Temperature cues phenological synchrony in ant‐mediated seed dispersal

Species‐specific climate responses within ecological communities may disrupt the synchrony of co‐evolved mutualisms that are based on the shared timing of seasonal events, such as seed dispersal by ants (myrmecochory). The spring phenology of plants and ants coincides with marked changes in temperature, light and moisture. We investigate how these environmental drivers influence both seed release by early and late spring woodland herb species, and initiation of spring foraging by seed‐dispersing ants. We pair experimental herbaceous transplants with artificial ant bait stations across north‐ and south‐facing slopes at two contrasting geographic locations. This use of space enables robust identification of plant fruiting and ant foraging cues, and the use of transplants permits us to assess plasticity in plant phenology. We find that warming temperatures act as the primary phenological cue for plant fruiting and ant foraging. Moreover, the plasticity in plant response across locations, despite transplants being from the same source, suggests a high degree of portability in the seed‐dispersing mutualism. However, we also find evidence for potential climate‐driven facilitative failure that may lead to phenological asynchrony. Specifically, at the location where the early flowering species (Hepatica nobilis) is decreasing in abundance and distribution, we find far fewer seed‐dispersing ants foraging during its fruit set than during that of the later flowering Hexastylis arifolia. Notably, the key seed disperser, Aphaenogaster rudis, fails to emerge during early fruit set at this location. At the second location, A. picea forages equally during early and late seed release. These results indicate that climate‐driven changes might shift species‐specific interactions in a plant–ant mutualism resulting in winners and losers within the myrmecochorous plant guild.     

Asymmetric effects of cooler and warmer winters on beech phenology last beyond spring

In temperate trees, the timings of plant growth onset and cessation affect biogeochemical cycles, water, and energy balance. Currently, phenological studies largely focus on specific phenophases and on their responses to warming. How differently spring phenology responds to the warming and cooling, and affects the subsequent phases, has not been yet investigated in trees. Here, we exposed saplings of Fagus sylvatica L. to warmer and cooler climate during the winter 2013–2014 by conducting a reciprocal transplant experiment between two elevations (1,340 vs. 371 m a.s.l., ca. 6°C difference) in the Swiss Jura mountains. To test the legacy effects of earlier or later budburst on the budset timing, saplings were moved back to their original elevation shortly after the occurrence of budburst in spring 2014. One degree decrease in air temperature in winter/spring resulted in a delay of 10.9 days in budburst dates, whereas one degree of warming advanced the date by 8.8 days. Interestingly, we also found an asymmetric effect of the warmer winter vs. cooler winter on the budset timing in late summer. Budset of saplings that experienced a cooler winter was delayed by 31 days compared to the control, whereas it was delayed by only 10 days in saplings that experienced a warmer winter. Budburst timing in 2015 was not significantly impacted by the artificial advance or delay of the budburst timing in 2014, indicating that the legacy effects of the different phenophases might be reset during each winter. Adapting phenological models to the whole annual phenological cycle, and considering the different response to cooling and warming, would improve predictions of tree phenology under future climate warming conditions.     

Spatiotemporal variation in avian migration phenology: citizen science reveals effects of climate change

A growing number of studies have documented shifts in avian migratory phenology in response to climate change, and yet there is a large amount of unexplained variation in the magnitude of those responses across species and geographic regions. We use a database of citizen science bird observations to explore spatiotemporal variation in mean arrival dates across an unprecedented geographic extent for 18 common species in North America over the past decade, relating arrival dates to mean minimum spring temperature. Across all species and geographic locations, species shifted arrival dates 0.8 days earlier for every °C of warming of spring temperature, but it was common for some species in some locations to shift as much as 3-6 days earlier per °C. Species that advanced arrival dates the earliest in response to warming were those that migrate more slowly, short distance migrants, and species with broader climatic niches. These three variables explained 63% of the interspecific variation in phenological response. We also identify a latitudinal gradient in the average strength of phenological response, with species shifting arrival earlier at southern latitudes than northern latitudes for the same degree of warming. This observation is consistent with the idea that species must be more phenologically sensitive in less seasonal environments to maintain the same degree of precision in phenological timing.     

Phenological changes and reduced seasonal synchrony in western Poland

Botanical gardens offer continuity for phenological recording in observers, protocols and plant specimens that may not be achievable from other sources. Here, we examine phenological change and synchrony from one such garden in western Poland. We analysed 66 botanical phenophases and 18 interphase intervals recorded between 1977 and 2007 from the Poznań Botanical Garden. These were examined for trends through time and responsiveness to temperature. Furthermore, we derived measures of synchrony for start of spring and end of autumn events to assess if these had changed over time. All 39 events with a mean date before mid-July demonstrated a significant negative relationship with temperature. Where autumn events were significantly related to temperature, they indicated a positive relationship. Typically, spring events showed an advance over time and autumn events a delay. Interphase intervals tended to lengthen over the study period. The measures of synchrony changed significantly over time suggesting less synchrony among spring events and also among autumn events. In combination, these results suggest increases in growing season length. However, responses to a changing climate were species-specific. Thus, the transitions from winter into spring and from autumn into winter are becoming less clearly defined.     

内蒙古中西部优势植物春季返青对降水的非线性响应

长期以来,研究植被物候变化与气候因子的关系多基于线性模型,事实上植被物候对气候变化的响应可能是非线性的。以1984—2017年内蒙古中西部温性典型草原和温性草原化荒漠长时间序列植被物候观测资料为基础,分析了近40年来气候变化背景下不同草地类型优势植物返青期变化特征及其对春季降水的非线性响应。结果表明:(1)温性典型草原冷蒿返青期主要受水分控制,与春季降水量表现为开口向下的二次函数关系。气候暖干化导致的水分亏缺是冷蒿返青期呈极显著延迟趋势(1.32 d/a)的主要原因;春季降水量超过60 mm时,冷蒿返青期表现出由延迟转变为提前的趋势。(2)温性草原化荒漠猫头刺返青期主要受热量控制。受春季显著升温影响,猫头刺返青期呈极显著提前趋势(0.63 d/a)。春季降水增多利于猫头刺提早返青,二者表现为开口向上的二次函数关系;春季降水量超过40 mm时,猫头刺返青期对降水的响应程度逐渐降低,这可能与荒漠植物本身的生理特性有关。     

Phenology of brown marmorated stink bug described using female reproductive development

Temperature‐based degree‐day models describe insect seasonality and to predict key phenological events. We expand on the use of a temperature‐based process defining timing of reproduction through the incorporation of female reproductive physiology for the invasive pentatomid species Halyomorpha halys, the brown marmorated stink bug. A five‐stage ranking system based on ovary development was able to distinguish between the reproductive statuses of field‐collected females. Application of this ranking method described aspects of H. halys’ seasonality, overwintering biology, and phenology across geographic locations. Female H. halys were collected in the US from NJ, WV, NC, OR, and two sites in PA in 2006–2008 (Allentown, PA only) and 2012–2014. Results identify that H. halys enters reproductive diapause in temperate locations in the fall and that a delay occurs in developmental maturity after diapause termination in the spring. Modification of the Snyder method to identify biofix determined 12.7‐hr photoperiod as the best fit to define initiation of reproduction in the spring. Applying the biofix, we demonstrated significant differences between locations for the rate at which the overwintering generation transition into reproductive status and the factors contributing to this difference require further study. For example, after including abiotic variables influencing development such as temperature and photoperiod (critical diapause cue), reproduction occurred earlier in OR and for an extended period in NJ. This data describe a method to investigate insect seasonality by incorporating physiological development across multiple regions that can clarify phenology for insects with overlapping generations.     

Phenological response to climate change in China: a meta‐analysis

The change in the phenology of plants or animals reflects the response of living systems to climate change. Numerous studies have reported a consistent earlier spring phenophases in many parts of middle and high latitudes reflecting increasing temperatures with the exception of China. A systematic analysis of Chinese phenological response could complement the assessment of climate change impact for the whole Northern Hemisphere. Here, we analyze 1263 phenological time series (1960–2011, with 20+ years data) of 112 species extracted from 48 studies across 145 sites in China. Taxonomic groups include trees, shrubs, herbs, birds, amphibians and insects. Results demonstrate that 90.8% of the spring/summer phenophases time series show earlier trends and 69.0% of the autumn phenophases records show later trends. For spring/summer phenophases, the mean advance across all the taxonomic groups was 2.75 days decade^?1 ranging between 2.11 and 6.11 days decade^?1 for insects and amphibians, respectively. Herbs and amphibians show significantly stronger advancement than trees, shrubs and insect. The response of phenophases of different taxonomic groups in autumn is more complex: trees, shrubs, herbs and insects show a delay between 1.93 and 4.84 days decade^?1, while other groups reveal an advancement ranging from 1.10 to 2.11 days decade^?1. For woody plants (including trees and shrubs), the stronger shifts toward earlier spring/summer were detected from the data series starting from more recent decades (1980s–2000s). The geographic factors (latitude, longitude and altitude) could only explain 9% and 3% of the overall variance in spring/summer and autumn phenological trends, respectively. The rate of change in spring/summer phenophase of woody plants (1960s–2000s) generally matches measured local warming across 49 sites in China (R = ?0.33, P < 0.05).     

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

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

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。     

Variation in spatial and temporal gradients in zooplankton spring development: the effect of climatic factors

1. We examined the temporal and spatial heterogeneity of zooplankton in lake surface waters during the spring of 3 years in Lake Washington, U.S.A., a large lake with a high production of sockeye salmon fry. 2. We show large within‐season and among‐year variation in the horizontal distribution of temperature, chlorophyll a concentration, and zooplankton in the lake. The main pattern, a delay in zooplankton population increase from the north‐ to the south‐end of the lake, recurred in each year and was persistent within each spring. 3. The delay is primarily caused by the development of a temperature gradient during spring warming, as cold mountain water enters the south end of the lake, while warm water enters the north end via a river draining a nearby lake. Climate factors, such as air temperature and precipitation during winter and spring, appear to influence the extent of the delay of zooplankton increase. 4. If the climate continues to warm, the temporal disconnection in zooplankton development between lake areas immediately influenced by cold river inflow and areas that are influenced by spring warming may increase in magnitude. Thus, the different areas of the lake may not contribute equally to fish production.     

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

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

气候变暖背景下青藏高原草本植物物候变化空间换时间预测

气候变暖背景下的植物物候变化广受关注, 然而常用的植物物候变化预测模型未充分考虑植物对环境的适应性, 给预测结果带来了较大的不确定性。该文基于2002-2011年青藏高原10个站点的地面物候观测资料以及年平均气温数据, 对空间换时间模型预测车前(Plantago asiatica)和蒲公英(Taraxacum mongolicum)各主要物候事件(展叶始期、开花始期和黄枯普遍期)变化的可行性及其在升温背景下的变化规律进行了分析。首先利用不同海拔高度的气温和物候事件分别与地理因子(经度、纬度和海拔)建立多元线性回归模型, 然后在此基础上剔除经度和纬度的影响, 单独考察海拔变化所引起的气温与植物物候变化, 最后以海拔高度作为桥梁来考察物候变化与温度变化的关系。结果表明, 采用各站点对应的海拔高度来模拟年平均气温空间差异的R²均大于0.89, 表明海拔梯度可以用来反映时间尺度下的年际温度变化; 车前和蒲公英各物候事件发生日期拟合值均与海拔高度变化关系显著, R²均大于0.70, 表明海拔变化是影响它们各物候事件变化的主要地理因子; 在物候事件发生日期拟合值和年平均气温拟合值的回归方程中, R²均大于0.93, 说明基于不同海拔高度模拟得到的年平均气温变化可以对时间尺度上车前和蒲公英的物候事件变化进行预测。空间换时间预测表明, 温度每升高1 ℃, 车前展叶始期和开花始期分别提前5.1和5.4 d, 而黄枯普遍期推迟4.8 d; 蒲公英展叶始期和开花始期分别提前6.5和7.8 d, 而黄枯普遍期推迟6.7 d。     

Altered geographic and temporal variability in phenology in response to climate change

Aim In response to recent climate warming, numerous studies have reported an earlier onset of spring and, to a lesser degree, a later onset of autumn, both determined from phenological observations. Here, we examine whether these reported changes have affected the synchronization of events on a regional level by examining temporal and spatial variability in phenology. In particular, we study whether years with earlier springs are associated with an altered spatial variability in phenology. Location Germany and the United Kingdom. Methods Plant phenological observations of 35 different phases (events such as flowering and leafing) collected by the German Weather Service (1951–2002) and butterfly phenological records of 29 species collected by the UK Butterfly Monitoring Scheme (1976–2003) are used. In these long‐term records, we examine the temporal (year‐to‐year) variability and the spatial (geographic or between site) variability with particular emphasis on how they vary with time of the year and with earliness or lateness of the phase. Results Early phenological events (i.e. spring) are more variable than later events, both in time and in space, although the pattern is clearer for plants than for butterflies. Confirming previous results, we find a clear relationship between the mean date of spring and summer phases and the degree to which they have become earlier. The spatial variability of spring events is greater in warmer years that have faster plant development. However, late spring and summer events do not show a consistent relationship. Autumn events are somewhat more spatially variable in years characterized by later seasons. Main conclusions This is the first examination of spatial variability of plant and animal phenological events at a multinational scale. Earlier spring events are likely to be associated with increased spatial variability in plants, although this is unlikely to also be true for summer events. If species experience differential changes in geographic variation this may disrupt interactions among them, e.g. in food webs. On the other hand, these may offer advantages for mobile species. Further research on linked species is recommended.     

Rapid northwards expansion of a forest insect pest attributed to spring phenology matching with sub‐Arctic birch

Species range displacements owing to shifts in temporal associations between trophic levels are expected consequences of climate warming. Climate‐induced range expansions have been shown for two irruptive forest defoliators, the geometrids Operophtera brumata and Epirrita autumnata, causing more extensive forest damage in sub‐Arctic Fennoscandia. Here, we document a rapid northwards expansion of a novel irruptive geometrid, Agriopis aurantiaria, into the same region, with the aim of providing insights into mechanisms underlying the recent geometrid range expansions and subsequent forest damage. Based on regional scale data on occurrences and a quantitative monitoring of population densities along the invasion front, we show that, since the first records of larval specimens in the region in 1997–1998, the species has spread northwards to approximately 70°N, and caused severe defoliation locally during 2004–2006. Through targeted studies of larval phenology of A. aurantiaria and O. brumata, as well as spring phenology of birch, along meso‐scale climatic gradients, we show that A. aurantiaria displays a similar dynamics and development as O. brumata, albeit with a consistent phenological lag of 0.75–1 instar. Experiments of the temperature requirements for egg hatching and for budburst in birch showed that this phenological lag is caused by delayed egg hatching in A. aurantiaria relative to O. brumata. A. aurantiaria had a higher development threshold (LDT_A.a.=4.71 °C, LDT_O.b.=1.41 °C), and hatched later and in less synchrony with budburst than O. brumata at the lower end of the studied temperature range. We can conclude that recent warmer springs have provided phenological match between A. aurantiaria and sub‐Arctic birch which may intensify the cumulative impact of geometrid outbreaks on this forest ecosystem. Higher spring temperatures will increase spring phenological synchrony between A. aurantiaria and its host, which suggests that a further expansion of the outbreak range of A. aurantiaria can be expected.     

Water temperature and stratification depth independently shift cardinal events during plankton spring succession

In deep temperate lakes, the beginning of the growing season is triggered by thermal stratification, which alleviates light limitation of planktonic producers in the surface layer and prevents heat loss to deeper strata. The sequence of subsequent phenological events (phytoplankton spring bloom, grazer peak, clearwater phase) results in part from coupled phytoplankton–grazer interactions. Disentangling the separate, direct effects of correlated climatic drivers (stratification‐dependent underwater light climate vs. water temperature) from their indirect effects mediated through trophic feedbacks is impossible using observational field data, which challenges our understanding of global warming effects on seasonal plankton dynamics. We therefore manipulated water temperature and stratification depth independently in experimental field mesocosms containing ambient microplankton and inocula of the resident grazer Daphnia hyalina. Higher light availability in shallower surface layers accelerated primary production, warming accelerated consumption and growth of Daphnia, and both factors speeded up successional dynamics driven by trophic feedbacks. Specifically, phytoplankton peaked and decreased earlier and Daphnia populations increased and peaked earlier at both shallower stratification and higher temperature. The timing of ciliate dynamics was unrelated to both factors. Volumetric peak densities of phytoplankton, ciliates and Daphnia in the surface layer were also unaffected by temperature but declined with stratification depth in parallel with light availability. The latter relationship vanished, however, when population sizes were integrated over the entire water column. Overall our results suggest that, integrated over the entire water column of a deep lake, surface warming and shallower stratification independently speed up spring successional events, whereas the magnitudes of phytoplankton and zooplankton spring peaks are less sensitive to these factors. Therefore, accelerated dynamics under warming need not lead to a trophic mismatch (given similar grazer inocula at the time of stratification). We emphasize that entire water column dynamics must be studied to estimate global warming effects on lake ecosystems.     

Predicting phenology shifts of herbaceous plants on the Qinghai-Xizang Plateau under climate warming with the space-for-time method

气候变暖背景下的植物物候变化广受关注, 然而常用的植物物候变化预测模型未充分考虑植物对环境的适应性, 给预测结果带来了较大的不确定性。该文基于2002-2011年青藏高原10个站点的地面物候观测资料以及年平均气温数据, 对空间换时间模型预测车前(Plantago asiatica)和蒲公英(Taraxacum mongolicum)各主要物候事件(展叶始期、开花始期和黄枯普遍期)变化的可行性及其在升温背景下的变化规律进行了分析。首先利用不同海拔高度的气温和物候事件分别与地理因子(经度、纬度和海拔)建立多元线性回归模型, 然后在此基础上剔除经度和纬度的影响, 单独考察海拔变化所引起的气温与植物物候变化, 最后以海拔高度作为桥梁来考察物候变化与温度变化的关系。结果表明, 采用各站点对应的海拔高度来模拟年平均气温空间差异的R²均大于0.89, 表明海拔梯度可以用来反映时间尺度下的年际温度变化; 车前和蒲公英各物候事件发生日期拟合值均与海拔高度变化关系显著, R²均大于0.70, 表明海拔变化是影响它们各物候事件变化的主要地理因子; 在物候事件发生日期拟合值和年平均气温拟合值的回归方程中, R²均大于0.93, 说明基于不同海拔高度模拟得到的年平均气温变化可以对时间尺度上车前和蒲公英的物候事件变化进行预测。空间换时间预测表明, 温度每升高1 ℃, 车前展叶始期和开花始期分别提前5.1和5.4 d, 而黄枯普遍期推迟4.8 d; 蒲公英展叶始期和开花始期分别提前6.5和7.8 d, 而黄枯普遍期推迟6.7 d。     

Warming counteracts defoliation‐induced mismatch by increasing herbivore‐plant phenological synchrony

Climate change is altering phenology; however, the magnitude of this change varies among taxa. Compared with phenological mismatch between plants and herbivores, synchronization due to climate has been less explored, despite its potential implications for trophic interactions. The earlier budburst induced by defoliation is a phenological strategy for plants against herbivores. Here, we tested whether warming can counteract defoliation‐induced mismatch by increasing herbivore‐plant phenological synchrony. We compared the larval phenology of spruce budworm and budburst in balsam fir, black spruce, and white spruce saplings subjected to defoliation in a controlled environment at temperatures of 12, 17, and 22°C. Budburst in defoliated saplings occurred 6–24 days earlier than in the controls, thus mismatching needle development from larval feeding. This mismatch decreased to only 3–7 days, however, when temperatures warmed by 5 and 10°C, leading to a resynchronization of the host with spruce budworm larvae. The increasing synchrony under warming counteracts the defoliation‐induced mismatch, disrupting trophic interactions and energy flow between forest ecosystem and insect populations. Our results suggest that the predicted warming may improve food quality and provide better growth conditions for larval development, thus promoting longer or more intense insect outbreaks in the future.     

Two sides of a coin: host‐plant synchrony fitness trade‐offs in the population dynamics of the western spruce budworm

Conifer‐feeding budworms emerge from overwintering sites as small larvae in early spring, several days before budburst, and mine old needles. These early‐emerging larvae suffer considerable mortality during this foraging period as they disperse in search of available, current‐year buds. Once buds flush, surviving budworms construct feeding shelters and must complete maturation before fresh host foliage senesces and lignifies later in the summer. Late‐developing larvae suffer greater mortality and survivors have lower fecundity when feeding on older foliage. Thus, there is a seasonal trade‐off in fitness associated with host synchrony: early‐emerging budworms have a greater risk of mortality during spring dispersal but gain better access to the most nutritious foliage, while, on the other hand, late‐emerging larvae incur a lower risk during the initial foraging period but must contend with rapidly diminishing resource quality at the end of the feeding period. We investigate the balance that results from these early‐season and late‐season synchrony fitness trade‐offs using the concept of the phenological window. Parameters associated with the variation in the phenological window are used to estimate generational fitness as a function of host‐plant synchrony. Because defoliation modifies these relationships, it is also included in the analysis. We show that fitness trade‐offs characterizing the phenological window result in a robust synchrony relationship between budworm and host plant over a wide geographic range in southern British Columbia, Canada.     

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.     

Food web de‐synchronization in England's largest lake: an assessment based on multiple phenological metrics

Phenological changes have been observed globally for marine, freshwater and terrestrial species, and are an important element of the global biological ‘fingerprint’ of climate change. Differences in rates of change could desynchronize seasonal species interactions within a food web, threatening ecosystem functioning. Quantification of this risk is hampered by the rarity of long‐term data for multiple interacting species from the same ecosystem and by the diversity of possible phenological metrics, which vary in their ecological relevance to food web interactions. We compare phenological change for phytoplankton (chlorophyll a), zooplankton (Daphnia) and fish (perch, Perca fluviatilis) in two basins of Windermere over 40 years and determine whether change has differed among trophic levels, while explicitly accounting for among‐metric differences in rates of change. Though rates of change differed markedly among the nine metrics used, seasonal events shifted earlier for all metrics and trophic levels: zooplankton advanced most, and fish least, rapidly. Evidence of altered synchrony was found in both lake basins, when combining information from all phenological metrics. However, comparisons based on single metrics did not consistently detect this signal. A multimetric approach showed that across trophic levels, earlier phenological events have been associated with increasing water temperature. However, for phytoplankton and zooplankton, phenological change was also associated with changes in resource availability. Lower silicate, and higher phosphorus, concentrations were associated with earlier phytoplankton growth, and earlier phytoplankton growth was associated with earlier zooplankton growth. The developing trophic mismatch detected between the dominant fish species in Windermere and important zooplankton food resources may ultimately affect fish survival and portend significant impacts upon ecosystem functioning. We advocate that future studies on phenological synchrony combine data from multiple phenological metrics, to increase confidence in assessments of change and likely ecological consequences.