Plant phenology, the annually recurring sequence of plant developmental stages, is important for plant functioning and ecosystem services and their biophysical and biogeochemical feedbacks to the climate system. Plant phenology depends on temperature, and the current rapid climate change has revived interest in understanding and modeling the responses of plant phenology to the warming trend and the consequences thereof for ecosystems. Here, we review recent progresses in plant phenology and its interactions with climate change. Focusing on the start (leaf unfolding) and end (leaf coloring) of plant growing seasons, we show that the recent rapid expansion in ground-and remote sensing-based phenology data acquisition has been highly beneficial and has supported major advances in plant phenology research.Studies using multiple data sources and methods generally agree on the trends of advanced leaf unfolding and delayed leaf coloring due to climate change, yet these trends appear to have decelerated or even reversed in recent years. Our understanding of the mechanisms underlying the plant phenology responses to climate warming is still limited. The interactions between multiple drivers complicate the modeling and prediction of plant phenology changes. Furthermore, changes in plant phenology have important implications for ecosystem carbon cycles and ecosystem feedbacks to climate, yet the quantification of such impacts remains challenging. We suggest that future studies should primarily focus on using new observation tools to improve the understanding of tropical plant phenology, on improving process-based phenology modeling, and on the scaling of phenology from species to landscape-level. K E Y W O R D S climate change, climatic feedback, ecological implications, leaf coloring, leaf unfolding, mechanisms and drivers, phenological modeling, plant phenology, satellite-derived phenology | 1923 PIAO et Al.

18The phenology of spring leaf unfolding influences regional and hemispheric-scale carbon 19 balances 2 , the long-term distribution of tree species 9 , and plant-animal interactions 10 . Changes in 20 the phenology of spring leaf unfolding can also exert biophysical feedbacks on climate by 21 modifying the surface albedo and energy budget 11,12 . Recent studies have reported significant 22 advances in spring phenology as a result of warming in most northern hemisphere regions 1,3,4 . 23Climate warming is projected to further increase 13 , but the future evolution of the phenology of 24 spring leaf unfolding remains uncertain -in view of the imperfect understanding of how the 25 underlying mechanisms respond to environmental stimuli 12,14 . In addition, the relative 26 contributions of each environmental stimulus, which together define the apparent temperature 27 sensitivity of the phenology of spring leaf unfolding (advances in days per degree Celsius 28 warming, S T ), may also change over time 6,8,15 . An improved characterization of the variation in 29 3 phenological responses to spring temperature is thus valuable, provided that it addresses temporal 1 and spatial scales relevant for regional projections. 2Numerous studies have reported advanced spring leaf unfolding which matches warming trends 3 over recent decades 1,3,4 . However, there is still debate regarding the linearity of leaf unfolding 4 response to the climate warming 6,7 . Recent experimental studies of warming using saplings have 5 shown that S T weakens as warming increases 7 . Experimental manipulation of temperature for 6 saplings or twigs, however, might elicit phenological responses that do not accurately reflect the 7 response of mature trees 16,17 . We therefore investigated the temporal changes in S T in adult trees 8 monitored in situ and exposed to real-world changes in temperature and other climate variables. 9These long-term data series were obtained across Central Europe from the Pan European regression for the entire period and for two 15-year periods, namely 1980-1994 and 1999-2013, 25 that had slight difference in preseason lengths (Extended Data Fig. 3a). The leaf unfolding dates (Fig. 1a). But the surprising result is that S T 3 significantly decreased by 40.0% from 4.0 ± 1.8 days °C -1 during 1980-1994 to 2.3 ± 1.6 days °C -4 1 during 1999-2013 (t=-37.3, df=5473, P<0.001) (Fig. 1b). All species show similar significant 5 decreases in S T (Fig. 1a), although the extent of reduction was species-specific. For example, 6Aesculus hippocastanum (see caption to Fig. 1 for English common names) had the largest 7 decrease in S T (-2.0 days °C -1 ), while S T decreased only slightly (but still significantly) in Fagus 8 sylvatica (-0.9 days °C -1 ) (Fig. 1a). Similar results were also obtained using a fixed preseason 9 length determined either in the time period 1980-1994 or in 1999-2013 10 and 3c). The declining S T could, however, also have been an artifact resulting from the 11 ‗encroachment' of leaf unfolding dates...

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.

The timing of the end of the vegetation growing season (EOS) plays a key role in terrestrial ecosystem carbon and nutrient cycles. Autumn phenology is, however, still poorly understood, and previous studies generally focused on few species or were very limited in scale. In this study, we applied four methods to extract EOS dates from NDVI records between 1982 and 2011 for the Northern Hemisphere, and determined the temporal correlations between EOS and environmental factors (i.e., temperature, precipitation and insolation), as well as the correlation between spring and autumn phenology, using partial correlation analyses. Overall, we observed a trend toward later EOS in ~70% of the pixels in Northern Hemisphere, with a mean rate of 0.18 ± 0.38 days yr . Warming preseason temperature was positively associated with the rate of EOS in most of our study area, except for arid/semi-arid regions, where the precipitation sum played a dominant positive role. Interestingly, increased preseason insolation sum might also lead to a later date of EOS. In addition to the climatic effects on EOS, we found an influence of spring vegetation green-up dates on EOS, albeit biome dependent. Our study, therefore, suggests that both environmental factors and spring phenology should be included in the modeling of EOS to improve the predictions of autumn phenology as well as our understanding of the global carbon and nutrient balances.

Recent temperature increases have elicited strong phenological shifts in temperate tree species, with subsequent effects on photosynthesis. Here, we assess the impact of advanced leaf flushing in a winter warming experiment on the current year's senescence and next year's leaf flushing dates in two common tree species: Quercus robur L. and Fagus sylvatica L. Results suggest that earlier leaf flushing translated into earlier senescence, thereby partially offsetting the lengthening of the growing season. Moreover, saplings that were warmed in winter-spring 2009-2010 still exhibited earlier leaf flushing in 2011, even though the saplings had been exposed to similar ambient conditions for almost 1 y. Interestingly, for both species similar trends were found in mature trees using a long-term series of phenological records gathered from various locations in Europe. We hypothesize that this longterm legacy effect is related to an advancement of the endormancy phase (chilling phase) in response to the earlier autumnal senescence. Given the importance of phenology in plant and ecosystem functioning, and the prediction of more frequent extremely warm winters, our observations and postulated underlying mechanisms should be tested in other species.climate change | tree phenology | spring flushing | leaf senescence L eaf phenology of temperate trees has recently received particular attention because of its sensitivity to the ongoing climate change (1-3), and because of its crucial role in the forest ecosystem, water and carbon balances, and species distribution (4-6).A wide variety of methods, such as long-term phenological records (7), indirect measurements of ecosystem greening by remote sensing using satellites or webcam digital images (8-10), and modeling approaches (11-13), have been applied to monitor and study phenological changes. These different approaches, conducted at different spatial scales (from individual plants to biomes), have documented a clear advancement of leaf flushing in temperate climate zones and, to a lesser extent, a delay in leaf senescence (14,15). Furthermore, various temperature manipulation experiments have simulated the impact of future winter warming on leaf phenology and confirmed an advancement in the timing of leaf flushing in response to warming (16-18). However, the response of leaf flushing to climate warming is highly nonlinear (16,19,20), because trees also depend on cold temperatures to break bud dormancy (21-23). This chilling requirement may not (fully) be met in a warming climate, especially at the southern edges of species distribution ranges (5,24,25).Most previous phenological studies have focused on specific phenophases, but how a phenological change (e.g., advanced leaf flushing) affects subsequent phenological events is rarely investigated. Nonetheless, the annual growth cycle of boreal and temperate trees forms an integrated system, where one phenophase in the cycle can affect the subsequent phases (26, 27). Such carryover effects have already been detected in fruit and nu...

Autumn phenology plays a critical role in regulating climate-biosphere interactions. However, the climatic drivers of autumn phenology remain unclear. In this study, we applied four methods to estimate the date of the end of the growing season (EOS) across China's temperate biomes based on a 30-year normalized difference vegetation index (NDVI) dataset from Global Inventory Modeling and Mapping Studies (GIMMS). We investigated the relationships of EOS with temperature, precipitation sum, and insolation sum over the preseason periods by computing temporal partial correlation coefficients. The results showed that the EOS date was delayed in temperate China by an average rate at 0.12 ± 0.01 days per year over the time period of 1982-2011. EOS of dry grassland in Inner Mongolia was advanced. Temporal trends of EOS determined across the four methods were similar in sign, but different in magnitude. Consistent with previous studies, we observed positive correlations between temperature and EOS. Interestingly, the sum of precipitation and insolation during the preseason was also associated with EOS, but their effects were biome dependent. For the forest biomes, except for evergreen needle-leaf forests, the EOS dates were positively associated with insolation sum over the preseason, whereas for dry grassland, the precipitation over the preseason was more dominant. Our results confirmed the importance of temperature on phenological processes in autumn, and further suggested that both precipitation and insolation should be considered to improve the performance of autumn phenology models.

One hundred years ago, Andrew D. Hopkins estimated the progressive delay in tree leaf-out with increasing latitude, longitude, and elevation, referred to as "Hopkins' bioclimatic law." What if global warming is altering this well-known law? Here, based on ∼20,000 observations of the leaf-out date of four common temperate tree species located in 128 sites at various elevations in the European Alps, we found that the elevation-induced phenological shift (EPS) has significantly declined from 34 d⋅1,000 m conforming to Hopkins' bioclimatic law in 1960, to 22 d⋅1,000 m in 2016, i.e., -35%. The stronger phenological advance at higher elevations, responsible for the reduction in EPS, is most likely to be connected to stronger warming during late spring as well as to warmer winter temperatures. Indeed, under similar spring temperatures, we found that the EPS was substantially reduced in years when the previous winter was warmer. Our results provide empirical evidence for a declining EPS over the last six decades. Future climate warming may further reduce the EPS with consequences for the structure and function of mountain forest ecosystems, in particular through changes in plant-animal interactions, but the actual impact of such ongoing change is today largely unknown.

While climate warming reduces the occurrence of frost events, the warming-induced lengthening of the growing season of plants in the Northern Hemisphere may actually induce more frequent frost days during the growing season (GSFDs, days with minimum temperature < 0 °C). Direct evidence of this hypothesis, however, is limited. Here we investigate the change in the number of GSFDs at latitudes greater than 30° N using remotely-sensed and in situ phenological records and three minimum temperature ( T min ) data sets from 1982 to 2012. While decreased GSFDs are found in northern Siberia, the Tibetan Plateau, and northwestern North America (mainly in autumn), ~43% of the hemisphere, especially in Europe, experienced a significant increase in GSFDs between 1982 and 2012 (mainly during spring). Overall, regions with larger increases in growing season length exhibit larger increases in GSFDs. Climate warming thus reduces the total number of frost days per year, but GSFDs nonetheless increase in many areas.