Changes in autumn senescence in northern hemisphere deciduous trees: a meta-analysis of autumn phenology studies

Background and Aims Many individual studies have shown that the timing of leaf senescence in boreal and temperate deciduous forests in the northern hemisphere is influenced by rising temperatures, but there is limited consensus on the magnitude, direction and spatial extent of this relationship.Methods A meta-analysis was conducted of published studies from the peer-reviewed literature that reported autumn senescence dates for deciduous trees in the northern hemisphere, encompassing 64 publications with observations ranging from 1931 to 2010.Key Results Among the meteorological measurements examined, October temperatures were the strongest predictors of date of senescence, followed by cooling degree-days, latitude, photoperiod and, lastly, total monthly precipitation, although the strength of the relationships differed between high- and low-latitude sites. Autumn leaf senescence has been significantly more delayed at low (25° to 49°N) than high (50° to 70°N) latitudes across the northern hemisphere, with senescence across high-latitude sites more sensitive to the effects of photoperiod and low-latitude sites more sensitive to the effects of temperature. Delays in leaf senescence over time were stronger in North America compared with Europe and Asia.Conclusions The results indicate that leaf senescence has been delayed over time and in response to temperature, although low-latitude sites show significantly stronger delays in senescence over time than high-latitude sites. While temperature alone may be a reasonable predictor of the date of leaf senescence when examining a broad suite of sites, it is important to consider that temperature-induced changes in senescence at high-latitude sites are likely to be constrained by the influence of photoperiod. Ecosystem-level differences in the mechanisms that control the timing of leaf senescence may affect both plant community interactions and ecosystem carbon storage as global temperatures increase over the next century.     

31种木本植物开花物候与系统发育的关系

植物物候通常被认为是由环境因素,如降水、温度和日照长度所决定,然而环境因素是否是物候唯一的决定因素仍然存在很大争议。谱系结构表征了植物在进化上的顺序,该发育时序是否对物候产生影响,当前仍然未知。在调查2016年春季新疆乌鲁木齐市最常见的31种木本植物的初始开花时间、败花时间和开花持续时间的基础上,通过分析植物开花物候的分布特征、开花物候在乔灌木间的差别、以及植物谱系距离与开花物候距离间的关系,试图揭示植物的开花物候和物种谱系(进化)顺序间的关系。结果表明:(1)新疆乌鲁木齐市31种木本植物的初始开花时间为4月18日±9d、败花时间为5月5日±12d、开花持续时间为(16±8)d;(2)乔木的初始开花时间和败花时间的标准差分别均低于灌木,乔木开花物候相对灌木更稳定;(3)乔木的初始开花和败花时间均显著早于灌木(P0.05),但开花持续时间在两者间未有显著性差异(P0.05);(3)31种木本植物间的初始开花时间距离、败花时间距离和开花持续时间距离均与物种谱系距离存在显著线性回归关系(P0.05)。综上可知:乔灌木在垂直空间上的分化使得木本植物的开花物候在植物生活型间存在不同。对植物的开花物候,除已被证明的降水、温度和日照长度等环境因素的影响外,物种进化顺序也可能造成了它在植物种间、时间和空间上的变异。     

西安木本植物物候与气候要素的关系

根据1963–2007年中国物候观测网西安观测站的物候和气温、降水资料,分析了西安站34种木本植物春季展叶始期、展叶盛期、始花期和盛花期等4个关键物候期的变化趋势、对气候变化的阶段响应特点及其与气温、降水变化的关系。结果表明,1963年以来,西安地区气温呈显著上升趋势,特别是1994年前后,气温发生明显突变,上升趋势更加明显;西安春季物候变化主要呈现提前趋势。在45年中,观测到的34种植物的展叶始期平均提前1天,展叶盛期平均提前1.4天,始花期平均提前9天,盛花期平均提前12天;以突变点为界,34个物种1995–2007年的4种物候期比1963–1994年平均提前了4.34±0.77天;春季物候期的早晚主要受春季气温的影响,特别是春季物候期发生当月和上一月的平均气温对物候期的影响最为显著。叶物候和物候发生期前一月的降水量有较为明显的相关关系,花物候期和降水的关系不明显。     

Responses of canopy duration to temperature changes in four temperate tree species: relative contributions of spring and autumn leaf phenology

While changes in spring phenological events due to global warming have been widely documented, changes in autumn phenology, and therefore in growing season length, are less studied and poorly understood. However, it may be helpful to assess the potential lengthening of the growing season under climate warming in order to determine its further impact on forest productivity and C balance. The present study aimed to: (1) characterise the sensitivity of leaf phenological events to temperature, and (2) quantify the relative contributions of leaf unfolding and senescence to the extension of canopy duration with increasing temperature, in four deciduous tree species (Acer pseudoplatanus, Fagus sylvatica, Fraxinus excelsior and Quercus petraea). For 3 consecutive years, we monitored the spring and autumn phenology of 41 populations at elevations ranging from 100 to 1,600 m. Overall, we found significant altitudinal trends in leaf phenology and species-specific differences in temperature sensitivity. With increasing temperature, we recorded an advance in flushing from 1.9 ± 0.3 to 6.6 ± 0.4 days °C⁻¹ (mean ± SD) and a 0 to 5.6 ± 0.6 days °C⁻¹ delay in leaf senescence. Together both changes resulted in a 6.9 ± 1.0 to 13.0 ± 0.7 days °C⁻¹ lengthening of canopy duration depending on species. For three of the four studied species, advances in flushing were the main factor responsible for lengthening canopy duration with increasing temperature, leading to a potentially larger gain in solar radiation than delays in leaf senescence. In contrast, for beech, we found a higher sensitivity to temperature in leaf senescence than in flushing, resulting in an equivalent contribution in solar radiation gain. These results suggest that climate warming will alter the C uptake period and forest productivity by lengthening canopy duration. Moreover, the between-species differences in phenological responses to temperature evidenced here could affect biotic interactions under climate warming.     

The timing of autumn senescence is affected by the timing of spring phenology: implications for predictive models

Autumn senescence regulates multiple aspects of ecosystem function, along with associated feedbacks to the climate system. Despite its importance, current understanding of the drivers of senescence is limited, leading to a large spread in predictions of how the timing of senescence, and thus the length of the growing season, will change under future climate conditions. The most commonly held paradigm is that temperature and photoperiod are the primary controls, which suggests a future extension of the autumnal growing season as global temperatures rise. Here, using two decades of ground‐ and satellite‐based observations of temperate deciduous forest phenology, we show that the timing of autumn senescence is correlated with the timing of spring budburst across the entire eastern United States. On a year‐to‐year basis, an earlier/later spring was associated with an earlier/later autumn senescence, both for individual species and at a regional scale. We use the observed relationship to develop a novel model of autumn phenology. In contrast to current phenology models, this model predicts that the potential response of autumn phenology to future climate change is strongly limited by the impact of climate change on spring phenology. Current models of autumn phenology therefore may overpredict future increases in the length of the growing season, with subsequent impacts for modeling future CO₂ uptake and evapotranspiration.     

Alteration of the phenology of leaf senescence and fall in winter deciduous species by climate change: effects on nutrient proficiency

Leaf senescence in winter deciduous species signals the transition from the active to the dormant stage. The purpose of leaf senescence is the recovery of nutrients before the leaves fall. Photoperiod and temperature are the main cues controlling leaf senescence in winter deciduous species, with water stress imposing an additional influence. Photoperiod exerts a strict control on leaf senescence at latitudes where winters are severe and temperature gains importance in the regulation as winters become less severe. On average, climatic warming will delay and drought will advance leaf senescence, but at varying degrees depending on the species. Warming and drought thus have opposite effects on the phenology of leaf senescence, and the impact of climate change will therefore depend on the relative importance of each factor in specific regions. Warming is not expected to have a strong impact on nutrient proficiency although a slower speed of leaf senescence induced by warming could facilitate a more efficient nutrient resorption. Nutrient resorption is less efficient when the leaves senesce prematurely as a consequence of water stress. The overall effects of climate change on nutrient resorption will depend on the contrasting effects of warming and drought. Changes in nutrient resorption and proficiency will impact production in the following year, at least in early spring, because the construction of new foliage relies almost exclusively on nutrients resorbed from foliage during the preceding leaf fall. Changes in the phenology of leaf senescence will thus impact carbon uptake, but also ecosystem nutrient cycling, especially if the changes are consequence of water stress.     

Temperature,precipitation, and insolation effects on autumn vegetation phenology in temperate China

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

From observations to experiments in phenology research: investigating climate change impacts on trees and shrubs using dormant twigs

Background and Aims Climate change is advancing the leaf-out times of many plant species and mostly extending the growing season in temperate ecosystems. Laboratory experiments using twig cuttings from woody plant species present an affordable, easily replicated approach to investigate the relative importance of factors such as winter chilling, photoperiod, spring warming and frost tolerance on the leafing-out times of plant communities. This Viewpoint article demonstrates how the results of these experiments deepen our understanding beyond what is possible via analyses of remote sensing and field observation data, and can be used to improve climate change forecasts of shifts in phenology, ecosystem processes and ecological interactions.Scope The twig method involves cutting dormant twigs from trees, shrubs and vines on a single date or at intervals over the course of the winter and early spring, placing them in containers of water in controlled environments, and regularly recording leaf-out, flowering or other phenomena. Prior to or following leaf-out or flowering, twigs may be assigned to treatment groups for experiments involving temperature, photoperiod, frost, humidity and more. Recent studies using these methods have shown that winter chilling requirements and spring warming strongly affect leaf-out and flowering times of temperate trees and shrubs, whereas photoperiod requirements are less important than previously thought for most species. Invasive plant species have weaker winter chilling requirements than native species in temperate ecosystems, and species that leaf-out early in the season have greater frost tolerance than later leafing species.Conclusions This methodology could be extended to investigate additional drivers of leaf-out phenology, leaf senescence in the autumn, and other phenomena, and could be a useful tool for education and outreach. Additional ecosystems, such as boreal, southern hemisphere and sub-tropical forests, could also be investigated using dormant twigs to determine the drivers of leaf-out times and how these ecosystems will be affected by climate change.     

Increased heat requirement for leaf flushing in temperate woody species over 1980–2012: effects of chilling,precipitation and insolation

Recent studies have revealed large unexplained variation in heat requirement‐based phenology models, resulting in large uncertainty when predicting ecosystem carbon and water balance responses to climate variability. Improving our understanding of the heat requirement for spring phenology is thus urgently needed. In this study, we estimated the species‐specific heat requirement for leaf flushing of 13 temperate woody species using long‐term phenological observations from Europe and North America. The species were defined as early and late flushing species according to the mean date of leaf flushing across all sites. Partial correlation analyses were applied to determine the temporal correlations between heat requirement and chilling accumulation, precipitation and insolation sum during dormancy. We found that the heat requirement for leaf flushing increased by almost 50% over the study period 1980–2012, with an average of 30 heat units per decade. This temporal increase in heat requirement was observed in all species, but was much larger for late than for early flushing species. Consistent with previous studies, we found that the heat requirement negatively correlates with chilling accumulation. Interestingly, after removing the variation induced by chilling accumulation, a predominantly positive partial correlation exists between heat requirement and precipitation sum, and a predominantly negative correlation between heat requirement and insolation sum. This suggests that besides the well‐known effect of chilling, the heat requirement for leaf flushing is also influenced by precipitation and insolation sum during dormancy. However, we hypothesize that the observed precipitation and insolation effects might be artefacts attributable to the inappropriate use of air temperature in the heat requirement quantification. Rather than air temperature, meristem temperature is probably the prominent driver of the leaf flushing process, but these data are not available. Further experimental research is thus needed to verify whether insolation and precipitation sums directly affect the heat requirement for leaf flushing.     

Herbarium specimens show patterns of fruiting phenology in native and invasive plant species across New England

Premise of the Study

Patterns of fruiting phenology in temperate ecosystems are poorly understood, despite the ecological importance of fruiting for animal nutrition and seed dispersal. Herbarium specimens represent an under‐utilized resource for investigating geographical and climatic factors affecting fruiting times within species, patterns in fruiting times among species, and differences between native and non‐native invasive species.

Methods

We examined over 15,000 herbarium specimens, collected and housed across New England, and found 3159 specimens with ripe fruits, collected from 1849–2013. We examined patterns in fruiting phenology among 37 native and 18 invasive woody plant species common to New England. We compared fruiting dates between native and invasive species, and analyzed how fruiting phenology varies with temperature, space, and time.

Key Results

Spring temperature and year explained a small but significant amount of the variation in fruiting dates. Accounting for the moderate phylogenetic signal in fruiting phenology, invasive species fruited 26 days later on average than native species, with significantly greater standard deviations.

Conclusions

Herbarium specimens can be used to detect patterns in fruiting times among species. However, the amount of intraspecific variation in fruiting times explained by temporal, geographic, and climatic predictors is small, due to a combination of low temporal resolution of fruiting specimens and the protracted nature of fruiting. Later fruiting times in invasive species, combined with delays in autumn bird migrations in New England, may increase the likelihood that migratory birds will consume and disperse invasive seeds in New England later into the year.     

Intercomparison, interpretation, and assessment of spring phenology in North America estimated from remote sensing for 1982–2006

Shifts in the timing of spring phenology are a central feature of global change research. Long‐term observations of plant phenology have been used to track vegetation responses to climate variability but are often limited to particular species and locations and may not represent synoptic patterns. Satellite remote sensing is instead used for continental to global monitoring. Although numerous methods exist to extract phenological timing, in particular start‐of‐spring (SOS), from time series of reflectance data, a comprehensive intercomparison and interpretation of SOS methods has not been conducted. Here, we assess 10 SOS methods for North America between 1982 and 2006. The techniques include consistent inputs from the 8 km Global Inventory Modeling and Mapping Studies Advanced Very High Resolution Radiometer NDVIg dataset, independent data for snow cover, soil thaw, lake ice dynamics, spring streamflow timing, over 16 000 individual measurements of ground‐based phenology, and two temperature‐driven models of spring phenology. Compared with an ensemble of the 10 SOS methods, we found that individual methods differed in average day‐of‐year estimates by ±60 days and in standard deviation by ±20 days. The ability of the satellite methods to retrieve SOS estimates was highest in northern latitudes and lowest in arid, tropical, and Mediterranean ecoregions. The ordinal rank of SOS methods varied geographically, as did the relationships between SOS estimates and the cryospheric/hydrologic metrics. Compared with ground observations, SOS estimates were more related to the first leaf and first flowers expanding phenological stages. We found no evidence for time trends in spring arrival from ground‐ or model‐based data; using an ensemble estimate from two methods that were more closely related to ground observations than other methods, SOS trends could be detected for only 12% of North America and were divided between trends towards both earlier and later spring.     

Interannual variation in reproductive phenology in a riverine fish assemblage: implications for predicting the effects of climate change and altered flow regimes

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Habitat-specific responses in the flowering phenology and seed set of alpine plants to climate variation: implications for global-change impacts

The timing of the snowmelt is a crucial factor in determining the phenological schedule of alpine plants. A long-term monitoring of snowmelt regimes in a Japanese alpine area revealed that the onset of the snowmelt season has been accelerated during the last 17 years in early snowmelt sites but that such a trend has not been detected in late snowmelt sites. This indicates that the global warming effect on the snowmelt pattern may be site-specific. The flowering phenology of fellfield plants in an exposed wind-blown habitat was consistent between an unusually warm year (1998) and a normal year (2001). In contrast, the flowering occurrence of snowbed plants varied greatly between the years depending on the snowmelt time. There was a large number of flowering species in the fellfield community from mid- to late to late June and from mid- to late July. The flowering peak of an early-melt snowbed plant community was in the middle of the flowering season and that of a late-melt snowbed community was in the early flowering season. These habitat-specific phenological patterns were consistent between 1998 and 2001. The effects of the variation in flowering timing on seed-set success were evaluated for an entomophilous snowbed herb, Peucedanum multivittatum, along the snowmelt gradient during a 5-year period. When flowering occurred prior to early August, mean temperature during the flowering season positively influenced the seed set. When flowering occurred later than early August, however, the plants enjoyed high seed-set success irrespective of temperature conditions if frost damage was absent. These observations are probably explained based on the availability of pollinators, which depends not only on ambient temperature but also on seasonal progress. These results suggest that the effects of climate change on biological interaction may vary depending on the specific habitat in the alpine ecosystem in which diverse snowmelt patterns create complicated seasonality for plants within a very localized area.     

Predicting spatial and temporal patterns of bud‐burst and spring frost risk in north‐west Europe: the implications of local adaptation to climate

The timing of spring bud‐burst and leaf development in temperate, boreal and Arctic trees and shrubs fluctuates from year to year, depending on meteorological conditions. Over several generations, the sensitivity of bud‐burst to meteorological conditions is subject to selection pressure. The timing of spring bud‐burst is considered to be under opposing evolutionary pressures; earlier bud‐burst increases the available growing season (capacity adaptation) but later bud‐burst decreases the risk of frost damage to actively growing parts (survival adaptation). The optimum trade‐off between these two forms of adaptation may be considered an evolutionarily stable strategy that maximizes the long‐term ecological fitness of a phenotype under a given climate. Rapid changes in climate, as predicted for this century, are likely to exceed the rate at which trees and shrubs can adapt through evolution or migration. Therefore the response of spring phenology will depend not only on future climatic conditions but also on the limits imposed by adaptation to current and historical climate. Using a dataset of bud‐burst dates from twenty‐nine sites in Finland for downy birch (Betula pubescens Ehrh.), we parameterize a simple thermal time bud‐burst model in which the critical temperature threshold for bud‐burst is a function of recent historical climatic conditions and reflects a trade‐off between capacity and survival adaptation. We validate this approach with independent data from eight independent sites outside Finland, and use the parameterized model to predict the response of bud‐burst to future climate scenarios in north‐west Europe. Current strategies for budburst are predicted to be suboptimal for future climates, with bud‐burst generally occurring earlier than the optimal strategy. Nevertheless, exposure to frost risk is predicted to decrease slightly and the growing season is predicted to increase considerably across most of the region. However, in high‐altitude maritime regions exposure to frost risk following bud‐burst is predicted to increase.     

Phenological change in a spring ephemeral: implications for pollination and plant reproduction

Climate change has had numerous ecological effects, including species range shifts and altered phenology. Altering flowering phenology often affects plant reproduction, but the mechanisms behind these changes are not well‐understood. To investigate why altering flowering phenology affects plant reproduction, we manipulated flowering phenology of the spring herb Claytonia lanceolata (Portulacaceae) using two methods: in 2011–2013 by altering snow pack (snow‐removal vs. control treatments), and in 2013 by inducing flowering in a greenhouse before placing plants in experimental outdoor arrays (early, control, and late treatments). We measured flowering phenology, pollinator visitation, plant reproduction (fruit and seed set), and pollen limitation. Flowering occurred approx. 10 days earlier in snow‐removal than control plots during all years of snow manipulation. Pollinator visitation patterns and strength of pollen limitation varied with snow treatments, and among years. Plants in the snow removal treatment were more likely to experience frost damage, and frost‐damaged plants suffered low reproduction despite lack of pollen limitation. Plants in the snow removal treatment that escaped frost damage had higher pollinator visitation rates and reproduction than controls. The results of the array experiment supported the results of the snow manipulations. Plants in the early and late treatments suffered very low reproduction due either to severe frost damage (early treatment) or low pollinator visitation (late treatment) relative to control plants. Thus, plants face tradeoffs with advanced flowering time. While early‐flowering plants can reap the benefits of enhanced pollination services, they do so at the cost of increased susceptibility to frost damage that can overwhelm any benefit of flowering early. In contrast, delayed flowering results in dramatic reductions in plant reproduction through reduced pollination. Our results suggest that climate change may constrain the success of early‐flowering plants not through plant‐pollinator mismatch but through the direct impacts of extreme environmental conditions.     

Genetic variation in productivity of foundation riparian species at the edge of their distribution: implications for restoration and assisted migration in a warming climate

We examined the hypothesis that genotypic variation among populations of commonly co‐occurring phreatophytic trees (Populus fremontii, Salix gooddingii) and the shrub (Salix exigua) regulates aboveground net primary productivity (ANPP) at a hot site at the edge of the species’ distribution. We used a provenance trial in which replicated genotypes from populations varying in mean annual temperature were transplanted to a common garden adjacent to the Lower Colorado River in southeastern California. The garden environment represented an extreme maximum temperature for the study species. Four major findings emerged: (1) Genotypic variation in ANPP was significant for all species with broad‐sense heritability (H²) across populations of 0.11, 0.13, and 0.10 for P. fremontii, S. gooddingii, and S. exigua, respectively, and within‐population H² ranging from 0.00 to 0.25, 0.00 to 0.44, and 0.02 to 0.21, respectively. (2) Population ANPP decreased linearly as mean annual maximum temperature (MAMT) transfer distance increased for both P. fremontii (r² = 0.64) and S. gooddingii (r² = 0.37), whereas it did not change for S. exigua; (3) Populations with similar MAMT to that of the common garden were 1.5 and 1.2 times more productive than populations with 5.0 °C MAMT transfer distances for P. fremontii and S. gooddingii, respectively; and (4) Variation in regression slopes among species for the relationship between ANPP and MAMT indicate species‐specific responses to temperature. As these plant species characterize a threatened habitat type and support a diverse community that includes endangered species, ecosystem restoration programs should consider using both local genotypes and productive genotypes from warmer environments to maximize productivity of riparian ecosystems in the face of global climate change.     

The carbon fertilization effect over a century of anthropogenic CO2 emissions: higher intracellular CO2 and more drought resistance among invasive and native grass species contrasts with increased water use efficiency for woody plants in the US Southwest

From 1890 to 2015, anthropogenic carbon dioxide emissions have increased atmospheric CO₂ concentrations from 270 to 400 mol mol^?1. The effect of increased carbon emissions on plant growth and reproduction has been the subject of study of free‐air CO₂ enrichment (FACE) experiments. These experiments have found (i) an increase in internal CO₂ partial pressure (c_i) alongside acclimation of photosynthetic capacity, (ii) variable decreases in stomatal conductance, and (iii) that increases in yield do not increase commensurate with CO₂ concentrations. Our data set, which includes a 115‐year‐long selection of grasses collected in New Mexico since 1892, is consistent with an increased c_i as a response to historical CO₂ increase in the atmosphere, with invasive species showing the largest increase. Comparison with Palmer Drought Sensitivity Index (PDSI) for New Mexico indicates a moderate correlation with Δ¹³C (r² = 0.32, P < 0.01) before 1950, with no correlation (r² = 0.00, P = 0.91) after 1950. These results indicate that increased c_i may have conferred some drought resistance to these grasses through increased availability of CO₂ in the event of reduced stomatal conductance in response to short‐term water shortage. Comparison with C₃ trees from arid environments (Pinus longaeva and Pinus edulis in the US Southwest) as well as from wetter environments (Bromus and Poa grasses in New Mexico) suggests differing responses based on environment; arid environments in New Mexico see increased intrinsic water use efficiency (WUE) in response to historic elevated CO₂ while wetter environments see increased c_i. This study suggests that (i) the observed increases in c_i in FACE experiments are consistent with historical CO₂ increases and (ii) the CO₂ increase influences plant sensitivity to water shortage, through either increased WUE or c_i in arid and wet environments, respectively.