Detecting nonlinear response of spring phenology to climate change by Bayesian analysis

The impact of climate change on the advancement of plant phenological events has been heavily studied in the last decade. Although the majority of spring plant phenological events have been trending earlier, this is not universally true. Recent work has suggested that species that are not advancing in their spring phenological behavior are responding more to lack of winter chill than increased spring heat. One way to test this hypothesis is by evaluating the behavior of a species known to have a moderate to high chilling requirement and examining how it is responding to increased warming. This study used a 60‐year data set for timing of leaf‐out and male flowering of walnut (Juglans regia) cultivar ‘Payne’ to examine this issue. The spring phenological behavior of ‘Payne’ walnut differed depending on bud type. The vegetative buds, which have a higher chilling requirement, trended toward earlier leaf‐out until about 1994, when they shifted to later leaf‐out. The date of male bud pollen shedding advanced over the course of the whole record. Our findings suggest that many species which have exhibited earlier bud break are responding to warmer spring temperatures, but may shift into responding more to winter temperatures (lack of adequate chilling) as warming continues.     

Chilling and heat requirements for leaf unfolding in European beech and sessile oak populations at the southern limit of their distribution range

With global warming, an advance in spring leaf phenology has been reported worldwide. However, it is difficult to forecast phenology for a given species, due to a lack of knowledge about chilling requirements. We quantified chilling and heat requirements for leaf unfolding in two European tree species and investigated their relative contributions to phenological variations between and within populations. We used an extensive database containing information about the leaf phenology of 14 oak and 10 beech populations monitored over elevation gradients since 2005. In parallel, we studied the various bud dormancy phases, in controlled conditions, by regularly sampling low- and high-elevation populations during fall and winter. Oak was 2.3 times more sensitive to temperature for leaf unfolding over the elevation gradient and had a lower chilling requirement for dormancy release than beech. We found that chilling is currently insufficient for the full release of dormancy, for both species, at the lowest elevations in the area studied. Genetic variation in leaf unfolding timing between and within oak populations was probably due to differences in heat requirement rather than differences in chilling requirement. Our results demonstrate the importance of chilling for leaf unfolding in forest trees and indicate that the advance in leaf unfolding phenology with increasing temperature will probably be less pronounced than forecasted. This highlights the urgent need to determine experimentally the interactions between chilling and heat requirements in forest tree species, to improve our understanding and modeling of changes in phenological timing under global warming.     

Chilling outweighs photoperiod in preventing precocious spring development

It is well known that increased spring temperatures cause earlier onset dates of leaf unfolding and flowering. However, a temperature increase in winter may be associated with delayed development when species' chilling requirements are not fulfilled. Furthermore, photosensitivity is supposed to interfere with temperature triggers. To date, neither the relative importance nor possible interactions of these three factors have been elucidated. In this study, we present a multispecies climate chamber experiment to test the effects of chilling and photoperiod on the spring phenology of 36 woody species. Several hypotheses regarding their variation with species traits (successional strategy, floristic status, climate of their native range) were tested. Long photoperiods advanced budburst for one‐third of the studied species, but magnitudes of these effects were generally minor. In contrast to prior hypotheses, photosensitive responses were not restricted to climax or oceanic species. Increased chilling length advanced budburst for almost all species; its effect greatly exceeding that of photoperiod. Moreover, we suggest that photosensitivity and chilling effects have to be rigorously disentangled, as the response to photoperiod was restricted to individuals that had not been fully chilled. The results indicate that temperature requirements and successional strategy are linked, with climax species having higher chilling and forcing requirements than pioneer species. Temperature requirements of invasive species closely matched those of native species, suggesting that high phenological concordance is a prerequisite for successful establishment. Lack of chilling not only led to a considerable delay in budburst but also caused substantial changes in the chronological order of species' budburst. The results reveal that increased winter temperatures might impact forest ecosystems more than formerly assumed. Species with lower chilling requirements, such as pioneer or invasive species, might profit from warming winters, if late spring frost events would in parallel occur earlier.     

Climate warming increases spring phenological differences among temperate trees

Climate warming has substantially advanced spring leaf flushing, but winter chilling and photoperiod co‐determine the leaf flushing process in ways that vary among species. As a result, the interspecific differences in spring phenology (IDSP) are expected to change with climate warming, which may, in turn, induce negative or positive ecological consequences. However, the temporal change of IDSP at large spatiotemporal scales remains unclear. In this study, we analyzed long‐term in‐situ observations (1951–2016) of six, coexisting temperate tree species from 305 sites across Central Europe and found that phenological ranking did not change when comparing the rapidly warming period 1984–2016 to the marginally warming period 1951–1983. However, the advance of leaf flushing was significantly larger in early‐flushing species EFS (6.7 ± 0.3 days) than in late‐flushing species LFS (5.9 ± 0.2 days) between the two periods, indicating extended IDSP. This IDSP extension could not be explained by differences in temperature sensitivity between EFS and LFS; however, climatic warming‐induced heat accumulation effects on leaf flushing, which were linked to a greater heat requirement and higher photoperiod sensitivity in LFS, drove the shifts in IDSP. Continued climate warming is expected to further extend IDSP across temperate trees, with associated implications for ecosystem function.     

Daylength helps temperate deciduous trees to leaf‐out at the optimal time

Global warming has led to substantially earlier spring leaf‐out in temperate‐zone deciduous trees. The interactive effects of temperature and daylength underlying this warming response remain unclear. However, they need to be accurately represented by earth system models to improve projections of the carbon and energy balances of temperate forests and the associated feedbacks to the Earth's climate system. We studied the control of leaf‐out by daylength and temperature using data from six tree species across 2,377 European phenological network ( www.pep725.eu ), each with at least 30 years of observations. We found that, in addition to and independent of the known effect of chilling, daylength correlates negatively with the heat requirement for leaf‐out in all studied species. In warm springs when leaf‐out is early, days are short and the heat requirement is higher than in an average spring, which mitigates the warming‐induced advancement of leaf‐out and protects the tree against precocious leaf‐out and the associated risks of late frosts. In contrast, longer‐than‐average daylength (in cold springs when leaf‐out is late) reduces the heat requirement for leaf‐out, ensuring that trees do not leaf‐out too late and miss out on large amounts of solar energy. These results provide the first large‐scale empirical evidence of a widespread daylength effect on the temperature sensitivity of leaf‐out phenology in temperate deciduous trees.     

From observations to experiments in phenology research: investigating climate change impacts on trees and shrubs using dormant twigs

Background and Aims Climate change is advancing the leaf-out times of many plant species and mostly extending the growing season in temperate ecosystems. Laboratory experiments using twig cuttings from woody plant species present an affordable, easily replicated approach to investigate the relative importance of factors such as winter chilling, photoperiod, spring warming and frost tolerance on the leafing-out times of plant communities. This Viewpoint article demonstrates how the results of these experiments deepen our understanding beyond what is possible via analyses of remote sensing and field observation data, and can be used to improve climate change forecasts of shifts in phenology, ecosystem processes and ecological interactions.Scope The twig method involves cutting dormant twigs from trees, shrubs and vines on a single date or at intervals over the course of the winter and early spring, placing them in containers of water in controlled environments, and regularly recording leaf-out, flowering or other phenomena. Prior to or following leaf-out or flowering, twigs may be assigned to treatment groups for experiments involving temperature, photoperiod, frost, humidity and more. Recent studies using these methods have shown that winter chilling requirements and spring warming strongly affect leaf-out and flowering times of temperate trees and shrubs, whereas photoperiod requirements are less important than previously thought for most species. Invasive plant species have weaker winter chilling requirements than native species in temperate ecosystems, and species that leaf-out early in the season have greater frost tolerance than later leafing species.Conclusions This methodology could be extended to investigate additional drivers of leaf-out phenology, leaf senescence in the autumn, and other phenomena, and could be a useful tool for education and outreach. Additional ecosystems, such as boreal, southern hemisphere and sub-tropical forests, could also be investigated using dormant twigs to determine the drivers of leaf-out times and how these ecosystems will be affected by climate change.     

Common garden comparison of the leaf‐out phenology of woody species from different native climates,combined with herbarium records,forecasts long‐term change

A well‐timed phenology is essential for plant growth and reproduction, but species‐specific phenological strategies are still poorly understood. Here, we use a common garden approach to compare biannual leaf‐out data for 495 woody species growing outdoors in Munich, 90% of them not native to that climate regime. For three species, data were augmented by herbarium dates for 140‐year‐long time series. We further meta‐analysed 107 temperate‐zone woody species in which leaf‐out cues have been studied, half of them also monitored here. Southern climate–adapted species flushed significantly later than natives, and photoperiod‐ and chilling‐ sensitive species all flushed late. The herbarium method revealed the extent of species‐specific climate tracking. Our results forecast that: (1) a northward expansion of southern species due to climate warming will increase the number of late flushers in the north, counteracting documented and expected flushing time advances; and (2) photoperiod‐ and chilling‐sensitive woody species cannot rapidly track climate warming.     

Changes in temperature sensitivity of spring phenology with recent climate warming in Switzerland are related to shifts of the preseason

The spring phenology of plants in temperate regions strongly responds to spring temperatures. Climate warming has caused substantial phenological advances in the past, but trends to be expected in the future are uncertain. A simple indicator is temperature sensitivity, the phenological advance statistically associated with a 1°C warmer mean temperature during the “preseason”, defined as the most temperature‐sensitive period preceding the phenological event. Recent analyses of phenological records have shown a decline in temperature sensitivity of leaf unfolding, but underlying mechanisms were not clear. Here, we propose that climate warming can reduce temperature sensitivity simply by reducing the length of the preseason due to faster bud development during this time period, unless the entire preseason shifts forward so that its temperature does not change. We derive these predictions theoretically from the widely used “thermal time model” for bud development and test them using data for 19 phenological events recorded in 1970–2012 at 108 stations spanning a 1600 m altitudinal range in Switzerland. We consider how temperature sensitivity, preseason start, preseason length and preseason temperature change (i) with altitude, (ii) between the periods 1970–1987 and 1995–2012, which differed mainly in spring temperatures, and (iii) between two non‐consecutive sets of 18 years that differed mainly in winter temperatures. On average, temperature sensitivity increased with altitude (colder climate) and was reduced in years with warmer springs, but not in years with warmer winters. These trends also varied among species. Decreasing temperature sensitivity in warmer springs was associated with a limited forward shift of preseason start, higher temperatures during the preseason and reduced preseason length, but not with reduced winter chilling. Our results imply that declining temperature sensitivity can result directly from spring warming and does not necessarily indicate altered physiological responses or stronger constraints such as reduced winter chilling.     

Larger temperature response of autumn leaf senescence than spring leaf‐out phenology

Climate warming is substantially shifting the leaf phenological events of plants, and thereby impacting on their individual fitness and also on the structure and functioning of ecosystems. Previous studies have largely focused on the climate impact on spring phenology, and to date the processes underlying leaf senescence and their associated environmental drivers remain poorly understood. In this study, experiments with temperature gradients imposed during the summer and autumn were conducted on saplings of European beech to explore the temperature responses of leaf senescence. An additional warming experiment during winter enabled us to assess the differences in temperature responses of spring leaf‐out and autumn leaf senescence. We found that warming significantly delayed the dates of leaf senescence both during summer and autumn warming, with similar temperature sensitivities (6–8 days delay per °C warming), suggesting that, in the absence of water and nutrient limitation, temperature may be a dominant factor controlling the leaf senescence in European beech. Interestingly, we found a significantly larger temperature response of autumn leaf senescence than of spring leaf‐out. This suggests a possible larger contribution of delays in autumn senescence, than of the advancement in spring leaf‐out, to extending the growing season under future warmer conditions.     

Experimental warming alters spring phenology of certain plant functional groups in an early successional forest community

Experimental study of the effects of projected climate change on plant phenology allows us to isolate effects of warming on life‐history events such as leaf out. We simulated a 2 °C temperature increase and 20% precipitation increase in a recently harvested temperate deciduous forest community in central Pennsylvania, USA, and observed the leaf out phenology of all species in 2009 and 2010. Over 130 plant species were monitored weekly in study plots, but due to high variability in species composition among plots, species were grouped into five functional groups: short forbs, tall forbs, shrubs, small trees, and large trees. Tall forbs and large trees, which usually emerge in the late spring, advanced leaf out 14–18 days in response to warming. Short forbs, shrubs, and small trees emerge early in spring and did not alter their phenology in response to warming or increased precipitation treatments. Earlier leaf out of tall forbs and large trees coincided with almost 3 weeks of increased community‐level leaf area index, indicating greater competition and a condensed spring green‐up period. While phenology of large trees and tall forbs appears to be strongly influenced by temperature‐based growth cues, our results suggest that photoperiod and chilling cues more strongly influence the leaf out of other functional groups. Reduced freeze events and warmer temperatures from predicted climate change will interact with nontemperature growth cues to have cascading consequences throughout the ecosystem.     

New insights on plant phenological response to temperature revealed from long‐term widespread observations in China

Constraints of temperature on spring plant phenology are closely related to plant growth, vegetation dynamics, and ecosystem carbon cycle. However, the effects of temperature on leaf onset, especially for winter chilling, are still not well understood. Using long‐term, widespread in situ phenology observations collected over China for multiple plant species, this study analyzes the quantitative response of leaf onset to temperature, and compares empirical findings with existing theories and modeling approaches, as implemented in 18 phenology algorithms. Results show that the growing degree days (GDD) required for leaf onset vary distinctly among plant species and geographical locations as well as at organizational levels (species and community), pointing to diverse adaptation strategies. Chilling durations (CHD) needed for releasing bud dormancy decline monotonously from cold to warm areas with very limited interspecies variations. Results also reveal that winter chilling is a crucial component of phenology models, and its effect is better captured with an index that accounts for the inhomogeneous effectiveness of low temperature to chilling rate than with the conventional CHD index. The impact of spring warming on leaf onset is nonlinear, better represented by a logistical function of temperature than by the linear function currently implemented in biosphere models. The optimized base temperatures for thermal accumulation and the optimal chilling temperatures are species‐dependent and average at 6.9 and 0.2°C, respectively. Overall, plants’ chilling requirement is not a constant, and more chilling generally results in less requirement of thermal accumulation for leaf onset. Our results clearly demonstrate multiple deficiencies of the parameters (e.g., base temperature) and algorithms (e.g., method for calculating GDD) in conventional phenology models to represent leaf onset. Therefore, this study not only advances our mechanistic and quantitative understanding of temperature controls on leaf onset but also provides critical information for improving existing phenology models.     

Climate change fingerprints in recent European plant phenology

A paper published in Global Change Biology in 2006 revealed that phenological responses in 1971–2000 matched the warming pattern in Europe, but a lack of chilling and adaptation in farming may have reversed these findings. Therefore, for 1951–2018 in a corresponding data set, we determined changes as linear trends and analysed their variation by plant traits/groups, across season and time as well as their attribution to warming following IPCC methodology. Although spring and summer phases in wild plants advanced less (maximum advances in 1978–2007), more (~90%) and more significant (~60%) negative trends were present, being stronger in early spring, at higher elevations, but smaller for nonwoody insect‐pollinated species. These trends were strongly attributable to winter and spring warming. Findings for crop spring phases were similar, but were less pronounced. There were clearer and attributable signs for a delayed senescence in response to winter and spring warming. These changes resulted in a longer growing season, but a constant generative period in wild plants and a shortened one in agricultural crops. Phenology determined by farmers’ decisions differed noticeably from the purely climatic driven phases with smaller percentages of advancing (~75%) trends, but farmers’ spring activities were the only group with reinforced advancement, suggesting adaptation. Trends in farmers’ spring and summer activities were very likely/likely associated with the warming pattern. In contrast, the advance in autumn farming phases was significantly associated with below average summer warming. Thus, under ongoing climate change with decreased chilling the advancing phenology in spring and summer is still attributable to warming; even the farmers’ activities in these seasons mirror, to a lesser extent, the warming. Our findings point to adaptation to climate change in agriculture and reveal diverse implications for terrestrial ecosystems; the strong attribution supports the necessary mediation of warming impacts to the general public.     

Shortened temperature‐relevant period of spring leaf‐out in temperate‐zone trees

Temperature during a particular period prior to spring leaf‐out, the temperature‐relevant period (TRP), is a strong determinant of the leaf‐out date in temperate‐zone trees. Climatic warming has substantially advanced leaf‐out dates in temperate biomes worldwide, but its effect on the beginning and length of the TRP has not yet been explored, despite its direct relevance for phenology modeling. Using 1,551 species–site combinations of long‐term (1951–2016) in situ observations on six tree species (namely, Aesculus hippocastanum, Alnus glutinosa, Betula pendula, Fagus sylvatica, Fraxinus excelsior, and Quercus robur) in central Europe, we found that the advancing leaf‐out was accompanied by a shortening of the TRP. On average across all species and sites, the length of the TRP significantly decreased by 23% (p < .05), from 60 ± 4 days during 1951–1965 to 47 ± 4 days during 2002–2016. Importantly, the average start date of the TRP did not vary significantly over the study period (March 2–5, DOY = 61–64), which could be explained by sufficient chilling over the study period in the regions considered. The advanced leaf‐out date with unchanged beginning of the TRP can be explained by the faster accumulation of the required heat due to climatic warming, which overcompensated for the retarding effect of shortening daylength on bud development. This study shows that climate warming has not yet affected the mean TRP starting date in the study region, implying that phenology modules in global land surface models might be reliable assuming a fixed TRP starting date at least for the temperate central Europe. Field warming experiments do, however, remain necessary to test to what extent the length of TRP will continue to shorten and whether the starting date will remain stable under future climate conditions.     

The Impact of Winter and Spring Temperatures on Temperate Tree Budburst Dates: Results from an Experimental Climate Manipulation

Budburst phenology is a key driver of ecosystem structure and functioning, and it is sensitive to global change. Both cold winter temperatures (chilling) and spring warming (forcing) are important for budburst. Future climate warming is expected to have a contrasting effect on chilling and forcing, and subsequently to have a non-linear effect on budburst timing. To clarify the different effects of warming during chilling and forcing phases of budburst phenology in deciduous trees, (i) we conducted a temperature manipulation experiment, with separate winter and spring warming treatments on well irrigated and fertilized saplings of beech, birch and oak, and (ii) we analyzed the observations with five temperature-based budburst models (Thermal Time model, Parallel model, Sequential model, Alternating model, and Unified model). The results show that both winter warming and spring warming significantly advanced budburst date, with the combination of winter plus spring warming accelerating budburst most. As expected, all three species were more sensitive to spring warming than to winter warming. Although the different chilling requirement, the warming sensitivity was not significantly different among the studied species. Model evaluation showed that both one- and two- phase models (without and with chilling, respectively) are able to accurately predict budburst. For beech, the Sequential model reproduced budburst dates best. For oak and birch, both Sequential model and the Thermal Time model yielded good fit with the data but the latter was slightly better in case of high parameter uncertainty. However, for late-flushing species, the Sequential model is likely be the most appropriate to predict budburst data in a future warmer climate.     

Chilling rather than photoperiod controls budburst for gymnosperm species in subtropical China

低温而不是光周期调控中国亚热带裸子植物的出芽物候 摘要：被子植物春季物候的调控机制已经得到了广泛的研究。然而,裸子植物和被子植物在3亿年前就产生分化,裸子植物与被子植物的物候可能是受不同的因素所调控。亚热带植物物候的调节机制在很大程度上尚不明确,亚热带裸子植物物候是否由冷激需求和光照调控仍未得到验证。本研究在人工气候箱中设置了3个冷激处理和3 个光周期处理,并对切枝的出芽期进行了为期8周的研究。实验中我们测试了8种裸子植物：柳杉(Cryptomeria japonica)、杉木(Cunninghamia lanceolata)、柏树(Cupressus funebris)、银杏(Ginkgo biloba)、水杉(Metasequoia glyptostroboides)、马尾松(Pinus massoniana)、金钱 松(Pseudolarix amabilis)和罗汉松(Podocarpus macrophyllus),检验其出芽物候是否对光周期敏感或者是否具有较强的冷激需求,以及这两种因素哪个对促进出芽更为重要。研究结果表明,对于裸子植物,冷 激促进了出芽并提高了出芽率,而且裸子植物需要适度的低温天数来实现出芽。有趣的是,在同一森 林中裸子植物比被子植物对积温的需求更高。与德国温带裸子植物(194–600 d · °C)相比,亚热带裸子植 物(814–1150 d · °C)对积温的需求更高。光周期对裸子植物出芽的影响较小,说明冷激对裸子植物出芽的 促进作用大于光周期。这些结果表明,随着全球气候持续变暖,冬季气温的升高不仅会影响亚热带被子植物也会影响裸子植物的物候,从而可能导致春季出芽期的延迟。     

Spring phenology at different altitudes is becoming more uniform under global warming in Europe

Under current global warming, high‐elevation regions are expected to experience faster warming than low‐elevation regions. However, due to the lack of studies based on long‐term large‐scale data, the relationship between tree spring phenology and the elevation‐dependent warming is unclear. Using 652k records of leaf unfolding of five temperate tree species monitored during 1951–2013 in situ in Europe, we discovered a nonlinear trend in the altitudinal sensitivity (S_A, shifted days per 100 m in altitude) in spring phenology. A delayed leaf unfolding (2.7 ± 0.6 days per decade) was observed at high elevations possibly due to decreased spring forcing between 1951 and 1980. The delayed leaf unfolding at high‐elevation regions was companied by a simultaneous advancing of leaf unfolding at low elevations. These divergent trends contributed to a significant increase in the S_A (0.36 ± 0.07 days 100/m per decade) during 1951–1980. Since 1980, the S_A started to decline with a rate of ?0.32 ± 0.07 days 100/m per decade, possibly due to reduced chilling at low elevations and improved efficiency of spring forcing in advancing the leaf unfolding at high elevations, the latter being caused by increased chilling. Our results suggest that due to both different temperature changes at the different altitudes, and the different tree responses to these changes, the tree phenology has shifted at different rates leading to a more uniform phenology at different altitudes during recent decades.     

Interactive climate factors restrict future increases in spring productivity of temperate and boreal trees

Climate warming is currently advancing spring leaf‐out of temperate and boreal trees, enhancing net primary productivity (NPP) of forests. However, it remains unclear whether this trend will continue, preventing for accurate projections of ecosystem functioning and climate feedbacks. Several ecophysiological mechanisms have been proposed to regulate the timing of leaf emergence in response to changing environmental cues, but the relative importance of those mechanisms remains unclear. Here, we use 727,401 direct phenological observations of common European forest trees to examine the dominant controls on leaf‐out. Using the emerging mechanisms, we forecast future trajectories of spring arrival and evaluate the consequences for forest carbon dynamics. By representing hypothesized relationships with autumn temperature, winter chilling, and the timing of spring onset, we accurately predicted reductions in the advance of leaf‐out. There was a strong consensus between our empirical model and existing process‐based models, revealing that the advance in leaf‐out will not exceed 2 weeks over the rest of the century. We further estimate that, under a ‘business‐as‐usual’ climate scenario, earlier spring arrival will enhance NPP of temperate and boreal forests by ~0.2 Gt per year at the end of the century. In contrast, previous estimates based on a simple degree‐day model range around 0.8 Gt. As such, the expected NPP is drastically reduced in our updated model relative to previous estimates—by a total of ~25 Gt over the rest of the century. These findings reveal important environmental constraints on the productivity of broad‐leaved deciduous trees and highlight that shifting spring phenology is unlikely to slow the rate of warming by offsetting anthropogenic carbon emissions.     

Shifting and extension of phenological periods with increasing temperature along elevational transects in southern Bavaria

The impact of global warming on phenology has been widely studied, and almost consistently advancing spring events have been reported. Especially in alpine regions, an extraordinary rapid warming has been observed in the last decades. However, little is known about phenological phases over the whole vegetation period at high elevations. We observed 12 phenological phases of seven tree species and measured air temperature at 42 sites along four transects of about 1000 m elevational range in the years 2010 and 2011 near Garmisch‐Partenkirchen, Germany. Site‐ and species‐specific onset dates for the phenological phases were determined and related to elevation, temperature lapse rates and site‐specific temperature sums. Increasing temperatures induced advanced spring and delayed autumn phases, in which both yielded similar magnitudes. Delayed leaf senescence could therefore have been underestimated until now in extending the vegetation period. Not only the vegetation period, but also phenological periods extended with increasing temperature. Moreover, sensitivity to elevation and temperature strongly depends on the specific phenological phase. Differences between species and groups of species (deciduous, evergreen, high elevation) were found in onset dates, phenological response rates and also in the effect of chilling and forcing temperatures. Increased chilling days highly reduced forcing temperature requirements for deciduous trees, but less for evergreen trees. The problem of shifted species associations and phenological mismatches due to species‐specific responses to increasing temperature is a recent topic in ecological research. Therefore, we consider our findings from this novel, dense observation network in an alpine area of particular importance to deepen knowledge on phenological responses to climate change.     

Shifts in the temperature‐sensitive periods for spring phenology in European beech and pedunculate oak clones across latitudes and over recent decades

Spring phenology of temperate trees has advanced worldwide in response to global warming. However, increasing temperatures may not necessarily lead to further phenological advance, especially in the warmer latitudes because of insufficient chilling and/or shorter day length. Determining the start of the forcing phase, that is, when buds are able to respond to warmer temperatures in spring, is therefore crucial to predict how phenology will change in the future. In this study, we used 4,056 leaf‐out date observations during the period 1969–2017 for clones of European beech (Fagus sylvatica L.) and pedunculate oak (Quercus robur L.) planted in 63 sites covering a large latitudinal gradient (from Portugal ~41°N to Norway ~63°N) at the International Phenological Gardens in order to (a) evaluate how the sensitivity periods to forcing and chilling have changed with climate warming, and (b) test whether consistent patterns occur along biogeographical gradients, that is, from colder to warmer environments. Partial least squares regressions suggest that the length of the forcing period has been extended over the recent decades with climate warming in the colder latitudes but has been shortened in the warmer latitudes for both species, with a more pronounced shift for beech. We attribute the lengthening of the forcing period in the colder latitudes to earlier opportunities with temperatures that can promote bud development. In contrast, at warmer or oceanic climates, the beginning of the forcing period has been delayed, possibly due to insufficient chilling. However, in spite of a later beginning of the forcing period, spring phenology has continued to advance at these areas due to a faster satisfaction of heat requirements induced by climate warming. Overall, our results support that ongoing climate warming will have different effects on the spring phenology of forest trees across latitudes due to the interactions between chilling, forcing and photoperiod.     

气候波动对西安39种木本植物展叶始期及其积温需求的影响

过去几十年来暖春等异常气候事件发生的频次和强度显著增加, 使植物春季物候期发生了明显变化。但异常气候事件对植物春季物候积温需求的影响仍不清楚, 限制了对未来物候变化预测精度的提升。该研究利用西安植物园1963-2018年39种木本植物的展叶始期和相应气象数据, 首先根据3-4月平均气温划分了偏冷年、正常年和偏暖年, 对比了冷暖年相对于正常年的展叶始期变化。其次, 利用3种积温算法计算了各植物逐年的展叶始期积温需求, 比较了积温需求在冷暖年和正常年的差异。最后, 评估了传统积温模型在模拟偏冷或偏暖年展叶始期时的误差。结果表明, 所有植物的展叶始期在偏暖年比正常年平均早8.6天, 而在偏冷年平均晚8.2天。在偏暖年, 大多数物种展叶始期的积温需求(以5 ℃为阈值, 平均257.5度日)显著高于正常年(平均195.1度日); 在偏冷年的积温需求(平均168.0度日)低于正常年, 但在统计上差异不显著。就不同类群而言, 古老类群相对于年轻类群在偏冷年的推迟天数更多, 积温需求变化较小, 但在偏暖年无显著差异。不同生活型间物候与积温需求变化也无显著差异。造成偏暖年积温需求增加的可能原因是偏暖年冬季气温较高, 导致植物受到的冷激程度减轻, 从而抑制了后续的展叶。在正常年, 积温模型模拟木本植物展叶始期的平均误差仅为0.4-1.9天。在偏暖年和偏冷年, 模拟值分别比观测值平均早4.1天和晚3.0天。因此在预测未来物候变化时, 需要考虑气候波动条件下的积温需求变化。