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.     

Temperature sensitivity of spring vegetation phenology correlates to within-spring warming speed over the Northern Hemisphere

The inter-annual shift of spring vegetation phenology relative to per unit change of preseason temperature, referred to as temperature sensitivity (days °C⁻¹), quantifies the response of spring phenology to temperature change. Temperature sensitivity was found to differ greatly among vegetation from different environmental conditions. Understanding the large-scale spatial pattern of temperature sensitivity and its underlying determinant will greatly improve our ability to predict spring phenology. In this study, we investigated the temperature sensitivity for natural ecosystems over the North Hemisphere (north of 30°N), based on the vegetation phenological date estimated from NDVI time-series data provided by the Advanced Very High Resolution Radiometer (AVHRR) and the corresponding climate dataset. We found a notable longitudinal change pattern with considerable increases of temperature sensitivity from inlands to most coastal areas and a less obvious latitudinal pattern with larger sensitivity in low latitude area. This general spatial variation in temperature sensitivity is most strongly associated with the within-spring warming speed (WWS; r = 0.35, p < 0.01), a variable describing the increase speed of daily mean temperature during spring within a year, compared with other factors including the mean spring temperature, spring precipitation and mean winter temperature. These findings suggest that the same magnitude of warming will less affect spring vegetation phenology in regions with higher WWS, which might partially reflect plants’ adaption to local climate that prevents plants from frost risk caused by the advance of spring phenology. WWS accounts for the spatial variation in temperature sensitivity and should be taken into account in forecasting spring phenology and in assessing carbon cycle under the projected climate warming.     

Estimating the ability of plants to plastically track temperature‐mediated shifts in the spring phenological optimum

One consequence of rising spring temperatures is that the optimum timing of key life‐history events may advance. Where this is the case, a population's fate may depend on the degree to which it is able to track a change in the optimum timing either via plasticity or via adaptation. Estimating the effect that temperature change will have on optimum timing using standard approaches is logistically challenging, with the result that very few estimates of this important parameter exist. Here we adopt an alternative statistical method that substitutes space for time to estimate the temperature sensitivity of the optimum timing of 22 plant species based on >200 000 spatiotemporal phenological observations from across the United Kingdom. We find that first leafing and flowering dates are sensitive to forcing (spring) temperatures, with optimum timing advancing by an average of 3 days °C^?1 and plastic responses to forcing between ?3 and ?8 days °C^?1. Chilling (autumn/winter) temperatures and photoperiod tend to be important cues for species with early and late phenology, respectively. For most species, we find that plasticity is adaptive, and for seven species, plasticity is sufficient to track geographic variation in the optimum phenology. For four species, we find that plasticity is significantly steeper than the optimum slope that we estimate between forcing temperature and phenology, and we examine possible explanations for this countergradient pattern, including local adaptation.     

A resurrection study reveals limited evolution of phenology in response to recent climate change across the geographic range of the scarlet monkeyflower

Premise of the studyAs global climate change alters drought regimes, rapid evolution of traits that facilitate adaptation to drought can rescue populations in decline. The evolution of phenological advancement can allow plant populations to escape drought, but evolutionary responses in phenology can vary across a species'' range due to differences in drought intensity and standing genetic variation.Methods Mimulus cardinalis, a perennial herb spanning a broad climatic gradient, recently experienced a period of record drought. Here, we used a resurrection study comparing flowering time and stem height at first flower of pre‐drought ancestors and post‐drought descendants from northern‐edge, central, and southern‐edge populations in a common environment to examine the evolution of drought escape across the latitudinal range.Key resultsContrary to the hypothesis of the evolution of advanced phenology in response to recent drought, flowering time did not advance between ancestors and descendants in any population, though storage condition and maternal effects could have impacted these results. Stem height was positively correlated with flowering time, such that plants that flowered earlier were shorter at first flower. This correlation could constrain the evolution of earlier flowering time if selection favors flowering early at a large size.ConclusionsThese findings suggest that rapid evolution of phenology will not rescue these populations from recent climate change. Future work is needed to examine the potential for the evolution of alternative drought strategies and phenotypic plasticity to buffer M. cardinalis populations from changing climate.     

A modelling analysis of the effects of climatic warming on the probability of spring frost damage to tree species in The Netherlands and Germany

Two studies presented in the literature ( Murray, Canned & Smith 1989 ; Hanninen 1991 ) evaluate the effect of increasing winter temperature on the probability of spring frost damage to trees, but yield contradictory results. It is unclear whether the disparity can be ascribed to the fact that different models were used, or is the result of different climatic warming scenarios being used, or is because the tree species at the different locations do indeed respond differently to warmer winters. To evaluate the effects of climatic warming to tree species in The Netherlands and in Germany, both models were fitted to long series of observations on the date of leaf unfolding of eleven tree species. The impact of the two scenarios (uniformly and non-uniformly changing winter temperature) on the date of leaf unfolding and on the probability of freezing temperature around that date was evaluated. To test the importance of adaptation to local climate, hypothetical provenance transfers were analysed. It was concluded that, for tree species in The Netherlands and Germany, the probability of spring frost damage will decrease. The contradictory results found in the literature could be ascribed to differences between provenances adapted to their local climate, and is not because different models and different climatic warming scenarios were used in these studies.     

Historical changes in the phenology of British Odonata are related to climate

Responses of biota to climate change take a number of forms including distributional shifts, behavioural changes and life history changes. This study examined an extensive set of biological records to investigate changes in the timing of life history transitions (specifically emergence) in British Odonata between 1960 and 2004. The results show that there has been a significant, consistent advance in phenology in the taxon as a whole over the period of warming that is mediated by life history traits. British odonates significantly advanced the leading edge (first quartile date) of the flight period by a mean of 1.51 ±0.060 (SEM, n=17) days per decade or 3.08±1.16 (SEM, n=17) days per degree rise in temperature when phylogeny is controlled for. This study represents the first review of changes in odonate phenology in relation to climate change. The results suggest that the damped temperature oscillations experienced by aquatic organisms compared with terrestrial organisms are sufficient to evoke phenological responses similar to those of purely terrestrial taxa.     

北半球中高纬度地区近30年植被春季物候温度敏感性

北半球气候变暖导致植被春季物候开始日期显著提前,温度对春季物候的促进作用是一个过程事件而非瞬时事件,且存在空间差异。该研究在以前研究的基础上,进一步分析温度对植被物候的作用方式,并探讨春季物候温度敏感性的空间特征及影响因素。利用GIMMS3g卫星植被指数产品,采用5种方法提取1982–2009年植被春季物候,并结合格网气象数据计算植被春季物候的温度敏感性,着重分析自然植被春季物候温度敏感性与环境因素的关系。结果表明,温度是北半球植被春季物候的主要制约因素,54%的像元显示温度最大效应发生在物候开始当月和之前一个月。温度主导的春季物候的像元中,91.3%的像元指示早春温度对物候开始的促进作用。植被春季物候的温度敏感性存在空间异质性,随着区域环境因素的不同,年际温度标准差、累积降水量和辐射对植被春季物候温度敏感性都具有各自或协同的调控作用。     

Divergent trends in the risk of spring frost damage to trees in Europe with recent warming

Frost events during the active growth period of plants can cause extensive frost damage with tremendous economic losses and dramatic ecological consequences. A common assumption is that climate warming may bring along a reduction in the frequency and severity of frost damage to vegetation. On the other hand, it has been argued that rising temperature in late winter and early spring might trigger the so called “false spring”, that is, early onset of growth that is followed by cold spells, resulting in increased frost damage. By combining daily gridded climate data and 1,489 k in situ phenological observations of 27 tree species from 5,565 phenological observation sites in Europe, we show here that temporal changes in the risk of spring frost damage with recent warming vary largely depending on the species and geographical locations. Species whose phenology was especially sensitive to climate warming tended to have increased risk of frost damage. Geographically, compared with continental areas, maritime and coastal areas in Europe were more exposed to increasing occurrence of frost and these late spring frosts were getting more severe in the maritime and coastal areas. Our results suggest that even though temperatures will be elevated in the future, some phenologically responsive species and many populations of a given species will paradoxically experience more frost damage in the future warming climate. More attention should be paid to the increased frost damage in responsive species and populations in maritime areas when developing strategies to mitigate the potential negative impacts of climate change on ecosystems in the near future.     

Velocity of temperature and flowering time in wheat – assisting breeders to keep pace with climate change

By accelerating crop development, warming climates may result in mismatches between key sensitive growth stages and extreme climate events, with severe consequences for crop yield and food security. Using recent estimates of gene responses to vernalization and photoperiod in wheat, we modelled the flowering times of all ‘potential’ genotypes as influenced by the velocity of climate change across the Australian wheatbelt. In the period 1957–2010, seasonal increases in temperature of 0.012 °C yr^?1 were recorded and changed flowering time of a mid‐season wheat genotype by an average ?0.074 day yr^?1, with flowering ‘velocity’ of up to 0.95 km yr^?1 towards the coastal edges of the wheatbelt; this is an estimate of how quickly the given genotype would have to be ‘moved’ across the landscape to maintain its original flowering time. By 2030, these national changes are projected to accelerate by up to 3‐fold for seasonal temperature and by up to 5‐fold for flowering time between now and 2030, with average national shifts in flowering time of 0.33 and 0.41 day yr^?1 between baseline and the worst climate scenario tested for 2030 and 2050, respectively. Without new flowering alleles in commercial germplasm, the life cycle of wheat crops is predicted to shorten by 2 weeks by 2030 across the wheatbelt for the most pessimistic climate scenario. While current cultivars may be otherwise suitable for future conditions, they will flower earlier due to warmer temperatures. To allow earlier sowing to escape frost, heat and terminal drought, and to maintain current growing period of early‐sown wheat crops in the future, breeders will need to develop and/or introduce new genetic sources for later flowering, more so in the eastern part of the wheatbelt.     

1982—2009年基于卫星数据的北半球中高纬地区植被春季物候动态及其与气候的关系

深入认识北半球植被物候在全球变暖背景下的动态变化特征,对于评估和预测生态系统结构和功能对气候变化的响应有重要的指示作用.遥感技术是获取北半球植被春季物候的最重要方法,但是由于物候提取算法的差异,目前还存在较大的不确定性.本文利用5种方法,基于卫星获取的归一化植被指数估算了北半球中高纬地区1982—2009年植被春季物候开始日期,分析了该日期的多年动态变化的时空特征,并探讨了气候变化对春季物候变化的影响.结果表明: 研究区植被春季物候开始日期呈现提前趋势,研究期间提前(4.0±0.8) d,其中,欧亚大陆提前速率为(0.22±0.04) d·a^-1,显著高于北美大陆的变化速率(0.03±0.02 d·a^-1);不同植被类型的变化趋势不同,5种方法都显示草地表现为显著提前趋势,而林地的提前趋势不显著.区域平均的植被春季物候开始日期的年际波动主要受春季温度的变化所驱动(r² =0.61,P<0.001), 温度每上升1 ℃,可以导致春季物候提前(3.2±0.5) d,而春季降水影响不显著(P>0.05).     

Using flowering times and leaf numbers to model the phases of photoperiod sensitivity in Antirrhinum majus L

A model has been developed that can be used to determine the phases of sensitivity to photoperiod for seedlings subjected to reciprocal transfers at regular intervals between long (LD) and short day (SD) conditions. The novel feature of this approach is that it enables the simultaneous analysis of the time to flower and number of leaves below the inflorescence. A range of antirrhinum cultivars were grown, all of which were shown to be quantitative long-day plants. Seedlings were effectively insensitive to photoperiod when very young (juvenile). However, after the end of the juvenile phase, SD delayed flowering and increased the number of leaves below the inflorescence. Plants transferred from LD to SD showed a sudden hastening of flowering and a decrease in leaf number once sufficient LD had been received for flower commitment. Photoperiod had little effect on the rate of flower development. The analysis clearly identified major cultivar differences in the length of the juvenile phase and the photoperiod-sensitive inductive phase in both LD and SD.     

Changes in phenological events in response to a global warming scenario reveal greater adaptability of winter annual compared with summer annual arabidopsis ecotypes

Background and AimsThe impact of global warming on life cycle timing is uncertain. We investigated changes in life cycle timing in a global warming scenario. We compared Arabidopsis thaliana ecotypes adapted to the warm/dry Cape Verdi Islands (Cvi), Macaronesia, and the cool/wet climate of the Burren (Bur), Ireland, Northern Europe. These are obligate winter and summer annuals, respectively.MethodsUsing a global warming scenario predicting a 4 °C temperature rise from 2011 to approx. 2080, we produced F₁ seeds at each end of a thermogradient tunnel. Each F₁ cohort (cool and warm) then produced F₂ seeds at both ends of the thermal gradient in winter and summer annual life cycles. F₂ seeds from the winter life cycle were buried at three positions along the gradient to determine the impact of temperature on seedling emergence in a simulated winter life cycle.Key ResultsIn a winter life cycle, increasing temperatures advanced flowering time by 10.1 d °C^–1 in the winter annual and 4.9 d °C^–1 in the summer annual. Plant size and seed yield responded positively to global warming in both ecotypes. In a winter life cycle, the impact of increasing temperature on seedling emergence timing was positive in the winter annual, but negative in the summer annual. Global warming reduced summer annual plant size and seed yield in a summer life cycle.ConclusionsSeedling emergence timing observed in the north European summer annual ecotype may exacerbate the negative impact of predicted increased spring and summer temperatures on their establishment and reproductive performance. In contrast, seedling establishment of the Macaronesian winter annual may benefit from higher soil temperatures that will delay emergence until autumn, but which also facilitates earlier spring flowering and consequent avoidance of high summer temperatures. Such plasticity gives winter annual arabidopsis ecotypes a distinct advantage over summer annuals in expected global warming scenarios. This highlights the importance of variation in the timing of seedling establishment in understanding plant species responses to anthropogenic climate change.     

The phenology of <Emphasis Type="Italic">Rubus fruticosus</Emphasis> in Ireland: herbarium specimens provide evidence for the response of phenophases to temperature,with implications for climate warming

To date, phenological research has provided evidence that climate warming is impacting both animals and plants, evidenced by the altered timing of phenophases. Much of the evidence supporting these findings has been provided by analysis of historic records and present-day fieldwork; herbaria have been identified recently as an alternative source of phenological data. Here, we used Rubus specimens to evaluate herbaria as potential sources of phenological data for use in climate change research and to develop the methodology for using herbaria specimens in phenological studies. Data relevant to phenology (collection date) were recorded from the information cards of over 600 herbarium specimens at Ireland’s National Herbarium in Dublin. Each specimen was assigned a score (0–5) corresponding to its phenophase. Temperature data for the study period (1852 – 2007) were obtained from the University of East Anglia’s Climate Research Unit (CRU); relationships between temperature and the dates of first flower, full flower, first fruit and full fruit were assessed using weighted linear regression. Of the five species of Rubus examined in this study, specimens of only one (R. fruticosus) were sufficiently abundant to yield statistically significant relationships with temperature. The results revealed a trend towards earlier dates of first flower, full flower and first fruit phenophases with increasing temperature. Through its multi-phenophase approach, this research serves to extend the most recent work—which validated the use of herbaria through use of a single phenophase—to confirm herbarium-based research as a robust methodology for use in future phenological studies.     

Changes in the light sensitivity of buried Polygonum aviculare seeds in relation to cold-induced dormancy loss: development of a predictive model

The effect of cold (stratification) temperature on changes in the sensitivity of Polygonum aviculare seeds to light was investigated. Seeds buried in pots were stored under stratification temperatures (1.6, 7 and 12 degrees C) for 137 d. Seeds exhumed at regular intervals during storage were exposed to different light treatments. Germination responses obtained for seeds exposed to different light treatments and stratification temperatures were used to develop a model to predict the sensitivity of buried seeds to light. Seed sensitivity to light increased as dormancy loss progressed, showing the successive acquisition of low-fluence responses (LFR), very low-fluence responses (VLFR), and the loss of the light requirement for germination for a fraction of the seed population. These changes were inversely correlated to stratification temperature, allowing the use of a thermal time index to relate observed changes in seed light sensitivity to stratification temperature. The rate of increase in sensitivity of P. aviculare seeds to light during stratification is inversely correlated to soil temperature, and these changes in light sensitivity could be predicted in relation to temperature using thermal-time models.