International Phenological Gardens Research Articles

Continental-scale evaluation of downy birch pollen production: Estimating the impacts of global change

The high prevalence of hay fever in Europe has raised concerns about the implications of climate change-induced higher temperatures on pollen production. Our study focuses on downy birch pollen production across Europe by analyzing 456 catkins during 2019–2021 in 37 International Phenological Gardens (IPG) spanning a large geographic gradient. As IPGs rely on genetically identical plants, we were able to reduce the effects of genetic variability. We studied the potential association with masting behavior and three model specifications based on mean and quantile regression to assess the impact of meteorology (e.g., temperature and precipitation) and atmospheric gases (e.g., ozone (O3) and carbon-dioxide (CO2)) on pollen and catkin production, while controlling for tree age approximated by stem circumference. The results revealed a substantial geographic variability in mean pollen production, ranging from 1.9 to 2.5 million pollen grains per catkin. Regression analyses indicated that elevated average temperatures of the previous summer corresponded to increased pollen production, while higher O3 levels led to a reduction. Additionally, catkins number was positively influenced by preceding summer's temperature and precipitation but negatively by O3 levels. The investigation of quantile effects revealed that the impacts of mean temperature and O3 levels from the previous summer varied throughout the conditional response distribution. We found that temperature predominantly affected trees characterized by a high pollen production. We therefore suggest that birches modulate their physiological processes to optimize pollen production under varying temperature regimes. In turn, O3 levels negatively affected trees with pollen production levels exceeding the conditional median. We conclude that future temperature increase might exacerbate pollen production while other factors may modify (decrease in the case of O3 and amplify for precipitation) this effect. Our comprehensive study sheds light on potential impacts of climate change on downy birch pollen production, which is crucial for birch reproduction and human health.

Comparison of the timing of spring phenological events between phenological garden trees and wild populations

Abstract Phenological research is engaged in monitoring the influence of climate change on the natural environment. The International Phenological Gardens (IPG) network provides a valuable dataset of standardized tree phenology records dating back to the mid-20th century. To make best use of this actively growing record, it is important to investigate how network data can be applied to predict the timing of phenological events in natural populations. This study compared clonally propagated IPG downy birch (Betula pubescens Ehrh.) and hazel (Corylus avellana L.) specimens of central European provenance to nearby wild populations at the western-most margin of the IPG network, in the south-west of Ireland. In addition to monitoring by trained scientists, observations by citizen scientists were included. The order of the timing of phenological events among sites was consistent across 2 years, confirming reproducibility of the results. IPG trees had the earliest B. pubescens leaf unfolding and C. avellana flowering dates of the sites studied. In addition, leaf unfolding occurred later in the wild populations than expected from the temperature responses of the B. pubescens and C. avellana IPG clones. Natural variation in phenology also exceeded the historical change observed at the IPG site, suggesting a potential genetic basis for climate adaptation. Trunk circumference, reflecting the age-dependent increase in tree size, was found to influence C. avellana phenology, with earlier timing of phenological events in larger trees. This finding highlights tree size as an important consideration in the management of phenological gardens and tree phenology research in general.

Phenological response to temperature variability and orography in Central Italy

Even if the sensitivity of vegetation phenology to climate change has been accepted on global and continental scales, the correlation between global warming and phenotypic variability shows a modulated answer depending on altitude, latitude, and the local seasonal thermal trend. To connect global patterns of change with local effects, we investigated the impact of the observed signal of warming found in Central Italy on two different willow species, Salix acutifolia and Salix smithiana, growing in three phenological gardens of the International Phenological Gardens’ network (IPG) located in different orographic positions. The time series of temperatures and phenological data for the period 2005–2018 were analysed first to find trends over time in the three gardens and then to correlate the recent local warming and the change in the two species phenology. The results confirmed the correlation between phenological trends and local trend of temperatures. In particular: budburst showed a trend of advancement of 1.4 days/year on average in all three gardens; flowering showed a divergent pattern between the gardens of either advancement of 1.0 days/year on average or delay of 1.1 days/year on average; while senescence showed a delay reaching even 3.3 days/year, although significant in only two gardens for both species. These trends were found to be correlated mainly with the temperatures of the months preceding the occurrence of the phase, with a shift in terms of days of the year (DOY) of the two species. Our conclusion is that the observed warming in Central Italy played a key role in controlling the phenophases occurrences of the two willow species, and that the orographic forcing leads to the different shift in DOY of phenophases (from 5 to 20 days) due to the local thermal forcing of the three phenological gardens.

Comparing in situ spring phenology and satellite-derived start of season at rural and urban sites in Ireland

ABSTRACT The timing of spring phenology marks the start of the growing season and the beginning of the carbon-uptake period. In order to accurately calculate carbon budgets across different vegetation types, reliable start-of-season data over relatively large areas is necessary. However, in-situ phenological observation networks are generally restricted in their geographical extent and limited to a small number of species, typically dominant trees. Satellite remote sensing can provide spatially extensive phenological information but requires validation with in-situ observations. Here, we examined trends (1968–2016) in the timing of leaf-unfolding (LU) as well as growing-season-length (GSL), derived from in-situ observations, of a suite of deciduous trees, at three rural sites and one urban site in Ireland, all of which are within the International Phenological Gardens network. We compared in-situ trends with satellite derived phenometrics, including start of greening increase and GSL, based on two-band Enhanced Vegetation Index (EVI2) from a combined AVHRR and MODIS time-series over the time period 1982–2016. The aim of this study was to assess the effectiveness of satellite remote sensing in capturing LU and GSL as determined by in-situ observations from sites dominated by varying land cover types. The timing of LU (DOY 111) at the urban site was significantly (p < 0.000) later than all rural sites, apart from one (1982–2016). The significantly (p < 0.000) longer (2–5 weeks) GSL (217 days), at the urban site, was thus driven by delayed leaf fall (LF). Satellite derived Start of Season (SOS) was consistently earlier than LU across all sites (RMSE 25–52d; MBE −5 to −50 d) whereas EVI2-derived GSL was consistently longer than in situ data (RMSE 65–102d; MBE 45 to 96 d). Overall, the discrepancies reported here between the timing of in-situ spring phenology and satellite-derived phenometrics at these sites were possibly due to a combination of factors including differences in scale between the two methods, the small number of cloned trees being monitored, which does not appear to represent the broader landscape vegetation, the heterogeneity of the landscape and technical differences between the satellite sensors used to construct the EVI2 time-series. Addressing these issues is challenging but engaging citizen scientists to monitor local vegetation would increase the spatial coverage of the in-situ observation network while also incorporating a broader range of species some of which would undoubtedly represent native vegetation.

Phenology of leaf development in European beech (Fagus sylvatica) on a site in Ljubljana, Slovenia in 2020

In spring of 2020 we observed leaf phenology in mature European beech (Fagus sylvatica) trees in Tivoli, Rožnik and Šišenski hrib Landscape Park in Ljubljana, Slovenia (46.05°N, 14.49°E, 310 m a. s. l.). A group of 11 trees was selected for daily monitoring of leaf development. We recorded seven phases from dormant buds, through leaf unfolding till development of mature leaves. At the same time, photos were taken to illustrate the leaf development. First developing leaves were observed on 4 April in one tree. General leaf unfolding, as defined by International Phenological Gardens (IPG), was observed in different trees between 7 and 25 April 2020. The occurrence and duration of individual phases of leaf development showed great variation within and between trees. General leaf unfolding of the tree included in the long-term monitoring program of the Environmental Agency of the Republic of Slovenia (ARSO) occurred on DOY 105 (14 April 2020), which is 4 days earlier than long-term average of the same tree/location, and this is ascribed to above average temperatures in the winter of 2019/2020.

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.

Utilizing a Thermal Time Model to Estimate Safe Times to Transplant Tilia Trees

City trees planted in parks and along streets are typically grown to large size in nurseries before being transplanted to their final growing sites. According to tendering rules within the European Union (EU), any business may compete for public contracts in any EU country, and this applies to purchases of valuable lots of nursery trees. There is however a risk of poor transplanting success if the trees are imported from very distant locations with a different pace of spring development. The aim of this study was to implement a Thermal Time model to predict the spring development of Tilia trees to find out in which geographical area the spring development is sufficiently similar to conditions in southern Finland, so that the success of transplantation of the trees is not unduly risked. We used phenological observations collected at the International Phenological Gardens (IPGs) over the whole of Europe, together with ERA-Interim weather data to estimate the model parameters, and then used the same date to predict the onset of leaf unfolding ofTilia during the years 1980 to 2015. Producing maps of phenological development of Tilia, we concluded that there are no large risks of frost damage if tree import area is limited to northern parts of Baltics or to the west coast of Scandinavia.

Fifteen-year phenological plant species and meteorological trends in central Italy

The present study was carried out in a phenological garden in central Italy that contains vegetative clones of shrubs and trees common to several international phenological gardens, such as Cornus sanguinea L.; Corylus avellana L.; Ligustrum vulgare L.; Robinia pseudoacacia L.; Salix acutifolia Willd. and Sambucus nigra L. Vegetative plant growth monitoring was carried out weekly using common international keys: BBCH07, bud break and leaf unfolding; BBCH19, young unfolded leaf; BBCH91, adult leaves; BBCH93, beginning of leaf colouring. The phenological dates thus obtained provide a model of the development for these different species in relation to the 15-year period of observation (1997-2011). From a meteorological point of view, temperature and precipitation trends were studied, with the highest anomalies during the study period recorded during the first 2months of the year (January, February). There was relative invariance in the manifestation of the open bud phase and the contemporary advance of the young open leaves phase, particularly from 2006. This was accompanied by shortening of the leaf opening period, which appeared due to more rapid spring temperature increases over the last few years. The advance tendency of the BBCH91 phase showed adult leaves from the first summer weeks with fully green foliage monitored for a long time. Generally, the autumn leaf colouring phase tended to remain constant, with the exception of Salix acutifolia and Sambucus nigra, for which, on the other hand, the first leaf development phases appeared to be most likely influenced by the photoperiod.

Recherches sur la phénologie de différentes espèces décidues sous climat méditerranéen

Phenological stages are the result of biorhythms and environmental factors, these last are probably the same ones that caused, during evolution, adjustments of the species to different climate. The present study was carried out in a Phenological Garden located in central Italy (Perugia, Umbria Region) which contains indicator species, common to all International Phenological Gardens. The aim of this study was to determine and analyse the average trends of development of eight plant species and their phenological adjustment to the Mediterranean environment, over a nine-year period (1997–2005). The results of the statistical analyses show a strong relationship between the temperature trends and vegetative seasonal evolutions interpreted by phenological data for all the species considered. Moreover, it was demonstrated that the plants studied may approach or close completely the timing gaps eventually created during the first phenological phases, adjusting thus the beginning of subsequent phenophases.

Changes in Tree Phenology: an Indicator of Spring Warming in Ireland?

Recent climate warming has been observed at the global scale, but by examining developmental stages of plant species (phenology) that are dependent on local climatic conditions, climate change at the local scale can be detected. There are four gardens in Ireland belonging to the International Phenological Gardens (IPG) network, which has recorded tree phenology for more than 30 years using a common collection of clonal tree species and cultivars. In this analysis two phenological stages were investigated */the beginning of the growing season (BGS) and the end of the growing season (EGS) */ in nine tree cultivars in relation to ambient air temperature. The length of the growing season (LGS) was determined from the number of days between BGS and EGS. Structural time series analysis was used to describe trends in the data. Overall BGS was the most responsive phenophase and was shown to start earlier in more recent years for some species at all sites. It is shown that these observations are due to recent climate change in the form of spring warming, particularly in the south-west of the country. Due to the limited number of observation sites and differences between species responses, we suggest that extrapolation of the results to larger geographical areas should be performed with caution.

CHANGES IN TREE PHENOLOGY: AN INDICATOR OF SPRING WARMING IN IRELAND?

Recent climate warming has been observed at the global scale, but by examining developmental stages of plant species (phenology) that are dependent on local climatic conditions, climate change at the local scale can be detected. There are four gardens in Ireland belonging to the International Phenological Gardens (IPG) network, which has recorded tree phenology for more than 30 years using a common collection of clonal tree species and cultivars. In this analysis two phenological stages were investigated—the beginning of the growing season (BGS) and the end of the growing season (EGS)— in nine tree cultivars in relation to ambient air temperature. The length of the growing season (LGS) was determined from the number of days between BGS and EGS. Structural time series analysis was used to describe trends in the data. Overall BGS was the most responsive phenophase and was shown to start earlier in more recent years for some species at all sites. It is shown that these observations are due to recent climate change in the form of spring warming, particularly in the south-west of the country. Due to the limited number of observation sites and differences between species responses, we suggest that extrapolation of the results to larger geographical areas should be performed with caution.

‘SSW to NNE’– North Atlantic Oscillation affects the progress of seasons across Europe

AbstractThree European plant phenological network datasets were analysed for latitudinal and longitudinal gradients of nine phenological ‘seasons’ spanning the entire year. The networks were: (1) the historical first European Phenological Network (1882–1941) by Hoffmann &amp; Ihne, (2) the network of the International Phenological Gardens in Europe (1959–1998), founded by Schnelle &amp; Volkert in 1957 and based on cloned plants, and (3) a dataset (1951–1998) that was recently collated during the EU Fifth Framework project POSITIVE, which included network data of seven Central and Eastern European countries. Our study is most likely the first, for over a century, to analyse average onset and year‐to‐year variability of the progress of seasons across a continent. For early, mid, and late spring seasons we found a marked progress of the seasonal onset from SW to NE throughout Europe, more precisely from WSW to ENE in early spring, then from SW to NE and finally from SSW to NNE in late spring, as exhibited by the relationship between latitudinal and longitudinal gradients. The movement of summer was more south to north directed, as the longitudinal gradient (west–east component) strongly declined or was even of opposite sign. Autumn, as shown by leaf colouring dates, arrived from NE to SW. Possible reasons for the differences among the three datasets are discussed. The annual variability of latitudinal and longitudinal gradients of the seasons across Europe was closely related to the North Atlantic Oscillation (NAO) index; in years with high NAO in both winter and spring, the west–east component of progress was more pronounced; in summer and autumn, the pattern of the seasons may be more uniform.

Atmospheric mechanisms governing the spatial and temporal variability of phenological phases in central Europe

AbstractA data set of 17 phenological phases from Germany, Austria, Switzerland and Slovenia spanning the time period from 1951 to 1998 has been made available for analysis together with a gridded temperature data set (1° × 1° grid) and the North Atlantic Oscillation (NAO) index time series. The disturbances of the westerlies constitute the main atmospheric source for the temporal variability of phenological events in Europe. The trend, the standard deviation and the discontinuity of the phenological time series at the end of the 1980s can, to a great extent, be explained by the NAO. A number of factors modulate the influence of the NAO in time and space. The seasonal northward shift of the westerlies overlaps with the sequence of phenological spring phases, thereby gradually reducing its influence on the temporal variability of phenological events with progression of spring (temporal loss of influence). This temporal process is reflected by a pronounced decrease in trend and standard deviation values and common variability with the NAO with increasing year‐day. The reduced influence of the NAO with increasing distance from the Atlantic coast is not only apparent in studies based on the data set of the International Phenological Gardens, but also in the data set of this study with a smaller spatial extent (large‐scale loss of influence). The common variance between phenological and NAO time series displays a discontinuous drop from the European Atlantic coast towards the Alps. On a local and regional scale, mountainous terrain reduces the influence of the large‐scale atmospheric flow from the Atlantic via a proposed ‘decoupling mechanism’. Valleys in mountainous terrain have the inclination to harbour temperature inversions over extended periods of time during the cold season, which isolate the valley climate from the large‐scale atmospheric flow at higher altitudes. Most phenological stations reside at valley bottoms and are thus largely decoupled in their temporal variability from the influence of the westerly flow regime (local‐scale loss of influence). This study corroborates an increasing number of similar investigations that find that vegetation does react in a sensitive way to variations of its atmospheric environment across various temporal and spatial scales. Copyright © 2002 Royal Meteorological Society.

Annual and spatial variability of the beginning of growing season in Europe in relation to air temperature changes

To investigate the annual and spatial variability in the beginning of growing season across Europe, phenological data of the International Phenological Gardens for the period 1969-1998 were used. The beginning of growing season (BGS) was defined as an average leaf unfolding index of 4 tree species (Betula pubescens, Prunus avium, Sorbus aucuparia and Ribes alpinum). The study shows significant changes in the mean air temperatures from February to April and in the average BGS in Europe since 1989. In the last decade the mean temperature in early spring increased by 0.8°C. As a result the average BGS advanced by 8 d. Between 1989 and 1998, 8 out of 10 years tend towards an earlier onset of spring. The earliest date was observed in 1990. The relationships between air temperature and the beginning of growing season across Europe were investigated by canonical correlation analysis (CCA). The spatial variability of both fields can be described by 3 pairs of CCA patterns. The first pattern, which explains most of the variance, shows a uniform structure with above (below) normal temperatures in whole Europe and consequently an advanced (delayed) beginning of growing season. The other 2 patterns show regional differences in the anomaly fields. Whereas the second CCA pattern has a meridional structure, the third pattern shows a zonal distribution. In all cases the anomalies of the regional air temperature and of the beginning of growing season corre- spond very well. The correlation coefficients between the anomaly fields range between 0.90 and 0.66. For all patterns appropriate examples in the observed data were found.

Response of tree phenology to climate change across Europe

To investigate the impact of recent climatic changes on the plant development in Europe, this study uses phenological data of the International Phenological Gardens for the period 1969–1998. For this study, the leafing dates of four tree species ( Betula pubescens, Prunus avium, Sorbus aucuparia and Ribes alpinum) were combined in an annual leaf unfolding index to define the beginning of growing season. The end of growing season was defined using the average leaf fall of B. pubescens, P. avium, Salix smithiana and R. alpinum. A nearly Europe-wide warming in the early spring (February–April) over the last 30 years (1969–1998) led to an earlier beginning of growing season by 8 days. The observed trends in the onset of spring corresponded well with changes in air temperature and circulation ( North Atlantic Oscillation Index (NAO-index)) across Europe. In late winter and early spring, the positive phase of NAO increased clearly, leading to prevailing westerly winds and thus to higher temperatures in the period February–April. Since the end of the 1980s the changes in circulation, air temperature and the beginning of spring time were striking. The investigation showed that a warming in the early spring (February–April) by 1°C causes an advance in the beginning of growing season of 7 days. The observed extension of growing season was mainly the result of an earlier onset of spring. An increase of mean annual air temperature by 1°C led to an extension of 5 days.

Trends in phenological phases in Europe between 1951 and 1996.

Increases in air temperature due to the anthropogenic greenhouse effect can be detected easily in the phenological data of Europe within the last four decades because spring phenological events are particularly sensitive to temperature. Our new analysis of observational data from the International Phenological Gardens in Europe for the 1959-1996 period revealed that spring events, such as leaf unfolding, have advanced on average by 6.3 days (-0.21 day/year), whereas autumn events, such as leaf colouring, have been delayed on average by 4.5 days (+0.15 day/year). Thus, the average annual growing season has lengthened on average by 10.8 days since the early 1960s. For autumn events, differences between mean trends of species could not be detected, but for spring events there were differences between species, with the higher trends for leaf unfolding and flowering of shrubs indicating that changes in events occurring in the early spring are more distinct. These observed trends in plant phenological events in the International Phenological Gardens and results of other phenological studies in Europe, summarised in this study, are consistent with AVHRR satellite measurements of the normalized difference vegetation index from 1981 to 1991 and with an analysis of long-term measurements of the annual cycle of CO2 concentration in Hawaii and Alaska, also indicating a global lengthening of the growing season.

Phenology and seasonality of woody plants: An unappreciated element in global change research?

It is regrettable, but not surprising, that phenology has received relatively little attention from ecologists. Phenological data are hard won, accumulating only slowly through careful, daily observations not well suited to the demands of a thesis project or a grant cycle. Organizing coordinated and standardized observations over many sites and many years is a daunting task not much in keeping with the priorities of most granting agencies. Until very recently, it was impractical to simulate realistic diurnal and seasonal climate regimes as a basis for controlled phenological experiments (Wang et al. 1994). Despite these difficulties work on the phenology of woody plants has continued and invites incorporation into a variety of ecological analyses. We convened a symposium at the XVth International Botanical Congress to highlight contemporary work on the phenology of woody species in the hope that this topic would gain wider recognition and support. The papers that follow include most of those presented at the symposium. Helmut Lieth, who has long appreciated the importance of phenological studies (1974), provided an excellent introduction to the symposium. He reported on the long tradition of phenological observation, including contemporary efforts like the International Phenological Gardens that include clonal plantings at sites throughout Europe (Polte-Rudolf 1993). He emphasized the availability of long-term historical records of phenological observations (Lieth 1974; Polte-Rudolf 1993), which provide a basis and reference for current work. Martin Lechowicz drew on some of these historical records to explore the interrelationships among reproductive events and foliar phenology in eastern North American deciduous trees. Kihachiro Kikuzawa presented an overview of his models for foliar phenology, including an outline of their recent extension to questions of coordination between canopy architecture, leaf physiology, and leaf phenology. Takayoshi Koike reports an experimental study that followed the phenological as well as physiological responses of tree seedlings to ele-