- Leaf-out and flowering are two key phenological events of plants, denoting the respective onsets of visible vegetative growth and reproduction during the year. For each species, the schedule of vegetative growth and reproduction is crucial to the maximization of its fitness. Warming-induced advances of leaf-out and flowering have been reported frequently; however, it is unclear whether the responses of the two events are equal for any given species.
- Using long-term phenological records in Europe, we examined simultaneously the responses of both leaf-out and flowering of four common temperate tree species to climate warming and further examined the effects of winter chilling, spring forcing and photoperiod on the responses of the two events.
- We found that regardless whether flowering or leaf-out occurred first, the first event advanced more than the second during 1950–2013, resulting in a prolonged time interval between the two events. The temporal changes were also supported by a similar geographical trend that the time interval between the two events increased from cold to warm sites. Due to the warming-induced reduction in chilling, the spring forcing accumulated until the second event was increased more than the forcing accumulated until the first event, and that reduced the temperature sensitivity of the second event. In addition to the effect of chilling, the shorter photoperiod, associated with the advanced spring phenology, was also likely to substantially increase the spring forcing accumulated until the second event, which thus slowed down its advance, compared to the advance of the first event. The relative contributions of chilling and photoperiod to the increased forcing varied between species and events, with chilling mostly outweighing photoperiod.
- Synthesis. This study provides the large-scale empirical evidence of prolonged time interval between leaf-out and flowering with climate warming. The unequal advances of the two events may alter the partition of resources between vegetative growth and reproduction and cause different changes of spring frost damage to vegetative and reproductive tissues, which may alter species fitness and further affect ecosystem structure and function.
Warming-induced shifts in the timing of phenological events have been frequently reported in recent decades (Cleland et al., 2007; Fitter & Fitter, 2002; Parmesan & Yohe, 2003; Root et al., 2003; Sherry et al., 2007), which affect nearly all aspects of ecology and evolution in the ecosystems (e.g. species interactions, population dynamics; Forrest & Miller-Rushing, 2010). Many studies have reported species-specific phenological shifts in response to climate change (Forrest & Miller-Rushing, 2010; Renner & Zohner, 2018) and found that phenological timing in early-season species was more responsive to warming than that in late-season species (Menzel et al., 2006; Miller-Rushing & Primack, 2008). Efforts have also been devoted to studies addressing responses of different phenological phases to the warming, such as the widely reported advances in spring leaf unfolding and delays in autumn leaf coloration (Chen et al., 2019; Menzel & Fabian, 1999), and the unequal advances of flowering and fruit ripening (Haggerty & Galloway, 2011; Post et al., 2008). However, little attention has been devoted to examining whether leaf-out and flowering of a given species respond equally or differently to climate warming.
Leaf-out and flowering are two key phenological events of plants, denoting the respective onsets of visible vegetative and reproductive development during the year. Warming-induced changes in the timing of these two phenological events affect the ecosystem functioning and ecosystem services in different ways (Sherry et al., 2007). Shifts in the vegetative phenology have considerable consequences on processes of ecosystem functioning, such as carbon uptake (Piao et al., 2017), whereas changes in reproductive phenology generally alter population and community dynamics in the future generations, thus affecting evolutionary processes (Fitter & Fitter, 2002; Sherry et al., 2007). For example, changes in flowering time may disrupt plant–pollinator interactions, particularly when the pollinators are seasonal (e.g. insects), and reduce seed production of plants and food resources to the pollinators, thereby influencing the survival and success of both species (Fitter & Fitter, 2002; Memmott et al., 2007). Differences in the shifts of flowering time may affect gene flow between species, and alter competitive interactions during reproduction, potentially altering species composition of the community (Sherry et al., 2007).
Leaf-out and flowering of any given species have evolved to occur in a predetermined sequence (Hall, 2000). In many species, leaf-out occurs before flowering, whereas in others, especially in many wind-pollinated broad-leaved trees, flowering occurs before the vegetative development, as the developing leaves would prevent the dispersion of pollen (Loescher et al., 1990). The two sequences reflect different strategies in partitioning the limited resources, particularly the stored resources acquired in the previous growing season, to vegetative and reproductive development, as the physiologically active organs (e.g. leaves, flowers) compete for resources (Gougherty & Gougherty, 2018; Lieberman, 1982). Flower-before-leaf species rely on the stored resources to support the reproductive development before the leaves develop, whereas leaf-before-flower species can utilize both stored and newly synthesized resources simultaneously and thus may have greater access to resources for reproduction following the onset of photosynthesis in leaves (Gough et al., 2010). Although recent studies suggest that the association between the timing of leaf-out and flowering may be weak (Ettinger et al., 2018; Mulder & Spellman, 2019), changes in the time lag between the two events may affect the degree of separation of resources for vegetative growth and reproduction within trees (Singh & Kushwaha, 2005). For example, Maust et al. (1999) found that, in some cultivated fruit trees, the accelerated development of flower buds may delay and suppress the emergence of leaves and canopy establishment. As the species have optimized the allocation of resources towards the maximization of fitness under historical climates (Cody, 1966; Hegazy et al., 2005), the possibly altered resources allocation may affect the species fitness and further affect ecosystem structure and function (Doust, 1989; King & Roughgarden, 1982; Kozłowski, 1992).
Warming-induced shifts in the timing of leaf-out and flowering also alter the exposure of vulnerable leaves and flowers to late spring frosts (Cannell, 1985; Hänninen, 1991, 2006; Vitasse et al., 2014), respectively, affecting the growth and reproduction of plants (Inouye, 2000). It has been reported that the temporal changes in the risk of frost damage vary between species: the species whose phenology is especially responsive to warming are more prone to increased risk of spring frost damage than the less responsive ones (Ma et al., 2019). Similarly, the possibly unequal responses of leaf-out and flowering for a given species may cause different changes in the risk of frost damage to leaves and flowers, which affect the vegetative growth and reproduction to different degrees.
Temperature is the primary environmental factor affecting spring phenology in temperate plants (Menzel et al., 2006). Plants often require a certain exposure to chilling temperatures during winter to release endodormancy before the vegetative bud burst, or flowering, can be triggered by a sufficient exposure to forcing temperatures (i.e. the sum of temperatures above a specific threshold required to cause ontogenetic development towards the visible phenological events, such as bud burst or flowering, henceforth ‘forcing’; Coville, 1920; Hänninen, 2016). Additionally, the reduction of chilling in a warmer climate may cause a nonlinear increase in the forcing requirement, and thus slow down, or even reverse, the warming-induced advance of spring phenology (Ford et al., 2016; Fu, Zhao, et al., 2015; Murray et al., 1989). As climate warming affects the accumulation of both chilling and forcing, their interactive effects on the timing of leaf-out and flowering may be unequal and thus cause different responses of the two phenological events (Flynn & Wolkovich, 2018; Hänninen & Tanino, 2011).
In addition to temperature, photoperiod (daylength) may also limit the ability of temperate plants to respond to climate warming (Körner & Basler, 2010; Marchin et al., 2015; Way & Montgomery, 2015; Zohner et al., 2016; Zohner & Renner, 2015). Although photoperiod does not change with warming, plants experience shorter photoperiod prevailing at the earlier occurrence of the spring phenological events (Flynn & Wolkovich, 2018). The associated shorter photoperiod, by substantially increasing the forcing requirement, may reduce the temperature sensitivity of spring phenology (Flynn & Wolkovich, 2018; Fu, Piao, et al., 2019; Fu, Zhang, et al., 2019). By comparing warming-induced spring phenological differences among temperate trees, Geng et al. (2020) recently found that late-season species have a higher sensitivity to photoperiod shortage and a greater increase in forcing requirement than early-season species, leading to a relatively smaller advance in late-season species and increased interspecific time differences in spring phenology. This pattern found between early- and late-season species may be extended to early and late phenological events of a given species. That is, given the predetermined sequence of leaf-out and flowering in each species, we expect a greater photoperiod limitation in the late event than in the early event. In addition, the shorter photoperiod due to advanced phenology may have a larger influence on the forcing requirement of the late event, probably leading to unequal advances of the two events. Given these complicated and interactive effects of temperature (winter chilling and spring forcing) and photoperiod, we hypothesize that leaf-out and flowering of a given temperate tree species respond differently to a warming climate, which consequently alters the time interval between the two spring phenological events.
Using observations of first leaf date (FLD) and first flower date (FFD) of four common temperate tree species in Europe during 1950–2013, we aimed (a) to detect and quantify the temporal changes in FLD and FFD and the time interval between them and (b) to further elucidate the explanations behind the observed trends. For the second purpose, we compared the changes of winter chilling, spring forcing and photoperiod between the two phenological events, and further examined the effect of reduced chilling and shorter photoperiod on the spring forcing accumulated until the two events. To support the temporal changes observed during 1950–2013, we also examined in a similar way differences of the timing of FLD and FFD and climatic indices among sites representing a gradient from cold to warm sites.
2 MATERIALS AND METHODS
2.1 In situ phenology dataset and climate data
Phenology dataset was obtained from the Pan European Phenology (PEP) network (www.pep725.eu; Templ et al., 2018), which provides a free access to in situ phenology records of a variety of plants across Europe. As we studied simultaneously the responses of leaf-out and flowering to climate warming, we could select only species where both events were recorded. Only for four tree species in the PEP dataset, sufficiently long-term records over a large geographical region are available. Out of the four species, three are deciduous (Alnus glutinosa, Fraxinus excelsior and Aesculus hippocastanum) and one is evergreen (Pinus sylvestris). We used both FLD and FFD of these four temperate tree species during 1950–2013. For the three deciduous species, FLD was determined as the date when first leaves unfolded (denoted as BBCH code 11 in the PEP dataset) and for the evergreen P. sylvestris, the date when first leaves separated (BBCH code 10). FLD indicates the start of the visible vegetative development in each species. For all four species, FFD was determined as the beginning of flowering, which is denoted as BBCH code 60 in the PEP dataset.
For each species, the following screening criteria were applied: (a) For each site, we used observations only in those years when both FLD and FFD were recorded and (b) We kept in the dataset sites with more than 20 years of observations during the period 1950–2013. In most sites, observations were available for many more years. Alternative time thresholds of 30 and 40 years were also used to test the robustness of the result. The geographical distribution of the in situ phenological observation sites for each species is provided in Figure S1. For each species, the time interval between FLD and FFD per year at each site was calculated by subtracting the date of the first event from the date of the second event. Based on the records across all years and all sites, in A. hippocastanum and P. sylvestris, leaf-out was taken as the first and flowering as the second event so that the time interval was computed as FFD-FLD, while in A. glutinosa and F. excelsior, flowering was taken as the first and leaf-out as the second event so that the time interval was calculated is FLD-FFD. The mean time interval between FLD and FFD for each species was computed as the average of the time intervals between FLD and FFD across all years and all sites. To show the results of four species with different mean time intervals between FLD and FFD, the relative time interval was calculated for each species as the time interval between the two events divided by the mean time interval.
Daily temperature data from a gridded climate dataset E-OBS with a spatial resolution of 0.25° was used in this study (Cornes et al., 2018). Data in E-OBS are based on EU-FP6 project ENSEMBLES (http://ensembles-eu.metoffice.com) and the ECA&D project (http://www.ecad.eu; Haylock et al., 2008). To better capture temperature variation in each site, in particular in the mountain areas, temperature data were adjusted using elevation difference between the site and the climate grid cell, based on a temperature lapse rate of 6.4°C/km (Olsson & Jönsson, 2014).
2.2 Temporal changes in FLD, FFD and the time interval between FLD and FFD
2.3 Temporal changes in winter chilling, spring forcing and photoperiod for FLD and FFD
For each species, LMMs (Equation 1), including phenological site as a random effect, were used to compute long-term changing rates of winter chilling, spring forcing and photoperiod for FLD and FFD. Alternatively, linear regressions were also used to examine the temporal changes of yearly mean values of three climatic indices across all studied sites and very similar results were obtained.
2.4 The influence of winter chilling and photoperiod on spring forcing
To examine the influence of the warming-induced reduction of chilling on the spring forcing, linear regression between yearly mean values of winter chilling and spring forcing was performed separately for FLD and FFD in each species. For FLD and FFD separately in each species, we also divided the data into three subsets, based on the photoperiod conditions prevailing at the corresponding phenological date: short (<1st quantile of photoperiod), medium (between 1st and 3rd quantiles) and long (>3rd quantile) photoperiod, and further checked the influence of chilling on spring forcing under three different photoperiod conditions. An analysis analogous to the one described above was carried out to check the effect of shorter photoperiod on the spring forcing, both for all data and for three subsets of different chilling conditions: low (<1st quantile of chilling), medium (between 1st and 3rd quantiles) and high (>3rd quantile) chilling. In addition, the relative influence of winter chilling and photoperiod on the spring forcing was further calculated to assess their relative contributions to the changes of spring forcing accumulated until FLD and FFD in each species (Grömping, 2006).
2.5 Differences of the phenological and climatic indices among sites representing a gradient from cold to warm sites
An analysis analogous to the one described above for the temporal changes was carried out geographically by comparing sites forming a temperature gradient from cold to warm sites. For each species, LMMs (Equation 1), including phenological site as a random effect, were used to compute differences of FLD and FFD, and of the winter chilling, spring forcing and photoperiod among sites with different site temperatures. Site temperature was calculated for each phenological observation site as the average of the mean annual temperatures across all years providing phenological observations. It summarizes the local climate of the sites and roughly captures the thermal conditions occurring during phenological development, thus representing spatial variation of climate among sites (Ma et al., 2018; Rossi et al., 2016). For the analysis in relation to site temperature, sites with extremely high or low temperatures (out of 99% quartile range) were excluded due to the small number of such sites.
3.1 Temporal changes of FLD, FFD and time interval between FLD and FFD
Both FLD and FFD significantly advanced during 1950–2013, with the shifting rate ranging from −1.4 to −3.8 days/decade (Table 1). In the two flower-before-leaf species (A. glutinosa and F. excelsior), FFD advanced more than FLD, while in the two leaf-before-flower species (A. hippocastanum and P. sylvestris), FLD was more responsive than FFD (Table 1; Figure S2). Thus, in all species, regardless whether flowering or leaf-out occurred first, the first event advanced more than the second event. Consequently, the time interval between the two events prolonged during 1950–2013 (Figure 1), with the rate varying from 0.6 to 1.3 days/decades (Table 1). The above results were based on phenological records at sites with time series longer than 20 years. We also carried out a robust analysis using smaller datasets with alterative time thresholds of 30 and 40 years. Regardless of the time threshold used, the prolonged time interval between leaf-out and flowering was always observed (Figure S3).
|Species||#obs||#sites||First leaf date (FLD)||First flower date (FFD)||Time interval of FLD and FFD (days)|
|Mean DOY||Rate (days/decade)||Response (days/°C)||Mean DOY||Rate (days/decade)||Response (days/°C)||Mean||Rate (days/decade)||Response (days/°C)|
|Aesculus hippocastanum||105,002||3,023||111 ± 11||−2.03 ± 0.02*||−5.29 ± 0.09*||130 ± 10||−1.44 ± 0.02*||−4.95 ± 0.07*||19 ± 9||0.58 ± 0.02*||0.34 ± 0.07*|
|Pinus sylvestris||39,262||1,331||131 ± 11||−2.38 ± 0.04*||−3.61 ± 0.16*||138 ± 10||−1.47 ± 0.03*||−2.88 ± 0.12*||7 ± 10||0.90 ± 0.04*||0.73 ± 0.15*|
|Alnus glutinosa||44,642||1,457||110 ± 13||−2.42 ± 0.04*||−4.74 ± 0.17*||74 ± 21||−3.75 ± 0.07*||−7.40 ± 0.27*||36 ± 19||1.33 ± 0.06*||2.65 ± 0.28*|
|Fraxinus excelsior||42,583||1,400||129 ± 10||−1.89 ± 0.03*||−4.24 ± 0.13*||118 ± 13||−2.98 ± 0.04*||−5.07 ± 0.18*||11 ± 11||1.09 ± 0.04*||0.83 ± 0.16*|
- * Denotes significance at p = 0.01. SD (standard deviation) of the mean value and SE (standard error) of the rate or the response value derived from LMMs are provided.
3.2 Temporal changes of winter chilling, spring forcing and photoperiod for FLD and FFD
In all species, the winter chilling accumulated for FLD and FFD reduced almost at the same rate during 1950–2013 (Figure 2a; Table S1). In the two leaf-before-flower species (A. hippocastanum and P. sylvestris), increased forcing was observed for both FLD and FFD, and the rate of increase was much higher in the second than in the first event (Figure 2b; Table S1). In the two flower-before-leaf species (A. glutinosa and F. excelsior), the second event FLD had increased forcing, but the first event FFD even had a slight decrease in forcing during the examined time period (Figure 2b; Table S1). Thus, in all four species, the increase in forcing was greater in the second event than in the first event during 1950–2013. With the advances of FLD and FFD, all species experienced the reduction in photoperiod for both events during 1950–2013 (Figure 2c). Moreover, in all species, due to the unequal advances of the two phenological events, the reduction of photoperiod in the first event was larger than that in second event (Figure 2c; Table S1).
3.3 The influence of winter chilling and photoperiod on spring forcing
In all species, as winter chilling reduced under climate warming, the spring forcing accumulated until both FFD and FLD increased, but the increasing rate of spring forcing was higher in the second event than in the first event (Figure 3a; Table S2). Similar results were observed for three subsets of the data with short, medium and long photoperiod conditions (Figure S4).
A negative correlation between photoperiod and spring forcing was found for both FFD and FLD of all species (Figure 3b). However, with the reduction of photoperiod, the increase in spring forcing was higher in the second than in the first event in most species, except A. hippocastanum (Figure 3b; Table S2). Similar results were observed for three subsets of the data with low, medium and high chilling conditions (Figure S5).
The relative influence of chilling and photoperiod to spring forcing differed among the two events and among the studied species. In most cases, chilling had a larger contribution to increased spring forcing than photoperiod, whereas in FFD of P. sylvestris and A. glutinosa, photoperiod played a greater role than chilling (Figure 4).
3.4 Differences of the phenological and climatic indices among sites representing a gradient from cold to warm sites
During 1950–2013, site temperature across the whole study area varied from 6.2 to 11.0°C, with an average of 8.9°C (Figure 5). Both FLD and FFD significantly advanced with increasing site temperature, with a response varying from −2.9 to −7.4 days/°C (Table 1; Figure S6). In all species, the first event responded to the site temperature more than the second event. Accordingly, the time interval between the two events lengthened with increasing site temperature at a response varying from 0.3 to 2.7 days/°C (Figure 5; Table 1).
With the increasing site temperatures, the winter chilling of both FFD and FLD decreased, the response to site temperature being almost the same for the two events (Figure S7a; Table S3). The spring forcing of FFD and FLD of all four species increased with site temperature (Figure S7b; Table S3). However, the increase in forcing was in all species higher in the second than in the first event, regardless whether FLD or FFD occurred first. The reduction of photoperiod in the first event was larger than that in the second event from cold to warm sites (Figure S7c; Table S3).
Although advances of both leaf-out and flowering of plants have been extensively reported (Cleland et al., 2007; Fitter & Fitter, 2002; Parmesan & Yohe, 2003; Root et al., 2003; Sherry et al., 2007), it is unclear whether the advances of the two events of a given species are equal. By simultaneously analysing the responses of both leaf-out and flowering timing of four tree species over time and space, we found that although both events advanced with elevated temperature, their advances were not equal. Rather, the first event was more responsive to warming climate than the second one, regardless whether flowering or leaf-out occurred first. Consequently, the time interval between leaf-out and flowering prolonged during 1950–2013, at a rate of 0.6–1.3 days/decades. Geographically, the time interval between the two phenological events enlarged from cold to warm sites, the response being 0.3–2.7 days/°C. The findings of the geographical analysis thus further support our results concerning the temporal changes. Additionally, the prolonged time interval was also accompanied by the reduced variability (increased synchrony) among populations of both leaf-out and flowering in the four examined species (Ma et al., 2018), further supporting the separation in time of the two events with climate warming. Due to limited data availability as described in the Section 2, only four species were examined in the present study. However, these four species included both flower-before-leaf and leaf-before-flower species, both deciduous and evergreen species, and both early- and late-season species, which could therefore reflect the responses of a variety of temperate tree species.
The schedule of vegetative growth and reproductive development is crucial to the maximization of species fitness (Doust, 1989; Kozłowski, 1992). Under historical climates, each species has evolved an optimal timing of both vegetative and reproductive phenology to enhance its fitness (Richardson et al., 2018). The prolonged time interval between leaf-out and flowering indicates an increasing time lag between the onset of vegetative growth and reproductive development with elevated temperature. The rates of time lag increase were in the present study moderate (0.58–1.33 days/decades). However, the time lag tends to increase further with continued warming, which probably affects the transfer and allocation of resources (e.g. carbohydrates, nutrients and water) between vegetative growth and reproduction (Kozłowski, 1992). In flower-before-leaf species, more stored resources might be devoted to support the flowering and subsequent reproductive development before the leaves develop (Gougherty & Gougherty, 2018). This may accelerate the development of fruit sets and delay vegetative development, resulting in low leaf/fruit ratios, as reported in cultivated fruit trees that flowering occurs before leaf-out (Maust et al., 1999). However, Bolmgren and Cowan (2008) found no relationship between flowering time and seed mass or plant height in woody species, and suggested that the stored resources may allow the decoupling of vegetative growth and reproduction. These inconsistent findings are probably because plants’ ‘decisions’ on resources storage and expenditure are complex and often include substantial time lags. In particular, perennial species allocate resources to growth and reproduction not only within the growing season but also between growing seasons (Johansson et al., 2013). This complicates the effect of shifted phenology on resources allocation within plants. In the case of leaf-before-flower species, more resources can be accumulated during the vegetative growth to better support the subsequent reproduction, thereby benefiting size and quality of fruits and seeds (Williamson et al., 2002). However, due to the time lags between resource availability and investment in reproduction and growth, it is also possible that resources are more completely devoted to vegetative growth (e.g. shoot, root) rather than reproduction. While this study focused on the response of timing of leaf-out and flowering and the underlying mechanisms, we call for further studies that simultaneously monitor the timing of phenological events and the allocation of resources within plants to better evaluate the consequences of altered phenology under climate warming.
The advanced leaf-out and flowering implies the possibly increased susceptibility of both newly developed leaves and flowers to spring frost damage (Augspurger, 2013; Liu et al., 2018; Ma et al., 2019). However, the greater advancing rates of the first event observed in all species suggest that the first event is more likely to have increased risk of frost damage than the second one (Ma et al., 2019). In flower-before-leaf species, warming increases the risk of frost damages more in reproductive than in vegetative tissues. These species would suffer losses of seed production, but not that much direct loss of carbon gain. In leaf-before-flower species, the situation would be reversed. It is possible that seed production is also reduced due to a severe loss of carbon uptake. These changes may affect the growth, survival and fitness of species, which may ultimately alter the structure and function of terrestrial ecosystems (Inouye, 2000; King & Roughgarden, 1982; Kozłowski, 1992).
The unequal advances of the two spring phenological events are partly attributable to warming-induced changes in winter chilling and spring forcing. Consistent with previous studies (Cannell & Smith, 1983; Fu, Piao, et al., 2015), we observed that under the reduction of winter chilling, spring forcing accumulated until the two events increased in all studied species. However, in all species, the increase in forcing was much greater in the second than in the first event (Figure 2b), indicating that the forcing needed for the second event was more sensitive to the reduced chilling than that for the first event (Figure 3a; Figure S4). This is also consistent with the nonlinear response of spring phenology to increased temperature, as reported in previous studies (Ford et al., 2016; Fu, Zhao, et al., 2015; Ma et al., 2018; Pope et al., 2013). The temporal changes were further supported by the similar geographical trend that the increase in forcing was higher in the second than in the first event as the chilling reduced from cold to warm sites (Figure S7; Table S3). Our results suggest that the second event has a higher chilling requirement, and thus the forcing was largely elevated when the chilling became inadequate. Consequently, a larger increase in forcing in the second event greatly counteracted the accelerating effect of warming so that the acceleration of second event caused by warming was less than that of the first event.
In addition to the effect of winter chilling, photoperiod is likely another environmental factor causing the unequal increases in spring forcing in two events. In agreement with previous studies (Flynn & Wolkovich, 2018; Fu, Piao, et al., 2019; Fu, Zhang, et al., 2019), the shorter photoperiod due to earlier spring phenology tended to increase the spring forcing of both leaf-out and flowering (Figure 3b). Except A. hippocastanum, the first event experienced a larger reduction in photoperiod but a lower increase in forcing, whereas the second event had a smaller reduction in photoperiod but a greater increase in forcing (Figure 3b; Table S2). Thus, in addition to the effect of reduced chilling, the influence of shorter photoperiod on the forcing accumulation was also larger in the second event, and therefore its advance with warming was reduced, as compared with the advance of the first event.
Although both reduced chilling and shorter photoperiod tended to increase the forcing of the two spring phenological events, their relative contributions to the increased forcing varied between species and phenological events (Figure 4). Generally, chilling outweighs photoperiod in increasing forcing and thus preventing too early development of two phenological events (Laube et al., 2014). However, the relative contributions of chilling and photoperiod to forcing had no consistent tendency between the first and the second events (Figure 4). As all climatic indices co-varied in the observational data, further temperature- and photoperiod-manipulation experiments are needed to better clarify and evaluate the independent and interactive effects of different climatic factors on the uneven advances of the two phenological events observed in the present study (Hänninen et al., 2019).
In this study, winter chilling and spring forcing were used to explain the different responses of leaf-out and flowering. Unfortunately, the experimental evidence for the details of chilling and forcing, such as temperature responses of chilling and forcing, and the time windows for chilling and forcing, remains extremely scarce for any given tree species and provenance (Hänninen, 2016; Hänninen et al., 2019). In the present study, the calculation of winter chilling and spring forcing followed Weinberger (1950), Cannell and Smith (1983), Murray et al. (1989), Hänninen (1990) and Fu, Zhao, et al. (2015); see Section 2). Similar to earlier studies examining long-term observational phenological records (Chen et al., 2019; Fu, Piao, et al., 2015; Fu, Zhao, et al., 2015; Ma et al., 2018), chilling and forcing in the present study should be considered as rough climatic indices approximating the climatic effects on the underlying ecophysiological phenomena, and correlating with the phenological timing in spring; rather than strict ecophysiological model variables (Chuine et al., 2013; Hänninen & Kramer, 2007) addressing the phenomena explicitly.
In all species, the spring forcing for leaf-out increased over time, in agreement with Fu, Piao, et al. (2015), whereas divergent changes in forcing for flowering were observed. The forcing needed for flowering increased in those species where flowering is the second event and decreased slightly in species where flowering is the first event (Figure 2b). In the first case, the changes of forcing required counteracted the accelerating effect of warming, whereas in the second case, the changes of forcing caused a further acceleration. Our results suggested that unlike leaf-out, the forcing required for flowering might not increase with climate warming in temperate woody species. However, further studies on more species are needed to examine whether this pattern generally exists in temperate tree species. Our results also implied the complexity of the responses of flowering phenology to warming temperatures. Previous studies (Chen et al., 2019; Fu, Piao, et al., 2015; Fu, Zhao, et al., 2015; Ma et al., 2018), as well as this one, typically focused on the effect of temperature in months prior to flowering (winter chilling and spring forcing) on the timing of flowering. Diggle and Mulder (2019) reported that temperature could affect flowering by altering development of buds in the year(s) prior to flowering. This suggested that temperature over the entire multi-year course of flower development needs to be examined to improve our understanding of the responses of flowering to warming temperatures.
A better understanding of long-term phenological responses of trees to climate warming is a prerequisite for assessing and predicting the impacts of climate warming on forest ecosystems (Forrest & Miller-Rushing, 2010). Our finding of unequal responses of leaf-out and flowering and the prolonged time interval between the two events deepens our understanding of how climate change impacts species-level phenology. Our findings may also be one manifestation of the mechanisms how climate warming causes profound changes in species fitness, distribution and co-evolution in temperate terrestrial ecosystems.
This project was funded by National Natural Science Foundation of China (31971499, 31600392, 41661144007 and 41861124001), Natural Science Foundation of Guangdong Province (2016A030310013, 2019B121202007) and the International Collaborative Key Project of the CAS (GJHZ1752). The authors acknowledge all members of the PEP725 network for collecting and providing the phenological data. The authors also acknowledge the E-OBS dataset from the EU-FP6 project ENSEMBLES (http://ensembles-eu.metoffice.com) and the data providers in the ECA&D project (http://www.ecad.eu).
J.-G.H., Q.M. and H.H. designed the study; Q.M. performed the analysis and wrote the manuscript with assistance from J.-G.H., H.H., X.L. and F.B. All authors discussed and commented on the manuscript.
The peer review history for this article is available at https://publons.com/publon/10.1111/1365-2745.13558.
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- 2013). Reconstructing patterns of temperature, phenology, and frost damage over 124 years: Spring damage risk is increasing. Ecology, 94, 41–50.
- 2014). Fitting linear mixed-effects models using lme4. arXiv Preprint arXiv:1406.5823.
- 2008). Time–size tradeoffs: A phylogenetic comparative study of flowering time, plant height and seed mass in a north-temperate flora. Oikos, 117, 424–429.
- 1985). Analysis of risks of frost damage to forest trees in Britain. In P. M. A. Tigerstedt, P. Puttonen, & V. Koski (Eds.), Crop physiology of forest trees, (pp. 153–166). Helsinki University Press.
- 1983). Thermal time, chill days and prediction of budburst in Picea sitchensis. Journal of Applied Ecology, 20, 951–963.
- 2019). Long-term changes in the impacts of global warming on leaf phenology of four temperate tree species. Global Change Biology, 25, 997–1004.
- 2013). Plant development models. In M. D. Schwartz (Ed.), Phenology: An integrative environmental science ( 2nd ed., pp. 275–293). Springer.
- 2007). Shifting plant phenology in response to global change. Trends in Ecology & Evolution, 22, 357–365.
- 1966). A general theory of clutch size. Evolution, 20, 174–184.
- 2018). An ensemble version of the E-OBS temperature and precipitation data sets. Journal of Geophysical Research: Atmospheres, 123, 9391–9409.
- 1920). The influence of cold in stimulating the growth of plants. Proceedings of the National Academy of Sciences of the United States of America, 6, 434–435.
- 2019). Diverse developmental responses to warming temperatures underlie changes in flowering phenologies. Integrative and Comparative Biology, 59, 559–570.
- 1989). Plant reproductive strategies and resource allocation. Trends in Ecology & Evolution, 4, 230–234.
- 2018). Phenological sequences: How early-season events define those that follow. American Journal of Botany, 105, 1771–1780.
- 2002). Rapid changes in flowering time in British plants. Science, 296, 1689–1691.
- 2018). Temperature and photoperiod drive spring phenology across all species in a temperate forest community. New Phytologist, 219, 1353–1362.
- 2016). Will changes in phenology track climate change? A study of growth initiation timing in coast Douglas-fir. Global Change Biology, 22, 3712–3723.
- 2010). Toward a synthetic understanding of the role of phenology in ecology and evolution. Philosophical Transactions of the Royal Society B: Biological Sciences, 365, 1301–3112.
- 2015). Increased heat requirement for leaf flushing in temperate woody species over 1980–2012: Effects of chilling, precipitation and insolation. Global Change Biology, 21, 2687–2697.
- 2019). Short photoperiod reduces the temperature sensitivity of leaf-out in saplings of Fagus sylvatica but not in horse chestnut. Global Change Biology, 25, 1696–1703.
- 2019). Daylength helps temperate deciduous trees to leaf-out at the optimal time. Global Change Biology, 25, 2410–2418.
- 2015). Declining global warming effects on the phenology of spring leaf unfolding. Nature, 526, 104–107.
- 2020). Climate warming increases spring phenological differences among temperate trees. Global Change Biology, 26, 5979–5987.
- 2010). Phenological and temperature controls on the temporal non-structural carbohydrate dynamics of Populus grandidentata and Quercus rubra. Forests, 1, 65–81.
- 2018). Sequence of flower and leaf emergence in deciduous trees is linked to ecological traits, phylogenetics, and climate. New Phytologist, 220, 121–131.
- 2006). Relative importance for linear regression in R: The package relaimpo. Journal of Statistical Software, 17, 1–27.
- 2011). Response of individual components of reproductive phenology to growing season length in a monocarpic herb. Journal of Ecology, 99, 242–253. https://doi.org/10.1111/j.1365-2745.2010.01744.x
- 2000). Evo-devo or devo-evo – Does it matter? Evolution & Development, 2, 177–178.
- 1990). Modelling bud dormancy release in trees from cool and temperate regions. Acta Forestalia Fennica, 213, 1–47.
- 1991). Does climatic warming increase the risk of frost damage in northern trees? Plant, Cell & Environment, 14, 449–454.
- 2006). Climate warming and the risk of frost damage to boreal forest trees: Identification of critical ecophysiological traits. Tree Physiology, 26, 889–898.
- 2016). Boreal and temperate trees in a changing climate: Modelling the ecophysiology of seasonality. Springer.
- 2007). A framework for modelling the annual cycle of trees in boreal and temperate regions. Silva Fennica, 41, 167–205. https://doi.org/10.14214/sf.313
- 2019). Experiments are necessary in process-based tree phenology modelling. Trends in Plant Science, 24, 199–209. https://doi.org/10.1016/j.tplants.2018.11.006
- 2011). Tree seasonality in a warming climate. Trends in Plant Science, 16, 412–416. https://doi.org/10.1016/j.tplants.2011.05.001
- 2008). A European daily high-resolution gridded data set of surface temperature and precipitation for 1950–2006. Journal of Geophysical Research: Atmospheres, 113(D20), 1950–2006. https://doi.org/10.1029/2008JD010201
- 2005). Growth and phenology of eight common weed species. Journal of Arid Environments, 61, 171–183. https://doi.org/10.1016/j.jaridenv.2004.07.005
- 2000). The ecological and evolutionary significance of frost in the context of climate change. Ecology Letters, 3, 457–463. https://doi.org/10.1046/j.1461-0248.2000.00165.x
- 2013). Climate change and the optimal flowering time of annual plants in seasonal environments. Global Change Biology, 19, 197–207. https://doi.org/10.1111/gcb.12006
- 1982). Graded allocation between vegetative and reproductive growth for annual plants in growing seasons of random length. Theoretical Population Biology, 22, 1–16. https://doi.org/10.1016/0040-5809(82)90032-6
- 2010). Phenology under global warming. Science, 327, 1461–1462. https://doi.org/10.1126/science.1186473
- 1992). Optimal allocation of resources to growth and reproduction: Implications for age and size at maturity. Trends in Ecology & Evolution, 7, 15–19. https://doi.org/10.1016/0169-5347(92)90192-E
- 2014). Chilling outweighs photoperiod in preventing precocious spring development. Global Change Biology, 20, 170–182. https://doi.org/10.1111/gcb.12360
- 1982). Seasonality and phenology in a dry tropical forest in Ghana. Journal of Ecology, 791–806. https://doi.org/10.2307/2260105
- 2018). Extension of the growing season increases vegetation exposure to frost. Nature Communications, 9, 426. https://doi.org/10.1038/s41467-017-02690-y
- 1990). Carbohydrate reserves, translocation, and storage in woody plant roots. HortScience, 25, 274–281. https://doi.org/10.21273/HORTSCI.25.3.274
- 2018). Reduced geographical variability in spring phenology of temperate trees with recent warming. Agricultural and Forest Meteorology, 256, 526–533. https://doi.org/10.1016/j.agrformet.2018.04.012
- 2019). Divergent trends in the risk of spring frost damage to trees in Europe with recent warming. Global Change Biology, 25, 351–360. https://doi.org/10.1111/gcb.14479
- 2020). Data from: Climate warming prolongs the time interval between leaf-out and flowering in temperate trees: Effects of chilling, forcing and photoperiod. Dryad Digital Repository, https://doi.org/10.5061/dryad.jdfn2z391
- 2015). Temperature alone does not explain phenological variation of diverse temperate plants under experimental warming. Global Change Biology, 21, 3138–3151. https://doi.org/10.1111/gcb.12919
- 1999). Flower bud density affects vegetative and fruit development in field-grown southern highbush blueberry. HortScience, 34, 607–610. https://doi.org/10.21273/HORTSCI.34.4.607
- 2007). Global warming and the disruption of plant–pollinator interactions. Ecology Letters, 10, 710–717. https://doi.org/10.1111/j.1461-0248.2007.01061.x
- 1999). Growing season extended in Europe. Nature, 397, 659. https://doi.org/10.1038/17709
- 2006). European phenological response to climate change matches the warming pattern. Global Change Biology, 12, 1969–1976. https://doi.org/10.1111/j.1365-2486.2006.01193.x
- 2008). Global warming and flowering times in Thoreau's concord: A community perspective. Ecology, 89, 332–341. https://doi.org/10.1890/07-0068.1
- 2019). Do longer growing seasons give introduced plants an advantage over native plants in Interior Alaska? Botany-Botanique, 97, 347–362. https://doi.org/10.1139/cjb-2018-0209
- 1989). Date of budburst of fifteen tree species in Britain following climatic warming. Journal of Applied Ecology, 26(2), 693–700. https://doi.org/10.2307/2404093
- 2014). Process-based models not always better than empirical models for simulating budburst of Norway spruce and birch in Europe. Global Change Biology, 20, 3492–3507. https://doi.org/10.1111/gcb.12593
- 2003). A globally coherent fingerprint of climate change impacts across natural systems. Nature, 421, 37–42. https://doi.org/10.1038/nature01286
- 2017). Weakening temperature control on the interannual variations of spring carbon uptake across northern lands. Nature Climate Change, 7, 359. https://doi.org/10.1038/nclimate3277
- 2013). Detecting nonlinear response of spring phenology to climate change by Bayesian analysis. Global Change Biology, 19, 1518–1525. https://doi.org/10.1111/gcb.12130
- 2008). Phenological sequences reveal aggregate life history response to climatic warming. Ecology, 89, 363–370. https://doi.org/10.1890/06-2138.1
- R Development Core Team. (2018). R: A language and environment for statistical computing. R Foundation for Statistical Computing.
- 2018). Climate change and phenological mismatch in trophic interactions among plants, insects, and vertebrates. Annual Review of Ecology, Evolution, and Systematics, 49, 165–182. https://doi.org/10.1146/annurev-ecolsys-110617-062535
- 2018). Ecosystem warming extends vegetation activity but heightens vulnerability to cold temperatures. Nature, 560, 368. https://doi.org/10.1038/s41586-018-0399-1
- 2003). Fingerprints of global warming on wild animals and plants. Nature, 421, 57–60. https://doi.org/10.1038/nature01333
- 2016). Pattern of xylem phenology in conifers of cold ecosystems at the Northern Hemisphere. Global Change Biology, 22, 3804–3813. https://doi.org/10.1111/gcb.13317
- 2007). Divergence of reproductive phenology under climate warming. Proceedings of the National Academy of Sciences of the United States of America, 104, 198–202. https://doi.org/10.1073/pnas.0605642104
- 2005). Diversity of flowering and fruiting phenology of trees in a tropical deciduous forest in India. Annals of Botany, 97, 265–276. https://doi.org/10.1093/aob/mcj028
- 2018). Pan European Phenological database (PEP725): A single point of access for European data. International Journal of Biometeorology, 62(6), 1109–1113. https://doi.org/10.1007/s00484-018-1512-8
- 2014). The interaction between freezing tolerance and phenology in temperate deciduous trees. Frontiers in Plant Science, 5, 541. https://doi.org/10.3389/fpls.2014.00541
- 2015). Photoperiod constraints on tree phenology, performance and migration in a warming world. Plant, Cell & Environment, 38, 1725–1736. https://doi.org/10.1111/pce.12431
- 1950). Chilling requirements of peach varieties. Proceedings of the American Society for Horticultural Science, 56, 122–128.
- 2002). Hydrogen cyanamide accelerates vegetative budbreak and shortens fruit development period of blueberry. HortScience, 37, 539–542. https://doi.org/10.21273/HORTSCI.37.3.539
- 2001). mgcv: GAMs and generalized ridge regression for R. R News, 1, 20–25.
- 2016). Day length unlikely to constrain climate-driven shifts in leaf-out times of northern woody plants. Nature Climate Change, 6, 1120. https://doi.org/10.1038/nclimate3138
- 2015). Perception of photoperiod in individual buds of mature trees regulates leaf-out. New Phytologist, 208, 1023–1030. https://doi.org/10.1111/nph.13510