Impact of climate change on plant phenology in Mediterranean ecosystems

Plant phenology is strongly controlled by climate and has consequently become one of the most reliable bioindicators of ongoing climate change. We used a dataset of more than 200 000 records for six phenological events of 29 perennial plant species monitored from 1943 to 2003 for a comprehensive assessment of plant phenological responses to climate change in the Mediterranean region. Temperature, precipitation and North Atlantic Oscillation (NAO) were studied together during a complete annual cycle before phenological events to determine their relative importance and potential seasonal carry‐over effects. Warm and dry springs under a positive phase of NAO advance flowering, leaf unfolding and fruiting dates and lengthen the growing season. Spatial variability of dates (range among sites) was also reduced during warm and dry years, especially for spring events. Climate during previous weeks to phenophases occurrence had the greatest impact on plants, although all events were also affected by climate conditions several months before. Immediate along with delayed climate effects suggest dual triggers in plant phenology. Climatic models accounted for more than 80% of variability in flowering and leaf unfolding dates, and in length of the growing season, but for lower proportions in fruiting and leaf falling. Most part of year‐to‐year changes in dates was accounted for temperature, while precipitation and NAO accounted for <10% of dates' variability. In the case of flowering, insect‐pollinated species were better modelled by climate than wind‐pollinated species. Differences in temporal responses of plant phenology to recent climate change are due to differences in the sensitivity to climate among events and species. Spring events are changing more than autumn events as they are more sensitive to climate and are also undergoing the greatest alterations of climate relative to other seasons. In conclusion, climate change has shifted plant phenology in the Mediterranean region.     

Alpine grassland plants grow earlier and faster but biomass remains unchanged over 35 years of climate change

Satellite data indicate significant advancement in alpine spring phenology over decades of climate warming, but corresponding field evidence is scarce. It is also unknown whether this advancement results from an earlier shift of phenological events, or enhancement of plant growth under unchanged phenological pattern. By analyzing a 35‐year dataset of seasonal biomass dynamics of a Tibetan alpine grassland, we show that climate change promoted both earlier phenology and faster growth, without changing annual biomass production. Biomass production increased in spring due to a warming‐induced earlier onset of plant growth, but decreased in autumn due mainly to increased water stress. Plants grew faster but the fast‐growing period shortened during the mid‐growing season. These findings provide the first in situ evidence of long‐term changes in growth patterns in alpine grassland plant communities, and suggest that earlier phenology and faster growth will jointly contribute to plant growth in a warming climate.     

Predicting insect phenology across space and time

Many species appear to be undergoing shifts in phenology, arising from climate change. To predict the direction and magnitude of future changes requires an understanding of how phenology depends on climatic variation. Species show large‐scale spatial variation in phenology (affected by differentiation among populations) as well as variation in phenology from year‐to‐year at the same site (affected predominantly by local plasticity). Teasing apart spatial and temporal variation in phenology should allow improved predictions of phenology under climate change. This study is the first to quantify large‐scale spatial and temporal variation in the entire emergence pattern of species, and to test the relationships found by predicting future data. We use data from up to 33 years of permanent transect records of butterflies in the United Kingdom to fit and test models for 15 butterfly species. We use generalized additive models to model spatial and temporal variation in the distribution of adult butterflies over the season, allowing us to capture changes in the timing of emergence peaks, relative sizes of peaks and/or number of peaks in a single analysis. We develop these models using data for 1973–2000, and then use them to predict phenologies from 2001 to 2006. For six of our study species, a model with only spatial variation in phenology is the best predictor of the future, implying that these species have limited plasticity. For the remaining nine species, the best predictions come from a model with both spatial and temporal variation in phenology; for four of these, growing degree‐days have similar effects over space and time, implying high levels of plasticity. The results show that statistical phenology models can be used to predict phenology shifts in a second time period, suggesting that it should be feasible to project phenologies under climate change scenarios, at least over modest time scales.     

The timing of autumn senescence is affected by the timing of spring phenology: implications for predictive models

Autumn senescence regulates multiple aspects of ecosystem function, along with associated feedbacks to the climate system. Despite its importance, current understanding of the drivers of senescence is limited, leading to a large spread in predictions of how the timing of senescence, and thus the length of the growing season, will change under future climate conditions. The most commonly held paradigm is that temperature and photoperiod are the primary controls, which suggests a future extension of the autumnal growing season as global temperatures rise. Here, using two decades of ground‐ and satellite‐based observations of temperate deciduous forest phenology, we show that the timing of autumn senescence is correlated with the timing of spring budburst across the entire eastern United States. On a year‐to‐year basis, an earlier/later spring was associated with an earlier/later autumn senescence, both for individual species and at a regional scale. We use the observed relationship to develop a novel model of autumn phenology. In contrast to current phenology models, this model predicts that the potential response of autumn phenology to future climate change is strongly limited by the impact of climate change on spring phenology. Current models of autumn phenology therefore may overpredict future increases in the length of the growing season, with subsequent impacts for modeling future CO₂ uptake and evapotranspiration.     

Unexpected role of winter precipitation in determining heat requirement for spring vegetation green‐up at northern middle and high latitudes

Heat requirement, expressed in growing degree days (GDD), is a widely used method to assess and predict the effect of temperature on plant development. Until recently, the analysis of spatial patterns of GDD requirement for spring vegetation green‐up onset was limited to local and regional scales, mainly because of the sparse and aggregated spatial availability of ground phenology data. Taking advantage of the large temporal and spatial scales of remote sensing‐based green‐up onset data, we studied the spatial patterns of GDD requirement for vegetation green‐up at northern middle and high latitudes. We further explored the correlations between GDD requirement for vegetation green‐up and previous winter season chilling temperatures and precipitation, using spatial partial correlations. We showed that GDD requirement for vegetation green‐up onset declines towards the north at a mean rate of 18.8 °C‐days per degree latitude between 35°N and 70°N, and vary significantly among different vegetation types. Our results confirmed that the GDD requirement for vegetation green‐up is negatively correlated with previous winter chilling, which was defined as the number of chilling days from the day when the land surface froze in the previous autumn to the day of green‐up onset. This negative correlation is a well‐known phenomenon from local studies. Interestingly, irrespective of the vegetation type, we also found a positive correlation between the GDD requirement and previous winter season precipitation, which was defined as the sum of the precipitation of the month when green‐up onset occur and the precipitation that occurred during the previous 2 months. Our study suggests that GDD requirement, chilling and precipitation may have complex interactions in their effects on spring vegetation green‐up phenology. These findings have important implications for improving phenology models and could therefore advance our understanding of the interplay between spring phenology and carbon fluxes.     

Strong evidence for changing fish reproductive phenology under climate warming on the Tibetan Plateau

Phenological responses to climate change have been widely observed and have profound and lasting effects on ecosystems and biodiversity. However, compared to terrestrial ecosystems, the long‐term effects of climate change on species’ phenology are poorly understood in aquatic ecosystems. Understanding the long‐term changes in fish reproductive phenology is essential for predicting population dynamics and for informing management strategies, but is currently hampered by the requirement for intensive field observations and larval identification. In this study, a very low‐frequency sampling of juveniles and adults combined with otolith measurements (long axis length of the first annulus; LAFA) of an endemic Tibetan Plateau fish (Gymnocypris selincuoensis) was used to examine changes in reproductive phenology associated with climate changes from the 1970s to 2000s. Assigning individual fish to their appropriate calendar year class was assisted by dendrochronological methods (crossdating). The results demonstrated that LAFA was significantly and positively associated with temperature and growing season length. To separate the effects of temperature and the growing season length on LAFA growth, measurements of larval otoliths from different sites were conducted and revealed that daily increment additions were the main contributor (46.3%), while temperature contributed less (12.0%). Using constructed water‐air temperature relationships and historical air temperature records, we found that the reproductive phenology of G. selincuoensis was strongly advanced in the spring during the 1970s and 1990s, while the increased growing season length in the 2000s was mainly due to a delayed onset of winter. The reproductive phenology of G. selincuoensis advanced 2.9 days per decade on average from the 1970s to 2000s, and may have effects on recruitment success and population dynamics of this species and other biota in the ecosystem via the food web. The methods used in this study are applicable for studying reproductive phenological changes across a wide range of species and ecosystems.     

Challenging a 15‐year‐old claim: The North Atlantic Oscillation index as a predictor of spring migration phenology of birds

Many migrant bird species that breed in the Northern Hemisphere show advancement in spring arrival dates. The North Atlantic Oscillation (NAO) index is one of the climatic variables that have been most often investigated and shown to be correlated with these changes in spring arrival. Although the NAO is often claimed to be a good predictor or even to have a marked effect on interannual changes in spring migration phenology of Northern Hemisphere breeding birds, the results on relations between spring migration phenology and NAO show a large variety, ranging from no, over weak, to a strong association. Several factors, such as geographic location, migration phase, and the NAO index time window, have been suggested to partly explain these observed differences in association. A combination of a literature meta‐analysis, and a meta‐analysis and sliding time window analysis of a dataset of 23 short‐ and long‐distance migrants from the constant‐effort trapping garden at Helgoland, Germany, however, paints a completely different picture. We found a statistically significant overall effect size of the NAO on spring migration phenology (coefficient = ?0.14, SE = 0.054), but this on average only explains 0%–6% of the variance in spring migration phenology across all species. As such, the value and biological meaning of the NAO as a general predictor or explanatory variable for climate change effects on migration phenology of birds, seems highly questionable. We found little to no definite support for previously suggested factors, such as geographic location, migration phenology phase, or the NAO time window, to explain the heterogeneity in correlation differences. We, however, did find compelling evidence that the lack of accounting for trends in both time series has led to strongly inflated (spurious) correlations in many studies (coefficient = ?0.13, SE = 0.019).     

Phenology dictates the impact of climate change on geographic distributions of six co‐occurring North American grasshoppers

Throughout the last century, climate change has altered the geographic distributions of many species. Insects, in particular, vary in their ability to track changing climates, and it is likely that phenology is an important determinant of how well insects can either expand or shift their geographic distributions in response to climate change. Grasshoppers are an ideal group to test the hypothesis that phenology correlates with range expansion, given that co‐occurring confamilial, and even congeneric, species can differ in phenology. Here, I tested the hypothesis that early‐ and late‐season species should possess different range expansion potentials, as estimated by habitat suitability from ecological niche models. I used nine different modeling techniques to estimate habitat suitability of six grasshopper species of varying phenology under two climate scenarios for the year 2050. My results suggest that, of the six species examined here, early‐season species were more sensitive to climate change than late‐season species. The three early‐season species examined here might shift northward during the spring, while the modeled geographic distributions of the three late‐season species were generally constant under climate change, likely because they were pre‐adapted to hot and dry conditions. Phenology might therefore be a good predictor of how insect distributions might change in the future, but this hypothesis remains to be tested at a broader scale.     

Interannual variability of plant phenology in tussock tundra: modelling interactions of plant productivity, plant phenology, snowmelt and soil thaw

We present a linked model of plant productivity, plant phenology, snowmelt and soil thaw in order to estimate interannual variability of arctic plant phenology and its effects on plant productivity. The model is tested using 8 years of soil temperature data, and three years of bud break data of Betula nana. Because the factors that trigger the end of the growing season of arctic vegetation are less well known than those of the start of the growing season, three hypotheses were formulated and tested for their effects on productivity and its sensitivity to climate change; the hypothesised factors determining the end of the growing season were frost, photoperiod and periodic constraints. The performance of the soil thermal model was good; both the onset of soil thaw in spring and the initiation of freezing in autumn were predicted correctly in most cases. The phenology model predicted the bud break date of Betula nana closely for the three different years. The soil thaw model predicted similar growing season start dates under current climate as the models based on sum of temperatures, but it made significantly different predictions under climate change scenarios, probably because of the non‐linear interactions between snowmelt and soil thaw. The uncertainty about the driving factors for the end of the growing season, in turn, resulted in uncertainty in the interannual variability of the simulated annual gross primary productivity (GPP). The interannual variability ranged from ? 25 to + 26% of the mean annual GPP for the frost hypothesis, from ? 20 to + 20% for the photoperiod hypothesis and only from ? 7 to + 7% for the periodic hypothesis. The different hypotheses also resulted in different sensitivity to climate change, with the frost hypothesis resulting in 30% higher annual GPP values than the periodic hypothesis when air temperatures were increased by 3 °C.     

Predicting xylem phenology in black spruce under climate warming

In the next century, the boreal ecosystems are projected to experience greater rates of warming than most other regions of the world. As the boreal forest constitutes a reservoir of trees of huge ecological importance and only partially known economic potential, any possible climate‐related change in plant growth and dynamics has to be promptly predicted and evaluated. A model for assessing xylem phenology in black spruce [Picea mariana (Mill.) B.S.P.] using daily temperatures and thermal thresholds was defined and applied to predict changes in onset, ending and duration of xylem growth under different warming scenarios with temperatures rising by up to 3 °C. This was achieved by collecting and analyzing a dataset obtained from a 7‐year monitoring of cambium phenology and wood formation on a weekly time‐scale in trees growing in four sites at different latitudes and altitudes in the Saguenay‐Lac‐Saint‐Jean region (Quebec, Canada). The onset of xylem growth occurred between mid‐May and early June while the end ranged between mid‐September and early October, resulting in a growing season of 101–141 days. The model predicted longer duration of xylem growth at higher temperatures, with an increase of 8–11 days/ °C, because of an earlier onset and later ending of growth. With an increase of 3 °C in the mean temperature during the year, the duration of xylem growth changed on average from 125 to 160 days. The predicted changes in cambial phenology could significantly affect future wood production of the boreal ecosystems.     

祁连山中部祁连圆柏年内径向生长对气候因子的响应

通过对祁连山中部葫芦沟流域的祁连圆柏连续采集微树芯,对其形成层活动和径向生长动态进行了连续两年的监测研究。结果表明,2012年细胞壁加厚和细胞成熟阶段开始时间分别发生在6月26日和7月24日,比2013年细胞壁加厚（6月22日）和细胞成熟阶段（6月26日）开始时间分别晚5 d和28 d。2012年细胞扩大、细胞壁加厚和细胞成熟阶段结束时间分别为7月16日、8月9日和9月8日,比2013年各阶段结束时间分别晚7、28 d和24 d。2012年最大细胞分裂速率为0.33细胞/d,共形成20.9个细胞,细胞分裂速率和木质部细胞总数均高于2013年。通过与附近气象站记录的气象数据进行对比,发现祁连圆柏生长开始时间在温暖年份显著早于寒冷年份,说明祁连圆柏的径向生长开始时间与温度有关。但2013年春季和夏初的高温导致区域干旱程度加剧,使祁连圆柏生长结束时间显著早于2012年,并导致2013年的木质部细胞总量和生长速率都小于2012年。研究表明,在寒冷干旱地区,尽管升温会使生长季提前,但升温导致的干旱胁迫可能对树木的生长速率和木质部细胞总量产生重要影响。     

Drought footprint on European ecosystems between 1999 and 2010 assessed by remotely sensed vegetation phenology and productivity

Drought affects more people than any other natural disaster but there is little understanding of how ecosystems react to droughts. This study jointly analyzed spatio‐temporal changes of drought patterns with vegetation phenology and productivity changes between 1999 and 2010 in major European bioclimatic zones. The Standardized Precipitation and Evapotranspiration Index (SPEI) was used as drought indicator whereas changes in growing season length and vegetation productivity were assessed using remote sensing time‐series of Normalized Difference Vegetation Index (NDVI). Drought spatio‐temporal variability was analyzed using a Principal Component Analysis, leading to the identification of four major drought events between 1999 and 2010 in Europe. Correspondence Analysis showed that at the continental scale the productivity and phenology reacted differently to the identified drought events depending on ecosystem and land cover. Northern and Mediterranean ecosystems proved to be more resilient to droughts in terms of vegetation phenology and productivity developments. Western Atlantic regions and Eastern Europe showed strong agglomerations of decreased productivity and shorter vegetation growing season length, indicating that these ecosystems did not buffer the effects of drought well. In a climate change perspective, increase in drought frequency or intensity may result in larger impacts over these ecosystems, thus management and adaptation strategies should be strengthened in these areas of concerns.     

Earlier breeding,lower success: does the spatial scale of climatic conditions matter in a migratory passerine bird?

Following over 20 years of research on the climatic effects on biodiversity we now have strong evidence that climate change affects phenology, fitness, and distribution ranges of different taxa, including birds. Bird phenology likely responds to changes in local weather. It is also affected by climatic year‐to‐year variations on larger scales. Although such scale‐related effects are common in ecology, most studies analyzing the effects of climate change were accomplished using climatic information on a single spatial scale. In this study, we aimed at determining the scale‐dependent sensitivity of breeding phenology and success to climate change in a migratory passerine bird, the barn swallow (Hirundo rustica). For both annual broods, we investigated effects of local weather (local scale) and the North Atlantic Oscillation (NAO, large scale) on the timing of breeding and breeding success. Consistent with previous studies in migratory birds we found that barn swallows in Eastern Germany bred progressively earlier. At the same time, they showed reduced breeding success over time in response to recent climatic changes. Responses to climatic variation were observed on both local and large climatic scales, but they differed with respect to the ecological process considered. Specifically, we found that the timing of breeding was primarily influenced by large‐scale NAO variations and to a lesser extent by local weather on the breeding grounds. Conversely, climatic conditions on the local scale affected breeding success, exclusively. The observed decrease in breeding success over years is likely a consequence of scale‐related mismatches between climatic conditions during different breeding phases. This provides further evidence that a species' response of earlier breeding may not be enough to cope with climate change. Our results emphasize the importance of considering the response of ecological processes along different climatic scales in order to better understand the complexity of climate change effects on biodiversity.     

Local and regional climate variables driving spring phenology of tortricid pests: a 36 year study

1. Insect phenology is driven by local climate variables, most notably temperature. Increased warming has been linked to advancements in critical phenophases such as the spring flight of reproductive adults in the mid‐Atlantic region of the U.S.A. 2. Local climate is governed by the fluctuations of large‐scale climate oscillations. In the northern hemisphere, both the North Atlantic Oscillation (NAO) and the Arctic Oscillation (AO) control the local autumn and winter severity. Low NAO and AO indices are associated with colder autumns and winters, which can delay spring phenology. 3. In this study, 36 years of data from experimental fruit orchards in Biglerville, Pennsylvania, were used to run partial least‐squares regressions in order to determine the climate variables related to the spring phenology of five tortricid pest species. 4. The phenology of the tortricid pests did not advance, even though there was evidence of warming at the research site. 5. Spring temperatures were found to be the most significant climate variables in determining the timing of the spring flights. However, autumn–winter temperatures were also important. 6. For the NAO and the AO, it was found that these oscillations affected the tortricid moths by influencing autumn–winter conditions. The oscillations of the NAO and AO can obscure long‐term changes in phenology. 7. These findings suggest that the inclusion of large‐scale climate oscillations can provide important insights into how climate conditions can influence insect phenology, and presents an opportunity for improving the ability to forecast spring emergence.     

Predicting spatial and temporal patterns of bud‐burst and spring frost risk in north‐west Europe: the implications of local adaptation to climate

The timing of spring bud‐burst and leaf development in temperate, boreal and Arctic trees and shrubs fluctuates from year to year, depending on meteorological conditions. Over several generations, the sensitivity of bud‐burst to meteorological conditions is subject to selection pressure. The timing of spring bud‐burst is considered to be under opposing evolutionary pressures; earlier bud‐burst increases the available growing season (capacity adaptation) but later bud‐burst decreases the risk of frost damage to actively growing parts (survival adaptation). The optimum trade‐off between these two forms of adaptation may be considered an evolutionarily stable strategy that maximizes the long‐term ecological fitness of a phenotype under a given climate. Rapid changes in climate, as predicted for this century, are likely to exceed the rate at which trees and shrubs can adapt through evolution or migration. Therefore the response of spring phenology will depend not only on future climatic conditions but also on the limits imposed by adaptation to current and historical climate. Using a dataset of bud‐burst dates from twenty‐nine sites in Finland for downy birch (Betula pubescens Ehrh.), we parameterize a simple thermal time bud‐burst model in which the critical temperature threshold for bud‐burst is a function of recent historical climatic conditions and reflects a trade‐off between capacity and survival adaptation. We validate this approach with independent data from eight independent sites outside Finland, and use the parameterized model to predict the response of bud‐burst to future climate scenarios in north‐west Europe. Current strategies for budburst are predicted to be suboptimal for future climates, with bud‐burst generally occurring earlier than the optimal strategy. Nevertheless, exposure to frost risk is predicted to decrease slightly and the growing season is predicted to increase considerably across most of the region. However, in high‐altitude maritime regions exposure to frost risk following bud‐burst is predicted to increase.     

Long‐term changes in autumn migration dates at the Strait of Gibraltar reflect population trends of soaring birds

A growing body of work shows that climate change is the cause of a number of directional shifts in the spring phenology of migratory birds. However, changes in autumn phenology are well studied and their consistency across species, as well as their link with population trends, remains uncertain. We investigate changes in the autumn migration dates of 11 species of soaring birds over the Strait of Gibraltar over a 16‐year period. Using models corrected for phylogeny, we assessed whether ecological and morphological characteristics, as well as population trends, account for interspecific shifts in migration times. We recorded different phenological changes in different periods of the migration season and suggest that these differences are due to age‐dependent responses. The variable best predicting advances in migration dates was population trend: species that did not advance their autumn migration dates were those showing a decline in their European breeding populations. We repeated our tests on a dataset representing the migration date of soaring birds across the Pyrenees Mountains and found that population trends at this site also predicted phenological shifts. Our results suggest that flexibility in migratory strategy and population trends may be related, such that different adaptive capacity in migration timing may be more relevant than other ecological traits in determining the conservation status of migratory birds in Europe and perhaps other regions.     

Climate change and fitness components of a migratory bird breeding in the Mediterranean region

The increase in spring temperatures in temperate regions over the last two decades has led to an advancing spring phenology, and most resident birds have responded to it by advancing their onset of breeding. The pied flycatcher (Ficedula hypoleuca) is a long‐distance migrant bird with a relatively late onset of breeding with respect to both resident birds and spring phenology in Europe. In the present correlational study, we show that some fitness components of pied flycatchers are suffering from climate change in two of the southernmost European breeding populations. In both montane study areas, temperature during May increased between 1980 and 2000 and an advancement of oak leafing was detected by using the normalized difference vegetation index (NDVI) to assess tree phenology. This might result in an advancement of the peak in availability of caterpillars, the main prey during the nestling stage. Over the past 18 yr, the time of egg laying and clutch size of pied flycatchers were not affected by the increase in spring temperatures in these Mediterranean populations. However, this increase seems to have an adverse effect on the reproductive output of pied flycatchers over the same period. Our data suggest that the mismatch between the timing of peak food supply and nestling demand caused by recent climate change might result in a reduction of parental energy expenditure that is reflected in a reduction of nestling growth and survival of fledged young in our study populations. The data seem to indicate that the breeding season has not shifted and it is the environment that has shifted away from the timing of the pied flycatcher breeding season. Mediterranean pied flycatchers were not able to advance their onset of breeding, probably, because they are constrained by their late arrival date and their restricted high altitude breeding habitat selection near the southern border of their range.     

Climate and the complexity of migratory phenology: sexes,migratory distance,and arrival distributions

The intra- and inter-season complexity of bird migration has received limited attention in climatic change research. Our phenological analysis of 22 species collected in Chicago, USA, (1979–2002) evaluates the relationship between multi-scalar climate variables and differences (1) in arrival timing between sexes, (2) in arrival distributions among species, and (3) between spring and fall migration. The early migratory period for earliest arriving species (i.e., short-distance migrants) and earliest arriving individuals of a species (i.e., males) most frequently correlate with climate variables. Compared to long-distance migrant species, four times as many short-distance migrants correlate with spring temperature, while 8 of 11 (73%) of long-distance migrant species’ arrival is correlated with the North Atlantic Oscillation (NAO). While migratory phenology has been correlated with NAO in Europe, we believe that this is the first documentation of a significant association in North America. Geographically proximate conditions apparently influence migratory timing for short-distance migrants while continental-scale climate (e.g., NAO) seemingly influences the phenology of Neotropical migrants. The preponderance of climate correlations is with the early migratory period, not the median of arrival, suggesting that early spring conditions constrain the onset or rate of migration for some species. The seasonal arrival distribution provides considerable information about migratory passage beyond what is apparent from statistical analyses of phenology. A relationship between climate and fall phenology is not detected at this location. Analysis of the within-season complexity of migration, including multiple metrics of arrival, is essential to detect species’ responses to changing climate as well as evaluate the underlying biological mechanisms.