controlled environment studies with long‐term data could drive a new generation of lab experiments, built on physiological insights, that would transform our fundamental understanding of phenology and improve predictions.
Species are altering their phenology to track warming temperatures. In forests, understorey plants experience tree canopy shading resulting in light and temperature conditions, which strongly deviate from open habitats. Yet, little is known about understorey phenology responses to forest microclimates.
We recorded flowering onset, peak, end and duration of 10 temperate forest understorey plant species in two mesocosm experiments to understand how phenology is affected by sub‐canopy warming and how this response is modulated by illumination, which is related to canopy change. Furthermore, we investigated whether phenological sensitivities can be explained by species' characteristics, such as thermal niche.
We found a mean advance of flowering onset of 7.1 d per 1°C warming, more than previously reported in studies not accounting for microclimatic buffering. Warm‐adapted species exhibited greater advances. Temperature sensitivity did not differ between early‐ and later‐flowering species. Experimental illumination did not significantly affect species' phenological temperature sensitivities, but slightly delayed flowering phenology independent from warming.
Our study suggests that integrating sub‐canopy temperature and light availability will help us better understand future understorey phenology responses. Climate warming together with intensifying canopy disturbances will continue to drive phenological shifts and potentially disrupt understorey communities, thereby affecting forest biodiversity and functioning.
High interannual variation in seed production in perennial plants can be synchronized at subcontinental scales with wide consequences for ecosystem functioning, but how such synchrony is generated is unclear. We investigated the factors contributing to masting synchrony in European beech, spanning an impressive 2000 km geographic range. Maximizing masting synchrony via spatial weather coordination, known as the Moran effect, requires distant populations to react simultaneously to weather conditions. A celestial cue that occurs simultaneously across the entire Hemisphere is the longest day (summer solstice). We show that European beech abruptly opens its temperature-sensing window on the solstice, hence widely separated populations all start responding to weather signals in the same week. This celestial "starting gun" generates ecological events with unparalleled spatial synchrony across the continent.
The Mediterranean Basin is one of the regions most affected by climate change. It is highly dependent on the impact of climate change on agricultural efficiency and food security. While rising temperatures and decreasing precipitation levels already impose great risks, the effects of compounding extreme events (CEEs) can be significantly more severe and amplify the risk. It is therefore of high importance to assess these risks under climate change on a regional level to implement efficient adaption strategies. This study focuses on False Spring Events (FSEs), which impose a high risk of crop losses during the beginning of the vegetation growing period, as well as Heat and Drought-based CEEs (HDCEs) in summer, for a high-impact future scenario (RCP8.5). The results for 2070–2099 are compared to 1970–1999. In addition, deviations of the near-surface atmospheric state under FSEs and HDCEs are investigated with the aim to improve the predictability of these events. We apply a multivariate, trend-conserving bias correction method (MBCn) accounting for temporal coherency between the inspected variables derived from EUR-CORDEX. This method proves to be a suitable choice for the assessment of percentile threshold-based CEEs. The results show a potential increase in frequency of FSEs for large portions of the study domain, especially impacting later stages of the warming period, caused by disproportionate changes in the behavior of warm phases and frost events. Frost events causing FSEs predominantly occur under high-pressure conditions and northerly to easterly wind flow. HDCEs are projected to significantly increase in frequency, intensity, and duration, mostly driven by dry, continental air masses. This intensification is multiple times higher than that of the univariate components. This study improves the understanding of the unfolding of climate change in the Mediterranean and shows the need for further, locally refined, investigations and adaptation strategies.
Given that already-observed temperature increase within cities far exceeds the projected global temperature rise by the end of the century, urban environments often offer a unique opportunity for studying ecosystem response to future warming. However, the validity of thermal gradients in space serving as a substitute for those in time is rarely tested. Here, we investigated vegetation phenology dynamics in China's 343 cities and empirically test whether phenological responses to spatial temperature rise in urban settings can substitute for those to temporal temperature rise in their natural counterparts based on satellite-derived vegetation phenology and land surface temperature from 2003 to 2018. We found prevalent advancing spring phenology with "high confidence" and delaying autumn phenology with "medium confidence" under the context of widespread urban warming. Furthermore, we showed that space cannot substitute for time in predicting phenological shifts under climate warming at the national scale and for most cities. The thresholds of ~11°C mean annual temperature and ~600 mm annual precipitation differentiated the magnitude of phenological sensitivity to temperature across space and through time. Below those thresholds, there existed stronger advanced spring phenology and delayed autumn phenology across the spatial urbanization gradients than through time, and vice versa. Despite the complex and diverse relationships between phenological sensitivities across space and through time, we found that the directions of the temperature changes across spatial gradients were converged (i.e., mostly increased), but divergent through temporal gradients (i.e., increased or decreased without a predominant direction). Similarly, vegetation phenology changes more uniformly over space than through time. These results suggested that the urban environments provide a real-world condition to understand vegetation phenology response under future warming.
Plant species are frequently
reported to undergo leaf-out and flowering in a consistent order from 1 year to the next; however, only a limited number of these findings arise from studies encompassing many species or sites. Here, we evaluate the consistency in the order species leafed out in the northeastern United States using observations contributed to the USA National Phenology Network’s Nature’s Notebook platform. We repeated this analysis for flowering, evaluating a total of 132 species across 84 sites. We documented a relatively high degree of consistency in the order of both events among individual plants, with higher consistency in flowering. A small number of species pairs exhibited very high consistency in phenological order across several sites. The majority of species pairs exhibited variability in how consistently they underwent either leaf-out or flowering from site to site, which could be the result of either plastic or locally adaptive responses. Our investigation revealed that neither functional type nor seasonal position played a major role in shaping how consistently species leafed out or flowered in the same order. Instead, we found the number of days separating the events and interannual variability in timing to be the most influential factors driving the consistency in ordering.
Climate warming has the potential to influence plant flowering phenology which in turn can have broader ecological consequences. Herbarium collections offer a source of historical plant data that makes possible the ability to document and better understand how warming climate can influence long-term shifts in flowering phenology. We examined the influence of annual, winter, and spring temperatures on the flowering phenology of herbarium specimens for 36 species collected from 1884–2015. We then compared the response to warming between native and non-native, woody and herbaceous, dry and fleshy fruit, and spring vs summer blooming species. Across all species, plants flowered 2.26 days earlier per 1 °C increase in annual average temperatures and 2.93 days earlier per 1 °C increase in spring onset average temperatures. Winter temperatures did not significantly influence flowering phenology. The relationship of temperature and flowering phenology was not significantly different between native and non-native species. Woody species flowered earlier than herbaceous species only in response to increasing annual temperatures. There was no difference in the phenological response between species with dry fruits and those fleshy fruits for any of the temperature periods. Spring blooming species exhibited a significantly greater phenological response to warming yearly average temperatures than summer blooming species. Although herbarium specimens can reveal climate change impacts on phenology, it is also evident that the phenological responses to warming vary greatly among species due to differences in functional traits such as those considered here, as well as other factors.
Temperature and light cues interact to control many biological processes. Experiments give researchers the ability to manipulate these environmental cues independently and can be designed to robustly quantify their individual and interactive effects on any particular biological activity. Such experiments have produced important insights into the environmental controls on numerous biological processes in both plant and animal taxa across terrestrial and aquatic environments. Testing the interactive effects of multiple environmental cues, however, requires experimental treatments to be fully independent; any unmeasured experimental covariation among treatments can result in incorrect conclusions.
Using a database of controlled environment experiments on the spring phenology of woody plants as a case study, we highlight how a common experimental set‐up, designed to parse the interactive effects of temperature and photoperiod on time to budburst, introduces a latent experimental covariation of these treatments by coupling photo‐ and thermoperiodicity. Using data simulations, algebraic corrections and a comparative analysis of published experiments, we demonstrate how this unmeasured experimental covariation biases statistical inference regarding the relative contribution of light and temperature cues to phenological variation.
We identify this experimental covariation in more than 40% of published phenology studies that manipulate photoperiod. Our analyses demonstrate that the coupling of thermo‐ and photoperiodicity results in the overestimation of the effect of photoperiod, the underestimation of forcing effects, and misleading conclusions about their interactions on phenology. This may, in part, explain why the significance of photoperiod cues for spring phenology is currently debated in the literature.
Accurate forecasting of how varying environmental conditions will impact the dynamics of biological events requires accurately quantifying cue responses. To this end, we present several options for statistical corrections and alternative experimental designs that can provide more robust estimates of the relative effects of temperature and photoperiod on phenology and many other biological processes controlled by temperature and light.
Read the free Plain Language Summary for this article on the Journal blog.
Predicting spring phenology in temperate forests is critical for forecasting important processes such as carbon storage. One major forecasting method for phenology is the growing degree day (GDD) model, which tracks heat accumulation. Forecasts using GDD models typically assume that the GDD threshold for a species is constant across diverse landscapes, but increasing evidence suggests otherwise. Shifts in climate with anthropogenic warming may change the required GDD. Variation in climate across space may also lead to variation in GDD requirements, with recent studies suggesting that fine-scale spatial variation in climate may matter to phenology. Here, we combine simulations, observations from an urban and a rural site, and Bayesian hierarchical models to assess how consistent GDD models of budburst are across species and space. We built GDD models using two different methods to measure climate data: on-site weather stations and local dataloggers. We find that estimated GDD thresholds can vary up to 20% across sites and methods. Our results suggest our studied urban site requires fewer GDDs until budburst and may have stronger microclimate effects than the studied rural site, though these effects depend on the method used to measure climate. Further, we find that GDD models are less accurate for early-active species and may become less accurate with warming. Our results suggest that local-scale forecasts based on GDD models for spring phenology should incorporate these inherent accuracy issues of GDD models, alongside the variations we found across space, species and warming. Testing whether these issues persist at larger spatial scales could improve forecasts for temperate forests.
Seed production in many plants is characterized by large interannual variation,
which is synchronized at subcontinental scales in some species but local in
others. The reproductive synchrony affects animal migrations, trophic responses
to resource pulses and the planning of management and conservation. Spatial
synchrony of reproduction is typically attributed to the Moran effect, but this alone is
unable to explain interspecific differences in synchrony. We show that interspecific
differences in the conservation of seed production-weather relationships combine
with the Moran effect to explain variation in reproductive synchrony. Conservative
timing of weather cues that trigger masting allows populations to be synchronized
at distances >1000km. Conversely, if populations respond to variable weather
signals, synchrony cannot be achieved. Our study shows that species vary in the
extent to which their weather cueing is spatiotemporally conserved, with important
consequences, including an interspecific variation of masting vulnerability to
climate change.
We studied local variations in temperature from winter to spring, and interpopulation variations in leaf out phenology (the day and the temperature sum for budburst and leaf expansion) of Siebold's beech (Fagus crenata) canopy trees. We focused on local topographic variation associated with the late frost regime for the canopy trees using 5–10 years of in situ observation of the temperature at 12 sites and leaf out phenology of two populations inhabiting a basin (basin populations) and 4 populations inhabiting hillside slopes (hillside slope populations) in the Hakkoda Mountains, northern Japan. The late frost regime differed between topographies; late frosts occurred during warmer periods in the basin compared to hillside slopes. The basin populations exhibited a larger temperature sum for leaf out than the hillside slope populations, regardless of altitude, suggesting that local variation in the late frost regime is an abiotic factor causing local variations in leaf out phenology. The six studied populations exhibited earlier days and smaller temperature sum of budburst in years with longer chilling duration. However, the extent of phenotypic plasticity in the temperature sum was small for the basin compared to hillside slopes. The temperature sum of leaf expansion in the hillside slope populations also negatively correlated with chilling duration, whereas that of the basin populations responded in the opposite direction. The safety margin from the last frost differed between the topographies, but not that from the last fatal frost, suggesting local adaptation to the late frost regime in each habitat. We studied interpopulation variations in leaf out phenology of Siebold's beech canopy trees along topographic variation associated with the late frost regime. Our analyses of temperature, leaf out phenology, and their relationships for the populations inhabiting a basin and hillside slopes in the Hakkoda Mountains suggest that local variation in the late frost regime is an abiotic factor causing interpopulation variation in leaf out phenology within a region, such that the basin populations exhibit later leaf out than the hillside slope populations.
Over the past decades, global warming has led to a lengthening of the time window during which temperatures remain favorable for carbon assimilation and tree growth, resulting in a lengthening of the green season. The extent to which forest green seasons have tracked the lengthening of this favorable period under climate warming, however, has not been quantified to date. Here, we used remote sensing data and long‐term ground observations of leaf‐out and coloration for six dominant species of European trees at 1773 sites, for a total of 6060 species‐site combinations, during 1980‐2016 and found that actual green season extensions (GS: 3.1 ± 0.1 d decade‐1) lag four times behind extensions of the potential thermal season (TS: 12.6 ± 0.1 d decade‐1). Similar but less pronounced differences were obtained using satellite‐derived vegetation phenology observations, i.e., a lengthening of 4.4 ± 0.13 d decade‐1 and 7.5 ± 0.13 d decade‐1 for GS and TS, respectively. This difference was mainly driven by the larger advance in the onset of the thermal season compared to the actual advance of leaf‐out dates (spring mismatch: 7.2 ± 0.1 d decade‐1), but to a less extents caused by a phenological mismatch between GS and TS in autumn (2.4 ± 0.1 d decade‐1). Our results showed that forest trees do not linearly track the new thermal window extension, indicating more complex interactions between winter and spring temperatures and photoperiod and a justification of demonstrating that using more sophisticated models that include the influence of chilling and photoperiod are needed to accurately predict spring phenological changes under warmer climate. They urge caution if such mechanisms are omitted to predict, for example, how vegetative health and growth, species distribution, and crop yields will change in the future.
Leaf phenology is one of the most reliable indicators of global warming in temperate regions because it is highly sensitive to temperatures. Temperature sensitivity (ST) is defined as the values of changed days of leaf flushing date (LUD) per degree increase in temperatures. Climate warming substantially advanced LUD in the temperate region, but its effect on ST of LUD is still not clear. We used spring phenological records of 12 woody plants in eastern China in the years of 1983–2014 to explore temporal and spatial changes of LUD and ST. Furthermore, we compared the difference of ST and preseason temperatures in two periods (1983–1997 and 2000–2014), and explored the main factors regulating ST. The results showed that the average LUD significantly advanced (−2.7 days 10 yr⁻¹). The mean LUD over the period 1983–2014 was in day of the year (DOY) 87 ± 7 across sites and species for the early leaf flushing species (EFS), and mean DOY 102 ± 5 for the late leaf flushing species (LFS). LUD was earlier in low latitude than that in high latitude. ST of Armeniaca vulgaris was the most sensitive to temperature across all sites (−3.66 d °C⁻¹), while Firmiana simplex was the most insensitive (−2.37 d °C⁻¹). LUD of EFS was more sensitive to temperature warming than that of LFS. At the same site, LUD of EFS would advance more obviously than that of LFS under global warming. For all species, ST decreased significantly with shorter preseason length and warmer temperatures at the preseason end. Our results had demonstrated a strong relationship between ST and the preseason length (mean temperature at the preseason end).
Vegetation phenology and its spatiotemporal driving factors are essential to reflect global climate change, the surface carbon cycle and regional ecology, and further quantitative studies on spatiotemporal heterogeneity and its two-way driving are needed. Based on MODIS phenology, meteorology, land cover and other data from 2001 to 2019, this paper analyzes the phenology change characteristics of the Yangtze River Delta from three dimensions: time, plane space and elevation. Then, the spatiotemporal heterogeneity of phenology and its driving factors are explored with random forest and geographic detector methods. The results show that (1) the advance of start of season (SOS) is insignificant—with 0.17 days per year; the end of season (EOS) shows a significant delay—0.48 days per year. The preseason temperature has a greater contribution to SOS, while preseason precipitation is main factor in determining EOS. (2) Spatial differences of the phenological index do not strictly obey the change rules of latitude at a provincial scale. The SOS of Jiangsu and Anhui is earlier than that of Zhejiang and Shanghai, and EOS shows an obvious double-clustering phenomenon. In addition, a divergent response of EOS with elevation grades is found; the most significant changes are observed at grades below 100 m. (3) Land cover (LC) type is a major factor of the spatial heterogeneity of phenology, and its change may also be one of the insignificant factors driving the interannual change of phenology. Furthermore, nighttime land surface temperature (NLST) has a relatively larger contribution to the spatial heterogeneity in non-core urban areas, but population density (PD) contributes little. These findings could provide a new perspective on phenology and its complex interactions between natural or anthropogenic factors.
Large-scale citizen science programs have the potential to support national climate and ecosystem assessments by providing data useful in estimating both status and trends in key phenomena. In this study, we demonstrate how opportunistic, unbalanced observations of biological phenomena contributed through a national-scale citizen science program can be used to (a) identify and evaluate candidate biotic climate change indicators and (b) generate yearly estimates of status of selected indicators. Using observations of plant phenology contributed to Nature’s Notebook, the USA National Phenology Network’s citizen science program, we demonstrate a procedure for identifying biotic indicators as well as several approaches leveraging these opportunistically-sampled data points to generate yearly status measures. Because the period of record for this dataset is relatively short and inconsistently sampled (13 yr), we focus on estimates of status, though over time, these measurements could be leveraged to also estimate trends. We first applied various spatial, seasonal, and biological criteria to narrow down the list of candidate indicators. We then constructed latitude-elevation models for individual species-phenophase events using all observations. This allowed us to visualize differences between predicted and reported phenophase onset dates in a year as anomalies, with the expectation that these anomalies—representing earlier or later activity in the species of interest—reflect plant response to local springtime temperatures. Plotting yearly anomalies revealed regions with geographic coherence as well as outliers. We also show how yearly anomaly values can be reduced to a single measure to characterize the early or late nature of phenological activity in a particular year. Finally, we demonstrate how the latitude-elevation models can be leveraged to characterize the pace at which phenological transitions occur along latitude gradients on a year-by-year basis.
Within the same forest stand, temperate deciduous trees generally exhibit a distinct pattern in leaf-out timing, with some species flushing earlier than other species. This study aimed to explain the timing of leaf-out of various temperate tree species in relation to the risk of freezing damage to leaves.
We combined long-term series of leaf-out date (14–32 years) of five temperate tree species located in both low and high elevations in Switzerland, daily minimum temperatures recorded on the same sites and species-specific freezing resistance (LT50) of emerging leaves. We calculated temperature safety margins (the temperature difference between absolute minimum temperature during leaf-out and species-specific LT50 values), and date safety margins (time lag between the last day when temperature falls below species-specific LT50 values and the date of leaf-out).
The timing of leaf-out occurred when the probability to encounter freezing damage approaches zero, irrespective of climatic conditions (low vs. high elevation) and species (early and late flushing species). In other words, trees leaf-out precisely at the beginning of the probabilistically safe period. Interestingly, the temperature safety margins did not differ significantly between low and high elevation. Yet, the date safety margin was smaller at high elevation, presumably due to a faster increase of temperature during the leaf-out period at high elevation.
When species-specific freezing resistance is taken into account, the time of leaf-out converges among species towards a marginal risk of freezing damage. Thus, leaf-out time has likely evolved in a way that the risk of freezing damage is minimized over a large spectrum of climatic conditions. Species with a small safety margin against freezing temperature, like Fagus sylvatica, appear to employ photoperiod co-control of spring phenology, whereas species with a large safety margin depend largely on temperature for the right timing of leaf-out.
Our results offer a new avenue to explain the differences in leaf-out timing among co-occurring tree species. They further suggest that in a warming climate, tree species can expand their distribution range to the extent their phenology matches the stochasticity of freezing temperatures in spring.
Earlier spring leaf unfolding is a frequently observed response of plants to climate warming. Many deciduous tree species require chilling for dormancy release, and warming-related reductions in chilling may counteract the advance of leaf unfolding in response to warming. Empirical evidence for this, however, is limited to saplings or twigs in climate-controlled chambers. Using long-term in situ observations of leaf unfolding for seven dominant European tree species at 1,245 sites, here we show that the apparent response of leaf unfolding to climate warming (ST, expressed in days advance of leaf unfolding per °C warming) has significantly decreased from 1980 to 2013 in all monitored tree species. Averaged across all species and sites, ST decreased by 40% from 4.0 ± 1.8 days °C(-1) during 1980-1994 to 2.3 ± 1.6 days °C(-1) during 1999-2013. The declining ST was also simulated by chilling-based phenology models, albeit with a weaker decline (24-30%) than observed in situ. The reduction in ST is likely to be partly attributable to reduced chilling. Nonetheless, other mechanisms may also have a role, such as 'photoperiod limitation' mechanisms that may become ultimately limiting when leaf unfolding dates occur too early in the season. Our results provide empirical evidence for a declining ST, but also suggest that the predicted strong winter warming in the future may further reduce ST and therefore result in a slowdown in the advance of tree spring phenology.
A revised and updated classification for the families of flowering plants is provided. Many recent studies have yielded increasingly detailed evidence for the positions of formerly unplaced families, resulting in a number of newly adopted orders, including Amborellales, Berberidopsidales, Bruniales, Buxales, Chloranthales, Escalloniales, Huerteales, Nymphaeales, Paracryphiales, Petrosaviales, Picramniales, Trochodendrales, Vitales and Zygophyllales. A number of previously unplaced genera and families are included here in orders, greatly reducing the number of unplaced taxa; these include Hydatellaceae (Nymphaeales), Haptanthaceae (Buxales), Peridiscaceae (Saxifragales), Huaceae (Oxalidales), Centroplacaceae and Rafflesiaceae (both Malpighiales), Aphloiaceae, Geissolomataceae and Strasburgeriaceae (all Crossosomatales), Picramniaceae (Picramniales), Dipentodontaceae and Gerrardinaceae (both Huerteales), Cytinaceae (Malvales), Balanophoraceae (Santalales), Mitrastemonaceae (Ericales) and Boraginaceae (now at least known to be a member of lamiid clade). Newly segregated families for genera previously understood to be in other APG-recognized families include Petermanniaceae (Liliales), Calophyllaceae (Malpighiales), Capparaceae and Cleomaceae (both Brassicales), Schoepfiaceae (Santalales), Anacampserotaceae, Limeaceae, Lophiocarpaceae, Montiaceae and Talinaceae (all Caryophyllales) and Linderniaceae and Thomandersiaceae (both Lamiales). Use of bracketed families is abandoned because of its unpopularity, and in most cases the broader circumscriptions are retained; these include Amaryllidaceae, Asparagaceace and Xanthorrheaceae (all Asparagales), Passifloraceae (Malpighiales), Primulaceae (Ericales) and several other smaller families. Separate papers in this same volume deal with a new linear order for APG, subfamilial names that can be used for more accurate communication in Amaryllidaceae s.l., Asparagaceace s.l. and Xanthorrheaceae s.l. (all Asparagales) and a formal supraordinal classification for the flowering plants.
Temperate climates are defined by distinct temperature seasonality with large and often unpredictable weather during any of the four seasons. To thrive in such climates, trees have to withstand a cold winter and the stochastic occurrence of freeze events during any time of the year. The physiological mechanisms trees adopt to escape, avoid, and tolerate freezing temperatures include a cold acclimation in autumn, a dormancy period during winter (leafless in deciduous trees), and the maintenance of a certain freezing tolerance during dehardening in early spring. The change from one phase to the next is mediated by complex interactions between temperature and photoperiod. This review aims at providing an overview of the interplay between phenology of leaves and species-specific freezing resistance. First, we address the long-term evolutionary responses that enabled temperate trees to tolerate certain low temperature extremes. We provide evidence that short term acclimation of freezing resistance plays a crucial role both in dormant and active buds, including re-acclimation to cold conditions following warm spells. This ability declines to almost zero during leaf emergence. Second, we show that the risk that native temperate trees encounter freeze injuries is low and is confined to spring and underline that this risk might be altered by climate warming depending on species-specific phenological responses to environmental cues.
Significance
A species’ climate niche summarizes the observed climatic conditions at its range limits. This information can be used to predict range shifts of species under climate change, but it does not explain why they occur under a given climate or are absent from another. Functional traits associated with the climate niche, however, allow for such an explanation. We show that key plant functional traits predict the climate ranges of North American trees and discuss the underlying filter mechanisms that define “no-go areas” for specific trait expressions. This approach replaces species idiosyncrasy by the generality of traits, puts biogeography on more functional grounds, and yields products that will serve the improvement of next generation global vegetation models.
The timing of phenological events exerts a strong control over ecosystem function and leads to multiple feedbacks to the climate system1. Phenology is inherently sensitive to temperature (although the exact sensitivity is disputed2) and recent warming is reported to have led to earlier spring, later autumn3,4 and increased vegetation activity5,6. Such greening could be expected to enhance ecosystem carbon uptake7,8, although reports also suggest decreased uptake for boreal forests4,9. Here we assess changes in phenology of temperate forests over the eastern US during the past two decades, and quantify the resulting changes in forest carbon storage. We combine long-term ground observations of phenology, satellite indices, and ecosystem-scale carbon dioxide flux measurements, along with 18 terrestrial biosphere models. We observe a strong trend of earlier spring and later autumn. In contrast to previous suggestions4,9 we show that carbon uptake through photosynthesis increased considerably more than carbon release through respiration for both an earlier spring and later autumn. The terrestrial biosphere models tested misrepresent the temperature sensitivity of phenology, and thus the e�ect on carbon uptake. Our analysis of the temperature–phenology–carbon coupling suggests a current and possible future enhancement of forest carbon uptake due to changes in phenology. This constitutes a negative feedback to climate change, and is serving to slow the rate of warming.
Poleward and upward shifts are the most frequent types of range shifts that have been reported in response to contemporary climate change. However, the number of reports documenting other types of range shifts – such as in east-west directions across longitudes or, even more unexpectedly, towards tropical latitudes and lower elevations – is increasing rapidly. Recent studies show that these range shifts may not be so unexpected once the local climate changes are accounted for. We here provide an updated synthesis of the fast-moving research on climate-related range shifts. By describing the current state of the art on geographical patterns of species range shifts under contemporary climate change for plants and animals across both terrestrial and marine ecosystems, we identifi ed a number of research shortfalls. In addition to the recognised geographic shortfall in the tropics, we found taxonomic and methodological shortfalls with knowledge gaps regarding range shifts of prokaryotes, lowland range shifts of terrestrial plants, and bathymetric range shifts of marine plants. Based on this review, we provide a research agenda for filling these gaps. We outline a comprehensive framework for assessing multidimensional changes in species distributions, which should then be contrasted with expectations based on climate change indices, such as velocity measures accounting for complex local climate changes. Finally, we propose a unified classification of geographical patterns of species range shifts, arranged in a bi-dimensional space defined by species’ persistence and movement rates. Placing the observed and expected shifts into this bi-dimensional space should lead to more informed assessments of extinction risks.
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.
This paper describes the construction of an updated gridded climate dataset (referred to as CRU TS3.10) from monthly observations at meteorological stations across the world's land areas. Station anomalies (from 1961 to 1990 means) were interpolated into 0.5° latitude/longitude grid cells covering the global land surface (excluding Antarctica), and combined with an existing climatology to obtain absolute monthly values. The dataset includes six mostly independent climate variables (mean temperature, diurnal temperature range, precipitation, wet-day frequency, vapour pressure and cloud cover). Maximum and minimum temperatures have been arithmetically derived from these. Secondary variables (frost day frequency and potential evapotranspiration) have been estimated from the six primary variables using well-known formulae. Time series for hemispheric averages and 20 large sub-continental scale regions were calculated (for mean, maximum and minimum temperature and precipitation totals) and compared to a number of similar gridded products. The new dataset compares very favourably, with the major deviations mostly in regions and/or time periods with sparser observational data. CRU TS3.10 includes diagnostics associated with each interpolated value that indicates the number of stations used in the interpolation, allowing determination of the reliability of values in an objective way. This gridded product will be publicly available, including the input station series (http://www.cru.uea.ac.uk/ and http://badc.nerc.ac.uk/data/cru/). © 2013 Royal Meteorological Society
Phylogeography posits that the sequence of speciation events within a clade should parallel the geographic migration and isolation of members of the clade through time. The primary historical features that govern migration and allopatry in land plants are changes in physical geography (e.g., oceans, mountains, and deserts) and in climate (e.g., moisture, temperature, and day length), features that are often interrelated. If we assume that living genera retain physiological stability through time, much as they retain the morphological features that allow their identification, then these environmental features of the geologic past may be used to test phylogeographic hypotheses of living genera based on phylogenetic analysis. The history of the climatic and geographic features of the Tertiary of the Northern Hemisphere agrees with many phylogenetically based phylogeographic hypotheses of living angiosperm genera but indicates that some hypotheses require reanalysis. While the parallel comparison of phylogenetic hypotheses and historical biogeographic evidence is in its infancy, the reciprocal illumination of the two approaches shows great promise for future application.
Time of spring leaf emergence varies consistently among deciduous tree species in the north temperate forests of both E North America and Eurasia. Tree species that leaf earliest have only narrow-diameter xylem vessels (diffuse-porous wood anatomy) and relatively low numbers of vessels per unit wood volume, eg most members of the genera Populus, Betula, Salix, Alnus, Ostrya, Acer, Carpinus, Prunus and Aesculus. Later-leafing trees are characterized by having distinctly larger-diameter xylem vessels produced in their early, spring wood (ring-porous wood anatomy) and/or, especially in diffuse-porous species, relatively high numbers of vessels per unit wood volume. Both these traits contribute to greater maximum potential water conduction capacity. Among diffuse-porous species earlier leafing is also associated with greater indeterminancy of shoot growth; the earliest-leafing taxa initially flush only a few early leaves followed by a series of individual morphologically distinct late leaves on some shoots through the summer (heterophylly). Cambial activity must precede leaf emergence in ring-porous species; this explains the relatively late leafing of ring-porous genera like Fraxinus, Quercus, Rhus, Ulmus, Sassafras, Morus, Maclura, Carya and Juglans. -from Author
A considerable number of studies have investigated the phenology of European beech using models, experimental controlled conditions, or descriptive surveys of patterns in situ. In spite of this interest, there is no consensus about the environmental factors controlling bud burst in beech, especially about the role of photoperiod and chilling temperature (cold temperature effective to release bud dormancy). However, recent experimental and modelling studies provide new insights into the means by which these environmental factors control beech phenology. This present contribution aims to reconcile contradictory hypotheses about the main environmental factors controlling bud burst date of European beech. First, we review the main published results on the environmental control of beech phenology both in controlled and in natural conditions. Second, supported by the findings of recent studies, we propose a new theory for the role of photoperiod during the chilling phase for explaining spatial and temporal variations in bud burst phenology of European beech. Examples using long-term data from the Swiss Alps and Germany are presented to support this theory. The possible impacts of future and ongoing climate warming on beech phenology are discussed. Finally, due to interactions between chilling, forcing temperature, and photoperiod, we assert that beech phenology follows a nonlinear trend across biogeographical gradients such as changes in elevation or latitude and that the bud burst date of beech is expected not to undergo significant changes in response to global warming, especially in warmer climates.
Background
Uncertainty in comparative analyses can come from at least two sources: a) phylogenetic uncertainty in the tree topology or branch lengths, and b) uncertainty due to intraspecific variation in trait values, either due to measurement error or natural individual variation. Most phylogenetic comparative methods do not account for such uncertainties. Not accounting for these sources of uncertainty leads to false perceptions of precision (confidence intervals will be too narrow) and inflated significance in hypothesis testing (e.g. p-values will be too small). Although there is some application-specific software for fitting Bayesian models accounting for phylogenetic error, more general and flexible software is desirable.
Methods
We developed models to directly incorporate phylogenetic uncertainty into a range of analyses that biologists commonly perform, using a Bayesian framework and Markov Chain Monte Carlo analyses.
Results
We demonstrate applications in linear regression, quantification of phylogenetic signal, and measurement error models. Phylogenetic uncertainty was incorporated by applying a prior distribution for the phylogeny, where this distribution consisted of the posterior tree sets from Bayesian phylogenetic tree estimation programs. The models were analysed using simulated data sets, and applied to a real data set on plant traits, from rainforest plant species in Northern Australia. Analyses were performed using the free and open source software OpenBUGS and JAGS.
Conclusions
Incorporating phylogenetic uncertainty through an empirical prior distribution of trees leads to more precise estimation of regression model parameters than using a single consensus tree and enables a more realistic estimation of confidence intervals. In addition, models incorporating measurement errors and/or individual variation, in one or both variables, are easily formulated in the Bayesian framework. We show that BUGS is a useful, flexible general purpose tool for phylogenetic comparative analyses, particularly for modelling in the face of phylogenetic uncertainty and accounting for measurement error or individual variation in explanatory variables. Code for all models is provided in the BUGS model description language.
Unlabelled:
Premise of the study:
It has been 8 years since the last comprehensive analysis of divergence times across the angiosperms. Given recent methodological improvements in estimating divergence times, refined understanding of relationships among major angiosperm lineages, and the immense interest in using large angiosperm phylogenies to investigate questions in ecology and comparative biology, new estimates of the ages of the major clades are badly needed. Improved estimations of divergence times will concomitantly improve our understanding of both the evolutionary history of the angiosperms and the patterns and processes that have led to this highly diverse clade. •
Methods:
We simultaneously estimated the age of the angiosperms and the divergence times of key angiosperm lineages, using 36 calibration points for 567 taxa and a "relaxed clock" methodology that does not assume any correlation between rates, thus allowing for lineage-specific rate heterogeneity. •
Key results:
Based on the analysis for which we set fossils to fit lognormal priors, we obtained an estimated age of the angiosperms of 167-199 Ma and the following age estimates for major angiosperm clades: Mesangiospermae (139-156 Ma); Gunneridae (109-139 Ma); Rosidae (108-121 Ma); Asteridae (101-119 Ma). •
Conclusions:
With the exception of the age of the angiosperms themselves, these age estimates are generally younger than other recent molecular estimates and very close to dates inferred from the fossil record. We also provide dates for all major angiosperm clades (including 45 orders and 335 families [208 stem group age only, 127 both stem and crown group ages], sensu APG III). Our analyses provide a new comprehensive source of reference dates for major angiosperm clades that we hope will be of broad utility.
We use eddy covariance measurements of net ecosystem productivity (NEP) from 21 FLUXNET sites (153 site-years of data) to investigate relationships between phenology and productivity (in terms of both NEP and gross ecosystem photosynthesis, GEP) in temperate and boreal forests. Results are used to evaluate the plausibility of four different conceptual models. Phenological indicators were derived from the eddy covariance time series, and from remote sensing and models. We examine spatial patterns (across sites) and temporal patterns (across years); an important conclusion is that it is likely that neither of these accurately represents how productivity will respond to future phenological shifts resulting from ongoing climate change. In spring and autumn, increased GEP resulting from an 'extra' day tends to be offset by concurrent, but smaller, increases in ecosystem respiration, and thus the effect on NEP is still positive. Spring productivity anomalies appear to have carry-over effects that translate to productivity anomalies in the following autumn, but it is not clear that these result directly from phenological anomalies. Finally, the productivity of evergreen needleleaf forests is less sensitive to phenology than is productivity of deciduous broadleaf forests. This has implications for how climate change may drive shifts in competition within mixed-species stands.
Despite the numerous studies which have been conducted during the past decade on species ranges and their relationship to the environment, our understanding of how environmental conditions shape species distribution is still far from complete. Yet, some process-based species distribution models have been able to simulate plants and insects distribution at a global scale. These models strongly rely on the completion of the annual cycle of the species and therefore on their accomplished phenology. In particular, they have shown that the northern limit of species' ranges appears to be caused mainly by the inability to undergo full fruit maturation, while the southern limit appears to be caused by the inability to flower or unfold leaves owing to a lack of chilling temperatures that are necessary to break bud dormancy. I discuss here why phenology is a key adaptive trait in shaping species distribution using mostly examples from plant species, which have been the most documented. After discussing how phenology is involved in fitness and why it is an adaptive trait susceptible to evolve quickly in changing climate conditions, I describe how phenology is related to fitness in species distribution process-based models and discuss the fate of species under climate change scenarios using model projections and experimental or field studies from the literature.
We present molecular dating analyses for land plants that incorporate 33 fossil calibrations, permit rates of molecular evolution to be uncorrelated across the tree, and take into account uncertainties in phylogenetic relationships and the fossil record. We attached a prior probability to each fossil-based minimum age, and explored the effects of relying on the first appearance of tricolpate pollen grains as a lower bound for the age of eudicots. Many of our divergence-time estimates for major clades coincide well with both the known fossil record and with previous estimates. However, our estimates for the origin of crown-clade angiosperms, which center on the Late Triassic, are considerably older than the unequivocal fossil record of flowering plants or than the molecular dates presented in recent studies. Nevertheless, we argue that our older estimates should be taken into account in studying the causes and consequences of the angiosperm radiation in relation to other major events, including the diversification of holometabolous insects. Although the methods used here do help to correct for lineage-specific heterogeneity in rates of molecular evolution (associated, for example, with evolutionary shifts in life history), we remain concerned that some such effects (e.g., the early radiation of herbaceous clades within angiosperms) may still be biasing our inferences.
Phenological events such as bud burst, flowering, and senescence have received increased interest in the light of global warming
(1–3). Spring events at temperate latitudes have advanced by 2.5 days per decade since 1971 (4). As global warming progresses, how will it affect the arrival of spring and the length of the growing season?
Dormancy release as influenced by duration of outdoor winter chilling in Florence (Italy) was studied under different photoperiodic and temperature treatments in collected twigs of two European (Ulmus glabra Huds. and Ulmus minor Mill.) and four Asian (Ulmus pumila L., Ulmus parvifolia Jacq., Ulmus macrocarpa Hance and Ulmus villosa Brandis) elm clones. Photoperiod had no effect on dormancy release, and there was no evidence that photoperiod affected bud burst during quiescence in the studied elm clones. Thermal time (day degrees >0 degrees C) to bud burst decreased in all the clones with increasing outdoor chilling. Although all the clones exhibited a rather weak dormancy, they significantly differed from each other. Dormancy was released earlier in the Asian than in the European clones, and the clones could be ranked from the U. pumila clone (very weak and short dormancy) to the U. minor clone (relatively stronger and longer dormancy), the other clones being intermediate. In all the clones except U. minor, the observed decrement in thermal time to bud burst was efficiently explained as an inverse exponential function of the number of chill days < or =5 degrees C received outdoor in autumn and winter. Endodormancy, as measured by the single-node cuttings test, was weak and short in all the clones. The latter result suggests that correlative inhibitions were largely responsible for preventing bud burst during winter in these elm clones.
Changes in phenology (seasonal plant and animal activity driven by environmental factors) from year to year may be a sensitive and easily observable indicator of changes in the biosphere. We have analysed data from more than 30 years of observation in Europe, and found that spring events, such as leaf unfolding, have advanced by 6 days, whereas autumn events, such as leaf colouring, have been delayed by 4.8 days. This means that the average annual growing season has lengthened by 10.8 days since the early 1960s. These shifts can be attributed to changes in air temperature.
Although now over 100 years old, the classification of climate originally formulated by Wladimir Köppen and modified by his collaborators and successors, is still in widespread use. It is widely used in teaching school and undergraduate courses on climate. It is also still in regular use by researchers across a range of disciplines as a basis for climatic regionalisation of variables and for assessing the output of global climate models. Here we have produced a new global map of climate using the Köppen-Geiger system based on a large global data set of long-term monthly precipitation and temperature station time series. Climatic variables used in the Köppen-Geiger system were calculated at each station and interpolated between stations using a two-dimensional (latitude and longitude) thin-plate spline with tension onto a 0.1°×0.1° grid for each continent. We discuss some problems in dealing with sites that are not uniquely classified into one climate type by the Köppen-Geiger system and assess the outcomes on a continent by continent basis. Globally the most common climate type by land area is BWh (14.2%, Hot desert) followed by Aw (11.5%, Tropical savannah). The updated world Köppen-Geiger climate map is freely available electronically at http://www.hydrol-earth-syst-sci.net/????.
While changes in spring phenological events due to global warming have been widely documented, changes in autumn phenology, and therefore in growing season length, are less studied and poorly understood. However, it may be helpful to assess the potential lengthening of the growing season under climate warming in order to determine its further impact on forest productivity and C balance. The present study aimed to: (1) characterise the sensitivity of leaf phenological events to temperature, and (2) quantify the relative contributions of leaf unfolding and senescence to the extension of canopy duration with increasing temperature, in four deciduous tree species (Acer pseudoplatanus, Fagus sylvatica, Fraxinus excelsior and Quercus petraea). For 3 consecutive years, we monitored the spring and autumn phenology of 41 populations at elevations ranging from 100 to 1,600 m. Overall, we found significant altitudinal trends in leaf phenology and species-specific differences in temperature sensitivity. With increasing temperature, we recorded an advance in flushing from 1.9 ± 0.3 to 6.6 ± 0.4 days °C-1 (mean ± SD) and a 0 to 5.6 ± 0.6 days °C-1 delay in leaf senescence. Together both changes resulted in a 6.9 ± 1.0 to 13.0 ± 0.7 days °C-1 lengthening of canopy duration depending on species. For three of the four studied species, advances in flushing were the main factor responsible for lengthening canopy duration with increasing temperature, leading to a potentially larger gain in solar radiation than delays in leaf senescence. In contrast, for beech, we found a higher sensitivity to temperature in leaf senescence than in flushing, resulting in an equivalent contribution in solar radiation gain. These results suggest that climate warming will alter the C uptake period and forest productivity by lengthening canopy duration. Moreover, the between-species differences in phenological responses to temperature evidenced here could affect biotic interactions under climate warming.
R package for Data Analysis using multilevel/hierarchical model