The process of adaptation is the result of stabilising selection caused by two opposite forces: protection against an unfavourable season (survival adaptation), and effective use of growing resources (capacity adaptation). As plant species have evolved different life strategies based on different trade offs between survival and capacity adaptations, different phenological responses are also expected among species. The aim of this study was to compare budburst responses of two opportunistic species (Betula pubescens, and Salix x smithiana) with that of two long-lived, late successional species (Fagus sylvatica and Tilia cordata) and consider their ecological significance. Thus, we performed a series of experiments whereby temperature and photoperiod were manipulated during dormancy. T. cordata and F. sylvatica showed low rates of budburst, high chilling requirements and responsiveness to light intensity, while B. pubescens and S. x smithiana had high rates of budburst, low chilling requirements and were not affected by light intensity. In addition, budburst in B. pubescens and S. x smithiana was more responsive to high forcing temperatures than in T. cordata and F. sylvatica. These results suggest that the timing of growth onset in B. pubescens and S. x smithiana (opportunistic) is regulated through a less conservative mechanism than in T. cordata and F. sylvatica (long-lived, late successional), and that these species trade a higher risk of frost damage for the opportunity of vigorous growth at the beginning of spring, before canopy closure. This information should be considered when assessing the impacts of climate change on vegetation or developing phenological models.

Accurate plant phenology (seasonal plant activity driven by environmental factors) models are vital tools for ecosystem simulation models and for predicting the response of ecosystems to climate change. Since the early 1970s, efforts have concentrated on predicting phenology of the temperate and boreal forests because they represent one-third of the carbon captured in plant ecosystems and they are the principal ecosystems with seasonal patterns of growth on Earth (one-fifth of the plant ecosystems area). Numerous phenological models have been developed to predict the growth timing of temperate or boreal trees. They are in general empirical, nonlinear and non-nested. For these reasons they are particularly difficult to fit, to test and to compare with each other. The methodological difficulties as well as the diversity of models used have greatly slowed down their improvement. The aim of this study was to show that the most widely used models simulating vegetative or reproductive phenology of trees are particular cases of a more general model. This unified model has three main advantages. First, it allows for a direct estimation of (i) the response of bud growth to either chilling or forcing temperatures and (ii) the periods when these temperatures affect the bud growth. Second, it can be simplified according to standard statistical tests for any particular species. Third, it provides a standardized framework for phenological models, which is essential for comparative studies as well as for robust model identification.Copyright 2000 Academic Press.

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.

We demonstrate that, beyond leaf phenology, the phenological cycles of wood and fine roots present clear responses to environmental drivers in temperate and boreal trees. These drivers should be included in terrestrial ecosystem models.

Accurate predictions of spring plant phenology with climate change are critical for projections of growing seasons, plant communities and a number of ecosystem services, including carbon storage. Progress towards prediction, however, has been slow because the major cues known to drive phenology - temperature (including winter chilling and spring forcing) and photoperiod - generally covary in nature and may interact, making accurate predictions of plant responses to climate change complex and nonlinear. Alternatively, recent work suggests many species may be dominated by one cue, which would make predictions much simpler. Here, we manipulated all three cues across 28 woody species from two North American forests. All species responded to all cues examined. Chilling exerted a strong effect, especially on budburst (-15.8 d), with responses to forcing and photoperiod greatest for leafout (-19.1 and -11.2 d, respectively). Interactions between chilling and forcing suggest that each cue may compensate somewhat for the other. Cues varied across species, leading to staggered leafout within each community and supporting the idea that phenology is a critical aspect of species' temporal niches. Our results suggest that predicting the spring phenology of communities will be difficult, as all species we studied could have complex, nonlinear responses to future warming.© 2018 The Authors. New Phytologist © 2018 New Phytologist Trust.

Under climate change, the reduction of frost risk, onset of warm temperatures and depletion of soil moisture are all likely to occur earlier in the year in many temperate regions. The resilience of tree species will depend on their ability to track these changes in climate with shifts in phenology that lead to earlier growth initiation in the spring. Exposure to warm temperatures ('forcing') typically triggers growth initiation, but many trees also require exposure to cool temperatures ('chilling') while dormant to readily initiate growth in the spring. If warming increases forcing and decreases chilling, climate change could maintain, advance or delay growth initiation phenology relative to the onset of favorable conditions. We modeled the timing of height- and diameter-growth initiation in coast Douglas-fir (an ecologically and economically vital tree in western North America) to determine whether changes in phenology are likely to track changes in climate using data from field-based and controlled-environment studies, which included conditions warmer than those currently experienced in the tree's range. For high latitude and elevation portions of the tree's range, our models predicted that warming will lead to earlier growth initiation and allow trees to track changes in the onset of the warm but still moist conditions that favor growth, generally without substantially greater exposure to frost. In contrast, toward lower latitude and elevation range limits, the models predicted that warming will lead to delayed growth initiation relative to changes in climate due to reduced chilling, with trees failing to capture favorable conditions in the earlier parts of the spring. This maladaptive response to climate change was more prevalent for diameter-growth initiation than height-growth initiation. The decoupling of growth initiation with the onset of favorable climatic conditions could reduce the resilience of coast Douglas-fir to climate change at the warm edges of its distribution.Published 2016. This article is a U.S. Government work and is in the public domain in the USA.

Recent studies have revealed large unexplained variation in heat requirement-based phenology models, resulting in large uncertainty when predicting ecosystem carbon and water balance responses to climate variability. Improving our understanding of the heat requirement for spring phenology is thus urgently needed. In this study, we estimated the species-specific heat requirement for leaf flushing of 13 temperate woody species using long-term phenological observations from Europe and North America. The species were defined as early and late flushing species according to the mean date of leaf flushing across all sites. Partial correlation analyses were applied to determine the temporal correlations between heat requirement and chilling accumulation, precipitation and insolation sum during dormancy. We found that the heat requirement for leaf flushing increased by almost 50% over the study period 1980-2012, with an average of 30 heat units per decade. This temporal increase in heat requirement was observed in all species, but was much larger for late than for early flushing species. Consistent with previous studies, we found that the heat requirement negatively correlates with chilling accumulation. Interestingly, after removing the variation induced by chilling accumulation, a predominantly positive partial correlation exists between heat requirement and precipitation sum, and a predominantly negative correlation between heat requirement and insolation sum. This suggests that besides the well-known effect of chilling, the heat requirement for leaf flushing is also influenced by precipitation and insolation sum during dormancy. However, we hypothesize that the observed precipitation and insolation effects might be artefacts attributable to the inappropriate use of air temperature in the heat requirement quantification. Rather than air temperature, meristem temperature is probably the prominent driver of the leaf flushing process, but these data are not available. Further experimental research is thus needed to verify whether insolation and precipitation sums directly affect the heat requirement for leaf flushing.© 2015 John Wiley & Sons Ltd.

Heat requirement, expressed in growing degree days (GDD), is a widely used method to assess and predict the effect of temperature on plant development. Until recently, the analysis of spatial patterns of GDD requirement for spring vegetation green-up onset was limited to local and regional scales, mainly because of the sparse and aggregated spatial availability of ground phenology data. Taking advantage of the large temporal and spatial scales of remote sensing-based green-up onset data, we studied the spatial patterns of GDD requirement for vegetation green-up at northern middle and high latitudes. We further explored the correlations between GDD requirement for vegetation green-up and previous winter season chilling temperatures and precipitation, using spatial partial correlations. We showed that GDD requirement for vegetation green-up onset declines towards the north at a mean rate of 18.8 °C-days per degree latitude between 35°N and 70°N, and vary significantly among different vegetation types. Our results confirmed that the GDD requirement for vegetation green-up is negatively correlated with previous winter chilling, which was defined as the number of chilling days from the day when the land surface froze in the previous autumn to the day of green-up onset. This negative correlation is a well-known phenomenon from local studies. Interestingly, irrespective of the vegetation type, we also found a positive correlation between the GDD requirement and previous winter season precipitation, which was defined as the sum of the precipitation of the month when green-up onset occur and the precipitation that occurred during the previous 2 months. Our study suggests that GDD requirement, chilling and precipitation may have complex interactions in their effects on spring vegetation green-up phenology. These findings have important implications for improving phenology models and could therefore advance our understanding of the interplay between spring phenology and carbon fluxes. © 2014 John Wiley & Sons Ltd.

Many temperate and boreal tree species have a chilling requirement, that is, they need to experience cold temperatures during fall and winter to burst bud normally in the spring. Results from trials with 11 Pacific Northwest tree species are consistent with the concept that plants can accumulate both chilling and forcing units simultaneously during the dormant season and they exhibit a tradeoff between amount of forcing and chilling. That is, the parallel model of chilling and forcing was effective in predicting budburst and well chilled plants require less forcing for bud burst than plants which have received less chilling. Genotypes differed in the shape of the possibility line which describes the quantitative tradeoff between chilling and forcing units. Plants which have an obligate chilling requirement (Douglas-fir, western hemlock, western larch, pines, and true firs) and received no or very low levels of chilling did not burst bud normally even with long photoperiods. Pacific madrone and western redcedar benefited from chilling in terms of requiring less forcing to promote bud burst but many plants burst bud normally without chilling. Equations predicting budburst were developed for each species in our trials for a portion of western North America under current climatic conditions and for 2080. Mean winter temperature was predicted to increase 3.2-5.5 degrees C and this change resulted in earlier predicted budburst for Douglas-fir throughout much of our study area (up to 74 days earlier) but later budburst in some southern portions of its current range (up to 48 days later) as insufficient chilling is predicted to occur. Other species all had earlier predicted dates of budburst by 2080 than currently. Recent warming trends have resulted in earlier budburst for some woody plant species; however, the substantial winter warming predicted by some climate models will reduce future chilling in some locations such that budburst will not consistently occur earlier.

Responses by flowering plants to climate change are complex and only beginning to be understood. Through analyses of 10,295 herbarium specimens of Himalayan Rhododendron collected by plant hunters and botanists since 1884, we were able to separate these responses into significant components. We found a lack of directional change in mean flowering time over the past 45 y of rapid warming. However, over the full 125 y of collections, mean flowering time shows a significant response to year-to-year changes in temperature, and this response varies with season of warming. Mean flowering advances with annual warming (2.27 d earlier per 1 °C warming), and also is delayed with fall warming (2.54 d later per 1 °C warming). Annual warming may advance flowering through positive effects on overwintering bud formation, whereas fall warming may delay flowering through an impact on chilling requirements. The lack of a directional response suggests that contrasting phenological responses to temperature changes may obscure temperature sensitivity in plants. By drawing on large collections from multiple herbaria, made over more than a century, we show how these data may inform studies even of remote localities, and we highlight the increasing value of these and other natural history collections in understanding long-term change.

Attempts to discuss the various aspects of plant dormancy can be bewildering due to the excessive number of nonphysiological, independent terms that have arisen over the years. In the context of field observations and orchard management, this terminology has often been adequate. However, in the complex realm of scientific description of the processes that constitute dormancy, the terminology has not been able to keep pace with physiological investigation. In 1985, a set of alternative terms, endodormancy, ectodormancy, and ecodormancy, were suggested to improve the situation (14). During the past 2 years, R. Darnell, J. Early, G. Martin, and I have reviewed the dormancy literature to evaluate the strengths and weaknesses of new and previous terms. At various times, N. Arroyave, R. Biasi, R. Femandez-Escobar, G. Stutte, and others from around the world have contributed greatly to discussion and critical analysis of the requirements for a physiological nomenclature. In 1986, ectodormancy was replaced by paradormancy (16) due to the former’s spoken and written similarities to ecodormancy. This paper summarizes the communicative burden presented by the current terminology, the evolution of the new terms, the universal classification system in which the terms are used, and the implications for future dormancy research. These topics are presented in greater detail elsewhere (15).

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. © 2013 John Wiley & Sons Ltd.

Studies on variations in chilling and heat accumulation in apple trees and their effects on first flowering date under climate change are important for guiding apple planting and productions. In this study, we carried out experiments in representative stations of apple planting areas in the northern China, including Fushan of Shandong, Wanrong of Shanxi, Xifeng of Gansu and Akesu of Xinjiang. The first flowering data and hourly temperature data during 1996-2018 were used to calculate the daily chilling and heat accumulation units by applying the dynamic model and growing degree hour model. Partial least squares regression (PLS) correlated daily chilling and heat units with the first flowering dates was used to identify the chilling and heat accumulation periods for apple flowering. We evaluated the impacts of temperatures during these periods on apples' flowering. Our results showed that the chilling accumulation period of apple trees in the examined sites started at October 1, ended in late February or mid-March, with chilling accumulations of 74.1-89.3 CP (chill portion). The heat accumulation periods were from late January to the first flowering dates with the heat accumulation of 4010-5770 GDH (growing degree hour). The chilling accumulation at Xifeng and Akesu was correlated positively with mean temperature during the respective accumulation period, with 3.8 and 5.0 CP enhancement following 1 ℃ increase during the accumulation period. Heat accumulation at all stations correlated positively with mean temperature during the respective accumulation period, with 725-967 GDH enhancement following a 1 ℃ increase during the accumulation period. Compared to the effects of chilling accumulation on tree flowering, the first flowering data of apples in the main planting areas were mainly affected by mean temperature during the heat accumulation period. Climate warming is beneficial for apple blossom and production in the areas with low mean temperature during the chilling accumulation period.

开展气候变化背景下苹果冷热积累变化及其对始花期的影响研究,对指导苹果种植及生产具有重要意义。本研究选取山东福山、山西万荣、甘肃西峰和新疆阿克苏代表中国北方苹果主产地,利用1996—2018年红富士苹果的始花期观测资料和逐时气温数据,采用动态模型、生长度小时模型分别计算逐日冷积累量(CP)和热积累量(GDH),并利用偏最小二乘回归法,对逐日冷、热积累量和各地苹果始花期进行相关分析,以明确各地苹果冷、热积累起止日期和积累量,以及冷、热积累期内温度变化对始花期的影响规律。结果表明: 我国北方主产地苹果冷积累时段集中于10月1日前后至2月中下旬或3月中旬,积累量为74.1～89.3 CP;热积累时段集中于1月下旬前后至始花期,积累量为4010～5770 GDH。西峰和阿克苏冷积累期内平均气温每升高1 ℃,冷积累量将分别增加3.8和5.0 CP;各地热积累期内平均气温每升高1 ℃,热积累量将增加725～967 GDH。与冷积累期内温度变化的影响效应相比,热积累期内温度变化主控我国北方主产地苹果始花期,且气候变暖总体有利于冷积累期内平均气温较低地区的苹果开花和生产。

Many fruit and nut trees must fulfill a chilling requirement to break their winter dormancy and resume normal growth in spring. Several models exist for quantifying winter chill, and growers and researchers often tacitly assume that the choice of model is not important and estimates of species chilling requirements are valid across growing regions. To test this assumption, Safe Winter Chill (the amount of winter chill that is exceeded in 90% of years) was calculated for 5,078 weather stations around the world, using the Dynamic Model [in Chill Portions (CP)], the Chilling Hours (CH) Model and the Utah Model [Utah Chill Units (UCU)]. Distributions of the ratios between different winter chill metrics were mapped on a global scale. These ratios should be constant if the models were strictly proportional. Ratios between winter chill metrics varied substantially, with the CH/CP ratio ranging between 0 and 34, the UCU/CP ratio between -155 and +20 and the UCU/CH ratio between -10 and +5. The models are thus not proportional, and chilling requirements determined in a given location may not be valid elsewhere. The Utah Model produced negative winter chill totals in many Subtropical regions, where it does not seem to be useful. Mean annual temperature and daily temperature range influenced all winter chill ratios, but explained only between 12 and 27% of the variation. Data on chilling requirements should always be amended with information on the location and experimental conditions of the study in which they were determined, ideally including site-specific conversion factors between winter chill models. This would greatly facilitate the transfer of such information across growing regions, and help prepare growers for the impact of climate change.

Leaf out phenology affects a wide variety of ecosystem processes and ecological interactions and will take on added significance as leaf out times increasingly shift in response to warming temperatures associated with climate change. There is, however, relatively little information available on the factors affecting species differences in leaf out phenology. An international team of researchers from eight Northern Hemisphere temperate botanical gardens recorded leaf out dates of c. 1600 woody species in 2011 and 2012. Leaf out dates in woody species differed by as much as 3 months at a single site and exhibited strong phylogenetic and anatomical relationships. On average, angiosperms leafed out earlier than gymnosperms, deciduous species earlier than evergreen species, shrubs earlier than trees, diffuse and semi-ring porous species earlier than ring porous species, and species with smaller diameter xylem vessels earlier than species with larger diameter vessels. The order of species leaf out was generally consistent between years and among sites. As species distribution and abundance shift due to climate change, interspecific differences in leaf out phenology may affect ecosystem processes such as carbon, water, and nutrient cycling. Our open access leaf out data provide a critical framework for monitoring and modelling such changes going forward. © 2014 The Authors. New Phytologist © 2014 New Phytologist Trust.

Plant phenology, the annually recurring sequence of plant developmental stages, is important for plant functioning and ecosystem services and their biophysical and biogeochemical feedbacks to the climate system. Plant phenology depends on temperature, and the current rapid climate change has revived interest in understanding and modeling the responses of plant phenology to the warming trend and the consequences thereof for ecosystems. Here, we review recent progresses in plant phenology and its interactions with climate change. Focusing on the start (leaf unfolding) and end (leaf coloring) of plant growing seasons, we show that the recent rapid expansion in ground- and remote sensing- based phenology data acquisition has been highly beneficial and has supported major advances in plant phenology research. Studies using multiple data sources and methods generally agree on the trends of advanced leaf unfolding and delayed leaf coloring due to climate change, yet these trends appear to have decelerated or even reversed in recent years. Our understanding of the mechanisms underlying the plant phenology responses to climate warming is still limited. The interactions between multiple drivers complicate the modeling and prediction of plant phenology changes. Furthermore, changes in plant phenology have important implications for ecosystem carbon cycles and ecosystem feedbacks to climate, yet the quantification of such impacts remains challenging. We suggest that future studies should primarily focus on using new observation tools to improve the understanding of tropical plant phenology, on improving process-based phenology modeling, and on the scaling of phenology from species to landscape-level.© 2019 John Wiley & Sons Ltd.

Monitoring phenology, the study of the timing of natural events, is an ancient practice that has experienced renewed relevance for scientific research interest in the wake of awareness of anthropogenic climate change. Spring onset has been occurring significantly earlier in temperate regions worldwide. Leaf out phenology has become particularly well studied is of particular interest because the emergence of leaves in the spring is extremely sensitive to temperature, and the leaf out timing of leaf out in temperate ecosystems marks the onset of the growing season and controls many essential ecosystem processes. This article reviews the current literature concerning the different methods used to study leaf out phenology, the controls on leaf out in temperate woody plants, and the effects of climate change on leaf out phenology. In addition to the traditional method of on-the-ground leaf out monitoring, new methods using remote sensing and dedicated cameras have been developed which allow scientists to track spring onset at a much larger scale than had previously been possible. Further work is needed on how leaf phenology will respond to future climate change, and the implications of this for animals and other species interactions among trophic levels.

Release of bud dormancy in perennial plants resembles vernalization in Arabidopsis thaliana and cereals. In both cases, a certain period of chilling is required for accomplishing the reproductive phase, and several transcription factors with the MADS-box domain perform a central regulatory role in these processes. The expression of DORMANCY-ASSOCIATED MADS-box (DAM)-related genes has been found to be up-regulated in dormant buds of numerous plant species, such as poplar, raspberry, leafy spurge, blackcurrant, Japanese apricot, and peach. Moreover, functional evidence suggests the involvement of DAM genes in the regulation of seasonal dormancy in peach. Recent findings highlight the presence of genome-wide epigenetic modifications related to dormancy events, and more specifically the epigenetic regulation of DAM-related genes in a similar way to FLOWERING LOCUS C, a key integrator of vernalization effectors on flowering initiation in Arabidopsis. We revise the most relevant molecular and genomic contributions in the field of bud dormancy, and discuss the increasing evidence for chromatin modification involvement in the epigenetic regulation of seasonal dormancy cycles in perennial plants.

The rise in spring temperatures over the past half-century has led to advances in the phenology of many nontropical plants and animals. As species and populations differ in their phenological responses to temperature, an increase in temperatures has the potential to alter timing-dependent species interactions. One species-interaction that may be affected is the competition for light in deciduous forests, where early vernal species have a narrow window of opportunity for growth before late spring species cast shade. Here we consider the Marsham phenology time series of first leafing dates of thirteen tree species and flowering dates of one ground flora species, which spans two centuries. The exceptional length of this time series permits a rare comparison of the statistical support for parameter-rich regression and mechanistic thermal sensitivity phenology models. While mechanistic models perform best in the majority of cases, both they and the regression models provide remarkably consistent insights into the relative sensitivity of each species to forcing and chilling effects. All species are sensitive to spring forcing, but we also find that vernal and northern European species are responsive to cold temperatures in the previous autumn. Whether this sensitivity reflects a chilling requirement or a delaying of dormancy remains to be tested. We then apply the models to projected future temperature data under a fossil fuel intensive emissions scenario and predict that while some species will advance substantially others will advance by less and may even be delayed due to a rise in autumn and winter temperatures. Considering the projected responses of all fourteen species, we anticipate a change in the order of spring events, which may lead to changes in competitive advantage for light with potential implications for the composition of temperate forests.© 2015 The Authors. Global Change Biology Published by John Wiley & Sons Ltd.

Siberia has undergone dramatic climatic changes due to global warming in recent decades. Yet, the ecological responses to these climatic changes are still poorly understood due to a lack of data. Here, we use a unique dataset from the Russian 'Chronicles of Nature' network to analyse long-term (1976-2018) phenological shifts in leaf out, flowering, fruiting and senescence of 67 common Siberian plant species. We find that Siberian boreal forest plants advanced their early-season (leaf out and flowering) and mid-season (fruiting) by 2.2, 0.7 and 1.6 days/decade, and delayed the onset of senescence by 1.6 days/decade during this period. These mean values, however, are subject to substantial intraspecific variability, which is partly explained by the plants' growth forms. Trees and shrubs advanced leaf out and flowering (-3.1 and -3.3. days/decade) faster than herbs (1 day/decade), presumably due to the more direct exposure of leaf and flower buds to ambient air for the woody vegetation. For senescence, we detected a reverse pattern: stronger delays in herbs (2.1 days/decade) than in woody plants (1.0-1.2 days/decade), presumably due to stronger effects of autumn frosts on the leaves of herbs. Interestingly, the timing of fruiting in all four growth forms advanced at similar paces, from 1.4 days/decade in shrubs to 1.7 days/decade in trees and herbs. Our findings point to a strong, yet heterogeneous, response of Siberian plant phenology to recent global warming. Furthermore, the results highlight that species- and growth form-specific differences among study species could be used to identify plants particularly at risk of decline due to their low adaptive capacity or a loss of synchronization with important interaction partners.This article is protected by copyright. All rights reserved.

Effects of temperature and photoperiod and their interactions on budburst and on the use of carbon reserves were examined in two Mediterranean oaks differing in wood anatomy and leaf habit. Seedlings of Quercus ilex subsp. ballota (evergreen and diffuse-porous wood) and Q. faginea (semi-deciduous and ring-porous wood) were grown under two temperatures (12 and 19 degrees C) and two photoperiods (10 and 16 h) in a factorial experiment. In the 16 h photoperiod at 19 degrees C, photosynthesis was suppressed in half of the seedlings by covering leaves with aluminium foil. The concentration of soluble sugars, starch and lipids in leaves, stems and roots was assessed before and after budburst. Under the 12 degrees C treatment (mean current temperature in early spring in the Iberian Peninsula), budburst in Q. faginea occurred earlier than in Q. ilex. Higher temperature promoted earlier budburst in both species, mostly under the 16 h photoperiod. This response was less pronounced in Q. faginea because its budburst was also controlled by photoperiod, and because this species needs to construct a new ring of xylem before budburst to supply its growth demands. Therefore, dates of budburst of the two species became closer to each other in the warmer treatment, which might alter competitive relations between the species with changing climate. While Q. ilex relied on carbon reserves for budburst, Q. faginea relied on both carbon reserves and current photoassimilates. The different responses of the two Quercus species to temperature and photoperiod related more to xylem structure than to the source of carbon used for budburst.

The main drivers of global environmental change (CO2 enrichment, nitrogen deposition, climate, biotic invasions and land use) cause extinctions and alter species distributions, and recent evidence shows that they exert pervasive impacts on various antagonistic and mutualistic interactions among species. In this review, we synthesize data from 688 published studies to show that these drivers often alter competitive interactions among plants and animals, exert multitrophic effects on the decomposer food web, increase intensity of pathogen infection, weaken mutualisms involving plants, and enhance herbivory while having variable effects on predation. A recurrent finding is that there is substantial variability among studies in both the magnitude and direction of effects of any given GEC driver on any given type of biotic interaction. Further, we show that higher order effects among multiple drivers acting simultaneously create challenges in predicting future responses to global environmental change, and that extrapolating these complex impacts across entire networks of species interactions yields unanticipated effects on ecosystems. Finally, we conclude that in order to reliably predict the effects of GEC on community and ecosystem processes, the greatest single challenge will be to determine how biotic and abiotic context alters the direction and magnitude of GEC effects on biotic interactions.

In a temperate climate, understory trees leaf out earlier than canopy trees, but the cause of this discrepancy remains unclear. This study aims to investigate whether this discrepancy results from ontogenic changes or from microclimatic differences. Seedlings of five deciduous tree species were grown in spring 2012 in the understory and at canopy height using a 45-m-high construction crane built into a mature mixed forest in the foothills of the Swiss Jura Mountains. The leaf development of these seedlings, as well as conspecific adults, was compared, taking into account the corresponding microclimate. The date of leaf unfolding occurred 10-40 d earlier in seedlings grown at canopy level than in conspecific adults. Seedlings grown in the understory flushed c. 6 d later than those grown at canopy height, which can be attributed to the warmer temperatures recorded at canopy height (c. 1°C warmer). This study demonstrates that later leaf emergence of canopy trees compared with understory trees results from ontogenic changes and not from the vertical thermal profile that exists within forests. This study warns against the assumption that phenological data obtained in warming and photoperiod experiments on juvenile trees can be used for the prediction of forest response to climate warming.© 2013 The Authors. New Phytologist © 2013 New Phytologist Trust.

Spring warming substantially advances leaf unfolding and flowering time for perennials. Winter warming, however, decreases chilling accumulation (CA), which increases the heat requirement (HR) and acts to delay spring phenology. Whether or not this negative CA-HR relationship is correctly interpreted in ecosystem models remains unknown. Using leaf unfolding and flowering data for 30 perennials in Europe, here we show that more than half (7 of 12) of current chilling models are invalid since they show a positive CA-HR relationship. The possible reason is that they overlook the effect of freezing temperature on dormancy release. Overestimation of the advance in spring phenology by the end of this century by these invalid chilling models could be as large as 7.6 and 20.0 days under RCPs 4.5 and 8.5, respectively. Our results highlight the need for a better representation of chilling for the correct understanding of spring phenological responses to future climate change.

Using first leaf unfolding data of Salix matsudana, Populus simonii, Ulmus pumila, and Prunus armeniaca, and daily mean temperature data during the 1981-2005 period at 136 stations in northern China, we fitted unified forcing and chilling phenology models and selected optimum models for each species at each station. Then, we examined performances of each optimum local species-specific model in predicting leaf unfolding dates at all external stations within the corresponding climate region and selected 16 local species-specific models with maximum effective predictions as the regional unified models in different climate regions. Furthermore, we validated the regional unified models using leaf unfolding and daily mean temperature data beyond the time period of model fitting. Finally, we substituted gridded daily mean temperature data into the regional unified models, and reconstructed spatial patterns of leaf unfolding dates of the four tree species across northern China during 1960-2009. At local scales, the unified forcing model shows higher simulation efficiency at 83% of data sets, whereas the unified chilling model indicates higher simulation efficiency at 17% of data sets. Thus, winter temperature increase so far has not yet significantly influenced dormancy and consequent leaf development of deciduous trees in most parts of northern China. Spatial and temporal validation confirmed capability and reliability of regional unified species-specific models in predicting leaf unfolding dates in northern China. Reconstructed leaf unfolding dates of the four tree species show significant advancements by 1.4-1.6 days per decade during 1960-2009 across northern China, which are stronger for the earlier than the later leaf unfolding species. Our findings suggest that the principal characteristics of plant phenology and phenological responses to climate change at regional scales can be captured by phenological and climatic data sets at a few representative locations.© 2012 Blackwell Publishing Ltd.

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. © 2014 John Wiley & Sons Ltd/CNRS.