The influence of local spring temperature variance on temperature sensitivity of spring phenology

The impact of climate warming on the advancement of plant spring phenology has been heavily investigated over the last decade and there exists great variability among plants in their phenological sensitivity to temperature. However, few studies have explicitly linked phenological sensitivity to local climate variance. Here, we set out to test the hypothesis that the strength of phenological sensitivity declines with increased local spring temperature variance, by synthesizing results across ground observations. We assemble ground‐based long‐term (20–50 years) spring phenology database (PEP725 database) and the corresponding climate dataset. We find a prevalent decline in the strength of phenological sensitivity with increasing local spring temperature variance at the species level from ground observations. It suggests that plants might be less likely to track climatic warming at locations with larger local spring temperature variance. This might be related to the possibility that the frost risk could be higher in a larger local spring temperature variance and plants adapt to avoid this risk by relying more on other cues (e.g., high chill requirements, photoperiod) for spring phenology, thus suppressing phenological responses to spring warming. This study illuminates that local spring temperature variance is an understudied source in the study of phenological sensitivity and highlight the necessity of incorporating this factor to improve the predictability of plant responses to anthropogenic climate change in future studies.     

Phenology in a warming world: differences between native and non‐native plant species

Phenology is a harbinger of climate change, with many species advancing flowering in response to rising temperatures. However, there is tremendous variation among species in phenological response to warming, and any phenological differences between native and non‐native species may influence invasion outcomes under global warming. We simulated global warming in the field and found that non‐native species flowered earlier and were more phenologically plastic to temperature than natives, which did not accelerate flowering in response to warming. Non‐native species' flowering also became more synchronous with other community members under warming. Earlier flowering was associated with greater geographic spread of non‐native species, implicating phenology as a potential trait associated with the successful establishment of non‐native species across large geographic regions. Such phenological differences in both timing and plasticity between native and non‐natives are hypothesised to promote invasion success and population persistence, potentially benefiting non‐native over native species under climate change.     

Prairie plant phenology driven more by temperature than moisture in climate manipulations across a latitudinal gradient in the Pacific Northwest,USA

Plant phenology will likely shift with climate change, but how temperature and/or moisture regimes will control phenological responses is not well understood. This is particularly true in Mediterranean climate ecosystems where the warmest temperatures and greatest moisture availability are seasonally asynchronous. We examined plant phenological responses at both the population and community levels to four climate treatments (control, warming, drought, and warming plus additional precipitation) embedded within three prairies across a 520 km latitudinal Mediterranean climate gradient within the Pacific Northwest, USA. At the population level, we monitored flowering and abundances in spring 2017 of eight range‐restricted focal species planted both within and north of their current ranges. At the community level, we used normalized difference vegetation index (NDVI) measured from fall 2016 to summer 2018 to estimate peak live biomass, senescence, seasonal patterns, and growing season length. We found that warming exerted a stronger control than our moisture manipulations on phenology at both the population and community levels. Warming advanced flowering regardless of whether a species was within or beyond its current range. Importantly, many of our focal species had low abundances, particularly in the south, suggesting that establishment, in addition to phenological shifts, may be a strong constraint on their future viability. At the community level, warming advanced the date of peak biomass regardless of site or year. The date of senescence advanced regardless of year for the southern and central sites but only in 2018 for the northern site. Growing season length contracted due to warming at the southern and central sites (~3 weeks) but was unaffected at the northern site. Our results emphasize that future temperature changes may exert strong influence on the timing of a variety of plant phenological events, especially those events that occur when temperature is most limiting, even in seasonally water‐limited Mediterranean ecosystems.     

Phenological response of tundra plants to background climate variation tested using the International Tundra Experiment

The rapidly warming temperatures in high-latitude and alpine regions have the potential to alter the phenology of Arctic and alpine plants, affecting processes ranging from food webs to ecosystem trace gas fluxes. The International Tundra Experiment (ITEX) was initiated in 1990 to evaluate the effects of expected rapid changes in temperature on tundra plant phenology, growth and community changes using experimental warming. Here, we used the ITEX control data to test the phenological responses to background temperature variation across sites spanning latitudinal and moisture gradients. The dataset overall did not show an advance in phenology; instead, temperature variability during the years sampled and an absence of warming at some sites resulted in mixed responses. Phenological transitions of high Arctic plants clearly occurred at lower heat sum thresholds than those of low Arctic and alpine plants. However, sensitivity to temperature change was similar among plants from the different climate zones. Plants of different communities and growth forms differed for some phenological responses. Heat sums associated with flowering and greening appear to have increased over time. These results point to a complex suite of changes in plant communities and ecosystem function in high latitudes and elevations as the climate warms.     

Contrasting effects of warming and increased snowfall on Arctic tundra plant phenology over the past two decades

Recent changes in climate have led to significant shifts in phenology, with many studies demonstrating advanced phenology in response to warming temperatures. The rate of temperature change is especially high in the Arctic, but this is also where we have relatively little data on phenological changes and the processes driving these changes. In order to understand how Arctic plant species are likely to respond to future changes in climate, we monitored flowering phenology in response to both experimental and ambient warming for four widespread species in two habitat types over 21 years. We additionally used long‐term environmental records to disentangle the effects of temperature increase and changes in snowmelt date on phenological patterns. While flowering occurred earlier in response to experimental warming, plants in unmanipulated plots showed no change or a delay in flowering over the 21‐year period, despite more than 1 °C of ambient warming during that time. This counterintuitive result was likely due to significantly delayed snowmelt over the study period (0.05–0.2 days/yr) due to increased winter snowfall. The timing of snowmelt was a strong driver of flowering phenology for all species – especially for early‐flowering species – while spring temperature was significantly related to flowering time only for later‐flowering species. Despite significantly delayed flowering phenology, the timing of seed maturation showed no significant change over time, suggesting that warmer temperatures may promote more rapid seed development. The results of this study highlight the importance of understanding the specific environmental cues that drive species’ phenological responses as well as the complex interactions between temperature and precipitation when forecasting phenology over the coming decades. As demonstrated here, the effects of altered snowmelt patterns can counter the effects of warmer temperatures, even to the point of generating phenological responses opposite to those predicted by warming alone.     

Seasonality in the equatorial tropics: Flower,fruit, and leaf phenology of montane trees in the highlands of Southwest Uganda

Phenology influences many forest functions and can inform forest conservation and management, yet representative phenological data for most common tropical forest tree species remain sparse or absent. Between June 2011 and December 2013, we investigated flowering, fruiting, and leafing patterns in the Bwindi Impenetrable National Park, a montane forest located near the equator in Uganda, drawing on 16,410 observations of 530 trees of 54 species located between 2066 and 2527 m in elevation. The park's climate is equatorial with two wet and dry seasons each year. Flowering and fruiting were strongly seasonal while patterns in leafing were less pronounced. Flower occurrence peaked at the beginning of the short dry season followed by a pronounced trough during the beginning and the middle of the short wet season. Fruit occurrence had a pronounced peak during high rainfall months in March through April with most fruits ripening during drier months in May through July. Fruit scarcity was observed for a 4-month period spanning September to December and most flushing of leaves noted at the end of the wet season in November and December. Our binomial generalized linear mixed models indicated that flowering and fruiting were negatively associated with temperature and that leafing activity was positively associated with rainfall and temperature. These findings are consistent with the insolation- and water-limitation hypotheses suggesting that the seasonally varying availability of resources such as light, water, and nutrients determines these phenological patterns. Ideally, prolonged, multi-year community-level studies would be supported so as to better characterize the influence of climate and of climate variability.     

河北省草本植物物候特征及其对气候变暖的响应

以1981—2006年河北省8个国家农业气象观测站的草本植物物候观测资料和47个气象站的地面观测资料为基础,运用EOF和REOF等统计学方法,研究了河北省草本植物物候期的变化特征及其对气候变暖的响应。结果表明:河北省草本植物展叶始期总体呈提前趋势,其中东部沿海平原提前趋势最大,中南部平原次之,西北部山区最小;黄枯始期主要表现出推迟趋势,生长季长度以延长趋势为主;春季气温对展叶始期的影响显著,河北省春季气温上升1℃,草本植物展叶始期提前4.1d;各站点生长季倾向率与年均温倾向率呈正相关,即年均温升幅大的站点,生长季延长的幅度也较大;草本植物物候变化特征及其对气候变暖的响应与木本植物基本一致,研究结果对丰富河北省物候与气候变化关系研究具有一定意义。     

European phenological response to climate change matches the warming pattern

Global climate change impacts can already be tracked in many physical and biological systems; in particular, terrestrial ecosystems provide a consistent picture of observed changes. One of the preferred indicators is phenology, the science of natural recurring events, as their recorded dates provide a high-temporal resolution of ongoing changes. Thus, numerous analyses have demonstrated an earlier onset of spring events for mid and higher latitudes and a lengthening of the growing season. However, published single-site or single-species studies are particularly open to suspicion of being biased towards predominantly reporting climate change-induced impacts. No comprehensive study or meta-analysis has so far examined the possible lack of evidence for changes or shifts at sites where no temperature change is observed. We used an enormous systematic phenological network data set of more than 125 000 observational series of 542 plant and 19 animal species in 21 European countries (1971–2000). Our results showed that 78% of all leafing, flowering and fruiting records advanced (30% significantly) and only 3% were significantly delayed, whereas the signal of leaf colouring/fall is ambiguous. We conclude that previously published results of phenological changes were not biased by reporting or publication predisposition: the average advance of spring/summer was 2.5 days decade⁻¹ in Europe. Our analysis of 254 mean national time series undoubtedly demonstrates that species' phenology is responsive to temperature of the preceding months (mean advance of spring/summer by 2.5 days°C⁻¹, delay of leaf colouring and fall by 1.0 day°C⁻¹). The pattern of observed change in spring efficiently matches measured national warming across 19 European countries (correlation coefficient r =−0.69, P <0.001).     

The roles of shifting and filtering in generating community‐level flowering phenology

Plant phenologies are key components of community assembly and ecosystem function, yet we know little about how phenological patterns differ among ecosystems. Community‐level phenological patterns may be driven by the filtering of species into communities based on their phenology or by intraspecific responses to local conditions that shift when species flower. To understand the relative roles of filtering and shifting on community‐level phenological patterns we compared patterns of first flowering dates (FFD) for herbaceous species at Konza Prairie, KS, USA with those from the colder Fargo, ND, USA area and from Chinnor, England, which has a less continental climate. Comparing patterns of FFD supports that Konza's flowering patterns are potentially influenced both by filtering species that flower early in the growing season and by phenological shifting. Konza species flowering dates were earlier in the spring and later in the fall compared to Fargo, but were not shifted compared to Chinnor, which had a unique suite of early‐flowering species. In all, comparing flowering phenology among three sites reveals that intraspecific responses to climate can generate phenological shifts that compress or stretch community‐level phenological patterns, while novel niches in phenological space can also alter community‐level patterns. Community flowering patterns related to climate suggest that climatic warming has the potential to further distribute flowering of the Konza flora over a longer period, but also could further open it to introductions of non‐native species that have evolved to flower early in the season.     

Prediction of Arctic plant phenological sensitivity to climate change from historical records

The pace of climate change in the Arctic is dramatic, with temperatures rising at a rate double the global average. The timing of flowering and fruiting (phenology) is often temperature dependent and tends to advance as the climate warms. Herbarium specimens, photographs, and field observations can provide historical phenology records and have been used, on a localised scale, to predict species’ phenological sensitivity to climate change. Conducting similar localised studies in the Canadian Arctic, however, poses a challenge where the collection of herbarium specimens, photographs, and field observations have been temporally and spatially sporadic. We used flowering and seed dispersal times of 23 Arctic species from herbarium specimens, photographs, and field observations collected from across the 2.1 million km² area of Nunavut, Canada, to determine (1) which monthly temperatures influence flowering and seed dispersal times; (2) species’ phenological sensitivity to temperature; and (3) whether flowering or seed dispersal times have advanced over the past 120 years. We tested this at different spatial scales and compared the sensitivity in different regions of Nunavut. Broadly speaking, this research serves as a proof of concept to assess whether phenology–climate change studies using historic data can be conducted at large spatial scales. Flowering times and seed dispersal time were most strongly correlated with June and July temperatures, respectively. Seed dispersal times have advanced at double the rate of flowering times over the past 120 years, reflecting greater late‐summer temperature rises in Nunavut. There is great diversity in the flowering time sensitivity to temperature of Arctic plant species, suggesting climate change implications for Arctic ecological communities, including altered community composition, competition, and pollinator interactions. Intraspecific temperature sensitivity and warming trends varied markedly across Nunavut and could result in greater changes in some parts of Nunavut than in others.     

西安和宝鸡木本植物花期物候变化及温度敏感度对比

植物物候是指示生态系统对气候变化响应的重要证据。已有研究多基于代表性站点的物候观测数据研究物候特征及其对气候变化的响应规律。同一气候区内,不同站点的物候变化及对温度变化响应的敏感度是否一致仍需深入探讨。本文选择同属于暖温带湿润区汾渭平原气候区的西安和宝鸡为研究区,利用"中国物候观测网"在两个站点21个共有物种的开花始期和开花末期数据,比较了1987—2016年两站点各植物花期物候变化特征及其对温度变化响应的敏感度差异。结果表明,西安和宝鸡各物种的开花始期和开花末期均以提前趋势为主。大部分物种开花始期在西安的提前趋势(平均趋势-0.57 d/a)明显强于在宝鸡的提前趋势(平均趋势-0.29 d/a),但开花末期趋势差异不显著。除紫薇和迎春的敏感度差异较大外,其他物种开花始期和开花末期的温度敏感度在两站点间非常接近,无显著差异。由此可见,在同一气候区的不同站点,因增温幅度不同,植物的始花期变化存在较大差异,不能用单站点的物候变化反映整个气候区的物候变化。但同一植物在单站点的温度敏感度可以较好的反映同一气候区其他站点的植物物候-气候关系。本文研究结果可为利用有限站点的物候观测数据分析区域物候变化及对气候变化的响应提供科学依据。     

Greater temperature sensitivity of plant phenology at colder sites: implications for convergence across northern latitudes

Warmer temperatures are accelerating the phenology of organisms around the world. Temperature sensitivity of phenology might be greater in colder, higher latitude sites than in warmer regions, in part because small changes in temperature constitute greater relative changes in thermal balance at colder sites. To test this hypothesis, we examined up to 20 years of phenology data for 47 tundra plant species at 18 high‐latitude sites along a climatic gradient. Across all species, the timing of leaf emergence and flowering was more sensitive to a given increase in summer temperature at colder than warmer high‐latitude locations. A similar pattern was seen over time for the flowering phenology of a widespread species, Cassiope tetragona. These are among the first results highlighting differential phenological responses of plants across a climatic gradient and suggest the possibility of convergence in flowering times and therefore an increase in gene flow across latitudes as the climate warms.     

Disentangling the paradox of insect phenology: are temporal trends reflecting the response to warming?

The strength and direction of phenological responses to changes in climate have been shown to vary significantly both among species and among populations of a species, with the overall patterns not fully resolved. Here, we studied the temporal and spatial variability associated with the response of several insect species to recent global warming. We use hierarchical models within a model comparison framework to analyze phenological data gathered over 40 years by the Japan Meteorological Agency on the emergence dates of 14 insect species at sites across Japan. Contrary to what has been predicted with global warming, temporal trends of annual emergence showed a later emergence day for some species and sites over time, even though temperatures are warming. However, when emergence data were analyzed as a function of temperature and precipitation, the overall response pointed out an earlier emergence day with warmer conditions. The apparent contradiction between the response to temperature and trends over time indicates that other factors, such as declining populations, may be affecting the date phenological events are being recorded. Overall, the responses by insects were weaker than those found for plants in previous work over the same time period in these ecosystems, suggesting the potential for ecological mismatches with deleterious effects for both suites of species. And although temperature may be the major driver of species phenology, we should be cautious when analyzing phenological datasets as many other factors may also be contributing to the variability in phenology.     

Photographs and herbarium specimens as tools to document phenological changes in response to global warming

Global warming is affecting natural systems across the world. Of the biological responses to warming, changes in the timing of phenological events such as flowering are among the most sensitive. Despite the recognized importance of phenological changes, the limited number of long-term records of phenological events has restricted research on the topic in most areas of the world. In a previous study in Boston (American Journal of Botany 91: 1260-1264), we used herbarium specimens and one season of field observations to show that plants flowered earlier as the climate warmed over the past 100 yr. In our new study, we found that two extra years of data did not strengthen the explanatory power of the analysis. Analysis of herbarium specimens without any field data yielded results similar to analyses that included field observations. In addition, we found that photographs of cultivated and wild plants in Massachusetts, data similar to that contained in herbarium specimens, show changes in flowering times that closely match independent data on the same species in the same locations. Dated photographs of plants in flower represent a new resource to extend the range of species and localities addressed in global-warming research.     

One man, 73 years, and 25 species. Evaluating phenological responses using a lifelong study of first flowering dates

Phenological shifts linked to global warming reflect the ability of organisms to track changing climatic conditions. However, different organisms track global warming differently and there is an increasing interest in the link between phenological traits and plant abundance and distribution. Long-term data sets are often used to estimate phenological traits to climate change, but so far little has been done to evaluate the quality of these estimates. Here, we use a 73-year long data series of first flowering dates for 25 species from north-temperate Sweden to evaluate (i) correlations between first flowering dates and year for different time periods and (ii) linear regression models between first flowering date and mean monthly temperatures in preceding months. Furthermore, we evaluate the potential of this kind of data to estimate the phenological temperature sensitivities (i.e. number of days phenological change per degree temperature change, β₆₀) in such models. The sign of the correlations between first flowering dates and year were highly inconsistent among different time periods, highlighting that estimates of phenological change are sensitive to the specific time period used. The first flowering dates of all species were correlated with temperature, but with large differences in both the strength of the response and the period(s) of the year that were most strongly associated with phenological variation. Finally, our analyses indicated that legacy data sets need to be relatively long-term to be useful for estimating phenological temperature sensitivities (β₆₀) for inter-specific comparisons. In 10-year long observation series only one out of 24 species reached ≥80 % probability of estimating temperature sensitivity (β₆₀) within a ±1 range, and 17 out of 24 species reached ≥80 % probability when observation series were 20 years or shorter. The standard error for β₆₀ ranged from 0.6 to 2.0 for 10-year long observation series, and 19 out of 24 species reached SE < 1 after 15 years. In general, late flowering species will require longer time series than early flowering species.     

Synchrony in the phenology of a culturally iconic spring flower

We examine the flowering phenology of the cultural iconic Spring Snowflake Leucojum vernum, a considerable tourist attraction, recorded from two sites in western Poland. Flowering dates at the two sites were closely correlated but about 6 days later at the more natural area. The end of flowering was associated with the start of canopy leafing. Early flowering was related to a longer flowering season which may benefit ecotourism under future climate warming.     

Herbarium specimens reveal the footprint of climate change on flowering trends across north‐central North America

Shifting flowering phenology with rising temperatures is occurring worldwide, but the rarity of co‐occurring long‐term observational and temperature records has hindered the evaluation of phenological responsiveness in many species and across large spatial scales. We used herbarium specimens combined with historic temperature data to examine the impact of climate change on flowering trends in 141 species collected across 116,000 km² in north‐central North America. On average, date of maximum flowering advanced 2.4 days °C⁻¹, although species‐specific responses varied from − 13.5 to + 7.3 days °C⁻¹. Plant functional types exhibited distinct patterns of phenological responsiveness with significant differences between native and introduced species, among flowering seasons, and between wind‐ and biotically pollinated species. This study is the first to assess large‐scale patterns of phenological responsiveness with broad species representation and is an important step towards understanding current and future impacts of climate change on species performance and biodiversity.     

Links between plant species’ spatial and temporal responses to a warming climate

To generate realistic projections of species’ responses to climate change, we need to understand the factors that limit their ability to respond. Although climatic niche conservatism, the maintenance of a species’s climatic niche over time, is a critical assumption in niche-based species distribution models, little is known about how universal it is and how it operates. In particular, few studies have tested the role of climatic niche conservatism via phenological changes in explaining the reported wide variance in the extent of range shifts among species. Using historical records of the phenology and spatial distribution of British plants under a warming climate, we revealed that: (i) perennial species, as well as those with weaker or lagged phenological responses to temperature, experienced a greater increase in temperature during flowering (i.e. failed to maintain climatic niche via phenological changes); (ii) species that failed to maintain climatic niche via phenological changes showed greater northward range shifts; and (iii) there was a complementary relationship between the levels of climatic niche conservatism via phenological changes and range shifts. These results indicate that even species with high climatic niche conservatism might not show range shifts as instead they track warming temperatures during flowering by advancing their phenology.     

The response of <Emphasis Type="Italic">Corylus avellana</Emphasis> L. phenology to rising temperature in north-eastern Slovenia

Knowledge of plant–weather relationships can improve crop management, resulting in higher quality and more stable crop yields. The annual timing of spring phenophases in mid-latitudes is largely a response to temperature, and reflects the thermal conditions of previous months. The effect of air temperature on the variability of hazelnut (Corylus avellana L.) phenophases (leafing, flowering) was investigated. Meteorological and phenological data for five cultivars were analysed over the periods 1969–1979 (P1) and 1994–2007 (P2) in Maribor, Slovenia. Phenological data series were correlated strongly to the temperature of the preceding months (R ²: 0.64–0.98) and better correlated to daily maximum and mean temperatures than to daily minimum temperatures. About 75% of phenophases displayed a tendency towards earlier appearance and a shorter flowering duration during P2, which could be explained by the significant temperature changes (+0.3°C/decade) from December to April between 1969 and 2007. An increase in air temperature of 1°C caused an acceleration in leafing by 2.5–3.9 days, with flowering showing higher sensitivity since a 1°C increase promoted male flowering by 7.0–8.8 days and female flowering by 6.3–8.9 days. The average rate of phenological change per degree of warming (days earlier per +1°C) did not differ significantly between P1 and P2. An estimation of chilling accumulation under field conditions during 1993–2009, between 1 November and 28 February, showed that all four of these months contributed approximately similar amounts of accumulated chilling units. The growing degree days (GDD) to flowering were calculated by an estimated base temperature of 2°C and 1 January as a starting date, given the most accurate calculations. In general, thermal requirements were greater in P2 than in P1, although this difference was not significant. Longer-time series data extended to other agricultural and wild plants would be helpful in tracking possible future changes in phenological responses to local climate.