Spring Plant Phenology Research Articles

Temperature sum models in plant spring phenology studies: two commonly used methods have different fields of application.

In studies of plant spring phenology, temperature sum models are traditional tools. They are used to quantify plant development in terms of accumulation of temperature-dependent developmental units, such as Growing Degree Hours, GDHs. A key parameter in these models is the threshold (or base) temperature, Tthr, representing the lower thermal limit for the development to occur. The parameter can be either estimated when the model is fitted into the data or fixed a priori. Here we examine the limitations of both methods and identify fields of applications for each of them.

Alpine plants exhibited deep supercooling upon exposed to episodic frost events during the growing season on the Qinghai-Tibet Plateau

Abstract Climatic warming has advanced the spring phenology of plants and disrupted the alignment of phenology with weather patterns. Such misalignments can cause problems as extreme weather events become more frequent and thus impact the survival, growth and reproduction of plants. To prevent freezing within their cells during the growing season, plants adopt a supercooling strategy. However, the weather event severity and seasonal timing may impact the plant’s recovery after a freezing event. We conducted experiments to investigate how extreme freezing events of four different severities impacted the supercooling points and senescence of two dominant alpine plant species, Potentilla saundersiana (mid-summer flowering) and Gentiana parvula (late-summer flowering) on the Qinghai-Tibet Plateau (QTP). We also explored how the phenological stage impacted P. saundersiana’s response to freezing events. We found that both species exhibited supercooling upon exposed to frost damage. However, the average supercooling point for P. saundersiana was −6.9°C and was influenced by minimum temperature, duration and phenological stage. Whereas, the average supercooling point for G. parvula was −4.8°C, and neither minimum temperature nor duration had an effect on the supercooling point. In addition, the minimum temperature treatment of −10°C caused death in both plants when held constant for 4 h. Our study provides the first experimental dataset exploring the supercooling points of alpine plants on the QTP. Given the increasing probability of alpine plants encounters frost events, these results are of great significance for understanding the growth and survival strategies of alpine plants to cope with the adverse effects of extreme climate.

Spatial Variation in Responses of Plant Spring Phenology to Climate Warming in Grasslands of Inner Mongolia: Drivers and Application.

Plant spring phenology in grasslands distributed in the Northern Hemisphere is highly responsive to climate warming. The growth of plants is intricately influenced by not only air temperature but also precipitation and soil factors, both of which exhibit spatial variation. Given the critical impact of the plant growth season on the livelihood of husbandry communities in grasslands, it becomes imperative to comprehend regional-scale spatial variation in the response of plant spring phenology to climate warming and the effects of precipitation and soil factors on such variation. This understanding is beneficial for region-specific phenology predictions in husbandry communities. In this study, we analyzed the spatial pattern of the correlation coefficient between the start date of the plant growth season (SOS) and the average winter-spring air temperature (WST) of Inner Mongolia grassland from 2003 to 2019. Subsequently, we analyzed the importance of 13 precipitation and soil factors for the correlation between SOS and average WST using a random forest model and analyzed the interactive effect of the important factors on the SOS using linear mixing models (LMMs). Based on these, we established SOS models using data from pastoral areas within different types of grassland. The percentage of areas with a negative correlation between SOS and average WST in meadow and typical grasslands was higher than that in desert grasslands. Results from the random forest model highlighted the significance of snow cover days (SCD), soil organic carbon (SOC), and soil nitrogen content (SNC) as influential factors affecting the correlation between SOS and average WST. Meadow grasslands exhibited significantly higher levels of SCD, SOC, and SNC compared to typical and desert grasslands. The LMMs indicated that the interaction of grassland type and the average WST and SCD can effectively explain the variation in SOS. The multiple linear models that incorporated both average WST and SCD proved to be better than models utilizing WST or SCD alone in predicting SOS. These findings indicate that the spatial patterns of precipitation and soil factors are closely associated with the spatial variation in the response of SOS to climate warming in Inner Mongolia grassland. Moreover, the average WST and SCD, when considered jointly, can be used to predict plant spring phenology in husbandry communities.

Spring phenology and pathogen infection affect multigenerational plant attackers throughout the growing season.

Climate change has been shown to advance spring phenology, increase the number of insect generations per year (multivoltinism) and increase pathogen infection levels. However, we lack insights into the effects of plant spring phenology and the biotic environment on the preference and performance of multivoltine herbivores and whether such effects extend into the later part of the growing season. To this aim, we used a multifactorial growth chamber experiment to examine the influence of spring phenology on plant pathogen infection, and how the independent and interactive effects of spring phenology and plant pathogen infection affect the preference and performance of multigenerational attackers (the leaf miner Tischeria ekebladella and the aphid Tuberculatus annulatus) on the pedunculate oak in the early, mid and late parts of the plant growing season. Pathogen infection was highest on late phenology plants, irrespective of whether inoculations were conducted in the early, mid or late season. The leaf miner consistently preferred to oviposit on middle and late phenology plants, as well as healthy plants, during all parts of the growing season, whereas we detected an interactive effect between spring phenology and pathogen infection on the performance of the leaf miner. Aphids preferred healthy, late phenology plants during the early season, healthy plants during the mid season, and middle phenology plants during the late season, whereas aphid performance was consistently higher on healthy plants during all parts of the growing season. Our findings highlight that the impact of spring phenology on pathogen infection and the preference and performance of insect herbivores is not restricted to the early season, but that its imprint is still present - and sometimes equally strong - during the peak and end of the growing season. Plant pathogens generally negatively affected herbivore preference and performance, and modulated the effects of spring phenology. We conclude that spring phenology and pathogen infection are two important factors shaping the preference and performance of multigenerational plant attackers, which is particularly relevant given the current advance in spring phenology, pathogen outbreaks and increase in voltinism with climate change.

Increasing importance of precipitation in spring phenology with decreasing latitudes in subtropical forest area in China

Climate warming has significantly advanced plant spring phenology in temperate and boreal biomes in the northern hemisphere. However, the response of subtropical forest phenology to climate change remains largely unclear. This study aimed to determine the spatiotemporal patterns of spring photosynthetic phenology in subtropical forests in China over the period 2002-2017 and explore its underlying mechanism in response to the changes of different climate variables. We applied four methods to extract the start of the photosynthetic period (SOP) from a solar–induced chlorophyll fluorescence (SIF) data set during the period 2002 to 2017, and determined correlations between SOP and environmental factors using partial correlation analyses. Overall, the SOP was advanced by 6.8 days. Furthermore, we found that the SIF-based SOP is highly correlated with the flux data–based photosynthetic onset dates, demonstrating that SIF can be a useful index in characterizing the photosynthetic phenology in subtropical forests. Interestingly, based on partial correlation analysation temperature dominated the SOP in the northern subtropical forest, but the importance of precipitation increased with decreasing latitudes, and the primary climatic control of SOP in southern monsoon evergreen forests is precipitation. These results suggested that the predicted increase in temperature and shift in precipitation regimes under ongoing climate change might potentially largely affect the photosynthetic phenology, and thus affect the carbon and water cycles in subtropical forests.

Contrasting dynamical responses of sympatric caribou and muskoxen to winter weather and earlier spring green-up in the Arctic

Alteration of local biodiversity by climate change may be especially impactful in the Arctic, where species richness is characteristically low and environmental conditions are changing rapidly. Two species of arctic large herbivores that survived rapid warming during the Pleistocene-Holocene transition, caribou and muskoxen, again face accelerated warming and changes in vegetation seasonality under contemporary climate change. While numerous studies have investigated the roles of weather and primary productivity in population dynamics of these species, opportunities for investigation of their dynamics in sympatric populations have been limited. We analyzed the population dynamics and offspring production of sympatric caribou and muskoxen at a study site in West Greenland over an 18-year period (2002–2019) during which the timing of spring green-up has advanced rapidly. In caribou, population growth rate and calf production were greater following warm winters but lower in years with earlier spring green-up. While calf production was highly variable, caribou abundance declined over the course of the study. In contrast, muskox population growth and calf production both increased following earlier springs. Moreover, muskox abundance increased over the course of the study, despite a negative association between their rate of increase and winter temperature, perhaps indicating that winter weather was less important than spring green-up timing in their dynamics. Hence, sympatric populations of these two herbivores displayed opposing demographic responses to winter weather and spring plant phenology at this shared location. These results emphasize the complexity of predicting large herbivore responses to climate change, and highlight the potential for impacts to species richness of large herbivore communities as the Arctic continues to warm.

Spatial and temporal shifts in photoperiod with climate change.

Climate change causes both temporal (e.g. advancing spring phenology) and geographic (e.g. range expansion poleward) species shifts, which affect the photoperiod experienced at critical developmental stages ('experienced photoperiod'). As photoperiod is a common trigger of seasonal biological responses - affecting woody plant spring phenology in 87% of reviewed studies that manipulated photoperiod - shifts in experienced photoperiod may have important implications for future plant distributions and fitness. However, photoperiod has not been a focus of climate change forecasting to date, especially for early-season ('spring') events, often assumed to be driven by temperature. Synthesizing published studies, we find that impacts on experienced photoperiod from temporal shifts could be orders of magnitude larger than from spatial shifts (1.6h of change for expected temporal vs 1min for latitudinal shifts). Incorporating these effects into forecasts is possible by leveraging existing experimental data; we show that results from growth chamber experiments on woody plants often have data relevant for climate change impacts, and suggest that shifts in experienced photoperiod may increasingly constrain responses to additional warming. Further, combining modeling approaches and empirical work on when, where and how much photoperiod affects phenology could rapidly advance our understanding and predictions of future spatio-temporal shifts from climate change.

Spatiotemporal variations in leaf-out phenology of typical European tree species and their responses to climate change.

Over the past decades, global warming significantly affected the spring phenology of plants. Many studies have reported the temporal and spatial patterns of spring phenological changes in China, but relatively less is known for that in Europe, which is also located in the temperate area of the Northern Hemisphere. To facilitate the regional comparison of phenological change and understand its response to climate change, we used the data of first leaf date (FLD) in Europe (1980-2014) and the corresponding meteorological data to examine the spatiotemporal variations in leaf-out phenology of four typical tree species (Aesculus hippocastanum, Betula pendula, Fagus sylvatica, and Quercus robur), and to identify the major climatic factors driving such variations. The results showed that the FLD of the four species in the study area advanced by 3.3-7.5 d·10 a-1 during 1980-2014. The FLD was delayed at a rate of 2.03-3.19 d per degree of latitude from south to north, of 0.19-0.80 d per degree of longitude from west to East (except for Fagus sylvatica), of 2.25-3.44 d·100 m-1 from low to high elevation. The advances in the FLD were mainly attributed to the increases of temperature in spring and the increases of precipitation in spring and winter. The rise of temperature in autumn and winter would delay FLD.

Satellite-observed decrease in the sensitivity of spring phenology to climate change under high nitrogen deposition

Spring phenology is a sensitive indicator of climate change and has substantial impacts on the carbon cycle. The global N cycle has been greatly disturbed by anthropogenic activities resulting in altered atmospheric N deposition worldwide. Research has been focused on the changes in the spring phenology and its covariations with climatic factors. However, the influences of N deposition on spring phenology have not been well documented to date. Herein, we investigated the effects of N deposition on the start of growing season (SOS) in continental United States (CONUS) during the years 1986–2015 using the normalized difference vegetation index (NDVI) datasets derived from both the third generation NDVI dataset and the Moderate Resolution Imaging Spectroradiometer (MODIS). We observed that N deposition could only explain approximately 5% of temporal variation in SOS in CONUS. However, the sensitivities of SOS in response to unit change in both temperature (ST) and precipitation (SP) showed clear decreasing spatial patterns with increasing N deposition. The ST generally decreased from −6 d/°C in low N deposition regions (<2 kg ha−1) to −4 d/°C in areas with N deposition >4 kg ha−1. Furthermore, the positive SP also showed a continuously decreasing pattern with the increase in N deposition, but the negative SP was gradually weakened when N deposition was >1.0 kg ha−1. The results have important implications as it reveals the role of N deposition on spring plant phenology, and strongly suggest the consideration of N deposition effects when analyzing or predicting spring phenology in response to future climate change.

Spring stomatal response to vapor pressure deficit as a marker for desert truffle fruiting

The cultivation of desert truffle Terfezia claveryi using Helianthemum almeriense as a host plant has recently become a solid alternative crop in the Mediterranean region due to its adaptation to arid and semiarid ecosystems, which are expected to increase during the following years because of climate change. However, management models are still being developed in order to improve and stabilize the production, which varies greatly from one year to another. According to gatherers and farmers, one of the key factors for desert truffle production is the plant phenology in spring, which, in turn, depends on environmental conditions. In this manuscript, we have characterized the physiological, morphological, and molecular responses of the mycorrhizal plants in spring, coinciding with the fructification period of the plant and fungal species. Thanks to this characterization, a sigmoidal relationship between stomatal conductance and vapor pressure deficit (VPD) was found, which can be used as a marker of plant phenological switch. In order to confirm that this phenology status is related to desert truffle fructification, this marker has been successfully correlated to total truffle production. The results of this manuscript suppose a big step forward that will help to develop management models for the desert truffle crop.

Effects of winter chilling vs. spring forcing on the spring phenology of trees in a cold region and a warmer reference region

Regions at high latitudes and high altitudes are undergoing a more pronounced winter warming than spring warming, and such asymmetric warming will affect chilling and forcing processes and thus the spring phenology of plants. We analyzed winter chilling and spring forcing accumulation in relation to the spring phenology of three tree species (Ulmus pumila, Populus simonii, and Syringa oblata) growing in a cold region (CR) compared with trees in a warmer reference region (WR), using the Dynamic Model and the Growing Degree Hour (GDH) model. We tested that forcing rather than chilling affects the spring phenology of trees in CR (hypothesis I), and that trees in CR have both lower mean chilling and forcing temperature and thus longer accumulation periods than trees in WR (hypothesis II). The modeling results confirmed that chilling and forcing occur simultaneously during the early spring when temperature gradually increases. In line with our hypotheses, forcing played a crucial role in spring phenology in CR, but chilling and forcing combined to determine spring phenology in WR. The temperature during the chilling and forcing periods was lower and the accumulation period started earlier and ended later in CR than in WR. Moreover, the chilling accumulation was broken into two periods by the low deep winter temperature in CR, and that interruption will be removed by future strong winter warming. Future asymmetric warming, with a stronger temperature increase in winter than in spring, could decrease the forcing accumulation effects and increase the chilling effects on the spring phenology of plants in CR. This change in the balance between chilling and forcing will lead to a shift in plant phenology, which will further have major impacts on biogeochemical cycles and on ecosystem functions and services.

Warming and precipitation addition interact to affect plant spring phenology in alpine meadows on the central Qinghai-Tibetan Plateau

Temperature and precipitation are primary regulators of plant phenology. However, our knowledge of how these factors might interact to affect plant phenology is incomplete. The Qinghai-Tibetan Plateau, a cold and high region, has experienced no consistent changes in spring phenology, despite a significant warming trend. We conducted a manipulative experiment of warming and precipitation addition in an alpine meadow on the Qinghai-Tibetan Plateau in 2015 (cold and wet), 2016 (warm and dry) and 2017 (mild and very wet). We found that warming increased annual variability of plant spring phenology. Warming delayed green up of all monitored species in 2016, advanced green up of early flowering species in 2015, and did not alter green up in 2017. For example, green up of the shallow rooted Kobresia pygmaea advanced 8 (± 2) days in 2015 and was delayed by 23 (± 3) days in a dry year (2016) under warming compared with control. Early spring precipitation addition can offset the delaying effects of warming in a dry year on the Qinghai-Tibetan Plateau. Under warming plus precipitation addition, community average green up advanced compared to control plots in 2015 and 2016, and community average flowering advanced for all three years. In 2016, flowering of K. pygmaea (an early flowering species) advanced under warming plus precipitation addition compared to control while flowering of other species did not change. Our results highlight that annual variation of soil moisture condition plays a critical role in determining the magnitude and direction of spring phenology response to warming. We provide insights in how plant spring phenology might change in a warmer future in the presence or absence of precipitation increase.

Effects of winter chilling and photoperiod on leaf-out and flowering in a subtropical evergreen broadleaved forest in China

Accurate forecasting of spring plant phenology is critical for understanding structural and functional changes in plant communities and their ecosystems in light of global warming. To date, the relative importance of winter chilling and photoperiod for leaf-out and flowering phenology remains unknown in subtropical and tropical forests. Here, we established a climate chamber experiment to test the effects of photoperiod and chilling on the timing of leaf-out and flowering for 37 subtropical woody species using dormant twigs. We found that most cuttings reached leaf-out, but only a few cuttings reached flowering. Longer chilling (including both moderate and strong chilling treatments) may improve leaf-out success and advance leaf-out timing, but it showed little effect on flowering. Moderate chilling was enough for the initiation of leaf-out. Photoperiod showed little effect on both leaf-out and flowering. To our knowledge, our study is the first to explore how different winter chilling conditions may lead to tree phenology progressing in various subtropical species in a new order and to show that leaf-out order is largely unpredictable when chilling requirements are not met. Our experiment indicates that dormant twigs of subtropical woody species can be successfully applied to leaf-out rather than flowering. Our results suggest that lack of chilling not only led to a considerable delay in leaf-out for subtropical species, but it also caused substantial changes in the order of species leaf-out. Thus, warmer winter temperatures might impact subtropical forest ecosystems more than formerly believed.

Diverging shifts in spring phenology in response to biodiversity loss in a subtropical forest

AbstractQuestionsDespite our increased understanding of how climate change influences plant phenology, it remains poorly understood whether diversity loss could alter phenology as well. Here we investigated the following: (a) do changes in plant diversity affect leaf‐out and flowering dates for woody species; (b) which group of variables are more important in influencing leaf‐out and flowering dates, abiotic variables (soil variables) or biotic variables (plant diversity)?Study siteA subtropical forest in the Biodiversity–Ecosystem Functioning Experiment of China, located in Jiangxi Province, China.MethodsSpecies were planted in various combinations to create plots with varying tree richness: 1, 2, 4, 8, 16 or 24 species. We monitored leaf‐out and flowering dates of eight randomly selected species in 17 plots in 2018. A linear model was used to test whether species diversity was a predictor of leaf‐out/flowering times for each species. We then fit linear mixed‐effects models to assess the combined influence of species diversity, soil Total Carbon and Total Nitrogen on the overall community.ResultsIn the low‐diversity plots, we found two species leafing out earlier, one leafing out later and four showing no significant difference. Leaf‐out date advanced an average of 0.3 days per species lost. Of all the biotic and abiotic predictor variables, Total Nitrogen was the only one significantly correlated with leaf‐out date. No significant correlation was found between species diversity and flowering date for any of the species.ConclusionsOur study provides the first empirical evidence concerning the effects of biodiversity loss on plant spring phenology for woody species. Our findings illustrate that fluctuation in plant diversity could alter the timing of leaf‐out and that abiotic variables may be more important than biotic variables in determining leaf‐out dates in subtropical forest. Overall, declining diversity may exacerbate the phenological changes attributed to rising global temperatures.

Local snow melt and temperature-but not regional sea ice-explain variation in spring phenology in coastal Arctic tundra.

The Arctic is undergoing dramatic environmental change with rapidly rising surface temperatures, accelerating sea ice decline and changing snow regimes, all of which influence tundra plant phenology. Despite these changes, no globally consistent direction of trends in spring phenology has been reported across the Arctic. While spring has advanced at some sites, spring has delayed or not changed at other sites, highlighting substantial unexplained variation. Here, we test the relative importance of local temperatures, local snow melt date and regional spring drop in sea ice extent as controls of variation in spring phenology across different sites and species. Trends in long-term time series of spring leaf-out and flowering (average span: 18years) were highly variable for the 14 tundra species monitored at our four study sites on the Arctic coasts of Alaska, Canada and Greenland, ranging from advances of 10.06days per decade to delays of 1.67days per decade. Spring temperatures and the day of spring drop in sea ice extent advanced at all sites (average 1°C per decade and 21days per decade, respectively), but only those sites with advances in snow melt (average 5days advance per decade) also had advancing phenology. Variation in spring plant phenology was best explained by snow melt date (mean effect: 0.45days advance in phenology per day advance snow melt) and, to a lesser extent, by mean spring temperature (mean effect: 2.39days advance in phenology per °C). In contrast to previous studies examining sea ice and phenology at different spatial scales, regional spring drop in sea ice extent did not predict spring phenology for any species or site in our analysis. Our findings highlight that tundra vegetation responses to global change are more complex than a direct response to warming and emphasize the importance of snow melt as a local driver of tundra spring phenology.

New satellite-based estimates show significant trends in spring phenology and complex sensitivities to temperature and precipitation at northern European latitudes

Recent climate warming has altered plant phenology at northern European latitudes, but conclusions regarding the spatial patterns of phenological change and relationships with climate are still challenging as quantitative estimates are strongly diverging. To generate consistent estimates of broad-scale spatially continuous spring plant phenology at northern European latitudes (> 50° N) from 2000 to 2016, we used a novel vegetation index, the plant phenology index (PPI), derived from MODerate-resolution Imaging Spectroradiometer (MODIS) data. To obtain realistic and strong estimates, the phenology trends and their relationships with temperature and precipitation over the past 17 years were analyzed using a panel data method. We found that in the studied region the start of the growing season (SOS) has on average advanced by 0.30 day year−1. The SOS showed an overall advancement rate of 2.47 day °C−1 to spring warming, and 0.18 day cm−1 to decreasing precipitation in spring. The previous winter and summer temperature had important effects on the SOS but were spatially heterogeneous. Overall, the onset of SOS was delayed 0.66 day °C−1 by winter warming and 0.56 day °C−1 by preceding summer warming. The precipitation in winter and summer influenced the SOS in a relatively weak and complex manner. The findings indicate rapid recent phenological changes driven by combined seasonal climates in northern Europe. Previously unknown spatial patterns of phenological change and relationships with climate drivers are presented that improve our capacity to understand and foresee future climate effects on vegetation.

A long‐term perspective on microclimate and spring plant phenology in the Western Cascades

AbstractPhenology—recurring seasonal events in an organism's life cycle—is largely driven by local climates &lt;1 km2 (microclimates), and changes in phenology are frequently used to indicate a species’ or community response to climate change. Phenological shifts can result in trophic asynchrony, population declines of higher‐level consumers, and reduction of plant fitness. While timing of phenological events is often correlated with elevation, studies have shown that microclimates created by areas of heterogeneous topography can be decoupled from regional climate patterns and that the distribution of microclimates does not always follow the elevation gradient. To examine the interaction between regional weather patterns and microclimate, and the subsequent effect of microclimate on phenology, we conducted standardized weekly spring phenology surveys of 18 native forest plants at the H.J. Andrews Experimental Forest in the Western Cascades from 2009 to 2016. We saw a high degree of inter‐annual variability of microclimate within and across sites, resulting in a changing pattern of microclimate diversity across the landscape from year to year. Most importantly, we saw that years with regional conditions predicted by continued climate change showed a loss of diversity in both microclimate and phenological events, with a more rapid advancement in bud break occurring at higher elevation sites. This study highlights the importance of understanding the interactions between regional and local processes that determine microclimate conditions and how those conditions influence patterns of plant phenology within forest communities, across mountain landscapes and over time, with implications for the capacity of mountainous regions to buffer local communities against the effects of climate change.

Development and analysis of spring plant phenology products: 36 years of 1-km grids over the conterminous US

Time series of phenological products provide information on the timings of recurrent biological events and on their temporal trends. This information is key to studying the impacts of climate change on our planet as well as for managing natural resources and agricultural production. Here we develop and analyze new long term phenological products: 1 km grids of the Extended Spring Indices (SI-x) over the conterminous United States from 1980 to 2015. These new products (based on Daymet daily temperature grids and created by using cloud computing) allow the analysis of two primary variables (first leaf and first bloom) and two derivative products (Damage Index and Last Freeze Day) at a much finer spatial resolution than previous gridded or interpolated products. Furthermore, our products provide enough temporal depth to reliably analyze trends and changes in the timing of spring arrival at continental scales. Validation results confirm that our products largely agree with lilac and honeysuckle leaf and flowering onset observations. The spatial analysis shows a significantly delayed spring onset in the northern US whereas in the western and the Great Lakes region, spring onset advances. The mean temporal variabilities of the indices were analyzed for the nine major climatic regions of the US and results showed a clear division into three main groups: early, average and late spring onset. Finally, the region belonging to each group was mapped. These examples show the potential of our four phenological products to improve understanding of the responses of ecosystems to a changing climate.

Temperature and photoperiod drive spring phenology across all species in a temperate forest community.

Accurate predictions of spring plant phenology with climate change are critical for projections of growing seasons, plant communities and a number of ecosystem services, including carbon storage. Progress towards prediction, however, has been slow because the major cues known to drive phenology - temperature (including winter chilling and spring forcing) and photoperiod - generally covary in nature and may interact, making accurate predictions of plant responses to climate change complex and nonlinear. Alternatively, recent work suggests many species may be dominated by one cue, which would make predictions much simpler. Here, we manipulated all three cues across 28 woody species from two North American forests. All species responded to all cues examined. Chilling exerted a strong effect, especially on budburst (-15.8d), with responses to forcing and photoperiod greatest for leafout (-19.1 and -11.2d, respectively). Interactions between chilling and forcing suggest that each cue may compensate somewhat for the other. Cues varied across species, leading to staggered leafout within each community and supporting the idea that phenology is a critical aspect of species' temporal niches. Our results suggest that predicting the spring phenology of communities will be difficult, as all species we studied could have complex, nonlinear responses to future warming.

New insights on plant phenological response to temperature revealed from long-term widespread observations in China.

Constraints of temperature on spring plant phenology are closely related to plant growth, vegetation dynamics, and ecosystem carbon cycle. However, the effects of temperature on leaf onset, especially for winter chilling, are still not well understood. Using long-term, widespread insitu phenology observations collected over China for multiple plant species, this study analyzes the quantitative response of leaf onset to temperature, and compares empirical findings with existing theories and modeling approaches, as implemented in 18 phenology algorithms. Results show that the growing degree days (GDD) required for leaf onset vary distinctly among plant species and geographical locations as well as at organizational levels (species and community), pointing to diverse adaptation strategies. Chilling durations (CHD) needed for releasing bud dormancy decline monotonously from cold to warm areas with very limited interspecies variations. Results also reveal that winter chilling is a crucial component of phenology models, and its effect is better captured with an index that accounts for the inhomogeneous effectiveness of low temperature to chilling rate than with the conventional CHD index. The impact of spring warming on leaf onset is nonlinear, better represented by a logistical function of temperature than by the linear function currently implemented in biosphere models. The optimized base temperatures for thermal accumulation and the optimal chilling temperatures are species-dependent and average at 6.9 and 0.2°C, respectively. Overall, plants' chilling requirement is not a constant, and more chilling generally results in less requirement of thermal accumulation for leaf onset. Our results clearly demonstrate multiple deficiencies of the parameters (e.g., base temperature) and algorithms (e.g., method for calculating GDD) in conventional phenology models to represent leaf onset. Therefore, this study not only advances our mechanistic and quantitative understanding of temperature controls on leaf onset but also provides critical information for improving existing phenology models.