Warming-induced phenological mismatch between trees and shrubs explains high-elevation forest expansion.

Despite the importance of species interaction in modulating the range shifts of plants, little is known about the responses of coexisting life forms to a warmer climate. Here, we combine long-term monitoring of cambial phenology in sympatric trees and shrubs at two treelines of the Tibetan Plateau, with a meta-analysis of ring-width series from 344 shrubs and 575 trees paired across 11 alpine treelines in the Northern Hemisphere. Under a spring warming of +1°C, xylem resumption advances by 2-4 days in trees, but delays by 3-8 days in shrubs. The divergent phenological response to warming was due to shrubs being 3.2 times more sensitive than trees to chilling accumulation. Warmer winters increased the thermal requirement for cambial reactivation in shrubs, leading to a delayed response to warmer springs. Our meta-analysis confirmed such a mechanism across continental scales. The warming-induced phenological mismatch may give a competitive advantage to trees over shrubs, which would provide a new explanation for increasing alpine treeline shifts under the context of climate change.

Disentangling the effects of vapor pressure deficit on northern terrestrial vegetation productivity.

The impact of atmospheric vapor pressure deficit (VPD) on plant photosynthesis has long been acknowledged, but large interactions with air temperature (T) and soil moisture (SM) still hinder a complete understanding of the influence of VPD on vegetation production across various climate zones. Here, we found a diverging response of productivity to VPD in the Northern Hemisphere by excluding interactive effects of VPD with T and SM. The interactions between VPD and T/SM not only offset the potential positive impact of warming on vegetation productivity but also amplifies the negative effect of soil drying. Notably, for high-latitude ecosystems, there occurs a pronounced shift in vegetation productivity's response to VPD during the growing season when VPD surpasses a threshold of 3.5 to 4.0 hectopascals. These results yield previously unknown insights into the role of VPD in terrestrial ecosystems and enhance our comprehension of the terrestrial carbon cycle's response to global warming.

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.

Effect of climate warming on the timing of autumn leaf senescence reverses after the summer solstice.

Climate change is shifting the growing seasons of plants, affecting species performance and biogeochemical cycles. Yet how the timing of autumn leaf senescence in Northern Hemisphere forests will change remains uncertain. Using satellite, ground, carbon flux, and experimental data, we show that early-season and late-season warming have opposite effects on leaf senescence, with a reversal occurring after the year's longest day (the summer solstice). Across 84% of the northern forest area, increased temperature and vegetation activity before the solstice led to an earlier senescence onset of, on average, 1.9 ± 0.1 days per °C, whereas warmer post-solstice temperatures extended senescence duration by 2.6 ± 0.1 days per °C. The current trajectories toward an earlier onset and slowed progression of senescence affect Northern Hemisphere-wide trends in growing-season length and forest productivity.

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.

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.

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.

Effects of Vegetation Phenology on Ecosystem Water Use Efficiency in a Semiarid Region of Northern China.

Water use efficiency (WUE) is an important ecosystem functional property for measuring coupled relationships of the carbon-water cycle. Both biotic and environmental factors significantly impact WUE in terrestrial ecosystems. Relationships between environmental factors and WUE have been well discussed in previous studies. Although the crucial role of vegetation phenology, a common indicator of climate-vegetation interactions, in regulating the WUE has been widely reported, the underlying mechanism has not yet to be fully elucidated. Here, we utilized multiple long-term remote sensing datasets to analyze the interannual changes in seasonal WUE, and discussed the potential associations between phenology and WUE in the Luanhe River basin, which is a typical semiarid region of China, from 1988 to 2015. Most of the pixels across Luanhe River basin showed increasing spring WUE and decreasing autumn WUE. The start of the growing season (SOS) was slightly advanced by an average of 0.06 days per year (d/y) in the whole study area, with a delayed trend (0.04 d/y) in the upper reaches region (UR) and an advanced trend (0.20 d/y) in the middle-lower reaches region (MLR). The end of the growing season (EOS) showed a generally delayed trend (0.11 d/y) across the basin. Furthermore, negative correlations were detected between spring WUE and SOS in the UR, while positive correlations were detected in the MLR. The opposite patterns of the relationship of autumn WUE and EOS were also found between UR and MLR. The results were attributed to the balance and compensation of biotic and abiotic factors in the regulation of ecosystem WUE. Our findings provide new insights into the interaction between vegetation dynamics and carbon-water cycle coupling.

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.

Spatial Difference of Interactive Effect Between Temperature and Daylength on Ginkgo Budburst.

Climate warming-induced shifts in spring phenology have substantially affected the structure and function of terrestrial ecosystems and global biogeochemical cycles. Spring phenology is primarily triggered by spring temperature and is also affected by daylength and winter chilling, yet the relative importance of these cues across spatial gradients remains poorly understood. Here, we conducted a manipulative experiment with two daylength and three temperature treatments to investigate spatial differences in the response of ginkgo budburst to temperature and daylength, using twigs collected at three sites across a spatial gradient: a control site at a low latitude and low elevation on Tianmu Mountain (TMlow), a low latitude and high elevation site on Tianmu Mountain (TMhigh), and a high latitude site on Jiufeng mountain (JF). The mechanisms were also tested using in situ phenological observations of ginkgo along latitudes in China. We found that, compared to TMlow individuals, budburst dates occurred 12.6 (JF) and 7.7 (TMhigh) days earlier in high-latitude and high-elevation individuals when exposed to the same temperature and daylength treatments. Importantly, daylength only affected budburst at low latitudes, with long days (16 h) advancing budburst in low-latitude individuals by, on average, 8.1 days relative to short-day (8 h) conditions. This advance was most pronounced in low-elevation/latitude individuals (TMlow = 9.6 days; TMhigh = 6.7 days; JF = 1.6 days). In addition, we found that the temperature sensitivity of budburst decreased from 3.4 to 2.4 days °C-1 along latitude and from 3.4 to 2.5 days °C-1 along elevation, respectively. The field phenological observations verified the experimental results. Our findings provide empirical evidence of spatial differences in the relative effects of spring temperature and daylength on ginkgo budburst, which improved our understanding of spatial difference in phenological changes and the responses of terrestrial ecosystem to climate change.

Climate warming shifts the time interval between flowering and leaf unfolding depending on the warming period.

The timing of flowering (FL) and leaf unfolding (LU) determine plants' reproduction and vegetative growth. Global warming has substantially advanced FL and LU of temperate and boreal plants, but their responses to warming differ, which may influence the time interval between FL and LU (∆LU-FL), thereby impacting plant fitness and intraspecific physiological processes. Based on twigs collected from two flowering-first tree species, Populus tomentosa and Amygdalus triloba, we conducted a manipulative experiment to investigate the effects of winter chilling, spring warming and photoperiod on the ∆LU-FL. We found that photoperiod did not affect the ∆LU-FL of Amygdalus triloba, but shortened ∆LU-FL by 5.1 d of Populus tomentosa. Interestingly, spring warming and winter chilling oppositely affected the ∆LU-FL of both species. Specifically, low chilling accumulation extended the ∆LU-FL by 3.8 and 9.4 d for Populus tomentosa and Amygdalus triloba, but spring warming shortened the ∆LU-FL by 4.1 and 0.2 d °C-1. Our results indicate that climate warming will decrease or increase the ∆LU-FL depending on the warming periods, i.e., spring or winter. The shifted time interval between flowering and leaf unfolding may have ecological effects including affecting pollen transfer efficiency and alter the structure and functioning of terrestrial ecosystem.

An earlier start of the thermal growing season enhances tree growth in cold humid areas but not in dry areas.

Climatic warming alters the onset, duration and cessation of the vegetative season. While previous studies have shown a tight link between thermal conditions and leaf phenology, less is known about the impacts of phenological changes on tree growth. Here, we assessed the relationships between the start of the thermal growing season and tree growth across the extratropical Northern Hemisphere using 3,451 tree-ring chronologies and daily climatic data for 1948-2014. An earlier start of the thermal growing season promoted growth in regions with high ratios of precipitation to temperature but limited growth in cold-dry regions. Path analyses indicated that an earlier start of the thermal growing season enhanced growth primarily by alleviating thermal limitations on wood formation in boreal forests and by lengthening the period of growth in temperate and Mediterranean forests. Semi-arid and dry subalpine forests, however, did not benefit from an earlier onset of growth and a longer growing season, presumably due to associated water loss and/or more frequent early spring frosts. These emergent patterns of how climatic impacts on wood phenology affect tree growth at regional to hemispheric scales hint at how future phenological changes may affect the carbon sequestration capacity of extratropical forest ecosystems.

Contrasting phenology responses to climate warming across the northern extra-tropics.

Climate warming has substantially advanced the timing of spring leaf-out of woody species at middle and high latitudes, albeit with large differences. Insights in the spatial variation of this climate warming response may therefore help to constrain future trends in leaf-out and its impact on energy, water and carbon balances at global scales. In this study, we used in situ phenology observations of 38 species from 2067 study sites, distributed across the northern hemisphere in China, Europe and the United States, to investigate the latitudinal patterns of spring leaf-out and its sensitivity (ST, advance of leaf-out dates per degree of warming) and correlation (RT, partial correlation coefficient) to temperature during the period 1980-2016. Across all species and sites, we found that ST decreased significantly by 0.15 ± 0.02 d °C-1 °N-1, and RT increased by 0.02 ± 0.001 °N-1 (both at P < 0.001). The latitudinal patterns in RT and ST were explained by the differences in requirements of chilling and thermal forcing that evolved to maximize tree fitness under local climate, particularly climate predictability and summed precipitation during the pre-leaf-out season. Our results thus showed complicated spatial differences in leaf-out responses to ongoing climate warming and indicated that spatial differences in the interactions among environmental cues need to be embedded into large-scale phenology models to improve the simulation accuracy.

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).

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.

Diverging models introduce large uncertainty in future climate warming impact on spring phenology of temperate deciduous trees.

Spring phenology influences terrestrial ecosystem carbon, water and energy exchanges between the biosphere and atmosphere. Accurate prediction of spring phenology is therefore a prerequisite to foresee the impacts of climate warming on terrestrial ecosystems. In the present study, we studied the model performance of four widely used process-based models of spring leaf unfolding, including both a one-phase model (not considering a chilling phase: the Thermal Time model) and three two-phase models (all accounting for a required chilling period: the Parallel model, the Sequential model, the Unified model). Models were tested on five deciduous tree species occurring across Europe. We specifically investigated the divergence of their phenology predictions under future climate warming scenarios and studied the differences in the chilling periods. We found that, in general, the two-phase models performed slightly better than the one-phase model when fitting to the observed data, with all two-phase models performing similarly. However, leaf unfolding projections diverged substantially among the two-phase models over the period 2070-2100. Furthermore, we found that the modeled end dates of the chilling periods in these models also diverged, with advances for both the Sequential and Parallel models during the period 2070-2100 (compared to the period 1980-2010), and delays in the Unified model. These findings thus highlight large uncertainty in the two-phase phenology models and confirm that the mechanism underlying the leaf unfolding process is not yet understood. We therefore urgently need an improved understanding of the leaf unfolding process in order to improve the representation of phenology in terrestrial ecosystem models.

Influences of Shifted Vegetation Phenology on Runoff Across a Hydroclimatic Gradient.

Climate warming has changed vegetation phenology, and the phenology-associated impacts on terrestrial water fluxes remain largely unquantified. The impacts are linked to plant adjustments and responses to climate change and can be different in different hydroclimatic regions. Based on remote sensing data and observed river runoff of hydrological station from six river basins across a hydroclimatic gradient from northeast to southwest in China, the relative contributions of the vegetation (including spring and autumn phenology, growing season length (GSL), and gross primary productivity) and climatic factors affecting the river runoffs over 1982-2015 were investigated by applying gray relational analysis (GRA). We found that the average GSLs in humid regions (190-241 days) were longer than that in semi-humid regions (186-192 days), and the average GSLs were consistently extended by 4.8-13.9 days in 1982-2015 period in six river basins. The extensions were mainly linked to the delayed autumn phenology in the humid regions and to advanced spring phenology in the semi-humid regions. Across all river basins, the GRA results showed that precipitation (r = 0.74) and soil moisture (r = 0.73) determine the river runoffs, and the vegetation factors (VFs) especially the vegetation phenology also affected the river runoffs (spring phenology: r = 0.66; GSL: r = 0.61; autumn phenology: r = 0.59), even larger than the contribution from temperature (r = 0.57), but its relative importance is climatic region-dependent. Interestingly, the spring phenology is the main VF in the humid region for runoffs reduction, while both spring and autumn growth phenology are the main VFs in the semi-humid region, because large autumn phenology delay and less water supply capacity in spring amplify the effect of advanced spring phenology. This article reveals diverse linkages between climatic and VFs, and runoff in different hydroclimatic regions, and provides insights that vegetation phenology influences the ecohydrology process largely depending on the local hydroclimatic conditions, which improve our understanding of terrestrial hydrological responses to climate change.

Climate warming increases spring phenological differences among temperate trees.

Climate warming has substantially advanced spring leaf flushing, but winter chilling and photoperiod co-determine the leaf flushing process in ways that vary among species. As a result, the interspecific differences in spring phenology (IDSP) are expected to change with climate warming, which may, in turn, induce negative or positive ecological consequences. However, the temporal change of IDSP at large spatiotemporal scales remains unclear. In this study, we analyzed long-term in-situ observations (1951-2016) of six, coexisting temperate tree species from 305 sites across Central Europe and found that phenological ranking did not change when comparing the rapidly warming period 1984-2016 to the marginally warming period 1951-1983. However, the advance of leaf flushing was significantly larger in early-flushing species EFS (6.7 ± 0.3 days) than in late-flushing species LFS (5.9 ± 0.2 days) between the two periods, indicating extended IDSP. This IDSP extension could not be explained by differences in temperature sensitivity between EFS and LFS; however, climatic warming-induced heat accumulation effects on leaf flushing, which were linked to a greater heat requirement and higher photoperiod sensitivity in LFS, drove the shifts in IDSP. Continued climate warming is expected to further extend IDSP across temperate trees, with associated implications for ecosystem function.

Soil thawing regulates the spring growth onset in tundra and alpine biomes.

Soil temperature remains isothermal at 0 °C and water shifts to a liquid phase during soil thawing. Vegetation may receive this process as a signal and a key to restore physiological activity. We aimed to show the relationship between the timing of soil thawing and the spring growth onset. We estimated the delay between the soil thawing and the spring growth onset in 78 sites of the FLUXNET network. We built a soil thawing map derived from modeling for the northern hemisphere and related it to the greenness onset estimated with satellite imagery. Spring onset estimated with GPP time series occurred shortly after soil surface thawing in tundra (1.1 ± 3.5 days) and alpine grasslands (16.6 ± 5.8 days). The association was weaker for deciduous forests (40.3 ± 4.2 days), especially where soils freeze infrequently. Needleleaved forests tended to start the growing season before the end of thawing (-17.4 ± 3.6 days), although observations from remote sensing (MODIS Land Cover Dynamics) indicated that the onset of greenness started after the thawing period (26.8 ± 3.2 days). This study highlights the role of soil temperature at the spring growth onset at high latitudes. Soil thawing becomes less relevant in temperate forests, where soil is occasionally frozen and other climate factors become more important.