Leaf Unfolding Dates Research Articles

A new algorithm for the estimation of leaf unfolding date using MODIS data over China’s terrestrial ecosystems

Using solely vegetation indices (VIs) from remote sensing is not always sufficient to accurately detect spring leaf phenology, i.e., the leaf unfolding date (LUD). Several current phenology products failed to provide reliable LUD estimates for specific regions and plant functional types, e.g., evergreen species at mid-low latitudes. Therefore, increasing efforts have been made to improve LUD modeling by combining VIs and meteorological variables. Temperature before the growing season (‘preseason’ henceforth) plays an important role in regulating spring phenology. With ground observations of LUD (LUDOBS) across different plant functional types (PFTs) in China during 2001–2014, we analyzed the response of LUDOBS to preseason temperature temporally and spatially, and proposed an improved LUD modeling algorithm by developing a temperature-based scale factor to adjust the traditional VI-based (i.e., two band enhanced vegetation index (EVI2)) LUD estimates. We found that the new algorithm can better characterize the spatial and temporal patterns of LUD variability for different PFTs, especially for evergreen species where MODIS phenology product failed to provide reliable LUD estimates. Furthermore, we investigated the spatio-temporal patterns of LUD over China with respect to both different vegetation types and climate systems. We showed that for ∼70% pixels, our new model predicted an overall later LUDs than MODIS phenology product, possibly suggesting an overestimated greening potential of China’s terrestrial ecosystems. Our study suggests that preseason temperature plays a previously neglected role in modeling spring LUD and instead of using VIs or temperature alone, a combination of temperature and VIs can improve the prediction of spring phenology.

近50年中国典型木本植物展叶始期温度敏感度变化及原因

近50年中国典型木本植物展叶始期温度敏感度变化及原因

Variations in the temperature sensitivity of spring leaf phenology from 1978 to 2014 in Mudanjiang, China.

Continuous long-term temperature sensitivity (ST) of leaf unfolding date (LUD) and main impacting factors in spring in the period 1978-2014 for 40 plant species in Mudanjiang, Heilongjiang Province, Northeast China, were analyzed by using observation data from the China Phenological Observation Network (CPON), together with the corresponding meteorological data from the China Meteorological Data Service Center. Temperature sensitivities, slopes of the regression between LUD and mean temperature during the optimum preseason (OP), were analyzed using 15-year moving window to determine their temporal trends. Major factors impacting ST were then chosen and evaluated by applying a random sampling method. The results showed that LUD was sensitive to mean temperature in a defined period before phenophase onset for all plant species analyzed. Over the period 1978-2014, the mean ST of LUD for all plant species was - 3.2 ± 0.49days°C-1. The moving window analysis revealed that 75% of species displayed increasing ST of LUD, with 55% showing significant increases (P < 0.05). ST for the other 25% exhibited a decreasing trend, with 17% showing significant decreases (P < 0.05). On average, ST increased by 16%, from - 2.8 ± 0.83days°C-1 during 1980-1994 to - 3.30 ± 0.65days°C-1 during 2000-2014. For species with later LUD and longer OP, ST tended to increase more, while species with earlier LUD and shorter OP tended to display a decreasing ST. The standard deviation of preseason temperature impacted the temporal variation in ST. Chilling conditions influenced ST for some species, but photoperiod limitation did not have significant or coherent effects on changes in ST.

Reply to communications by Fu et al. international journal of biometeorology.

Temperature sensitivity of plant phenology (ST) is a determining factor of as to what degree climate change impacts on plant species. Fu et al . (Int J Biometeorol 60:1611-1613, 2016) claimed that long long-term linear trends mask phenological shifts. However, the decreased and increased ST was both found in warming scenarios. The conceptual scheme telling the nonlinear relationship between spring temperature and leaf unfolding date proposed by Fu et al . (Int J Biometeorol 60:1611-1613, 2016) cannot be supported by observation data across Europe. Therefore, linking declined ST to climate warming is misleading, and future ST changes are more uncertain than they suggested.

Leaf unfolding of Tibetan alpine meadows captures the arrival of monsoon rainfall.

The alpine meadow on the Tibetan Plateau is the highest and largest pasture in the world, and its formation and distribution are mainly controlled by Indian summer monsoon effects. However, little is known about how monsoon-related cues may trigger spring phenology of the vast alpine vegetation. Based on the 7-year observations with fenced and transplanted experiments across lower to upper limits of Kobresia meadows in the central plateau (4400–5200 m), we found that leaf unfolding dates of dominant sedge and grass species synchronized with monsoon onset, regardless of air temperature. We also found similar patterns in a 22-year data set from the northeast plateau. In the monsoon-related cues for leaf unfolding, the arrival of monsoon rainfall is crucial, while seasonal air temperatures are already continuously above 0 °C. In contrast, the early-emerging cushion species generally leafed out earlier in warmer years regardless of precipitation. Our data provide evidence that leaf unfolding of dominant species in the alpine meadows senses the arrival of monsoon-season rainfall. These findings also provide a basis for interpreting the spatially variable greening responses to warming detected in the world’s highest pasture, and suggest a phenological strategy for avoiding damages of pre-monsoon drought and frost to alpine plants.

Evaluating phenological models for the prediction of leaf-out dates in six temperate tree species across central Europe

Inter-annual variation in climate is reflected by changes in the timing of phenology. Over the last decades a considerable number of models have been developed in order to explain the inter-annual variation of spring phenology in trees. Contrary to empirical models, “process-based” models aim at simulating physiological processes in order to yield more realistic predictions of growing season onset dates. Despite the increasing knowledge on the environmental controls of seasonal dormancy in trees, the detailed action and interaction of the involved environmental drivers (chilling, photoperiod and warm temperature) remains to be elucidated. This study aims at a uniform comparison of a wide range of existing models (and new recombinations), on a multitude of long-term observation series in six tree species across central Europe, using extensive cross-validation. Even though the assessed models differ in the phases of dormancy and environmental drivers accounted for, they yielded a surprisingly similar quality of prediction of leaf unfolding dates. Depending on the species, the lowest average prediction errors for leaf unfolding (RMSE) ranged from 7 to 9 days for the dataset pooled across sites and years and from 4 to 6 days for site-specific predictions, in absence of any obvious geographical pattern. Simple models, that feature ecodormancy release only, performed similar or better than more complex models, which additionally include endodormancy release through chilling temperatures. Model parameterisation tended to converge towards similar behaviour and models with many parameters tended to overfit on the 40 year time-series of leaf unfolding. Additionally, all models tended to underestimate the inter-annual variation of leaf unfolding and failed to predict very early or late dates of leaf unfolding in certain years. The transfer of site-specific parameters to other sites was associated with an almost doubling of the average prediction error, independent of distance and climatic similarity between the calibration and validation sites. The findings challenge the accurate implementation of the physiological processes controlling spring phenology in the models and highlight shortcomings associated with model parameterisation on observational time-series only.

Divergent responses of leaf phenology to changing temperature among plant species and geographical regions

Shifts in plants' phenophases caused by climate change can strongly affect the ecosystem structure and function. Temperature sensitivity, which is expressed as the date of phenological event change for per degree Celsius change of temperature (days °C−1), has been widely used to characterize the plants' responses to changed temperature. In this study, we analyzed the temperature sensitivity of leaf phenology (leaf unfolding date, LUD; leaf falling date, LFD) for more than 700 plant species based on the phenological observations at 56 sites in China from 1963 to 1988. Our results suggested significant spatial and interspecific variations in the responses of leaf phenology to changing temperature. Approximately 48.8% cases of LUD advanced significantly (p &lt; 0.1) with the increasing spring temperature and 33.9% cases of LFD delayed significantly with increasing autumn temperature. The spring events were overall more sensitive to temperature than autumn events. Although the LUD of plants in warmer regions was more sensitive to changing temperature, the temperature sensitivities of LFD for plants in warmer regions were not significantly different from that for plants in cooler regions. Moreover, for spring phenology, many sites suggested higher temperature sensitivity for species that unfold their leaves earlier. For autumn phenology, species with later leaf‐falling dates were generally more sensitive to temperature. Differences in species' responses to temperature that caused the discrepant changes in species' growing season can strongly impact vegetation dynamic and ecosystem function, and thus should be considered more when predicting the effects of climate warming on the biosphere.

Declining global warming effects on the phenology of spring leaf unfolding.

Earlier spring leaf unfolding is a frequently observed response of plants to climate warming. Many deciduous tree species require chilling for dormancy release, and warming-related reductions in chilling may counteract the advance of leaf unfolding in response to warming. Empirical evidence for this, however, is limited to saplings or twigs in climate-controlled chambers. Using long-term in situ observations of leaf unfolding for seven dominant European tree species at 1,245 sites, here we show that the apparent response of leaf unfolding to climate warming (ST, expressed in days advance of leaf unfolding per °C warming) has significantly decreased from 1980 to 2013 in all monitored tree species. Averaged across all species and sites, ST decreased by 40% from 4.0 ± 1.8 days °C(-1) during 1980-1994 to 2.3 ± 1.6 days °C(-1) during 1999-2013. The declining ST was also simulated by chilling-based phenology models, albeit with a weaker decline (24-30%) than observed in situ. The reduction in ST is likely to be partly attributable to reduced chilling. Nonetheless, other mechanisms may also have a role, such as 'photoperiod limitation' mechanisms that may become ultimately limiting when leaf unfolding dates occur too early in the season. Our results provide empirical evidence for a declining ST, but also suggest that the predicted strong winter warming in the future may further reduce ST and therefore result in a slowdown in the advance of tree spring phenology.

Leaf onset in the northern hemisphere triggered by daytime temperature.

Recent warming significantly advanced leaf onset in the northern hemisphere. This signal cannot be accurately reproduced by current models parameterized by daily mean temperature (Tmean). Here using in situ observations of leaf unfolding dates (LUDs) in Europe and the United States, we show that the interannual anomalies of LUD during 1982–2011 are triggered by daytime (Tmax) more than by nighttime temperature (Tmin). Furthermore, an increase of 1 °C in Tmax would advance LUD by 4.7 days in Europe and 4.3 days in the United States, more than the conventional temperature sensitivity estimated from Tmean. The triggering role of Tmax, rather than the Tmin or Tmean variable, is also supported by analysis of the large-scale patterns of satellite-derived vegetation green-up in spring in the northern hemisphere (>30°N). Our results suggest a new conceptual framework of leaf onset using daytime temperature to improve the performance of phenology modules in current Earth system models.

Patterns of late spring frost leaf damage and recovery in a European beech (Fagus sylvatica L.) stand in south-eastern Germany based on repeated digital photographs.

Damage by late spring frost is a risk deciduous trees have to cope with in order to optimize the length of their growing season. The timing of spring phenological development plays a crucial role, not only at the species level, but also at the population and individual level, since fresh new leaves are especially vulnerable. For the pronounced late spring frost in May 2011 in Germany, we studied the individual leaf development of 35 deciduous trees (mainly European beech Fagus sylvatica L.) at a mountainous forest site in the Bayerischer Wald National Park using repeated digital photographs. Analyses of the time series of greenness by a novel Bayesian multiple change point approach mostly revealed five change points which almost perfectly matched the expected break points in leaf development: (i) start of the first greening between day of the year (DOY) 108–119 (mean 113), (ii) end of greening, and (iii) visible frost damage after the frost on the night of May 3rd/4th (DOY 123/124), (iv) re-sprouting 19–38 days after the frost, and (v) full maturity around DOY 178 (166–184) when all beech crowns had fully recovered. Since frost damage was nearly 100%, individual susceptibility did not depend on the timing of first spring leaf unfolding. However, we could identify significant patterns in fitness linked to an earlier start of leaf unfolding. Those individuals that had an earlier start of greening during the first flushing period had a shorter period of recovery and started the second greening earlier. Thus, phenological timing triggered the speed of recovery from such an extreme event. The maximum greenness achieved, however, did not vary with leaf unfolding dates. Two mountain ashes (Sorbus aucuparia L.) were not affected by the low temperatures of -5°C. Time series analysis of webcam pictures can thus improve process-based knowledge and provide valuable insights into the link between phenological variation, late spring frost damage, and recovery within one stand.

Recent spring phenology shifts in western Central Europe based on multiscale observations

AbstractAimAlthough numerous studies have reported advanced Northern Hemisphere spring phenology since the 1980s, recent studies based on remote sensing have reported a reversal or deceleration of this trend. This study aimed (1) to fully understand recent spring phenology shifts using both in situ observations and satellite‐based normalized difference vegetation index (NDVI) datasets, and (2) to test whether the NDVI methods capture the trends observed in situ.LocationWestern Central Europe.MethodsTemporal spring phenology trends (leaf unfolding dates) were examined using 1,001,678 in situ observations of 31 plant species at 3984 stations, as well as NDVI‐based start‐of‐season dates, obtained using five different methods, across the pixels that included the phenology stations.ResultsIn situ and NDVI observations both indicated that spring phenology significantly advanced during the period 1982–2011 at an average rate of −0.45 days yr−1. This trend was not uniform across the period and significantly weakened over the period 2000–2011. Furthermore, opposite trends were found between in situ and NDVI observations over the period 2000–2011. Averaged over all species, the in situ observations indicated a slower but still advancing trend for leaf unfolding, whereas the NDVI series showed a delayed spring phenology.Main conclusionsThe recent trend reversal in the advancement of spring phenology in western Central Europe is likely to be related to the response of early spring species to the cooling trend in late winter. In contrast, late spring species continued to exhibit advanced leaf unfolding, which is consistent with the warming trend during spring months. Because remote sensing does not distinguish between species, the signal of growing‐season onset may only reflect the phenological dynamics of these earliest species in the pixel, even though most species still exhibit advancing trends.

Modeling and predicting spring land surface phenology of the deciduous broadleaf forest in northern China

Using normalized difference vegetation index data, we fitted unified forcing and chilling phenology models to start date of the growing season (SOS) during 1982 to 2006 and selected optimum models for each pixel. Then, we validated performances of optimum models in extrapolating SOS dates during 2007 to 2011. Moreover, we reconstructed SOS time series over 1950 to 2005 and predicted decadal mean anomalies of SOS dates over 2006 to 2100 under scenarios of the representative concentration pathway (RCP) 4.5 and 8.5. Finally, we compared structures and parameters of the satellite data-based phenology model with those of the ground-based leaf unfolding model. Results show that the unified forcing model has higher simulation parsimony and efficiency than the unified chilling model at 96.4% of pixels. The external validation confirmed feasibility of the unified forcing model in predicting the SOS date. Across the entire region, predicted SOS dates indicate significant advancements by 0.65–1.79 days per decade. Taking the mean SOS date during 1961 to 1990 as the reference value, the absolute values of decadal mean anomalies of the SOS date represent an overall increase with the time. Consequently, the average SOS date during 2091 to 2100 would be 11.8–20.0 days earlier than the average SOS date during 1961 to 1990. At pixel scales, the absolute values of decadal mean anomalies of the SOS date under the RCP 8.5 scenario display mostly a latitudinal gradient from south to north. Similar distribution ranges of parameter d and e of the ground-based and satellite data-based phenology models demonstrate that the satellite-derived SOS date has consistent response to air temperature with the leaf unfolding date of dominant deciduous trees, which implies that the predicted start of the growing season may to some extent reflect changing tendency of the ground leafing phenology in the 21st century.

Sensitivity of leaf unfolding to experimental warming in three temperate tree species

Phenological events are sensitive to climate change, and a clear advancement of spring leaf phenology has been well documented. However, the observed phenological trends cannot be directly used to forecast future changes because the underlying mechanisms are still unclear. We conducted a two-year experimental warming experiment using one-meter-high saplings of birch (Betula pendula L.), oak (Quercus robur L.) and beech (Fagus sylvatica L.). The main objective of this study was to quantify the temperature sensitivity of leaf unfolding to six different warming levels. The results suggested that leaf unfolding dates were significantly advanced with warming for all species in both experimental years. However, different warming treatments elicited different leaf unfolding responses. At low and moderate warming (<+4°C), the sensitivity of leaf unfolding to temperature (changes in days per °C) increased with warming in all three studied species. For birch, the temperature sensitivity continued to increase with additional warming. For oak and beech, in contrast, the temperature sensitivity dramatically decreased when warming exceeded +4°C. Our findings confirm that continued and intense warming may not result in further advances of leaf unfolding in the late successional species oak and beech, if the warming exceeds a certain threshold leading to insufficient chilling temperatures for dormancy release.

Elevational adaptation and plasticity in seedling phenology of temperate deciduous tree species

Phenological events, such as the initiation and the end of seasonal growth, are thought to be under strong evolutionary control because of their influence on tree fitness. Although numerous studies highlighted genetic differentiation in phenology among populations from contrasting climates, it remains unclear whether local adaptation could restrict phenological plasticity in response to current warming. Seedling populations of seven deciduous tree species from high and low elevations in the Swiss Alps were investigated in eight common gardens located along two elevational gradients from 400 to 1,700 m. We addressed the following questions: are there genetic differentiations in phenology between populations from low and high elevations, and are populations from the upper elevational limit of a species' distribution able to respond to increasing temperature to the same extent as low-elevation populations? Genetic variation of leaf unfolding date between seedlings from low and high populations was detected in six out of seven tree species. Except for beech, populations from high elevations tended to flush later than populations from low elevations, emphasizing that phenology is likely to be under evolutionary pressure. Furthermore, seedlings from high elevation exhibited lower phenological plasticity to temperature than low-elevation provenances. This difference in phenological plasticity may reflect the opposing selective forces involved (i.e. a trade-off between maximizing growing season length and avoiding frost damages). Nevertheless, environmental effects were much stronger than genetic effects, suggesting a high phenological plasticity to enable tree populations to track ongoing climate change, which includes the risk of tracking unusually warm springs followed by frost.

Regional unified model‐based leaf unfolding prediction from 1960 to 2009 across northern China

Using first leaf unfolding data of Salix matsudana, Populus simonii, Ulmus pumila, and Prunus armeniaca, and daily mean temperature data during the 1981-2005 period at 136 stations in northern China, we fitted unified forcing and chilling phenology models and selected optimum models for each species at each station. Then, we examined performances of each optimum local species-specific model in predicting leaf unfolding dates at all external stations within the corresponding climate region and selected 16 local species-specific models with maximum effective predictions as the regional unified models in different climate regions. Furthermore, we validated the regional unified models using leaf unfolding and daily mean temperature data beyond the time period of model fitting. Finally, we substituted gridded daily mean temperature data into the regional unified models, and reconstructed spatial patterns of leaf unfolding dates of the four tree species across northern China during 1960-2009. At local scales, the unified forcing model shows higher simulation efficiency at 83% of data sets, whereas the unified chilling model indicates higher simulation efficiency at 17% of data sets. Thus, winter temperature increase so far has not yet significantly influenced dormancy and consequent leaf development of deciduous trees in most parts of northern China. Spatial and temporal validation confirmed capability and reliability of regional unified species-specific models in predicting leaf unfolding dates in northern China. Reconstructed leaf unfolding dates of the four tree species show significant advancements by 1.4-1.6days per decade during 1960-2009 across northern China, which are stronger for the earlier than the later leaf unfolding species. Our findings suggest that the principal characteristics of plant phenology and phenological responses to climate change at regional scales can be captured by phenological and climatic data sets at a few representative locations.

Diversity of leaf unfolding dynamics among tree species: New insights from a study along an altitudinal gradient

Leaf unfolding is a key ecosystem parameter controlling carbon and water fluxes and affecting forest dynamics. This parameter is highly sensitive to temperature and, consequently, often used as an indicator of global change. In this paper, we analyzed weekly leaf unfolding dynamics for seven temperate species (Fagus sylvatica L., Acer opalus Mill., Sorbus aria L., Quercus pubescens Willd. Abies alba Mill., Pinus sylvestris L., Pinus nigra Arnold). The effects of temperature on leaf unfolding were studied in situ using several methods and proxies. First, in a spatial approach, leaf unfolding dates were measured along two altitudinal gradients situated on the north and south face of the Mont Ventoux to test altitudinal and slope effects. Second, in a temporal approach, the year effect was analyzed on the north face by comparing two contrasted years (2006 and 2007). Finally, the role of temperature was investigated directly by linking leaf unfolding patterns and temperatures recorded during the leaf unfolding process itself.Two major conclusions were obtained. First, three distinct leaf unfolding patterns were revealed: a rapid sigmoid pattern for the deciduous species group, a slow kinetic pattern for the pines and an intermediate pattern for A. alba. Second, we found an unexpected pattern of variation in the response to spatial or temporal variation of temperature. The more sensitive a species was to temperature variations between years, the less sensitive it was to temperature variations due to altitude. Finally, we discuss that these results can be correlated to two major life history traits: evergreen vs. deciduous and shade tolerant vs. shade intolerant.

Quantifying phenological plasticity to temperature in two temperate tree species

Summary 1. Phenotypic plasticity allows large shifts in the timing of phenology within one single generation and drives phenotypic variability under environmental changes, thus it will enhance the inherent adaptive capacities of plants against future changes of climate. 2. Using five common gardens set along an altitudinal gradient (100–1600 m asl.), we experimentally examined the phenotypic plasticity of leaf phenology in response to temperature increase for two temperate tree species (Fagus sylvatica and Quercus petraea). We used seedlings from three populations of each species inhabiting different altitudes (400, 800 and 1200 m asl.). Leaf unfolding in spring and leaf senescence in autumn were monitored on seedlings for 2 years. 3. Overall, a high phenological plasticity was found for both species. The reaction norms of leaf unfolding date to temperature linearly accelerated for both species with an average shift of −5·7 days per degree increase. Timing of leaf senescence exhibited hyperbolic trends for beech due to earlier senescence at the lowest elevation garden and no or slight trends for oak. There was no difference in the magnitude of phenological plasticity among populations from different elevations. For both species, the growing season length increased to reach maximum values at about 10–13 °C of annual temperature according to the population. 4. Since the magnitude of phenological plasticity is high for all the tested populations, they are likely to respond immediately to temperature variations in terms of leaf phenology. Consequently the mid‐ to high‐elevation populations are likely to experience a longer growing season with climate warming. The results suggest that climate warming could lengthen the growing season of all populations over the altitudinal gradient, although the low‐elevation populations, especially of beech, may experience accelerated senescence and shorter growing season due to drought and other climate changes associated with warming.

Monitoring elevation variations in leaf phenology of deciduous broadleaf forests from SPOT/VEGETATION time-series

In mountain forest ecosystems where elevation gradients are prominent, temperature gradient-based phenological variability can be high. However, there are few studies that assess the capability of remote sensing observations to monitor ecosystem phenology along elevation gradients, despite their relevance under climate change. We investigated the potential of medium resolution remotely sensed data to monitor the elevation variations in the seasonal dynamics of a temperate deciduous broadleaf forested ecosystem. Further, we explored the impact of elevation on the onset of spring leafing. This study was based on the analysis of multi-annual time-series of VEGETATION data acquired over the French Pyrenees Mountain Region (FPMR), in conjunction with simultaneous ground-based observations of leaf phenology made for two dominant tree species in the region (oak and beech). The seasonal variations in the perpendicular vegetation index (PVI) were analyzed during a five-year period (2002 to 2006). The five years of data were averaged into a one sole year in order to fill the numerous large spatio-temporal gaps due to cloud and snow presence – frequent in mountains – without altering the temporal resolution. Since a VEGETATION pixel (1 km²) includes several types of land cover, the broadleaf forest-specific seasonal dynamics of PVI was reconstructed pixel-by-pixel using a temporal unmixing method based on a non-parametric statistical approach. The spatial pattern of the seasonal response of PVI was clearly consistent with the relief. Nevertheless the elevational or geographic range of tree species, which differ in their phenology sensitivity to temperature, also has a significant impact on this pattern. The reduction in the growing season length with elevation was clearly observable from the delay in the increase of PVI in spring and from the advance of its decrease in the fall. The elevation variations in leaf flushing timing were estimated from the temporal change in PVI in spring over the study area. They were found to be consistent with those measured in situ ( R2 > 0.95). It was deduced that, over FPMR, the mean delay of leaf flushing timing for every 100 m increase in elevation was estimated be approximately 2.3 days. The expected estimation error of satellite-based leaf unfolding date for a given elevation was approximately 2 days. This accuracy can be considered as satisfactory since it would allow us to detect changes in leafing timing of deciduous broadleaf forests with a magnitude equivalent to that due to an elevation variation of 100 m (2.3 days on average), or in other words, to that caused by a variation in the mean annual air temperature of 0.5 °C. Although averaging the VEGETATION data over five years led to a loss of interannual information, it was found to be a robust approach to characterise the elevation variations in spring leafing and its long-term trends.

Changes in leaf phenology of three European oak species in response to experimental climate change

*Because the phenology of trees is strongly driven by environmental factors such as temperature, climate change has already altered the vegetative and reproductive phenology of many species, especially in the temperate zone. Here, we aimed to determine whether projected levels of warming for the upcoming decades will lead to linear changes in the phenology of trees or to more complex responses. *We report the results of a 3-yr common garden experiment designed to study the phenological response to artificial climate change, obtained through experimental warming and reduced precipitation, of several populations of three European oaks, two deciduous species (Quercus robur, Quercus pubescens) and one evergreen species (Quercus ilex), in a Mediterranean site. *Experimental warming advanced the seedlings' vegetative phenology, causing a longer growing season and higher mortality. However, the rate of advancement of leaf unfolding date was decreased with increasing temperature. Conversely, soil water content did not affect the phenology of the seedlings or their survival. *Our results show that the phenological response of trees to climate change may be nonlinear, and suggest that predictions of phenological changes in the future should not be built on extrapolations of current observed trends.

Impact of climate change on plant phenology in Mediterranean ecosystems

AbstractPlant 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 &lt;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.