Effects of experimental shifts in flowering phenology on plant-pollinator interactions

Climate change has led to phenological shifts in flowering plants and insect pollinators, causing concern that these shifts will disrupt plant-pollinator mutualisms. We experimentally investigated how shifts in flowering onset affect pollinator visitation for 14 native perennial plant species, six of which have exhibited shifts to earlier flowering over the last 70 years and eight of which have not. We manipulated flowering onset in greenhouses and then observed pollinator visitation in the field. Five of six species with historically advanced flowering received more visits when flowering was experimentally advanced, whereas seven of eight species with historically unchanged flowering received fewer visits when flowering earlier. This pattern suggests that species unconstrained by pollinators have advanced their flowering, whereas species constrained by pollinators have not. In contrast to current concern about phenological mismatches disrupting plant-pollinator mutualisms, mismatches at the onset of flowering are not occurring for most of our study species.     

Biodiversity ensures plant–pollinator phenological synchrony against climate change

Climate change has the potential to alter the phenological synchrony between interacting mutualists, such as plants and their pollinators. However, high levels of biodiversity might buffer the negative effects of species‐specific phenological shifts and maintain synchrony at the community level, as predicted by the biodiversity insurance hypothesis. Here, we explore how biodiversity might enhance and stabilise phenological synchrony between a valuable crop, apple and its native pollinators. We combine 46 years of data on apple flowering phenology with historical records of bee pollinators over the same period. When the key apple pollinators are considered altogether, we found extensive synchrony between bee activity and apple peak bloom due to complementarity among bee species’ activity periods, and also a stable trend over time due to differential responses to warming climate among bee species. A simulation model confirms that high biodiversity levels can ensure plant–pollinator phenological synchrony and thus pollination function.     

Methods in phenological mapping

Summary Phenological maps of flowering provide useful information about both spatial and temporal patterns of pollen emission, and their use could bring a substantial improvement of aerobiological forecasts. This paper presents a method for preparing flowering maps by computer on the basis of phenological data and topography. Data drawn from topographic maps are processed with the aid of an empirical model, based on the relationships between phenology and environment, for obtaining a phenological delay matrix. From this matrix it is possible to derive automatically various kinds of maps (chronological, synoptical and differential). An application is described, relating to the blooming patterns of a set of wild plants in a mountainous area of Northern Italy.     

Phylogenetic conservatism and trait correlates of spring phenological responses to climate change in northeast China

Climate change has resulted in major changes in plant phenology across the globe that includes leaf‐out date and flowering time. The ability of species to respond to climate change, in part, depends on their response to climate as a phenological cue in general. Species that are not phenologically responsive may suffer in the face of continued climate change. Comparative studies of phenology have found phylogeny to be a reliable predictor of mean leaf‐out date and flowering time at both the local and global scales. This is less true for flowering time response (i.e., the correlation between phenological timing and climate factors), while no study to date has explored whether the response of leaf‐out date to climate factors exhibits phylogenetic signal. We used a 52‐year observational phenological dataset for 52 woody species from the Forest Botanical Garden of Heilongjiang Province, China, to test phylogenetic signal in leaf‐out date and flowering time, as well as, the response of these two phenological traits to both temperature and winter precipitation. Leaf‐out date and flowering time were significantly responsive to temperature for most species, advancing, on average, 3.11 and 2.87 day/°C, respectively. Both leaf‐out and flowering, and their responses to temperature exhibited significant phylogenetic signals. The response of leaf‐out date to precipitation exhibited no phylogenetic signal, while flowering time response to precipitation did. Native species tended to have a weaker flowering response to temperature than non‐native species. Earlier leaf‐out species tended to have a greater response to winter precipitation. This study is the first to assess phylogenetic signal of leaf‐out response to climate change, which suggests, that climate change has the potential to shape the plant communities, not only through flowering sensitivity, but also through leaf‐out sensitivity.     

西双版纳地区鞘花的繁殖物候特征及影响因素

桑寄生植物作为关键种和关键性食物资源在生态系统中扮演着重要角色,其鞘花的繁殖物候特征不仅会影响自身的繁殖适合度而且还会影响依赖于其获取食物资源的动物。为了解鞘花的繁殖物候特征及其影响因素,探究其与寄主植物和种子散布者之间的相互作用关系。该研究以西双版纳地区分布的鞘花为对象,通过定期观测鞘花和其寄主植物木荷的繁殖物候,测量它们的生物学特性和温湿度等环境因子,并分析鞘花在个体水平和种群水平上的繁殖物候特征以及寄主植物和温湿度对其繁殖物候的影响。结果表明:(1)鞘花的开花物候属于集中大量开花模式,整个种群的花期和果期的持续时间分别约为20 d和72 d,花期和果期的同步性指数都较高,6月中旬鞘花果实被取食的数量和速率最大,之后逐渐降低。(2)鞘花的始花期与木荷的始花期相关性较高,花期和果期与木荷的繁殖物候基本重叠。(3)每月开花和果熟的个体数量与同期和前一个月的平均温度和相对湿度的相关关系均不显著。总之,桑寄生植物的繁殖物候特征可能受到较多因素的影响,若想全面了解半寄生植物的繁殖物候特征,就要综合考虑生物和非生物等多种因子的共同作用。     

Genetic and physiological bases for phenological responses to current and predicted climates

We are now reaching the stage at which specific genetic factors with known physiological effects can be tied directly and quantitatively to variation in phenology. With such a mechanistic understanding, scientists can better predict phenological responses to novel seasonal climates. Using the widespread model species Arabidopsis thaliana, we explore how variation in different genetic pathways can be linked to phenology and life-history variation across geographical regions and seasons. We show that the expression of phenological traits including flowering depends critically on the growth season, and we outline an integrated life-history approach to phenology in which the timing of later life-history events can be contingent on the environmental cues regulating earlier life stages. As flowering time in many plants is determined by the integration of multiple environmentally sensitive gene pathways, the novel combinations of important seasonal cues in projected future climates will alter how phenology responds to variation in the flowering time gene network with important consequences for plant life history. We discuss how phenology models in other systems—both natural and agricultural—could employ a similar framework to explore the potential contribution of genetic variation to the physiological integration of cues determining phenology.     

Delayed reproduction in Arabidopsis thaliana improves fitness in soil with suboptimal phosphorus availability

Low phosphorus availability (low P) often delays flowering and maturity in annual plants, while abiotic stress generally accelerates flowering and maturity. The utility of this response is unknown. We hypothesize that phenological delay in low P is beneficial by permitting more time for phosphorus acquisition and utilization. We grew seven genotypes of Arabidopsis thaliana with contrasting phenology in high and low P. Low P delayed bolting and maturity in all genotypes. Low P decreased root length, but not root-length duration (the integral of root length over time), because phenological delay allowed low-P plants to compensate for shorter root length. Root-length duration was correlated with phosphorus accumulation. Leaf phosphorus duration (the integral of leaf phosphorus over time) was correlated with reproductive biomass, indicating the utility of increased phosphorus utilization. Phenological delays accounted for up to 30% of biomass production when low-P plants were compared to models of plants with no delays. These results support the hypothesis that phenological delay in low P is adaptive and leads to increased phosphorus acquisition and utilization. Because low P conditions are prevalent, understanding the utility of this response could be useful in crop breeding and in predicting plant responses to global climate change.     

Beyond gradual warming: extreme weather events alter flower phenology of European grassland and heath species

Shifts in the phenology of plant and animal species or in the migratory arrival of birds are seen as ‘fingerprints’ of global warming. However, even if such responses have been documented in large continent‐wide datasets of the northern hemisphere, all studies to date correlate the phenological pattern of various taxa with gradual climatic trends. Here, we report a previously unobserved phenomenon: severe drought and heavy rain events caused phenological shifts in plants of the same magnitude as one decade of gradual warming. We present data from two vegetation periods in an experimental setting containing the first evidence of shifted phenological response of 10 grassland and heath species to simulated 100‐year extreme weather events in Central Europe. Averaged over all species, 32 days of drought significantly advanced the mid‐flowering date by 4 days. The flowering length was significantly extended by 4 days. Heavy rainfall (170 mm over 14 days) had no significant effect on the mid‐flowering date. However, heavy rainfall reduced the flowering length by several days. Observed shifts were species‐specific, (e.g. drought advanced the mid‐flowering date for Holcus lanatus by 1.5 days and delayed the mid‐flowering date for Calluna vulgaris by 5.7 days, heavy rain advanced mid‐flowering date of Lotus corniculatus by 26.6 days and shortened the flowering length of the same species by 36.9 days). Interestingly, the phenological response of individual species was modified by community composition. For example, the mid‐flowering date of C. vulgaris was delayed after drought by 9.3 days in communities composed of grasses and dwarf shrubs compared with communities composed of dwarf shrubs only. This indicates that responses to extreme events are context specific. Additionally, the phenological response of experimental communities to extreme weather events can be modified by the functional diversity of a stand. Future studies on phenological response patterns related to climate change would profit from explicitly addressing the role of extreme weather events.     

Urbanisation induces early flowering: evidence from <Emphasis Type="Italic">Platanus acerifolia</Emphasis> and <Emphasis Type="Italic">Prunus cerasus</Emphasis>

The effect of towns on plant phenology, i.e. advancement of spring development compared with a rural environment, via the urban heat island (UHI) phenomenon, has been shown for many towns in many countries. This work combines experimental and observational methodology to provide a better and deeper view of climatic habitat in an urban context with a view to understanding the relationship between plant development and urban climate on the intra-urban scale (by taking into account town structure). A dense network of 17 meteorological stations was set up in Rennes, France, enabling us to identify and quantify climatic changes associated with the UHI. Meanwhile, phenological observations were made during early spring (March and April) in 2005 on Platanus acerifolia and Prunus cerasus to study the relationship between climatic and phenological data. The results show that there is both a climatic gradient and a developmental gradient corresponding to the type of urbanisation in the town of Rennes. The town influences plant phenology by reducing the diurnal temperature range and by increasing the minimum temperature as one approaches the town centre. The influence of ground cover type (plants or buildings) on development is also shown. The developmental phases of preflowering and flowering are influenced to differing extents by climatic variables. The period during which climatic variables are effective before a given developmental phase varies considerably. The preflowering phases are best correlated with the mean of the minimum air temperature for the 15-day period before the observation, whereas flowering appears to be more dependent on the mean of the daily diurnal temperature range for the 8 days preceding the observation.     

Forecasting flowering dates of lawn species with air temperature: Application boundaries of the linear approach

Summary A modelling analysis was performed on the phenological data collected for three years in a lawn located at the Operational Meteorological Centre of S. Pietro Capofiume, Bologna, Italy. The data concern the flowering of up to 56 wild species and were taken according to a seven-stage phenological key. The analysis was performed in order to verify the predictive limits of the degreeday model, an approach assuming a linear functional relationship between air temperature and the rate of phenological development. The procedure we followed consists in the heuristic assessment of the three parameters characterizing the linear model, that is the starting date before which the temperature has no influence on the anthesic development, the base temperature, and the temperature sum. With that in mind, we determined the temperature sums for all the pairs of parameter values taken in the range (– ÷ 15° C) for base temperatures, and in the range (January I^m ÷ flowering date) for starting dates. Not all the species examined produced stable parameter sets but a test of the latter against independent data showed data, where applicable, the linear approach provides a reliable forecasting tool. The linear approach was also applied in order to determine the existence of leading species, that is species whose flowering dates could represent the staring date of temperature accumulation in order to forecast the flowering date of later species. In this case the determination of base temperatures and temperature sums derives from the assumption that when the leading species attains flowering the predicted one has reached an unknown but fixed fraction of its own phenological development. We applied this procedure to all the possible pairs of species and in this case the stability test produced a drastic selection among them.     

Climate change and the optimal flowering time of annual plants in seasonal environments

Long‐term phenology monitoring has documented numerous examples of changing flowering dates during the last century. A pivotal question is whether these phenological responses are adaptive or not under directionally changing climatic conditions. We use a classic dynamic growth model for annual plants, based on optimal control theory, to find the fitness‐maximizing flowering time, defined as the switching time from vegetative to reproductive growth. In a typical scenario of global warming, with advanced growing season and increased productivity, optimal flowering time advances less than the start of the growing season. Interestingly, increased temporal spread in production over the season may either advance or delay the optimal flowering time depending on overall productivity or season length. We identify situations where large phenological changes are necessary for flowering time to remain optimal. Such changes also indicate changed selection pressures. In other situations, the model predicts advanced phenology on a calendar scale, but no selection for early flowering in relation to the start of the season. We also show that the optimum is more sensitive to increased productivity when productivity is low than when productivity is high. All our results are derived using a general, graphical method to calculate the optimal flowering time applicable for a large range of shapes of the seasonal production curve. The model can thus explain apparent maladaptation in phenological responses in a multitude of scenarios of climate change. We conclude that taking energy allocation trade‐offs and appropriate time scales into account is critical when interpreting phenological patterns.     

Phenological diversity in tropical forests

One of the most intriguing and complex characteristics of reproductive phenology in tropical forests is high diversity within and among forests. To understand such diversity, Newstrom et al. provided a systematic framework for the classification of tropical flowering phenology. They adopted frequency and regularity as criteria with priority, and classified plants in La Selva, Costa Rica, where most plants reproduced more than once a year irregularly. Many other studies have demonstrated annual cycles corresponding to rainfall patterns at the community level in Neotropical forests, including La Selva. On the other hand, supraannual flowering synchronized among various plant species, called general flowering, is known from aseasonal lowland dipterocarp forests in Southeast Asia. Within both forests, a wide spectrum of flowering patterns is found. This range of patterns suggests the great potential of tropical phenological studies to explore the selective pressures on phenology. Various abiotic and biotic factors can be selective agents. The shared pollinators hypothesis suggests that plant species sharing pollinators segregate flowering temporarily to minimize interspecific overlap in flowering times and thus minimize ineffective pollination or competition for pollinators, indicating strong phylogenetic constraints in timing and variation of flowering. Comparison of phenology within and among forests may help our understanding of phenological diversity. Attempts are now being made to develop a common language to communicate concepts and render interpretations of data more compatible among investigators and to create a network to promote comparative studies. Received: September 8, 2000 / Accepted: January 30, 2001     

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.     

Habitat-specific responses in the flowering phenology and seed set of alpine plants to climate variation: implications for global-change impacts

The timing of the snowmelt is a crucial factor in determining the phenological schedule of alpine plants. A long-term monitoring of snowmelt regimes in a Japanese alpine area revealed that the onset of the snowmelt season has been accelerated during the last 17 years in early snowmelt sites but that such a trend has not been detected in late snowmelt sites. This indicates that the global warming effect on the snowmelt pattern may be site-specific. The flowering phenology of fellfield plants in an exposed wind-blown habitat was consistent between an unusually warm year (1998) and a normal year (2001). In contrast, the flowering occurrence of snowbed plants varied greatly between the years depending on the snowmelt time. There was a large number of flowering species in the fellfield community from mid- to late to late June and from mid- to late July. The flowering peak of an early-melt snowbed plant community was in the middle of the flowering season and that of a late-melt snowbed community was in the early flowering season. These habitat-specific phenological patterns were consistent between 1998 and 2001. The effects of the variation in flowering timing on seed-set success were evaluated for an entomophilous snowbed herb, Peucedanum multivittatum, along the snowmelt gradient during a 5-year period. When flowering occurred prior to early August, mean temperature during the flowering season positively influenced the seed set. When flowering occurred later than early August, however, the plants enjoyed high seed-set success irrespective of temperature conditions if frost damage was absent. These observations are probably explained based on the availability of pollinators, which depends not only on ambient temperature but also on seasonal progress. These results suggest that the effects of climate change on biological interaction may vary depending on the specific habitat in the alpine ecosystem in which diverse snowmelt patterns create complicated seasonality for plants within a very localized area.     

浙江古田山亚热带常绿阔叶林开花物候:气候因素、系统发育关系和功能性状的影响

植物的开花物候受气候因素、植物系统发育关系和功能性状的影响。然而当前植物开花物候研究中未见同时考虑这3个因素的报道。为了解它们相互之间的影响, 本研究利用中国东部地区浙江省古田山国家级自然保护区亚热带常绿阔叶林24 ha大样地(GTS; 118°03′50′′-118°11′12.2′′ E, 29°10′19′′-29°17′41′′ N)设置的130个种子雨收集器5年的开花数据检验这3个因素对开花的影响。结果表明, 古田山植物的开花高峰期集中在5月, 群落开花格局明显受温度和降雨的影响。利用植物DNA条形码数据研究发现, 植物间系统发育关系对古田山植物开花时间有显著影响, 亲缘关系近的物种开花时间更相近。植物的平均开花时间受最大树高的影响, 但不受传粉方式、花色、种子质量和扩散方式的影响。该研究结果说明气候因素、植物系统发育关系和功能性状都可能影响植物开花物候格局, 同时考虑这3个因素能够帮助我们更好地理解开花物候格局。     

Predictors of plant phenology in a diverse high‐latitude alpine landscape: growth forms and topography

Question: Different plant growth forms may have distinctly different functioning in ecosystems. Association of phenological patterns with growth form will therefore help elucidate the role of phenology in an ecosystem. We ask whether growth forms of common vascular plants differ in terms of vegetative and flowering phenology, and if such phenological differences are consistent across environmental gradients caused by landscape‐scale topography. Location: A high‐latitude alpine landscape in Finnmark County, Norway (70°N). Methods: We assessed vegetative and flowering phenology repeatedly in five growth forms represented by 11 common vascular plant species across an altitudinal gradient and among differing slope aspects. Results: Species phenology clustered well according to growth form, and growth form strongly explained variation in both flowering and vegetative phenology. Altitude and aspect were poor predictors of phenological variation. Vegetative phenology of the growth forms, ranked from slowest to fastest, was in the order evergreen shrubs <sedges‐deciduous shrubs <grasses <forbs, while a reverse ranking was found for flowering phenology. Conclusion: Growth form‐specific phenological patterns are associated with fundamentally different abilities for resource acquisition and resource conservation. The weak effect of landscape‐scale topographic factors indicates that variation within growth forms is mainly influenced by local environmental factors not accounted for in this study. On the basis of these results, we argue that growth forms should be considered as predictors of phenology together with the customary use of topography and normalized difference vegetation index, especially when assessing the role of phenology in an ecosystem.     

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.     

POLLINATOR-MEDIATED SELECTION ON FLORAL DISPLAY AND FLOWERING TIME IN THE PERENNIAL HERB ARABIDOPSIS LYRATA

The evolution of floral display and flowering time in animal-pollinated plants is commonly attributed to pollinator-mediated selection. Yet, the causes of selection on flowering phenology and traits contributing to floral display have rarely been tested experimentally in natural populations. We quantified phenotypic selection on morphological and phenological characters in the perennial, outcrossing herb Arabidopsis lyrata in two years using female reproductive success as a proxy of fitness. To determine whether selection on floral display and flowering phenology can be attributed to interactions with pollinators, selection was quantified both for open-pollinated controls and for plants receiving supplemental hand-pollination. We documented directional selection for many flowers, large petals, late start of flowering, and early end of flowering. Seed output was pollen-limited in both years and supplemental hand-pollination reduced the magnitude of selection on number of flowers, and reversed the direction of selection on end of flowering. The results demonstrate that interactions with pollinators may affect the strength of selection on floral display and the direction of selection on phenology of flowering in natural plant populations. They thus support the contention that pollinators can drive the evolution of both floral display and flowering time.     

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.     

植物与传粉者物候错配效应研究进展

开花植物与传粉者之间稳定互惠模式的建立是维持互作双方种群适合度的关键。在全球变化的背景下,植物与传粉者对温度、融雪、人类活动等外界扰动的响应差异,易于引起两者关键物候期的不同步发生,由此可能减少传粉互作的重叠时间,改变相互作用的成本和收益,进而对两者的种群动态产生潜在的深远影响（即物候错配效应）。近年来国内外对植物花期与传粉者活动物候的错配研究主要集中在两方面：一是物候错配现象发生的原因及机制;二是这种物候错配带来的生态后果,尤其是对互惠双方种群动态的影响。但由于研究方法及数据获取等方面的局限性,物候错配研究仍存在一些薄弱环节,如物候匹配模式对环境变化的响应机制、传粉效率对错配效应的调节影响、物候数据获取的独立性等。本文综述了植物-传粉者物候错配效应的最新研究进展,并对未来的研究展望进行初步探讨,以期为物种多样性、动植物种群动态的合理预测等方面的研究提供有益的参考。