Widespread decline in winds delayed autumn foliar senescence over high latitudes.

The high northern latitudes (>50°) experienced a pronounced surface stilling (i.e., decline in winds) with climate change. As a drying factor, the influences of changes in winds on the date of autumn foliar senescence (DFS) remain largely unknown and are potentially important as a mechanism explaining the interannual variability of autumn phenology. Using 183,448 phenological observations at 2,405 sites, long-term site-scale water vapor and carbon dioxide flux measurements, and 34 y of satellite greenness data, here we show that the decline in winds is significantly associated with extended DFS and could have a relative importance comparable with temperature and precipitation effects in contributing to the DFS trends. We further demonstrate that decline in winds reduces evapotranspiration, which results in less soil water losses and consequently more favorable growth conditions in late autumn. In addition, declining winds also lead to less leaf abscission damage which could delay leaf senescence and to a decreased cooling effect and therefore less frost damage. Our results are potentially useful for carbon flux modeling because an improved algorithm based on these findings projected overall widespread earlier DFS than currently expected by the end of this century, contributing potentially to a positive feedback to climate.

Poleward shifts in the maximum of spring phenological responsiveness of Ginkgo biloba to temperature in China.

Global warming is advancing the timing of spring leaf-out in temperate and boreal plants, affecting biological interactions and global biogeochemical cycles. However, spatial variation in spring phenological responsiveness to climate change within species remains poorly understood. Here, we investigated variation in the responsiveness of spring phenology to temperature (RSP; days to leaf-out at a given temperature) in 2754 Ginkgo biloba twigs of trees distributed across subtropical and temperate regions in China from 24°N to 44°N. We found a nonlinear effect of mean annual temperature on spatial variation in RSP, with the highest response rate at c. 12°C and lower response rates at warmer or colder temperatures due to declines in winter chilling accumulation. We then predicted the spatial maxima in RSP under current and future climate scenarios, and found that trees are currently most responsive in central China, which corresponds to the species' main distribution area. Under a high-emission scenario, we predict a 4-degree latitude shift in the responsiveness maximum toward higher latitudes over the rest of the century. The identification of the nonlinear responsiveness of spring phenology to climate gradients and the spatial shifts in phenological responsiveness expected under climate change represent new mechanistic insights that can inform models of spring phenology and ecosystem functioning.

Radiation-constrained boundaries cause nonuniform responses of the carbon uptake phenology to climatic warming in the Northern Hemisphere.

Climatic warming has lengthened the photosynthetically active season in recent decades, thus affecting the functioning and biogeochemistry of ecosystems, the global carbon cycle and climate. Temperature response of carbon uptake phenology varies spatially and temporally, even within species, and daily total intensity of radiation may play a role. We empirically modelled the thresholds of temperature and radiation under which daily carbon uptake is constrained in the temperate and cold regions of the Northern Hemisphere, which include temperate forests, boreal forests, alpine and tundra biomes. The two-dimensionality of the temperature-radiation constraint was reduced to one single variable, θ, which represents the angle in a polar coordinate system for the temperature-radiation observations during the start and end of the growing season. We found that radiation will constrain the trend towards longer growing seasons with future warming but differently during the start and end of season and depending on the biome type and region. We revealed that radiation is a major factor limiting photosynthetic activity that constrains the phenology response to temperature during the end-of-season. In contrast, the start of the carbon uptake is overall highly sensitive to temperature but not constrained by radiation at the hemispheric scale. This study thus revealed that while at the end-of-season the phenology response to warming is constrained at the hemispheric scale, at the start-of-season the advance of spring onset may continue, even if it is at a slower pace.

Global warming is increasing the discrepancy between green (actual) and thermal (potential) seasons of temperate trees.

Over the past decades, global warming has led to a lengthening of the time window during which temperatures remain favorable for carbon assimilation and tree growth, resulting in a lengthening of the green season. The extent to which forest green seasons have tracked the lengthening of this favorable period under climate warming, however, has not been quantified to date. Here, we used remote sensing data and long-term ground observations of leaf-out and coloration for six dominant species of European trees at 1773 sites, for a total of 6060 species-site combinations, during 1980-2016 and found that actual green season extensions (GS: 3.1 ± 0.1 day decade-1 ) lag four times behind extensions of the potential thermal season (TS: 12.6 ± 0.1 day decade-1 ). Similar but less pronounced differences were obtained using satellite-derived vegetation phenology observations, that is, a lengthening of 4.4 ± 0.13 and 7.5 ± 0.13 day decade-1 for GS and TS, respectively. This difference was mainly driven by the larger advance in the onset of the thermal season compared to the actual advance of leaf-out dates (spring mismatch: 7.2 ± 0.1 day decade-1 ), but to a less extent caused by a phenological mismatch between GS and TS in autumn (2.4 ± 0.1 day decade-1 ). Our results showed that forest trees do not linearly track the new thermal window extension, indicating more complex interactions between winter and spring temperatures and photoperiod and a justification of demonstrating that using more sophisticated models that include the influence of chilling and photoperiod is needed to accurately predict spring phenological changes under warmer climate. They urge caution if such mechanisms are omitted to predict, for example, how vegetative health and growth, species distribution and crop yields will change in the future.

Winter warming offsets one half of the spring warming effects on leaf unfolding.

Winter temperature-related chilling and spring temperature-related forcing are two major environmental cues shaping the leaf-out date of temperate species. To what degree insufficient chilling caused by winter warming would slow phenological responses to spring warming remains unclear. Using 27,071 time series of leaf-out dates for 16 tree species in Europe, we constructed a phenological model based on the linear or exponential function between the chilling accumulation (CA) and forcing requirements (FR) of leaf-out. We further used the phenological model to quantify the relative contributions of chilling and forcing on past and future spring phenological change. The results showed that the delaying effect of decreased chilling on the leaf-out date was prevalent in natural conditions, as more than 99% of time series exhibited a negative relationship between CA and FR. The reduction in chilling linked to winter warming from 1951 to 2014 could offset about one half of the spring phenological advance caused by the increase in forcing. In future warming scenarios, if the same model is used and a linear, stable correlation between CA and FR is assumed, declining chilling will continuously offset the advance of leaf-out to a similar degree. Our study stresses the importance of assessing the antagonistic effects of winter and spring warming on leaf-out phenology.

Soil moisture regulates warming responses of autumn photosynthetic transition dates in subtropical forests.

Autumn phenology plays a key role in regulating the terrestrial carbon and water balance and their feedbacks to the climate. However, the mechanisms underlying autumn phenology are still poorly understood, especially in subtropical forests. In this study, we extracted the autumn photosynthetic transition dates (APTD) in subtropical China over the period 2003-2017 based on a global, fine-resolution solar-induced chlorophyll fluorescence (SIF) dataset (GOSIF) using four fitting methods, and then explored the temporal-spatial variations of APTD and its underlying mechanisms using partial correlation analysis and machine learning methods. We further predicted the APTD shifts under future climate warming conditions by applying process-based and machine learning-based models. We found that the APTD was significantly delayed, with an average rate of 7.7 days per decade, in subtropical China during 2003-2017. Both partial correlation analysis and machine learning methods revealed that soil moisture was the primary driver responsible for the APTD changes in southern subtropical monsoon evergreen forest (SEF) and middle subtropical evergreen forest (MEF), whereas solar radiation controlled the APTD variations in the northern evergreen-broadleaf deciduous mixed forest (NMF). Combining the effects of temperature, soil moisture and radiation, we found a significantly delayed trend in APTD during the 2030-2100 period, but the trend amplitude (0.8 days per decade) was much weaker than that over 2003-2017. In addition, we found that machine learning methods outperformed process-based models in projecting APTD. Our findings generate from different methods highlight that soil moisture is one of the key players in determining autumn photosynthetic phenological processes in subtropical forests. To comprehensively understand autumn phenological processes, in-situ manipulative experiments are urgently needed to quantify the contributions of different environmental and physiological factors in regulating plants' response to ongoing climate change.

Impact of microclimatic conditions and resource availability on spring and autumn phenology of temperate tree seedlings.

Microclimatic effects (light, temperature) are often neglected in phenological studies and little information is known about the impact of resource availability (nutrient and water) on tree's phenological cycles. Here we experimentally studied spring and autumn phenology in four temperate trees in response to changes in bud albedo (white-painted vs black-painted buds), light conditions (nonshaded vs c. 70% shaded), water availability (irrigated, control and reduced precipitation) and nutrients (low vs high availability). We found that higher bud albedo or shade delayed budburst (up to +12 d), indicating that temperature is sensed locally within each bud. Leaf senescence was delayed by high nutrient availability (up to +7 d) and shade conditions (up to +39 d) in all species, except oak. Autumn phenological responses to summer droughts depended on species, with a delay for cherry (+7 d) and an advance for beech (-7 d). The strong phenological effects of bud albedo and light exposure reveal an important role of microclimatic variation on phenology. In addition to the temperature and photoperiod effects, our results suggest a tight interplay between source and sink processes in regulating the end of the seasonal vegetation cycle, which can be largely influenced by resource availability (light, water and nutrients).

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.

Global warming leads to more uniform spring phenology across elevations.

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-1 conforming to Hopkins' bioclimatic law in 1960, to 22 d⋅1,000 m-1 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.

Modeling leaf senescence of deciduous tree species in Europe.

Autumnal leaf senescence signals the end of photosynthetic activities in temperate deciduous trees and consequently exerts a strong control on various ecological processes. Predicting leaf senescence dates (LSD) with high accuracy is thus a prerequisite for better understanding the climate-ecosystem interactions. However, modeling LSD at large spatial and temporal scales is challenging. In this study, first, we used 19972 site-year records (848 sites and four deciduous tree species) from the PAN European Phenology network to calibrate and evaluate six leaf senescence models during the period 1980-2013. Second, we extended the spatial analysis by repeating the procedure across Europe using satellite-derived end of growing season and a forest map. Overall, we found that models that considered photoperiod and temperature interactions outperformed models using simple temperature or photoperiod thresholds for Betula pendula, Fagus sylvatica and Quercus robur. On the contrary, no model displayed reasonable predictions for Aesculus hippocastanum. This inter-model comparison indicates that, contrary to expectation, photoperiod does not significantly modulate the accumulation of cooling degree days (CDD). On the other hand, considering the carryover effect of leaf unfolding date could promote the models' predictability. The CDD models generally matched the observed LSD at species level and its interannual variation, but were limited in explaining the inter-site variations, indicating that other environmental cues need to be considered in future model development. The discrepancies remaining between model simulations and observations highlight the need of manipulation studies to elucidate the mechanisms behind the leaf senescence process and to make current models more realistic.