Abstract
Spring warming substantially advances leaf unfolding and flowering time for perennials. Winter warming, however, decreases chilling accumulation (CA), which increases the heat requirement ...(HR) and acts to delay spring phenology. Whether or not this negative CA-HR relationship is correctly interpreted in ecosystem models remains unknown. Using leaf unfolding and flowering data for 30 perennials in Europe, here we show that more than half (7 of 12) of current chilling models are invalid since they show a positive CA-HR relationship. The possible reason is that they overlook the effect of freezing temperature on dormancy release. Overestimation of the advance in spring phenology by the end of this century by these invalid chilling models could be as large as 7.6 and 20.0 days under RCPs 4.5 and 8.5, respectively. Our results highlight the need for a better representation of chilling for the correct understanding of spring phenological responses to future climate change.
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.
This review examines the recent progresses in plant phenology and its interactions with climate change. Over its long history, phenology has grown from an empirical subject of observing and recording the timing of annual natural events for specific species to a comprehensive field that involves expanded observations, experiments, modeling, as well as the ecological consequences and climatic feedbacks of phenological changes. This review also emphasizes the need for future studies on the understanding of tropical plant phenology with new tools, on improving process‐based modeling, and on the scaling of phenology from species level to landscape level.
Current understanding of autumn phenological responses to climate change in deciduous tree species remains limited, mainly due to the difficulties in defining autumn events and the lack of knowledge ...about its mechanism. Here we applied a method based on measuring chlorophyll A (Chla) content in leaf tissue during the entire autumn senescence processes to appropriately quantify autumn phenological processes. Beginning of leaf coloring could be defined as when about 50% of the Chl was lost. End of leaf coloring could be defined as when about 95% of the Chl was lost. Then the mechanism behind the timing of autumn senescence responses to climate change through hormone regulation was studied for the first time. Four dominate deciduous tree species with representative senescence type (Salix babylonica, Ginkgo biloba, Acer mono, Cotinus coggygria) were chosen as the subject of study. Variations in climate factors (temperature, day length, precipitation, humidity) were recorded and nine major endogenous hormones (IAA, IPA, ZR, DHZR, GA
, GA
, ABA, MeJA, BR) in leaf tissues were monitored during the entire autumn senescence processes. The experimental results verified temperature and day length are the major climate factors affecting autumn phenology. Low temperature and short day length could result in the decrease of ZR level and the increase of ABA level in leaf tissue, which directly trigger/promote senescence. Meanwhile, low temperature and short day length could cause the decrease of MeJA level and the increase of GA
and GA
level, which regulate the timing of autumn senescence indirectly through ZR, ABA, and IAA. Our study improves the understanding of autumn phenological response to climate change in deciduous trees.
The effects of winter chilling, spring forcing temperature, and photoperiod on spring phenology are well known for many European and North American species, but the environmental cues that regulate ...the spring phenology of East Asian species have not yet been thoroughly investigated. Here, we conducted a growth chamber experiment to test the effects of chilling (controlled by different lengths of exposure to natural chilling conditions), forcing temperature (12, 15, or 18°C) and photoperiod (14 or 10 h) on first flowering date (FFD) of six woody species (three shrubs and three trees) native to East Asia. The three-way analysis of variance (ANOVA) separately for each species showed that the effects of chilling and forcing temperature were significant for almost all species (
< 0.05). Averaged over all chilling and photoperiod treatments, the number of days until FFD decreased by 2.3-36.1 days when the forcing temperature increased by 3°C. More chilling days reduced the time to FFD by 0.7-26 days, when averaged over forcing and photoperiod treatments. A longer photoperiod could advance the FFD by 1.0-5.6 days, on average, but its effect was only significant for two species (including one tree and one shrub). The effects of forcing temperature and photoperiod interacted with chilling for half of the studied species, being stronger in the low chilling than high chilling treatment. These results could be explained by the theory and model of growing degree-days (GDD). Increased exposure to chilling coupled to a longer photoperiod reduced the GDD requirement for FFD, especially when plants grew under low chilling conditions. However, shrubs (except
) had lower chilling and heat requirements than trees, suggesting that, by leafing out sooner, they engage in a more opportunistic life strategy to maximize their growing season, especially before canopy closure from trees' foliage. Our results confirmed the varying effects of these three cues on the flowering phenology of woody species native to East Asia. In future climate change scenarios, spring warming is likely to advance the spring phenology of those woody species, although the reduced chilling and shorter photoperiod may partly offset this spring warming effect.
•Increased drought and heat events in the pre-growing season were observed over the past two decades in Central Asia.•The contribution of extreme climate to autumn phenology was almost twice that of ...mean climate in grassland.•Decreased heavy rain and increased heat stress were the dominant factors driving the advanced autumn phenology of grassland.•The effect of extreme climate tended to weaken at higher elevations.
Over the past half-century, there has been a significant rise in the frequency and intensity of extreme climate events in dryland ecosystems. While vegetation phenology acts as an important indicator of how ecosystems respond to climate change, the impact of extreme climate events on autumn phenology in dryland ecosystems remains uncertain. In this study, we firstly assessed the temporal variations in the end of growing season (EOS) in Central Asia using the Normalized Difference Vegetation Index and enhanced vegetation index over 2001–2018. Then, we assessed the impacts of eight climate indices, which capture the average and extreme conditions of the local climate, on EOS across diverse vegetation types using linear mixed models. Finally, we conducted partial correlation analysis to explore how the primary influencing factors affect EOS along an elevational gradient. Our results suggested increased occurrences of drought and heat events in the pre-growing season (April–September) in Central Asia. Under the background, a general trend towards earlier EOS (ca. 1.01 days/decade) was observed for grassland. This trend was mostly attributed to the changes in extreme climate indices (CIextreme), especially heavy rainfall and heat stress. The total explanatory power of CIextreme was almost twice that of mean climate indices (CImean). However, the impact of CIextreme was less pronounced in regions with elevations exceeding 1500 m. For forests and shrublands, the EOS exhibited delaying trend of 1.29 days/decade and advancing trend of 1.21 days/decade, respectively. Contrary to grasslands, the variations in EOS of forests and shrublands were largely influenced by the shift of CImean, especially mean minimum temperature and accumulated precipitation. The contribution of CIextreme accounted for only 1/6 of the contribution of CImean, likely attributed to the adaptation of forests to cold conditions and shrublands to arid conditions. The results provide valuable insights into the phenological response to extreme climate events and serve as a reference for ecosystem management in arid regions.
•Partial Least Squares regression can illustrate tree responses during dormancy.•Phenology responses to chill and heat accumulation rates vary by species and site.•Walnuts in California responded to ...variation in chill accumulation.•Heat accumulation was more important for cherries and chestnuts in cold-winter sites.•Delayed phenology in warm years may indicate vulnerability to climate change.
Temperate-zone trees must fulfill cultivar-specific chilling and heat requirements during the dormant period, in order to produce leaves and flowers in the following growing season. Timing and accumulation rate of chill and heat are understood to determine the timing of spring events, but both processes are difficult to observe in dormant tree buds. Where long-term phenological observations are available, Partial Least Squares (PLS) regression offers a statistical opportunity to delineate phases of chill and heat accumulation and determine the climatic requirements of trees. This study uses PLS regression to explore how the timing of spring events of chestnut in China, cherry in Germany and walnut in California is related to variation in the daily rates of chill and heat accumulation, as calculated with horticultural models. Dependent variables were 39 years of flowering dates for chestnuts in Beijing (China), 25 years of cherry bloom in Klein-Altendorf (Germany) and 54 years of walnut leaf emergence in Davis (California, USA). These were related to daily accumulation rates of chill, calculated with the Dynamic Model, and heat, calculated with the Growing Degree Hours Model. Compared to an earlier version of the procedure, in which phenological dates were related to unprocessed temperature data, delineation of chilling and forcing phases was much clearer when using horticultural metrics to quantify chill and heat. Chestnut bloom in the cold-winter climate of Beijing was found to depend primarily on the rate of heat accumulation, while cherry bloom in the temperate climate of Germany showed dependence on both chill and heat accumulation rates. The timing of walnut leaf emergence in the mild-winter climate of California depended much more strongly on chill accumulation rates. Chilling (in Chill Portions=CP) and heat (in Growing Degree Hours=GDH) requirements determined based on PLS regression were 79.8±5.3 CP and 13,466±1918 GDH for chestnut bloom in Beijing, 104.2±8.9 CP and 2698±1183 GDH for cherry bloom in Germany, and 37.5±5.0 CP and 11,245±1697 GDH for walnut leaf emergence in California. Spring phases of cherry in Klein-Altendorf and especially chestnut in Beijing will likely continue to advance in response to global warming, while for walnut in California, inadequate chilling may cause delays in flowering and leaf emergence. Such delays could serve as an early-warning indicator that future productivity may be threatened by climate change. The R package ‘chillR’ makes the method used in this study available for wider use.
Leaf phenology has been shown to be one of the most important indicators of the effects of climate change on biological systems. Few such studies have, however, been published detailing the ...relationship between phenology and climate change in Asian contexts. With the aim of quantifying species’ phenological responsiveness to temperature and deepening understandings of spatial patterns of phenological and climate change in China, this study analyzes the first leaf date (FLD) and the leaf coloring date (LCD) from datasets of four woody plant species, Robinia pseudoacacia, Ulmus pumila, Salix babylonica, and Melia azedarach, collected from 1963 to 2009 at 47 Chinese Phenological Observation Network (CPON) stations spread across China (from 21° to 50° N). The results of this study show that changes in temperatures in the range of 39–43 days preceding the date of FLD of these plants affected annual variations in FLD, while annual variations in temperature in the range of 71–85 days preceding LCD of these plants affected the date of LCD. Average temperature sensitivity of FLD and LCD for these plants was −3.93 to 3.30 days °C⁻¹ and 2.11 to 4.43 days °C⁻¹, respectively. Temperature sensitivity of FLD was found to be stronger at lower latitudes or altitude as well as in more continental climates, while the response of LCD showed no consistent pattern. Within the context of significant warming across China during the study period, FLD was found to have advanced by 5.44 days from 1960 to 2009; over the same period, LCD was found to have been delayed by 4.56 days. These findings indicate that the length of the growing season of the four plant species studied was extended by a total of 10.00 days from 1960 to 2009. They also indicate that phenological response to climate is highly heterogeneous spatially.
Plant phenological events are sensitive indicators of climate change, and their change could markedly affect the structure and function of ecosystems. Previous studies have revealed the ...spatiotemporal variations in the phenological events of woody plants. However, limited studies have focused on the phenophases of herbaceous plants. In this study, by using a meta-analysis method, we extracted information about the phenological changes in herbaceous plants in China’s grasslands from existing studies (including the period, station, species, phenophases, phenological trends, and climatic determinants) and analyzed the patterns manifested in the dataset. The results showed that the spring phenophases (e.g., first leaf date and first flowering date) of the herbaceous plants mainly advanced over the past 30 years, but a large difference existed across grassland types. The spring phenophases of forages (species from the Cyperaceae, Gramineae, and Leguminosae families) became earlier in the desert steppe and alpine steppe but showed no apparent trends in the alpine meadow and even became later in the meadow steppe and typical steppe. In most cases, the increase in spring temperatures and precipitation promoted the greening up of herbaceous plants, while sunshine duration was positively correlated with the green-up date of herbaceous plants. For the autumn phenophases, the proportions of the earlier and later trends were very close, but the trends varied among the grassland types. The leaf coloring dates of the forages were delayed in the meadow steppe and alpine steppe but showed no distinct pattern in the typical steppe or alpine meadow and even became earlier in the desert steppe. In most cases, the increase in growing season temperature led to an earlier leaf coloring date of the herbaceous plants, but the increase in the preseason precipitation delayed the leaf coloring date. Our results suggested that the phenophases of herbaceous plants have complicated responses to multiple environmental factors, which makes predicting future phenological changes difficult.
The climate warming that has occurred over the past decades may benefit plant growth and development because it reduces the severity of frost events. However, these rising temperatures may also lead ...to diminished frost hardiness in plants due to their insufficient hardening. Despite climate warming exerting such dual effects on frost damage, how this might change the frost damage of woody plants remains unknown. Here, we conducted a laboratory experiment that used the relative electrolyte leakage method to derive species-specific model parameters for frost hardiness and a damage model. Then we simulated the daily frost hardiness and damage of five typical temperate tree species (
Ulmus pumila
,
Robinia pseudoacacia
,
Fraxinus chinensis
,
Salix babylonica
, and
Armeniaca vulgaris
), from 1980 to 2015, in Beijing, China. The root mean square error (RMSE) between observed and predicted frost damage ranged from 3.58% to 7.65%. According to our simulation results, frost hardiness has declined over this 36-year period due to insufficient cold hardening of plants in autumn coupled with rapid dehardening in spring; however, the percentage of frost damage incurred by the five species showed a declining trend because of the reduced frequency and intensity of frost events. Thus, decreased frost severity may, to a large extent, offset the negative effects of diminished frost hardiness such that the frost risk faced by temperate forests may well remain constant or decline with continued climate warming.
The peak of growing season (POG) represents the timing of the maximum capacity of vegetation photosynthesis and acts as a crucial phenological indicator for the carbon cycle in terrestrial ...ecosystems. However, little is known about how POG responds to extreme climate events such as drought across different biomes. Based on two drought indices, we analyzed the temporal–spatial pattern of drought and POG in China and then investigated how drought influenced the POG in different periods of the early season through correlation analysis. In general, a trend towards increased aridity and earlier POG was found in most areas. The impact of drought on POG differed among periods. On the one hand, an earlier POG enabled plants to reduce evapotranspiration and mitigate the risk of severe summer drought. On the other hand, the drought that occurred in spring impeded plant growth and caused a delay in spring phenology, thereby postponing POG. Summer drought led to an earlier POG in relatively dry biomes but inversely led to a later peak in photosynthetic activity in wetter biomes. We also observed a 1-month/2-month lagged effect of drought on POG in almost half of the areas and a 2-month/ 3-month cumulative effect of drought in the north of 50° N. These findings enhance our understanding of carbon uptake in terrestrial ecosystems by clarifying the mechanisms by which climate change impacts vegetation growth and photosynthetic activity.
PDF
