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Spring predictability explains different leaf-out strategies in the woody floras of North America, Europe and East Asia
Abstract
Intuitively, interannual spring temperature variability (STV) should influence the leaf-out strategies of temperate zone woody species, with high winter chilling requirements in species from regions where spring warming varies greatly among years. We tested this hypothesis using experiments in 215 species and leaf-out monitoring in 1585 species from East Asia (EA), Europe (EU) and North America (NA). The results reveal that species from regions with high STV indeed have higher winter chilling requirements, and, when grown under the same conditions, leaf out later than related species from regions with lower STV. Since 1900, STV has been consistently higher in NA than in EU and EA, and under experimentally short winter conditions NA species required 84% more spring warming for bud break, EU ones 49% and EA ones only 1%. These previously unknown continental-scale differences in phenological strategies underscore the need for considering regional climate histories in global change models.
Supplementary resource (1)
... The delayed recovery of photosynthetic capacity and CO 2 assimilation in spring is also an adaptation mechanism of plants to escape the damage from potential frost events (Vitasse et al., 2014;Liu et al., 2018). In climates with low spring temperatures and with high spring temperature variability, and consequently a high probability of late frost events, plants tend to leaf-out late (specifically for deciduous trees forest) and at the same time deploy higher leaf freezing resistance (Zohner et al., 2017). This results in a later recovery of photosynthetic activity compared with regions with mild temperature variability (Zohner et al., 2017(Zohner et al., , 2020. ...
... In climates with low spring temperatures and with high spring temperature variability, and consequently a high probability of late frost events, plants tend to leaf-out late (specifically for deciduous trees forest) and at the same time deploy higher leaf freezing resistance (Zohner et al., 2017). This results in a later recovery of photosynthetic activity compared with regions with mild temperature variability (Zohner et al., 2017(Zohner et al., , 2020. For instance, Zohner et al. (2020) found Northern America to harbour in general tree species with a more cautious leaf-out strategy compared with Europe and East Asia, which is mainly due to the plants being exposed to higher interannual spring temperature variability there (Zohner et al., 2017). ...
... This results in a later recovery of photosynthetic activity compared with regions with mild temperature variability (Zohner et al., 2017(Zohner et al., , 2020. For instance, Zohner et al. (2020) found Northern America to harbour in general tree species with a more cautious leaf-out strategy compared with Europe and East Asia, which is mainly due to the plants being exposed to higher interannual spring temperature variability there (Zohner et al., 2017). This phenomenon is also consistent with our comparison between modelled and observed GPP (Figs 2, S3): most North American sites exhibit a distinct GPP overestimation in the spring, while the GPP overestimation is not evident for many sites in Europe, especially the sites located in regions with a maritime climate in western Europe. ...
Land carbon dynamics in temperate and boreal ecosystems are sensitive to environmental change. Accurately simulating gross primary productivity (GPP) and its seasonality is key for reliable carbon cycle projections. However, significant biases have been found in early spring GPP simulations of northern forests, where observations often suggest a later resumption of photosynthetic activity than predicted by models. Here, we used eddy covariance-based GPP estimates from 39 forest sites that differ by their climate and dominant plant functional types. We used a mechanistic and an empirical light use efficiency (LUE) model to investigate the magnitude and environmental controls of delayed springtime photosynthesis resumption (DSPR) across sites. We found DSPR reduced ecosystem LUE by 30-70% at many, but not all site-years during spring. A significant depression of LUE was found not only in coniferous but also at deciduous forests and was related to combined high radiation and low minimum temperatures. By embedding cold-acclimation effects on LUE that considers the delayed effects of minimum temperatures, initial model bias in simulated springtime GPP was effectively resolved. This provides an approach to improve GPP estimates by considering physiological acclimation and enables more reliable simulations of photosynthesis in northern forests and projections in a warming climate.
... Lechowicz (1984) introduced the idea of phylogenetic constraints on xylem anatomy and freezing tolerance as a potential driver of spring foliar phenology, indicating evolutionary history may influence the phenological strategies of co-occurring species. A similar mechanism was suggested by Zohner and Renner (2017) that invokes the role of historical climatic variability in the timing of spring budbreak, which varies across continents and may drive phenological differences between co-occurring native and invasive species (Zohner et al., 2017). On the other hand, phenological differences between native and invasive species are often stronger in autumn than in spring (Fridley, 2012;Gallinat et al., 2015), and there are few explanations for delayed invader leaf senescence Yin et al., 2015). ...
... Lechowicz (1984) introduced the idea of phylogenetic constraints on xylem anatomy and freezing tolerance as a potential driver of spring foliar phenology, indicating evolutionary history may influence the phenological strategies of co-occurring species. A similar mechanism was suggested by Zohner and Renner (2017) that invokes the role of historical climatic variability in the timing of spring budbreak, which varies across continents and may drive phenological differences between co-occurring native and invasive species (Zohner et al., 2017). On the other hand, phenological differences between native and invasive species are often stronger in autumn than in spring (Fridley, 2012;Gallinat et al., 2015), and there are few explanations for delayed invader leaf senescence Yin et al., 2015). ...
... Although we did not detect trait-based evidence for strong growthsurvival trade-offs within native species, the absence of any native species expressing both fast growth and a long growing season as a result of high leaf investment begs explanation. One possibility is that the environmental history of North America has selected against deciduous lineages of long leaf duration as a result of unpredictable spring and autumn climate compared to much of Eurasia (Zohner & Renner, 2017), a hypothesis borne out in greater chilling requirements for budbreak in North American species (Zohner et al., 2017). Many Eurasian temperate forests also experience longer growing seasons as a result of maritime influences such as the Gulf Stream (Palter, 2015) that may predispose Eurasian lineages to extended leaf display. ...
Successful control and prevention of biological invasions depend on identifying traits of non‐native species that promote fitness advantages in competition with native species. Here, we show that, among 76 native and non‐native woody plants of deciduous forests of North America, invaders express a unique functional syndrome that combines high metabolic rate with robust leaves of longer lifespan and a greater duration of annual carbon gain, behaviours enabled by seasonally plastic xylem structure and rapid production of thin roots. This trait combination was absent in all native species examined and suggests the success of forest invaders is driven by a novel resource‐use strategy. Furthermore, two traits alone—annual leaf duration and nuclear DNA content—separated native and invasive species with 93% accuracy, supporting the use of functional traits in invader risk assessments. A trait syndrome reflecting both fast growth capacity and understorey persistence may be a key driver of forest invasions. We show that non‐native, invasive woody plants of North American deciduous forests express a unique functional syndrome combining traits associated with both high growth potential and high shade tolerance. This syndrome was absent in all native species examined and involves an integrated growth strategy reflecting leaf, stem and root traits.
... These findings are an important step towards explaining the spatial variability in S T , but only a limited fraction of such variability was explained. Meanwhile, exposure to chilling days, spring frost, interannual spring temperature variability, and photoperiod could regulate plant spring phenological response to temperature and thus may play a role in the spatial variations in S T , but evidence is limited to a few regional studies (Basler and Körner, 2012;Flynn and Wolkovich, 2018;Fu et al., 2014;Körner and Basler, 2010;Wang et al., 2014;Zohner et al., 2017). ...
... The spring phenology of plants reflects a trade-off between avoidance of frost damage (survival) and early leaf-out for carbon gain (Bennie et al., 2010;Tang et al., 2016). Plants living in unstable, fluctuating, or harsh temperature conditions may adopt a conservative phenological strategy to avoid unfavorable temperature environments and be relatively insensitive to a temperature increase in spring Zohner et al., 2017). In contrast, plants in mild temperature conditions may face less risk of frost damage and take greater advantage of a warmer spring, demonstrating a less conservative phenological strategy . ...
... Some factors have also been proposed to explain spatial variations in S T in a few regional studies, including exposure to chilling in dormant period (Fu et al., 2014), spring frost risk , interannual spring temperature variability (Zohner et al., 2017) and daylength (Basler and Körner, 2012;Flynn and Wolkovich, 2018;Körner and Basler, 2010). We thus examined whether the spatial relationship between S T and temperature seasonality was contributed by those factors using the same method for MAT or mean VGD. ...
The temperature sensitivity (ST) of the vegetation greenup onset date (VGD) is critical for the assessment and prediction of phenological response to climate warming. Spatial variations in ST, though well documented based on satellite observations in recent studies, have remained largely under-explained. We determined VGD from satellite observation of the normalized difference vegetation index over the period 2000–2018 and showed that ST is substantially smaller in areas with stronger temperature seasonality (i.e. the multiyear mean of standard deviations of monthly mean temperature over a 12-month period). Spatially, ST averaged over each 2 °C bin of temperature seasonality increased from about −10.0 days K⁻¹ in areas with temperature seasonality of about 3.5 °C to about −3.3 to −2.3 days K⁻¹ in areas with temperature seasonality between 15.0 and 22.3 °C. Statistical analyses suggest that this pattern was not related with spatial variations in the length of chilling exposure, spring frost risk, inter-annual variability of spring temperature, or photoperiod. Rather, it may occur because areas with stronger temperature seasonality have stronger pre-VGD constraints because of a lower temperature and a faster temperature increase from the onset of greenup to summer, which could result in faster leaf development rates and thus higher speeds of completion of leaf development. Our results also show that the greater ST associated with higher mean annual temperature and multiyear mean VGD across the northern middle and high latitudes observed in previous studies is probably caused by temperature seasonality. This study deepens our understanding of the spatial variation in the temperature sensitivity of vegetation spring leafing phenology in the Northern Hemisphere.
... on species and location, leaf emergence has advanced by 3-8 days for every degree increase in air temperature (Cook et al., 2012;Menzel & Fabian, 1999;Zohner & Renner, 2014). However, a growing body of evidence suggests that this past trend cannot be used to predict future responses because other environmental factors may constrain the future advances in spring phenology (Laube et al., 2014;Polgar, Gallinat, & Primack, 2014;Zohner, Benito, Fridley, Svenning, & Renner, 2017;Zohner, Benito, Svenning, & Renner, 2016). Apart from spring temperature, most trees rely on additional factors, including winter chilling and day length, that are likely to become limiting in the future (Laube et al., 2014;Polgar et al., 2014;Zohner et al., 2016Zohner et al., , 2017). ...
... However, a growing body of evidence suggests that this past trend cannot be used to predict future responses because other environmental factors may constrain the future advances in spring phenology (Laube et al., 2014;Polgar, Gallinat, & Primack, 2014;Zohner, Benito, Fridley, Svenning, & Renner, 2017;Zohner, Benito, Svenning, & Renner, 2016). Apart from spring temperature, most trees rely on additional factors, including winter chilling and day length, that are likely to become limiting in the future (Laube et al., 2014;Polgar et al., 2014;Zohner et al., 2016Zohner et al., , 2017). Yet, a lack of information about the existence, or relative importance of these drivers, translates to high uncertainty in model predictions of future forest phenology (Basler, 2016). ...
... Three main factors-autumn temperatures (Fu et al., 2014;Heide, 2003), winter chilling (Laube et al., 2014;Luedeling, Girvetz, Semenov, & Brown, 2011;Yu, Luedeling, & Xu, 2010;Zohner et al., 2017), and day length (Heide, 1993a(Heide, , 1993bKörner & Basler, 2010)-have been proposed to control spring leaf-out by modulating the amount of warming that trees require to leaf-out. These factors serve trees as a safety mechanism to prevent precocious leaf-out in case of an early warm spell when the risk of nightly freezing is still high (Körner & Basler, 2010;Zohner, Mo, Sebald, & Renner, 2020). ...
Climate warming is currently advancing spring leaf‐out of temperate and boreal trees, enhancing net primary productivity (NPP) of forests. However, it remains unclear whether this trend will continue, preventing for accurate projections of ecosystem functioning and climate feedbacks. Several ecophysiological mechanisms have been proposed to regulate the timing of leaf emergence in response to changing environmental cues, but the relative importance of those mechanisms remains unclear. Here, we use 727,401 direct phenological observations of common European forest trees to examine the dominant controls on leaf‐out. Using the emerging mechanisms, we forecast future trajectories of spring arrival and evaluate the consequences for forest carbon dynamics. By representing hypothesized relationships with autumn temperature, winter chilling, and the timing of spring onset, we accurately predicted reductions in the advance of leaf‐out. There was a strong consensus between our empirical model and existing process‐based models, revealing that the advance in leaf‐out will not exceed 2 weeks over the rest of the century. We further estimate that, under a ‘business‐as‐usual’ climate scenario, earlier spring arrival will enhance NPP of temperate and boreal forests by ~0.2 Gt per year at the end of the century. In contrast, previous estimates based on a simple degree‐day model range around 0.8 Gt. As such, the expected NPP is drastically reduced in our updated model relative to previous estimates—by a total of ~25 Gt over the rest of the century. These findings reveal important environmental constraints on the productivity of broad‐leaved deciduous trees and highlight that shifting spring phenology is unlikely to slow the rate of warming by offsetting anthropogenic carbon emissions.
... There is growing evidence that suggests interannual spring temperature variability (STV) influences regional strategies in phenology (40). Species from areas with high STV have higher chilling requirements to ward against inappropriate leafing and subsequent frost damage (40). ...
... There is growing evidence that suggests interannual spring temperature variability (STV) influences regional strategies in phenology (40). Species from areas with high STV have higher chilling requirements to ward against inappropriate leafing and subsequent frost damage (40). In addition, research suggests that regions with warmer, earlier springs house species with greater extent of photoperiodic control (29). ...
... Geographical Range Predicts Response to Warming. Across geographic gradients, some studies of leafing phenology have focused on ecotypic variation within species (37,(66)(67)(68)(69), while others compared species with different climatic ranges (29,40,70,71). Results of the role of geography provide conflicting or incomplete stories. ...
Changes in plant phenology associated with climate change have been observed globally. What is poorly known is whether and how phenological responses to climate warming will differ from year to year, season to season, habitat to habitat, or species to species. Here, we present 5 y of phenological responses to experimental warming for 10 subboreal tree species. Research took place in the open-air B4WarmED experiment in Minnesota. The design is a two habitat (understory and open) × three warming treatments (ambient, +1.7 °C, +3.4 °C) factorial at two sites. Phenology was measured twice weekly during the growing seasons of 2009 through 2013. We found significant interannual variation in the effect of warming and differences among species in response to warming that relate to geographic origin and plant functional group. Moreover, responses to experimental temperature variation were similar to responses to natural temperature variation. Warming advanced the date of budburst more in early compared to late springs, suggesting that to simulate interannual variability in climate sensitivity of phenology, models should employ process-based or continuous development approaches. Differences among species in timing of budburst were also greater in early compared to late springs. Our results suggest that climate change—which will make most springs relatively “early”—could lead to a future with more variable phenology among years and among species, with consequences including greater risk of inappropriately early leafing and altered interactions among species.
... using the gbif function of the R-package dismo (Hijmans et al., 2011). Filtering scripts were applied to exclude unreliable records and reduce spatial clustering using the following three criteria (see Zohner et al., 2016Zohner et al., , 2017: For each species, we removed (1) records from continents where the species is not native, (2) coordinate duplicates at a resolution of 2.5 arc min, and (3) records based on fossil material, germplasm (cultivated plants), or literature. After applying the filtering scripts, we were left with a total of 479,488 occurrence records (on average 3175 occurrence records per species, minimally 30 occurrence records per species [threshold used by Zohner et al., 2016Zohner et al., , 2017). ...
... Filtering scripts were applied to exclude unreliable records and reduce spatial clustering using the following three criteria (see Zohner et al., 2016Zohner et al., , 2017: For each species, we removed (1) records from continents where the species is not native, (2) coordinate duplicates at a resolution of 2.5 arc min, and (3) records based on fossil material, germplasm (cultivated plants), or literature. After applying the filtering scripts, we were left with a total of 479,488 occurrence records (on average 3175 occurrence records per species, minimally 30 occurrence records per species [threshold used by Zohner et al., 2016Zohner et al., , 2017). Occurrences were then queried against a grid file (2.5 arc min spatial resolution) for MAT from the Worldclim version 2.0 data set (Hijmans et al., 2011;Fick and Hijmans, 2017). ...
... Number of leaf primordia in buds, leaf teeth, thickness, MAT, and venation refer to species values (i) in Appendix S1, α refers to the intercept, β refers to the estimated slopes of the respective variable, habit refers to the random intercept effect of whether a species has a shrub-or tree-like growth, and family refers to the family-level Non craspedodromous random intercept effect inserted in the binary leaf venation and leaf teeth submodels (Eqs. 1 and 2). In contrast to previous studies (Zohner et al., 2016(Zohner et al., , 2017, we did not insert a genus-level random effect because this prevented model convergence; the subpopulations of the model became too small (each genus, on average, included only two species). The variables leaf primordium number, leaf teeth, and leaf thickness were log-transformed to obtain normally distributed vectors. ...
Premise
The proportion of woody dicots with toothed leaves increases toward colder regions, a relationship used to reconstruct past mean annual temperatures. Recent hypotheses explaining this relationship are that (1) leaves in colder regions are thinner, requiring thick veins for support and water supply, with the resulting craspedodromous venation leading to marginal teeth (support–supply hypothesis) or that (2) teeth are associated with the packing of leaf primordia in winter buds (bud‐packing hypothesis).
Methods
We addressed these hypotheses by examining leaf thickness, number of primordia in buds, growing season length (mean annual temperature, MAT), and other traits in 151 deciduous woody species using georeferenced occurrences and a Bayesian model controlling for phylogeny. We excluded evergreen species because longer leaf life spans correlate with higher leaf mass per area, precluding the detection of independent effects of leaf thickness on leaf‐margin type.
Results
The best model predicted toothed leaves with 94% accuracy, with growing season length the strongest predictor. Neither leaf thickness nor number of leaves preformed in buds significantly influenced margin type, rejecting the support–supply and bud‐packing hypotheses.
Conclusions
A direct selective benefit of leaf teeth via a carbon gain early in the spring as proposed by Royer and Wilf (2006) would match the strong correlation between toothed species occurrence and short growing season found here using Bayesian hierarchical models. Efforts should be directed to physiological work quantifying seasonal photosynthate production in toothed and nontoothed leaves.
... Similarly, it has been proposed that plants in locales with intermittent snow cover or early spring snow melt benefit from requirements for long photoperiods or late flowering even in fully inductive conditions to avoid frost damage, as snow cover insulates low-growing plants (Kinmonth-Schultz et al., 2021;Lewandowska-Sabat et al., 2017;Montesinos-Navarro et al., 2011;Suter et al., 2014;Wang et al., 2014). Neither relationship has been comprehensively tested at the microclimate level, although work at the continental scale supports this hypothesis (Zohner et al., 2017). ...
... Hence, populations may rely less on photoperiodic cues for flowering, and instead opportunistically exploit high temperatures for maximized growth and reproduction. Our findings differ from the later leaf-out strategies that occurred in woody species from northern-hemisphere continents with greater variation in spring temperatures (Zohner et al., 2017). However, that study considered continental-scale standard deviation over 100 years in the mean minimum temperature from March to May, thus they could not parse when spring temperatures began to increase nor microclimate differences. ...
Conservative flowering behaviours, such as flowering during long days in summer or late flowering at a high leaf number, are often proposed to protect against variable winter and spring temperatures which lead to frost damage if premature flowering occurs. Yet, due the many factors in natural environments relative to the number of individuals compared, assessing which climate characteristics drive these flowering traits has been difficult. We applied a multidisciplinary approach to 10 winter-annual Arabidopsis thaliana populations from a wide climactic gradient in Norway. We used a variable reduction strategy to assess which of 100 climate descriptors from their home sites correlated most to their flowering behaviours when tested for responsiveness to photoperiod after saturation of vernalization; then, assessed sequence variation of 19 known environmental-response flowering genes. Photoperiod responsiveness inversely correlated with interannual variation in timing of growing season onset. Time to flowering appeared driven by growing season length, curtailed by cold fall temperatures. The distribution of FLM, TFL2 and HOS1 haplotypes, genes involved in ambient temperature response, correlated with growing-season climate. We show that long-day responsiveness and late flowering may be driven not by risk of spring frosts, but by growing season temperature and length, perhaps to opportunistically maximize growth.
... Hence, photoperiodic sensitive species are likely to be more constraint in their adaptation to rising spring temperatures compared to photoperiodic insensitive species in order to benefit from a longer favorable window for their development. However, the photoperiodic sensitivity of species is difficult to quantify and seems to be more prevalent for species growing in ecosystems with shorter winters (Zohner et al., 2016(Zohner et al., , 2017Geng et al., 2022) 2). Consequently, further warming, could result in contrasting effects within and between ecosystems depending on species specific chilling, forcing and photoperiod requirements and the ability to compensate deficient drivers, which might also change the susceptibility of late-spring frost damages in a given ecosystem. ...
... Regions with a distinct transition from cool winter to warm summer might favor species that readily react to forcing temperatures whereas regions with high temperature fluctuation during the winter spring transition (from year to year but also within the season) might favor species that rely on additional cues such as chilling temperatures and/or photoperiod (Zohner et al., 2017;Geng et al., 2022). Consistently, North American trees seem to have a higher chilling and forcing requirement than Central European and East Asian species, matching the long-term risk of damaging frosts in these regions (Zohner et al., 2020). ...
Winter chilling, spring forcing temperature and photoperiod are the most important drivers explaining the spatial and temporal variability of spring phenology in temperate trees. However, how these factors interact with each other on dormancy release and spring budburst date remains unclear and varies greatly depending on species. Our knowledge is also limited as to whether heat accumulation of forcing temperatures that trigger bud break in spring is a linear or non-linear process. Here, we aimed at experimentally quantifying the effect of chilling, forcing, photoperiod and their interactions on the budburst dates of nine different temperate tree species from East Asia (near Beijing, China) and Central Europe (near Zurich, Switzerland), including six phylogenetically related species (same genus). We conducted a full factorial experiment in climate chambers using two chilling (low and high, i.e., 0 vs. 56 days at 2°C after sampling at the end of December), four forcing (5, 10, 15, and 20°C), and two photoperiod (8 vs. 16 h) treatments simultaneously in Beijing and Zurich. We found that species growing near Beijing responded more readily to forcing conditions than species of the same genus growing near Zurich regardless of chilling treatment. Budburst timing of most species but European beech was marginally, if at all, affected by photoperiod. Furthermore, our results suggest that linear heat accumulation, as commonly used with the growing degree hours (GDH) model, could result in accurate prediction of budburst date depending on the temperature threshold used as a basis for heat accumulation. Our results also demonstrate the important role of chilling in shaping the sensitivity and rate of forcing accumulation to trigger budburst and suggest that species-specific sigmoid relationship for accumulating heat that accounts for prior chilling exposure may yield better predictions of budburst dates. Our results suggest that deciduous trees may have adapted their chilling and forcing requirements in regards to the predictability of winter-spring transition and late spring frosts. A less predictable winter-spring transition, as observed in Central Europe, could have driven species evolution towards higher chilling and forcing requirements compared to species growing in a more predictable climate of Northeastern Asia. Our cross-continental experiment therefore suggests that the spring phenology of East Asian species is tighter coupled to spring forcing temperature than Central European forests.
... The main trigger for tree leaf-out is thought to be the accumulation of warm air temperatures (forcing), but tree phenology also responds to photoperiod and chilling (Basler & Korner, 2014;Laube et al., 2014;Zohner et al., 2016Zohner et al., , 2017Zohner & Renner, 2015), while spring-flowering herbs respond largely to soil temperature and snow depth (Jánosi et al., 2020;Pardee et al., 2019). However, the relationship between air temperatures, soil temperature, and snow depth is not straightforward because higher air temperatures are linked to decreased snow depth, and snow acts to insulate soil from temperature oscillations during winter. ...
... As for trees, their response to warming temperatures is mediated by interactions with chilling and photoperiod (Basler & Korner, 2014;Laube et al., 2014;Zohner et al., 2016;Zohner & Renner, 2015). In particular, the shorter day lengths in late winter may prevent leafing out in response to warmer temperatures, and this photoperiodic constraint may be particularly acute at high latitudes (Flynn & Wolkovich, 2018;Fu et al., 2012Fu et al., , 2015Fu et al., , 2019Zohner et al., 2017;Zohner & Renner, 2014. ...
The phenologies of co‐occurring trees and spring‐blooming understory herbs in northeastern North American hardwood forests appear to be regulated by different environmental drivers – air temperature and soil temperature/snowpack, respectively. Accordingly, it has been hypothesized that climate change–driven asymmetry in the advancement of canopy leaf‐out relative to the timing of understory growth could reduce photosynthetic rates and reproductive success of understory herbs through greater early‐season shading.
To determine whether trees and spring‐flowering forest herbs are advancing their phenologies at different rates with respect to increasing global temperatures, we examined the phenological responses to warming of 10 species of trees and 11 species of spring‐flowering forest herbs (8045 observations from 965 sites) in northeastern North America using 13 years of data collected by citizen scientists under the auspices of the USA‐National Phenology Network.
Contrary to expectation, the degree of advancement of leaf‐out as a function of temperature was greater in spring‐flowering forest herbs than in trees, with a mean response rate of −4.9 days/°C (95% BCI [−5.2, −4.6]) for spring‐flowering forest herbs vs. −3.3 days/°C (95% BCI [−3.5, −3.1]) for trees. However, the response to temperature was not consistent across the latitudinal range, with spring‐flowering forest herbs responding more strongly to warming than trees at middle (40–44°N) and higher (45–48°N) latitudes but not at lower latitudes (35–39°N).
Synthesis . In contrast to previous suggestions, our study shows spring‐flowering forest herbs advancing their phenology at a higher rate than trees with respect to warming through most of the latitudinal range investigated, which could translate into a longer growing season and increased carbon uptake for spring‐flowering forest herbs as spring temperatures rise.
... In recent times, shifting phenology is considered to be one of the pronounced responses of vegetation to global climate change (Zohner et al. 2017;Liu and Zhang 2020). The ongoing climate warming is causing either a significant advancement in spring flowering phenology in temperate ecosystems or a significant delay in summer flowering phenology of many plant species, thereby altering their key ecological processes and biotic interactions (Chuine and Beaubien 2001;Elzinga et al. 2007;Cleland et al. 2012;Fridley 2012;Iler et al. 2021;Rosbakh et al. 2021). ...
... Generally, the phenological response in a particular region depends upon the regional climate and is expected to be species-specific (Gillooly et al. 2001), as the sensitivity to seasonal warming differs amongst species (Fitter and Fitter 2002;Sherry et al. 2007;Zohner et al. 2017Zohner et al. , 2016Laube et al. 2014a, b). The closely related species show different phenological responses to climate warming, with certain species responding much faster than the others (Miller-Rushing and Inouye 2009). ...
Experimental evidences in support of climate warming–driven phenological shifts are still scarce, particularly from the developing world. Here, we investigated the effect of experimental warming on flowering phenology of selected woody plants in Kashmir Himalaya. We selected the twigs of four congeneric pairs of temperate woody species (Prunus, Populus, Ulmus, Viburnum)—typical spring-flowering plants in the region. Using randomised block design, we monitored these winter dormant twigs in controlled growth chambers to study the effect of different temperature regimes (9, 17, 20 and 23 °C) and species identity on the patterns of phenological shifts. We observed a significant phenological shift in all the species showing preponement in the first flower out and senescence phases ranging from 0.56 to 3.0 and 0.77 to 4.04 days per degree increase in temperature, respectively. The duration of flowering phase in all the species showed a corresponding decrease along the gradient of increasing temperature, which was more driven by preponement of the flower senescence than the start of flower- ing. The patterns of phenological shifts were highly species-specific, and the magnitude of these shifts significantly varied in all the four pairs of congeneric species despite their phylogenetic similarity. Our study provides experimental support to the previous long-term observation and herbarium-based studies showing that the patterns of phenological shifts in response to global climate warming are likely to vary between species, even those belonging to same evolutionary stock. Our findings highlight that a one-size-fits-all strategy to manage the likely impacts of climate warming–induced phenological shifts will seldom succeed, and should instead be designed for the specific phenological responses of species and regions.
... Regional variation in climate change concerns patterns in, for example, overall warming, precipitation and the seasonal distribution of change 6 . Thus, changes in phenology can be expected to track local changes in the timing of abiotic or climatically driven events, within the constraints set by the utilization of and sensitivity to cues of the regional species assemblage [18][19][20] . Such local and regional variation in drivers 19,21,22 and sensitivity towards them 18,20 can be reflected in spatiotemporal variation in phenological shifts 4,8,15,23,24 . ...
... Thus, changes in phenology can be expected to track local changes in the timing of abiotic or climatically driven events, within the constraints set by the utilization of and sensitivity to cues of the regional species assemblage [18][19][20] . Such local and regional variation in drivers 19,21,22 and sensitivity towards them 18,20 can be reflected in spatiotemporal variation in phenological shifts 4,8,15,23,24 . Although the few studies analysing geographically (and/or joint responses to unmeasured variables)? ...
... The sensitivity of trees and shrubs to LSFs is determined by the freezing resistance of their young leaves and their phenological strategy, that is, how soon after the first spring warming they leaf-out. Species with "cautious" phenological strategies that do not leaf-out unless they have experienced sufficient winter chilling and/or day lengths, regardless of short warm spells in spring, should be favored in areas with frequent severe LSFs (29,30). By contrast, "opportunistic" species that leaf-out early, even after short periods of warming, should be common in areas where phenological tracking of spring temperature carries no risk because LSFs are unlikely (31). ...
... To maximize growing-season length and minimize late-frost damage, plants exhibit locally adapted leaf-out strategies that may also reflect the geographic variation in LSFs. Flora-wide differences in leaf-out strategies were first found in common garden experiments that included up to 1,585 species of temperate and boreal trees, shrubs, and climbers from Asia, Europe, and North America (29,30). That experimental work, however, did not focus on late-frost damage and resistance strategies to late frost. ...
Late-spring frosts (LSFs) affect the performance of plants and animals across the world’s temperate and boreal zones, but despite their ecological and economic impact on agriculture and forestry, the geographic distribution and evolutionary impact of these frost events are poorly understood. Here, we analyze LSFs between 1959 and 2017 and the resistance strategies of Northern Hemisphere woody species to infer trees’ adaptations for minimizing frost damage to their leaves and to forecast forest vulnerability under the ongoing changes in frost frequencies. Trait values on leaf-out and leaf-freezing resistance come from up to 1,500 temperate and boreal woody species cultivated in common gardens. We find that areas in which LSFs are common, such as eastern North America, harbor tree species with cautious (late-leafing) leaf-out strategies. Areas in which LSFs used to be unlikely, such as broad-leaved forests and shrublands in Europe and Asia, instead harbor opportunistic tree species (quickly reacting to warming air temperatures). LSFs in the latter regions are currently increasing, and given species’ innate resistance strategies, we estimate that ∼35% of the European and ∼26% of the Asian temperate forest area, but only ∼10% of the North American, will experience increasing late-frost damage in the future. Our findings reveal region-specific changes in the spring-frost risk that can inform decision-making in land management, forestry, agriculture, and insurance policy.
... Regional variation in climate change concerns patterns in, for example, overall warming, precipitation and the seasonal distribution of change 6 . Thus, changes in phenology can be expected to track local changes in the timing of abiotic or climatically driven events, within the constraints set by the utilization of and sensitivity to cues of the regional species assemblage [18][19][20] . Such local and regional variation in drivers 19,21,22 and sensitivity towards them 18,20 can be reflected in spatiotemporal variation in phenological shifts 4,8,15,23,24 . ...
... Thus, changes in phenology can be expected to track local changes in the timing of abiotic or climatically driven events, within the constraints set by the utilization of and sensitivity to cues of the regional species assemblage [18][19][20] . Such local and regional variation in drivers 19,21,22 and sensitivity towards them 18,20 can be reflected in spatiotemporal variation in phenological shifts 4,8,15,23,24 . Although the few studies analysing geographically (and/or joint responses to unmeasured variables)? ...
... Regional variation in climate change concerns patterns in, for example, overall warming, precipitation and the seasonal distribution of change 6 . Thus, changes in phenology can be expected to track local changes in the timing of abiotic or climatically driven events, within the constraints set by the utilization of and sensitivity to cues of the regional species assemblage [18][19][20] . Such local and regional variation in drivers 19,21,22 and sensitivity towards them 18,20 can be reflected in spatiotemporal variation in phenological shifts 4,8,15,23,24 . ...
... Thus, changes in phenology can be expected to track local changes in the timing of abiotic or climatically driven events, within the constraints set by the utilization of and sensitivity to cues of the regional species assemblage [18][19][20] . Such local and regional variation in drivers 19,21,22 and sensitivity towards them 18,20 can be reflected in spatiotemporal variation in phenological shifts 4,8,15,23,24 . Although the few studies analysing geographically (and/or joint responses to unmeasured variables)? ...
Ongoing climate change can shift organism phenology in ways that vary depending on species, habitats and climate factors studied. To probe for large-scale patterns in associated phenological change, we use 70,709 observations from six decades of systematic monitoring across the former Union of Soviet Socialist Republics. Among 110 phenological events related to plants, birds, insects, amphibians and fungi, we find a mosaic of change, defying simple predictions of earlier springs, later autumns and stronger changes at higher latitudes and elevations. Site mean temperature emerged as a strong predictor of local phenology, but the magnitude and direction of change varied with trophic level and the relative timing of an event. Beyond temperature-associated variation, we uncover high variation among both sites and years, with some sites being characterized by disproportionately long seasons and others by short ones. Our findings emphasize concerns regarding ecosystem integrity and highlight the difficulty of predicting climate change outcomes. The authors use systematic monitoring across the former USSR to investigate phenological changes across taxa. The long-term mean temperature of a site emerged as a strong predictor of phenological change, with further imprints of trophic level, event timing, site, year and biotic interactions.
... For 28 woody species from two North American forests, additional chilling at 4°C for 30 days can advance bud break by 15.8 days (Flynn and Wolkovich 2018). The chilling requirement is especially pronounced in species from northeastern North America, characterized by high interannual spring temperature variability (Zohner et al. 2017). This chillingdriven safety mechanism can avoid early bud development during unfavorable late-winter conditions, thus reducing the risk of frost damage. ...
... Like other phenological events, bud break is based on the perception of photoperiodic and thermal cues (Cooke et al. 2012). In North America where spring temperature varies greatly among years, most woody species require higher winter chilling for bud break (Zohner et al. 2017). These species with high chilling requirement are unable to react to spring warming when experiencing short or mild winters (Laube et al. 2014;Zohner and Renner 2015). ...
Assisted migration, the human-mediated movement of species and populations, is one adaptive strategy to climate change. Plant phenology affects the survival and distribution of species to local conditions, and its potential modifications need to be explored in the context of assisted migration. We conducted identical experiments in January and April (experiment I and II) and monitored the timing of bud break in sugar maple ( Acer saccharum Marshall) under cooling and longer photoperiod to simulate a northward migration. The budbreak in experiment II started 55 days earlier than experiment I. In experiment I, longer photoperiod was more effective than warming in advancing bud break. Compared to experiment II, cooling and long photoperiod had stronger effect in experiment I . Our results demonstrated the significant effect of chilling and confirmed that photoperiod outweighs temperature in initiating bud break when the chilling requirement is unfulfilled. These findings suggest that the future mild winters in the southern range of sugar maple may reduce chilling accumulation and result in the delayed bud break. Sugar maples migrating northward could benefit from longer day lengths, which could partly counteract the delayed effects of colder springs in northern regions, thus ensuring a sufficient growth period.
... The sensitivity of trees and shrubs to LSFs is determined by the freezing resistance of their young leaves and their phenological strategy, that is, how soon after the first spring warming they leaf-out. Species with "cautious" phenological strategies that do not leaf-out unless they have experienced sufficient winter chilling and/or day lengths, regardless of short warm spells in spring, should be favored in areas with frequent severe LSFs (29,30). By contrast, "opportunistic" species that leaf-out early, even after short periods of warming, should be common in areas where phenological tracking of spring temperature carries no risk because LSFs are unlikely (31). ...
... To maximize growing-season length and minimize late-frost damage, plants exhibit locally adapted leaf-out strategies that may also reflect the geographic variation in LSFs. Flora-wide differences in leaf-out strategies were first found in common garden experiments that included up to 1,585 species of temperate and boreal trees, shrubs, and climbers from Asia, Europe, and North America (29,30). That experimental work, however, did not focus on late-frost damage and resistance strategies to late frost. ...
Late-spring frosts (LSFs) affect the performance of plants and animals across the world’s temperate and boreal zones, but despite their ecological and economic impact on agriculture and forestry, the geographic distribution and evolutionary impact of these frost events are poorly understood. Here, we analyze LSFs between 1959 and 2017 and the resistance strategies of Northern Hemisphere woody species to infer trees’ adaptations for minimizing frost damage to their leaves and to forecast forest vulnerability under the ongoing changes in frost frequencies. Trait values on leaf-out and leaf-freezing resistance come from up to 1,500 temperate and boreal woody species cultivated in common gardens. We find that areas in which LSFs are common, such as eastern North America, harbor tree species with cautious (late-leafing) leaf-out strategies. Areas in which LSFs used to be unlikely, such as broad-leaved forests and shrublands in Europe and Asia, instead harbor opportunistic tree species (quickly reacting to warming air temperatures). LSFs in the latter regions are currently increasing, and given species’ innate resistance strategies, we estimate that ∼35% of the European and ∼26% of the Asian temperate forest area, but only ∼10% of the North American, will experience increasing late-frost damage in the future. Our findings reveal region-specific changes in the spring-frost risk that can inform decision-making in land management, forestry, agriculture, and insurance policy.
– https://www.dora.lib4ri.ch/wsl/islandora/object/wsl:23373
– https://doi.org/10.1073/pnas.1920816117
... The sensitivity of trees and shrubs to LSFs is determined by the freezing resistance of their young leaves and their phenological strategy, that is, how soon after the first spring warming they leaf-out. Species with "cautious" phenological strategies that do not leaf-out unless they have experienced sufficient winter chilling and/or day lengths, regardless of short warm spells in spring, should be favored in areas with frequent severe LSFs (29,30). By contrast, "opportunistic" species that leaf-out early, even after short periods of warming, should be common in areas where phenological tracking of spring temperature carries no risk because LSFs are unlikely (31). ...
... To maximize growing-season length and minimize late-frost damage, plants exhibit locally adapted leaf-out strategies that may also reflect the geographic variation in LSFs. Flora-wide differences in leaf-out strategies were first found in common garden experiments that included up to 1,585 species of temperate and boreal trees, shrubs, and climbers from Asia, Europe, and North America (29,30). That experimental work, however, did not focus on late-frost damage and resistance strategies to late frost. ...
Late-spring frosts (LSFs) affect the performance of plants and animals across the world's temperate and boreal zones, but despite their ecological and economic impact on agriculture and forestry, the geographic distribution and evolutionary impact of these frost events are poorly understood. Here, we analyze LSFs between 1959 and 2017 and the resistance strategies of Northern Hemisphere woody species to infer trees' adaptations for minimizing frost damage to their leaves and to forecast forest vulnerability under the ongoing changes in frost frequencies. Trait values on leaf-out and leaf-freezing resistance come from up to 1,500 temperate and boreal woody species cultivated in common gardens. We find that areas in which LSFs are common, such as eastern North America, harbor tree species with cautious (late-leafing) leaf-out strategies. Areas in which LSFs used to be unlikely, such as broad-leaved forests and shrublands in Europe and Asia, instead harbor opportunistic tree species (quickly reacting to warming air temperatures). LSFs in the latter regions are currently increasing, and given species' innate resistance strategies, we estimate that ∼35% of the European and ∼26% of the Asian temperate forest area, but only ∼10% of the North American, will experience increasing late-frost damage in the future. Our findings reveal region-specific changes in the spring-frost risk that can inform decision-making in land management, forestry, agriculture, and insurance policy.
... Trees use a combination of day length and temperature (often measured as growing degree days) as cues to time their leaf expansion. Different tree species have a different sensitivity to these cues and differ in the exact conditions they require to expand their leaves (Lechowicz 1984, Vitasse & Basler 2013, Morin et al. 2010, Gerst et al. 2017, Zohner et al. 2017). Leaf-out timing therefore differs between species and the order in which trees expand their leaves in spring remains relatively constant over the years (Wesolowski & Rowinski 2006). ...
... Since the selection pressures driving leaf expansion phenology in trees seem fairly simple and strong, we would expect relatively low intraspecific variation in this trait (Zohner et al. 2017). However, in addition to the interspecific differences in the timing of leaf expansion, intraspecific differences occur as well (Wesolowski & Rowinski 2006, Cole & Sheldon 2017, Lechowicz 1984. ...
... Under conditions with shorter winters, vegetation needs more heat to germinate. The proportion of heat demand was the highest in North America and the lowest in East Asia (Zohner et al., 2017). Therefore, in a warmer climate, rising temperatures may lead to a significant advance in the SOS in Asia. ...
... Under conditions with shorter winters, vegetation needs more heat to germinate. The proportion of heat demand was the highest in North America and the lowest in East Asia (Zohner et al., 2017). Therefore, in a warmer climate, rising temperatures may lead to a significant advance in the SOS in Asia. ...
Global climate change has led to significant changes in land surface phenology. At present, research on the factors influencing the start of the growing season (SOS) mainly focuses on single factor effects, such as temperature and precipitation, ignoring the combined action of multiple factors. The impact of multiple factors on the spatial and temporal patterns of the SOS in the Northern Hemisphere is not clear, and it is necessary to combine multiple factors to quantify the degrees of influence of different factors on the SOS. Based on the GIMMS3g NDVI dataset, CRU climate data and other factor data, we used geographic detector model, random forest regression model, multiple linear regression, partial correlation analysis and Sen + Mann-Kendall trend analysis to explore the variation of the SOS in the Northern Hemisphere to reveal the main driving factors and impact threshold of 17 influencing factors on the SOS. The results showed that (1) during the past 34 years (1982-2015), the SOS in Europe and Asia mainly showed an advancing trend, whereas the SOS in North America mainly showed a delaying trend. (2) The SOS was mainly controlled by frost frequency, temperature and humidity. Increasing frost frequency inhibited the advancement of the SOS, and increasing temperature and humidity promoted the advancement of the SOS. (3) There were thresholds for the influences of the driving factors on the SOS. Outside the threshold ranges, the response mechanism of the SOS to driving factors changed. The results are important for understanding the response of the SOS to global climate change.
... The determination of the GUD is a trade-off between the growth strategies of reducing growing risks and increasing resource utilization during the growing season [51,52]. Plants growing under unstable spring temperature conditions will adopt a conservative phenological strategy to reduce their risk from climate change or natural disasters [53,54]. Higher daytime temperatures could also exacerbate drought effects [55]. ...
The rise in global average surface temperature has promoted the advancement of spring vegetation phenology. However, the response of spring vegetation phenology to different temperature parameters varies. The Mongolian Plateau, one of the largest grasslands in the world, has green-up dates (GUDs) with unclear sensitivity to different temperature parameters. To address this issue, we investigated the responses of GUDs to different temperature parameters in the Mongolian Plateau grasslands. The results show that GUDs responded significantly differently to changes in near-surface temperature (TMP), near-surface temperature maximum (TMX), near-surface temperature minimum (TMN), and diurnal temperature range (DTR). GUDs advanced as TMP, TMX, and TMN increased, with TMN having a more significant effect, whereas increases in DTR inhibited the advancement of GUDs. GUDs were more sensitive to TMX and TMN than to TMP. The sensitivity of GUDs to DTR showed an increasing trend from 1982 to 2015 and showed this parameter’s great importance to GUDs. Our results also show that the spatial and temporal distributions of temperature sensitivity are only related to temperature conditions in climatic zones instead of whether they are arid.
... Indeed, climate indices describing acute climatic events that are biologically meaningful for tree growth are difficult to compute for several reasons. First, while evidence of frost injuries associated with late spring frosts have been reported, the timing of cold dehardening and the temperature thresholds leading to tree damage remains unclear (e.g., 0 • C, Zohner et al., 2020a; −2 • C, Vitasse et al., 2019; −4 • C, Moreau et al., 2020a,b, herein), and varies intra-and inter-specifically (Zohner et al., 2017(Zohner et al., , 2020a, which complicates the identification of such events. Moreover, few studies investigated the tree physiological processes associated with frost events in situ (Mayr et al., 2020), as most were conducted in laboratory (e.g., Zhu et al., 2001;Mayr et al., 2003). ...
Boreal forests are experiencing severe climatic changes that vary widely across the broad geographic distribution of the biome. The changes are greatest near the subarctic treeline where trees often exhibit high climatic sensitivity because climatic conditions approach the limits of their physiological tolerance. Despite the importance of subarctic boreal forests, the lack of field-acquired growth data remains a critical issue that limits the generalization of forest productivity models across the entire boreal biome. Using tree-ring chronologies from remote stands distributed along three latitudinal gradients ranging from 65 to 102°W, we investigated recent trends in black spruce growth and their relationships with recent climate warming near the subarctic treeline in eastern Canada. Our results show a generally positive effect of temperature and a negative effect of precipitation, both indicating that black spruce growth is temperature-limited near its northern range limit. However, we observed a strong gradient in temperature-growth coupling within a small latitudinal gradient (about one degree of latitude), where strong temperature constraints appear limited to the northernmost, coldest stands. Moreover, the positive growth response to temperature decreased from wetter to dryer sites and climate-growth coupling declined over the study period in the driest sites. These results suggest that the growth increase associated with warmer temperature may be limited by reduced precipitation and potential moisture limitation. Lastly, our results suggest that acute climatic events have the potential to induce abrupt shifts in tree climate-growth relationships. Such results indicate that the expected beneficial effect of warming on high latitude tree growth may be less generalized and more complex than previously thought in northeastern Canada, perhaps due to factors other than temperature, which might confound the climate-growth coupling southwards. Thus, our results highlight the need for a better understanding of additional growth drivers in these poorly studied regions and for physiologically informed definitions of acute climatic events, in order to refine broad-scale forest productivity modeling.
... In temperate ecosystems, plant phenological events are found to be sensitive to environmental factors such as photoperiod, temperature, and winter chilling [15]. For example, temperature and day length together affect tree leafing pattern [16], spring temperature (forcing temperature) and late frost affect rate of bud burst [15] and spring temperature variability affects the phenological patterns of the plant [17]. Thus, changes in environmental factors are critical in determining the response of tree phenological events such as the onset, peak, and end of the phenological events as well as their durations [18]. ...
Phenology, an important ecological attribute, deals with the development of vegetative and reproductive parts of trees called "phenophases", which are important determinants of primary productivity and sensitive to climate change. The present study recorded various phenophases of major tree species (i.e., Quercus leucotrichophora, Rhododendron arboreum, and Myrica esculenta) as per the two-digit numerical system of Biologische Bundesanstalt, Bundessortenamt, Chemische Industrie (BBCH) scale. A total of 72 individual trees, twenty-four from each species, distributed between 1400 and 1980 m. a.s.l elevations were tagged and measured fortnightly for two consecutive years (2019-2021) in the moist temperate forest of Western Himalaya and compared with earlier existing records. Various phenophases were correlated with climatic factors along with duration and thermal time for each phenological growth stage. We found 24 growth stages for Q. leucotrichophora and M. esculenta and 28 for R. arboreum distributed across seven principal growth stages (e.g. bud development, 0; leaf development, 1; shoot development, 3; inflorescence development, 5; flower development, 6; fruit development, 7; and fruit maturation, 8) of trees as per BBCH scale. Maximum growing degree was 748.87 and 627.95 days recorded for R. arboreum and M. esculenta during leaf development, and 796.17 days for Q. leucotrichophora during fruit development. Flower emergence was observed pre, during, and post-emergence of new leaves for R. arboreum, M. esculenta, and Q. leucotrichophora, respectively, which varied at spatial scale with previous findings. Longevity of fruit development to ripening took 17, 4, and 2 months, respectively in Q. leucotrichophora, R. arboreum and M. esculenta. Duration of leaf initiation and flowering was positively correlated with climatic variables, whereas, the reverse was observed for fruiting in the studied tree species. The study concludes that the variations in phenophases of the three species were strongly influenced by climatic variations, especially minimum temperature. The result of the present study would be important in enabling us to formulate efficient forest management strategies by understanding the short-term adaptation of the climate-sensitive important tree species in the western Himalaya.
... The general consistency between our findings suggests that phenology data from herbarium collections are good indicators of patterns in natural systems 29-31 , a point supported by a recent study of phenological sensitivity derived from herbaria and from observed citizen science data 32 . These herbarium-based results provide evidence that phenological sensitivity differs across the temperate forest biome (but see ref. 33 for evidence of differences in response to warming and chilling accumulation). To our knowledge, our study is the first to contrast overstory and understory phenology across multiple continents and, therefore, to find differences in phenological sensitivity between trees and forest wildflowers across continents. ...
Temperate understory plant species are at risk from climate change and anthropogenic threats that include increased deer herbivory, habitat loss, pollinator declines and mismatch, and nutrient pollution. Recent work suggests that spring ephemeral wildflowers may be at additional risk due to phenological mismatch with deciduous canopy trees. The study of this dynamic, commonly referred to as “phenological escape”, and its sensitivity to spring temperature is limited to eastern North America. Here, we use herbarium specimens to show that phenological sensitivity to spring temperature is remarkably conserved for understory wildflowers across North America, Europe, and Asia, but that canopy trees in North America are significantly more sensitive to spring temperature compared to in Asia and Europe. We predict that advancing tree phenology will lead to decreasing spring light windows in North America while spring light windows will be maintained or even increase in Asia and Europe in response to projected climate warming. Climate change may be inducing phenological mismatches between trees and understory plants. Here, phenological models based on long-term data from herbarium specimens indicate that spring ephemeral wildflowers are more vulnerable to such mismatches in North America than in Eurasia.
... As such, accurate predictions of future carbon uptake require an understanding of major phenological processes like spring leaf out or autumn leaf senescence. While the timing of leaf out is mainly driven by temperature (Zohner et al., 2016(Zohner et al., , 2017, the environmental drivers of autumn leaf senescence are less clear (Gallinat et al., 2015), and predictions of future growing-season length thus remain highly uncertain (Richardson et al., 2012). Autumn senescence has traditionally been thought to be primarily driven by temperature and daylength (Krol et al., 1995;Rosenthal and Camm, 1997), while additional variation can be explained by factors, such as nutrient (Sigurdsson, 2001) and water statuses (Leuzinger et al., 2005), pathogen infections (Mutz et al., 2021), and air pollution (Gielen et al., 2007). ...
The growing-season length of temperate and boreal trees has a strong effect on the global carbon cycle. Yet, a poor understanding of the drivers of phenological processes, such as autumn leaf senescence in deciduous trees, limits our capacity to estimate growing-season lengths under climate change. While temperature has been shown to be an important driver of autumn leaf senescence, carbon source–sink dynamics have been proposed as a mechanism that could help explain variation of this important process. According to the carbon sink limitation hypothesis, senescence is regulated by the interplay between plant carbon source and sink dynamics, so that senescence occurs later upon low carbon inputs (source) and earlier upon low carbon demand (sink). Here, we manipulated carbon source–sink dynamics in birch saplings (Betula pendula) to test the relevance of carbon sink limitation for autumn leaf senescence and photosynthetic decline in a widespread deciduous tree. Specifically, we conducted a gradient of leaf and bud removal treatments and monitored the effects on autumnal declines in net photosynthesis and the timing of leaf senescence. In line with the carbon sink limitation hypothesis, we observed that leaf removal tended to increase total leaf-level autumn photosynthesis and delayed the timing of senescence. Conversely, we did not observe an effect of bud removal on either photosynthesis or senescence, which was likely caused by the fact that our bud removal treatment did not considerably affect the plant carbon sink. While we cannot fully rule out that the observed effect of leaf removal was influenced by possible treatment-level differences in leaf age or soil resource availability, our results provide support for the hypothesis of carbon sink limitation as a driver of growing-season length and move the scientific field closer to narrowing the uncertainty in climate change predictions.
... For annual plants, such high autocorrelation gives high predictability of climates between generations. Although the standard deviation between years can also estimate environmental predictability (Zohner et al. 2017), they are found not significantly to explain the genotypic variation of transgenerational plasticities. Therefore, the finding suggests that random evolutionary processes are not sufficient to explain the divergence among genotypes, and selection by regional climatic predictability may play a role in driving the geographic divergence of transgenerational plasticity. ...
Transgenerational plasticity is the plastic response of offspring to ancestral environments. Theoretical studies and experimental evolution have demonstrated the importance of environmental predictability in driving the evolution of transgenerational plasticity. Nevertheless, the contribution of environmental predictability to the variation of transgenerational plasticity in nature remains unexplored. Here, we took advantage of the natural variation of Arabidopsis thaliana, and employed genotypes collected from different geographic locations to explore their transgenerational effects in response to drought and nutrient addition. We found that transgenerational plasticity depended on the offspring environment and the genotype. In particular, we found that genotypes with greater transgenerational plasticity in reproductive traits came from locations with greater temporal autocorrelation of annual temperature and precipitation. These results suggest that the evolutionary process shaping natural variation of transgenerational effect is not random, and the predictability of natural environments may contribute to the evolution of transgenerational effects. While the robustness of our study is limited by the number of genotypes analyzed, we hope this study provides an incentive to conduct a more comprehensive analysis towards understanding natural divergence of transgenerational plasticity.
... While much work in studying invaders' phenology has focused on flowering and leaf-out (e.g., [87] ), we focused on germination and growth traits here as they are some of the most important for granting invasive success [ 50 , 68 ]: invasive success requires the capacity to germinate in novel environments and grow rapidly enough to compete with native flora (see [32] , and papers reviewed therein; [ 13 , 35 ]). Therefore, germination success (whether a seed germinates), germination timing (days between exposure to warm temperature and germi-nation), and growth rate (cm/day) may represent key invasion traits. ...
Plant invasions are increasing due to globalization and environmental change, including through anthropogenic climate change. Yet we lack an understanding of how some species be- come widespread invaders while others do not. Two competing mechanisms have been posited: post-introduction rapid evolution to the novel environments of the introduced range and broad environmental tolerance in the native population that makes invaders tolerant of di- verse introduced environments. Each mechanism has implications for how invaders respond to climate change: either by evolving with future climates, or already being tolerant of diverse current/future climates. Disentangling these mechanisms requires investigating how evolution versus tolerance drive invasion traits (germination success and timing; growth rate). Here, we tested for evidence of rapid evolution in these traits by using growth chambers to pro- vide common climates for seven herbaceous plant species sampled from multiple populations in their native (European) and introduced (North American) ranges. Chambers provided two levels of stratification—to simulate different winter lengths—and four temperature levels post- stratification—to simulate different spring conditions. We used Bayesian multilevel models to examine responses, while controlling for population and seed family. Across all species, trait responses were largely similar between native and introduced populations, except in response to particular climates representing cold winters and warm springs where introduced popula- tions germinated later and grew faster. Our results suggest that broad environmental tolerance, not rapid evolution, likely underlies invasion success for these invaders—and may sustain their spread with continued warming—but species may evolve in response to specific combinations of winter and spring climatic regimes.
... Over the recent decades, climate warming has spurred substantial phenological shifts in biological organisms across the globe (Parmesan and Yohe, 2003;Menzel et al., 2006;Zohner et al., 2017;Liu and Zhang, 2020). The seasonal spring phenology events in plants, in particular flowering, are highly sensitive to the ongoing climate change. ...
In an age of anthropocene, shifting plant phenology is one of the most striking biological indicators of global environmental change. Majority of the studies reporting shifts in plant phenology are available from the North America and Europe and largely scarce from the developing world, including the Himalaya; and studies integrating multiple methodological approaches to investigate the climate-driven phenological shifts are too rare. Here, we report the shifts in spring flowering phenology of model plant species, Sternbergia vernalis in response to the changing climate in Kashmir Himalaya, by integrating decadal field observational records with long-term herbarium and dated-photograph data, and supported with experimental evidences. Our results revealed a significant increasing trend of 0.038, 0.016 and 0.023 °C/year in the annual mean maximum temperature (Tmax), mean minimum temperature (Tmin) and diurnal temperature range (DTR) respectively; but an insignificant decreasing trend in annual precipitation of −1.24 mm/year over the last four decades (1980–2019) in this Himalayan region. The flowering phenology of S. vernalis has significantly advanced by 11.8 days/°C and 27.8 days/°C increase in Tmax and Tmin respectively, indicating that the climate warming has led to substantial shifts in flowering phenology of the model plant species. We also observed a strong association of seasonal Tmax (December–February) and DTR on the early onset of spring flowering, however precipitation had no significant effect on the timing of flowering. The greenhouse experiment results further supported a significant effect of temperature in triggering the phenological shifts, wherein the model plant grown under different temperature treatments flowered 9–20 days earlier compared to the control. Our study showcases the integrated use of multiple methodological approaches for unravelling the long-term phenological shifts in response to climate change, and contributes in filling the knowledge gaps in the phenological research from the developing world in general and the Himalaya in particular.
... Furthermore, this latitudinal pattern in temperature sensitivity was also found in plant species groups along latitudinal gradients (Lapenis et al., 2014;Park et al., 2018;Zhang et al., 2015), and for vegetation types across latitudes in the Northern Hemisphere (Shen et al., 2014). This pattern might result from long-term adaptation to unstable temperature conditions, such as higher variance in spring temperatures Zohner et al., 2017) and larger seasonal temperature ranges (Lapenis et al., 2014;Zhang et al., 2015) at high latitudes; reduced phenological sensitivity to temperature might help plants avoid frost risk in unstable temperature conditions at higher latitudes. Because of long-term adaptation to local climate, this latitudinal pattern in phenological sensitivity is likely to be connected to geographic variation in population genetics (Banta et al., 2012;Liang, 2016). ...
Latitudinal patterns can reveal important ecological processes. The temporal overlap and divergence in flowering along latitudinal gradients is tightly related to intraspecific gene flow and interspecific interactions. Recent studies have predicted that global warming has led to more uniform spring and summer plant phenology across latitudes, but direct evidence is limited. Here, we test changes in the latitudinal pattern of peak flowering of a perennial herb Spiranthes sinensis (Orchidaceae) during 1901–2017 across ~40° of latitude in eastern Asia, spanning humid to water-limited regions. We found that flowering phenology did not vary significantly across latitudes in water-limited regions. However, global warming has significantly increased temporal divergence in flowering phenology across latitudes in humid regions—each 1 °C warming in mean annual temperature leads to an increased divergence of 2.47 days across 1° of latitude. Significantly stronger temperature sensitivity at lower latitudes is likely responsible for the increased phenological divergence. Additionally, we found that the phenological divergence is larger at lower latitudes in humid regions. These findings provide empirical evidence of variation in the latitudinal phenology shift at longer temporal and larger spatial scales under climate change, and highlight its potential role in ecosystem functioning, such as intraspecific gene flow and interspecific interaction.
... than later spring (April and May); in contrast, climate warming in May was greater than in February and March (Figure 2a). Next, we estimated mean temperature and its variability (1 × SD) during the most TRP (Zohner, Benito, Fridley, Svenning, & Renner, 2017). These results indicate that the climate variation, more than warming, may drive the extended time difference in leaf flushing between EFS and LFS, assuming that the temperature sensitivity of EFS and LFS was identical. ...
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 spatio‐temporal scales remains unclear. In this study, we analyzed long‐term in‐situ observations (1951−2016) of six, co‐existing 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 d) than in late‐flushing‐species LFS (5.9 ± 0.2 d) 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.
... Such safe strategies might include to react only to very strong, reliable cues-those with high predictability. For instance, the different levels of spring predictability across North America, Europe and East Asia explained the differences in leaf-unfolding strategies in their woody floras: in regions with high variability, woody species have higher winter chilling requirements and need longer periods above a certain temperature threshold to start to leafout compared to species in regions with lower variability [48]. Second, in more variable environments, we expect transitions with more intermediate stages-which provide flexibility in the timing of life-history stages [49]. ...
The timing of migration and migratory steps is highly relevant for fitness. Because environmental conditions vary between years, the optimal time for migration varies accordingly. Therefore, migratory animals could clearly benefit from acquiring information as to when it is the best time to migrate in a specific year. Thus, environmental predictability and variability are fundamental characteristics of migration systems but their relationship and consequence for migratory progression has remained unexplored. We develop a simple dynamic model to identify the optimal migration behaviour in environments that differ in predictability, variability and the number of intermediate stop-over sites. Our results indicate that higher predictability along migration routes enables organisms to better time migration when phenology deviates from its long-term average and thus, increases fitness. Information is particularly valuable in highly variable environments and in the final migration-step, i.e. before the destination. Furthermore, we show that a general strategy for obtaining information in relatively uninformative but variable environments is using intermediate stop-over sites that enable migrants to better predict conditions ahead. Our study contributes to a better understanding of the relationship between animal movement and environmental predictability—an important, yet underappreciated factor that strongly influences migratory progression.
... showing that warming requirements (degree-day accumulation) to leaf-out in temperate trees decrease with increasing duration of winter chilling and day length (Harrington & Gould, 2015;Heide, 1993;Laube et al., 2014;Zohner, Benito, Fridley, Svenning, & Renner, 2017;Zohner, Benito, Svenning, & Renner, 2016). Effective winter chilling, however, does not linearly increase with winter duration because negative temperatures are less effective than temperatures slightly above zero (Harrington, Gould, & St.Clair, 2010;Körner et al., 2016;Vitasse et al., 2018). ...
Aim
Trees need to avoid frost damage to their young leaves by leafing out after the occurrence of the last frost, yet they also need to start photosynthesis early in the season to achieve sufficient growth. This trade‐off leads to the hypothesis that ‘safety margins’ against spring frost should become shorter, the longer the winter duration, perhaps reaching an asymptotic limit where frost damage would occur in most years. Physiologically, shorter safety margins in high‐latitude ecotypes might be achieved by lower degree‐day requirements for leaf‐out, compared to low‐latitude ecotypes.
Location
Europe.
Time period
1902–2009.
Major taxa studied
Temperate trees.
Methods
Using herbarium collections of Acer platanoides , Carpinus betulus , Fagus sylvatica and Prunus spinosa made over 108 years at 40° to 60° N latitude, we related historic leaf‐out dates to winter and spring temperatures (chilling and degree‐days), winter duration, and date of last frost occurrence in the relevant years and locations.
Results
In all species, frost safety margins decreased towards high‐latitude regions with long winters, with each day increase in winter duration reducing frost safety margins by 0.48 days in Fagus and 0.32–0.21 days in Prunus , Acer and Carpinus . These latitudinal differences correlate with northern ecotypes’ shorter degree‐day requirements for leaf‐out.
Main conclusions
The decline in spring frost safety margins in regions with long winters supports the new hypothesis that species may reach their geographic range limit where they ‘bump up’ against experiencing regular frost injury to their young leaves. Larger datasets are necessary to further corroborate our hypothesis and future efforts should thus be directed toward increasing the latitudinal range of existing phenological databases.
... Understanding the environmental drivers of leaf-out is thus essential to forecasting ecosystem responses to global climate change. These drivers have long been thought to be species-specific combinations of spring temperature, winter chilling, and increasing day length during spring (Heide, 1993a,b;Laube et al., 2014a;Polgar et al., 2014;Zohner & Renner, 2015;Zohner et al., 2016Zohner et al., , 2017. Temperature-related increases in air humidity were suggested as an alternative trigger of the spring bud break recently, based on experimental results from nine Eurasian and American tree species, including two needleleaved trees (Laube et al., 2014b). ...
The timing of spring leaf emergence in temperate regions directly influences global biogeochemical cycles and species interactions (Richardson et al. 2013). Understanding the environmental drivers of leaf‐out is thus essential to forecasting ecosystem responses to global climate change. These drivers have long been thought to be species‐specific combinations of spring temperature, winter chilling, and increasing day length during spring (Heide 1993a,b; Laube et al. 2014a; Polgar et al. 2014; Zohner and Renner 2015; Zohner et al. 2016, 2017).
... The latitudinal trends we observe are also correlated with spring temperature variability, which might be particularly important in the evolution of species-level differences in flowering time. Zohner et al. (2017) observed greater chilling requirements and later leafout dates in species adapted to regions with high levels of spring temperature variability, and we see a parallel trend: the species that occurs in the region with the highest spring temperature variability (V. lentago) flowers later than more southern species, even where they are sympatric. ...
Premise:
We take an integrative approach in assessing how introgression and Pleistocene climate fluctuations have shaped the diversification of the core Lentago clade of Viburnum, a group of five interfertile species with broad areas of sympatry. We specifically tested whether flowering time plays a role in maintaining species isolation.
Methods:
RAD-seq data for 103 individuals were used to infer the species relationships and the genetic structure within each species. Flowering times were compared among species on the basis of historical flowering dates documented by herbarium specimens.
Results:
Within each species, we found a strong relationship between flowering date and latitude, such that southern populations flower earlier than northern ones. In areas of sympatry, the species flower in sequence rather than simultaneously, with flowering dates offset by ≥9 d for all species pairs. In two cases it appears that the offset in flowering times is an incidental consequence of adaptation to differing climates, but in the recently diverged sister species V. prunifolium and V. rufidulum, we find evidence that reinforcement led to reproductive character displacement. Long-term trends suggest that the two northern-most species are flowering earlier in response to recent climate change.
Conclusions:
We argue that speciation in the Lentago clade has primarily occurred through ecological divergence of allopatric populations, but differences in flowering time were essential to maintain separation of incipient species when they came into secondary contact. This combination of factors may underlie diversification in many other plant clades.
Both biotic and abiotic factors restrict changes in autumn phenology, yet their effects remain ambiguous, which hinders the accurate prediction of phenology under future climate change. In this study, based on the phenological records of 135 tree species at ten sites in China during 1979–2018, we first investigated the effects of climatic factors (temperature, precipitation, insolation and wind speed) and spring phenology on interannual changes in leaf coloring date (LCD) with the partial correlation analysis, and assessed the relative importance of phylogeny and native climate to LCD differences among species by using multivariate regression and phylogenetic eigenvector regression approach. The results showed that the effects of climate factors on interannual changes in LCD were more significant than spring phenology. In general, temperature played a more important role in cold regions (e.g. the northeast region), while the control of insolation on LCD was stronger in the warmer and wetter regions (e.g. the north, east and southwest regions). In addition, the effects of precipitation and wind speed were more evident in arid regions (e.g. the northwest region). We also found considerable effects of both native climate and phylogeny on the LCD differences among species, despite the contribution of native climate being almost 2~5 times greater than that of the phylogeny. Our findings confirmed and quantified the combined effects of climate, spring phenology and phylogeny on the autumn phenology of plants, which could help better understand the driving factors and influencing mechanism of plant phenology and provide a reference for the calibration and optimization of phenological models.
Deciduous trees, shrubs and forest wildflowers may be advancing their leaf‐out phenology at different rates in response to a warming climate. A mismatch between understory and overstory phenology may lead to a reduction of understory light levels in the early spring, which is a critical period when many spring‐blooming wildflowers achieve highest photosynthetic rates. However, the extent of this phenomenon beyond a single site or region is largely unknown.
Using 3083 herbarium specimens collected between 1870 and 2019 across eastern North America, we assessed leaf‐out and flowering times of 10 tree species (6 native, 4 non‐native), 4 shrub species (2 native, 2 non‐native) and 7 wildflower species (6 native, 1 non‐native). We paired phenological data with historical climate data to quantify differences in phenological sensitivity to spring temperature across canopy strata, across species' geographical ranges and between native and non‐native species.
Predicted phenological mismatches between native trees and wildflowers differed across large spatial scales, with wildflower populations in warmer regions of North America more likely to be affected. Overall, native tree species leafed out 3.6 days earlier per °C spring warming, while native wildflower species advanced their flowering times by 3.2 days per °C, resulting in phenological mismatch as wildflowers experience fewer days before tree leaf‐out at warmer temperatures. Native trees and wildflowers in the warmer, southern part of their ranges advanced their spring phenology 2 and 1.5 times faster, respectively, than those in colder, northern locations. The phenological sensitivity of non‐native plants was less variable across their ranges. Non‐native trees and shrubs exhibited greater phenological sensitivity than native wildflowers. Notably, phenological sensitivities differed substantially among wildflower species, suggesting that certain species are more likely to be affected by phenological mismatch as climate warming progresses.
Synthesis : Our results provide new insight into novel phenological responses within and among species across a wide geographical range and the potential impact of competition and interactions with non‐native invasive species. This research highlights the value of newly‐available digitized museum collections in phenological research to cover longer time periods, wider spatial areas and a greater diversity of species than otherwise possible.
Yellow and red autumn leaves are typical of many temperate/boreal woody plants. Since the 19th century, it has been either considered the non‐functional outcome of chlorophyll degradation that unmasks the pre‐existing yellow and red pigments or that the de novo synthesis of red anthocyanins in autumn leaves indicated that it should have a physiological function, although it was commonly ignored. Defending free amino acids and various other resources released especially following the breakdown of the photosynthetic system, and mobilizing them for storage in other organs before leaf fall, is the cornerstone of both the physiological and anti‐herbivory hypotheses about the functions of yellow and red autumn leaf colouration. The complicated phenomenon of conspicuous autumn leaf colouration has received significant attention since the year 2000, especially because ecologists started paying attention to its anti‐herbivory potential. The obvious imperfection of the hypotheses put forth in several papers stimulated many other scientists. Hot debates among physiologists, among ecologists, and between physiologists and ecologists have been common since the year 2000, first because the various functions of yellow and red autumn leaf colouration are non‐exclusive, and second because many scientists were trained to focus on a single subject. Here, I will review the debates, especially between the photoprotective and the anti‐herbivory hypotheses, and describe both the progress in their understanding and the required progress. Yellow and red autumn leaves typical to temperate/boreal trees defend important resources released following the photosynthetic system breakdown, and mobilized for storage to be used in the next spring. This coloration, especially red, defends from excess light and oxidative stress and against herbivores. I describe the hypotheses, findings and disagreements about the functions and evolution of yellow/red autumn leaves.
The ongoing phenological changes in vegetation on the Qinghai–Tibetan Plateau could modify land surface and atmospheric processes. In this Review, we summarize these changes, their drivers and the resulting impacts. The start of the growing season advanced by 9.4 ± 2.2 days during 1982–1999 and 8.3 ± 2.0 days over 2000–2020, and the end of season delayed by 8.2 ± 1.9 days during 2000–2020. The main identified drivers of these changes are warming temperatures and increasing precipitation, but their impacts vary substantially across the Qinghai–Tibetan Plateau. Other factors, such as grazing and nitrogen deposition, also potentially influence phenological changes, but these relationships are poorly constrained. In manipulation experiments, grazing and nitrogen addition have no individual effects on most phenophase timings at the population level, but nitrogen addition markedly delays flowering. Additionally, there are carry-over effects between phenophases that control subsequent temperature and precipitation responses. Phenological changes in turn could alter species interactions, modulate carbon and water cycling, and affect Asian monsoons and spring rainfall over eastern China, but evidence of these interactions is limited. Harmonization of remote-sensing-based and in situ observations, and simultaneous testing of both biotic and abiotic factors, are needed for a mechanistic understanding of Qinghai–Tibetan Plateau phenology dynamics.
This review describes, in chronological order, the research topics in which I have been involved over the past 40 years, a time during which the study of plant evolution, systematics, and biodiversity has moved from relying solely on morphology to relying mostly on DNA sequences and now partially assembled genomes. When I began to do systematics, traveling to tropical countries for fieldwork was a big draw and probably influenced my initial choice of plant groups to work on. In 1989, I made a conscious decision to shift my focus from monographs, floras, and herbarium-based species discovery to the evolution of plant sexual systems and the functioning of unisexual flowers, selecting first Siparunaceae and then Cucurbitaceae as suitable groups. I also became an early adopter of molecular clock approaches in the study of biogeography and plant/animal mutualisms, and was involved in the discovery of natural horizontal gene transfers in seed plants, which in turn led to an interest in mitochondrial and plastid genomes in parasitic plants. Three topics, bee behaviour on flowers, the evolution of ant/plant interactions, and plant phenology, have accompanied me from my dissertation to the present, while others, such as molecular cytogenetics, grew from the interests and expertise of students. The breadth of topics reflects a great change in systematics since the 1980s, namely the increasing role of collaborations. Monographs, floras, and cladistics (when morphology based) used to be done in isolation. With DNA data came lab work, bioinformatics, and both the need and the possibility to collaborate, which brought systematists out of their niche, gave comparative biology a huge push, and resulted in a better integration of biodiversity studies within biology.
Understanding the breadth and complexity of changes in phenology is limited by the availability of long‐term historical data sets with broad geographic range.
We compare a recently discovered historical data set of plant phenology observations collected across the state of New York (1826–1872) to contemporary volunteer‐contributed observations (2009–2017) to evaluate changes in plant phenology between time periods. These multi‐site, multi‐taxa phenology data matched with temperature data uniquely extend historical observations back in time prior to the major atmospheric effects of the Industrial Revolution.
The majority of the 36 trees, shrubs and forbs that comprised our analysable data set flowered and leafed out earlier in contemporary years than in the early to mid‐19th century. This shift is associated with a warming trend in mean January‐to‐April temperatures, with flowering and leafing advancing on average 3 days/°C earlier. On average, plants flowered 10.5 days earlier and leafed out 19 days earlier in the contemporary period. Urban areas exhibit more advanced phenology than their rural counterparts overall, and insect‐pollinated trees show more advanced phenology than wind‐pollinated trees and seasonality and growth form explain significant variation in flowering phenology. The greatest rates of temperature sensitivity and change between time periods for flowering are seen in early‐season species, particularly trees. Changes in the timing of leaf out are the most advanced for trees and shrubs in urban areas.
Synthesis . Citizen science observations across two centuries reveal a dramatic, climate‐driven shift to earlier leaf out and flowering. The magnitude of advancement varies across settings, species and functional groups, and illustrates how long‐term monitoring and citizen science efforts are invaluable for ecological forecasting and discovery.
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.
Plant phenology research has surged in recent decades, in part due to interest in phenological sensitivity to climate change and the vital role phenology plays in ecology. Many local‐scale studies have generated important findings regarding the physiology, responses, and risks associated with shifts in plant phenology. By comparison, our understanding of regional‐ and global‐scale phenology has been largely limited to remote sensing of green‐up without the ability to differentiate among plant species. However, a new generation of analytical tools and data sources—including enhanced remote sensing products, digitized herbarium specimen data, and public participation in science—now permits investigating patterns and drivers of phenology across extensive taxonomic, temporal, and spatial scales, in an emerging field that we call macrophenology. Recent studies have highlighted how phenology affects dynamics at broad scales, including species interactions and ranges, carbon fluxes, and climate. At the cusp of this developing field of study, we review the theoretical and practical advances in four primary areas of plant macrophenology: (1) global patterns and shifts in plant phenology, (2) within‐species changes in phenology as they mediate species' range limits and invasions at the regional scale, (3) broad‐scale variation in phenology among species leading to ecological mismatches, and (4) interactions between phenology and global ecosystem processes. To stimulate future research, we describe opportunities for macrophenology to address grand challenges in each of these research areas, as well as recently available data sources that enhance and enable macrophenology research.
Ecosystems in the Anthropocene face pressures from multiple, interacting forms of environmental change. These pressures, resulting from land use change, altered hydrologic regimes, and climate change, will likely change the synchrony of ecosystem processes as distinct components of ecosystems are impacted in different ways. However, discipline-specific definitions and ad hoc methods for identifying synchrony and asynchrony have limited broader synthesis of this concept among studies and across disciplines. Drawing on concepts from ecology, hydrology, geomorphology, and biogeochemistry, we offer a unifying definition of synchrony for ecosystem science and propose a classification framework for synchrony and asynchrony of ecosystem processes. This framework classifies the relationships among ecosystem processes according to five key aspects: (1) the focal variables or relationships representative of the ecosystem processes of interest, (2) the spatial and temporal domain of interest, (3) the structural attributes of drivers and focal processes, (4) consistency in the relationships over time, and (5) the degree of causality among focal processes. Using this classification framework, we identify and differentiate types of synchrony and asynchrony, thereby providing the basis for comparing among studies and across disciplines. We apply this classification framework to existing studies in the ecological, hydrologic, geomorphic, and biogeochemical literature and discuss potential analytical tools that can be used to quantify synchronous and asynchronous processes. Furthermore, we seek to promote understanding of how different types of synchrony or asynchrony may shift in response to ongoing environmental change by providing a universal definition and explicit types and drivers with this framework.
Climate change has emerged as the main threat to global biodiversity and even the protected areas (PAs) are not immune to this problem. Here, we have focused on PAs with the aim of assessing the impacts of climate change on their habitat suitability and their effectiveness to protect threatened species, in this case three endemic Spanish plants: Isatis platyloba, Rhaponticum exaltatum and Succisella microcephala. We used the machine-learning technique called Maxent that is able to protect the potential species distribution under four future climate scenarios. Our results show a strong reduction of the potential areas with high suitability for Isatis platyloba. By contrast, for Rhaponticum exaltatum and Succisella microcephala our results suggested an increase of potential habitats. Regarding to the PAs specially designed to protect some important populations of these species, most of them would be located in areas with high suitability for all species in the future. Our study supports the necessity of the proposed Plant Micro-reserves to guarantee the preservation of these three species and, most importantly, can serve as a model to evaluate the efficiency of a given PA in protecting any species taking into account the climate change scenario.
Supplemental data for this article is available online at https://doi.org/10.1080/11263504.2021.1918777.
Native and nonnative plant species can exhibit differences in the timing of their reproductive phenology and their phenological sensitivity to climate. These contrasts may influence species' interactions and the invasion potential of nonnative species; however, a limited number of phenology studies expressly consider phenological mismatches among native and nonnative species over broad spatial or temporal scales. To fill this knowledge gap, we used two complementary approaches: First, we quantified the flowering phenology of native and nonnative plants at five old‐field sites across a spatially extensive range of eastern North America. Second, we used herbarium records to compare the sensitivity of flowering and fruiting phenology to climate across a 114‐yr time period in a subset of common old‐field species in southwestern Pennsylvania. Across the study region, nonnatives reproduced substantially earlier in the growing season than natives, suggesting that nonnatives occupy a unique phenological niche (0.55 months earlier flowering across the North American study sites; 50.1 d earlier flowering and 17.5 d earlier fruiting in southwestern Pennsylvania). Both natives and nonnatives advanced their reproductive phenology between 1900 and 2014 but exhibited contrasting phenological sensitivity to climate factors. During the flowering stage of phenology, nonnatives were more sensitive to changes in precipitation than natives and generally delayed flowering in wetter years. Nonnative plants had greater sensitivity and advanced fruiting when the month preceding fruiting was warmer, while native plants had greater sensitivity and advanced fruiting when the three‐month period preceding fruiting was warmer. Our findings suggest that nonnative old‐field species occupy an earlier phenological niche relative to native species, which may facilitate their invasion into old‐field communities. However, given the different sensitivities of native and nonnative plants to climate factors, present‐day patterns of phenology are likely to shift with future climate changes, potentially leading to novel species interactions that may influence the outcomes of invasion.
Many understory woody invasive plants in North America leaf out earlier or retain leaves later than their native associates. This extended leaf phenology is thought to grant invasive species an advantage over native species because spring and fall are crucial times for light access and carbon acquisition in understory habitats. However, it is unclear whether this advantage persists at northern latitudes where freezing temperatures constrain growing season length and low light levels reduce carbon gain. To investigate the costs and benefits of extended leaf phenology at northern latitudes, we observed leaf phenology, estimated total carbon gain, measured growth, and tested susceptibility to freezing temperatures for four native and four invasive woody shrubs in a disturbed forest in northern Minnesota, USA. We found that the invaders leafed out simultaneously with the natives in the spring but retained their leaves later in the autumn than native species. This extended fall phenology did not enable greater total carbon gain for the invaders because they assimilated less carbon earlier in the year than the natives. There was also no significant difference between native and invasive species in their susceptibility to freezing temperatures. Instead freezing tolerance related more to native range then leaf phenology. Our results suggest that freezing temperatures do not limit invasive species’ northern expansion and instead indicate that at the northern edge of their ranges, these species may lose any competitive advantage granted by extended leaf phenology over their native associates. This study demonstrates the importance of considering latitude and forest structure when investigating phenology and growth.
Temperate forests are widely invaded by shade-tolerant shrubs and trees, including those of Eastern North America (ENA). However, it remains unknown whether these invaders are 'pre-adapted' for success in their new ranges due to unique aspects of their evolutionary history, or whether selection due to enemy release or other post-introduction processes have driven rapid evolution in the invaded range. We sampled leaf traits of populations of woody understory invaders across light gradients in their native range in Japan and in their invaded ENA range to examine potential phenotypic shifts related to carbon gain and nitrogen use between ranges. We also measured leaf traits in three co-occurring ENA native shrub species. In their invaded range, invaders invested significantly less in leaf chlorophyll content (both per unit leaf mass and area) compared to native range populations of the same species, yet maintained similar rates of photosynthesis in low light. In addition, compared to ENA natives, ENA invaders displayed greater trait variation in response to increasing light availability (forest edges, gaps), giving them a potential advantage over ENA natives in a variety of light conditions. We conclude that, for this group of species, newly evolved phenotypes in the invaded range are more important than preadaptation for their success as shade-tolerant forest invaders.
Extreme climate events (ECEs) such as severe droughts, heat waves and late spring frosts are rare but exert a paramount role in shaping tree species distributions. The frequency of such ECEs is expected to increase with climate warming, threatening the sustainability of temperate forests. Here, we analyzed 2844 tree‐ring width series of five dominant European tree species from 104 Swiss sites ranging from 400 to 2200 m a.s.l. for the period 1930–2016. We found that (i) the broadleaved oak and beech are sensitive to late frosts that strongly reduce current year growth; however, tree growth is highly resilient and fully recovers within two years; (ii) radial growth of the conifers larch and spruce is strongly and enduringly reduced by spring droughts—these species are the least resistant and resilient to droughts; (iii) oak, silver fir, and to a lower extent beech, show higher resistance and resilience to spring droughts and seem therefore better adapted to the future climate. Our results allow a robust comparison of the tree growth responses to drought and spring frost across large climatic gradients and provide striking evidence that the growth of some of the most abundant and economically important European tree species will be increasingly limited by climate warming. These results could serve for supporting species selection to maintain the sustainability of forest ecosystem services under the expected increase in ECEs.
A spatially explicit global map of tree symbioses with nitrogen-fixing bacteria and mycorrhizal fungi reveals that climate variables are the primary drivers of the distribution of different types of symbiosis.
Shifts in vegetation phenology are a key example of the biological effects of climate change1-3. However, there is substantial uncertainty about whether these temperature-driven trends will continue, or whether other factors-for example, photoperiod-will become more important as warming exceeds the bounds of historical variability4,5. Here we use phenological transition dates derived from digital repeat photography6 to show that experimental whole-ecosystem warming treatments7 of up to +9 °C linearly correlate with a delayed autumn green-down and advanced spring green-up of the dominant woody species in a boreal Picea-Sphagnum bog. Results were confirmed by direct observation of both vegetative and reproductive phenology of these and other bog plant species, and by multiple years of observations. There was little evidence that the observed responses were constrained by photoperiod. Our results indicate a likely extension of the period of vegetation activity by 1-2 weeks under a 'CO2 stabilization' climate scenario (+2.6 ± 0.7 °C), and 3-6 weeks under a 'high-CO2 emission' scenario (+5.9 ± 1.1 °C), by the end of the twenty-first century. We also observed severe tissue mortality in the warmest enclosures after a severe spring frost event. Failure to cue to photoperiod resulted in precocious green-up and a premature loss of frost hardiness8, which suggests that vulnerability to spring frost damage will increase in a warmer world9,10. Vegetation strategies that have evolved to balance tradeoffs associated with phenological temperature tracking may be optimal under historical climates, but these strategies may not be optimized for future climate regimes. These in situ experimental results are of particular importance because boreal forests have both a circumpolar distribution and a key role in the global carbon cycle11.
While climate warming reduces the occurrence of frost events, the warming-induced lengthening of the growing season of plants in the Northern Hemisphere may actually induce more frequent frost days during the growing season (GSFDs, days with minimum temperature < 0 °C). Direct evidence of this hypothesis, however, is limited. Here we investigate the change in the number of GSFDs at latitudes greater than 30° N using remotely-sensed and in situ phenological records and three minimum temperature (Tmin) data sets from 1982 to 2012. While decreased GSFDs are found in northern Siberia, the Tibetan Plateau, and northwestern North America (mainly in autumn), ~43% of the hemisphere, especially in Europe, experienced a significant increase in GSFDs between 1982 and 2012 (mainly during spring). Overall, regions with larger increases in growing season length exhibit larger increases in GSFDs. Climate warming thus reduces the total number of frost days per year, but GSFDs nonetheless increase in many areas.
Background:
Leaf out times of temperate forest trees are a prominent determinant of global carbon dynamics throughout the year. Abiotic cues of leaf emergence are well studied but investigation of the relative roles of shared evolutionary history (phylogeny) and local adaptation to climate in determining the species-level responses to these cues is needed to better apprehend the effect of global change on leaf emergence. We explored the relative importance of phylogeny and climate in determining the innate leaf out phenology across the temperate biome.
Methods:
We used an extensive dataset of leaf-out dates of 1126 temperate woody species grown in eight Northern Hemisphere common gardens. For these species, information on the native climate and phylogenetic position was collected. Using linear regression analyses, we examine the relative effect of climate variables and phylogeny on leaf out variation among species.
Results:
Climate variables explained twice as much variation in leaf out timing as phylogenetic information, a process that was driven primarily by the complex interactive effects of multiple climate variables. Although the primary climate factors explaining species-level variation in leaf-out timing varied drastically across different families, our analyses reveal that local adaptation plays a stronger role than common evolutionary history in determining tree phenology across the temperate biome.
Conclusions:
In the long-term, the direct effects of physiological adaptation to abiotic effects of climate change on forest phenology are likely to outweigh the indirect effects mediated through changes in tree species composition.
The length of the vegetation period (LVP), which is the time between leaf-out and leaf senescence, affects numerous ecosystem functions, including biogeochemical cycles and interspecific interactions. The evolutionary mechanisms determining LVP, however, are poorly understood, and thus, it is unknown whether innate LVPs differ between eastern North American (ENA), European and East Asian species. Here we monitored LVP in 2014–2015 in 396 Northern Hemisphere woody species grown in a common garden. We found that ENA species, under the same conditions, have three weeks (11%) shorter vegetation periods than their European and East Asian relatives, because their leaves flushed 9 ± 4 and 13 ± 4 days later and senesced 9 ± 4 and 11 ± 4 days earlier. LVPs of species introduced from Eurasia into ENA are therefore longer than those of native species, suggesting that the spread of non-natives might alter seasonal forest productivity in ENA. LVP between naturalized invasive and non-invasive species, however, did not differ, rejecting the common assumption that longer leaf presentation generally fosters invasive success. A likely explanation for the shorter LVP of ENA species is that region’s uniquely high inter-annual temperature variation. These results highlight the footprint of regional climate history, which will affect forest response to climate change.
We investigated how deciduous trees can adjust their freezing resistance in response to temperature during the progress of the ecodormancy phase, from midwinter to budburst.
We regularly sampled twigs of four different temperate deciduous tree species from January to the leaf‐out date. Using computer‐controlled freezers and climate chambers, the freezing resistance of buds was measured directly after sampling and also after the application of artificial hardening and dehardening treatments, simulating cold and warm spells. The thermal time to budburst in forcing conditions ( c . 20°C) was also quantified at each sampling as a proxy for dormancy depth.
Earlier flushing species showed higher freezing resistance than late flushing species at either similar bud development stage or similar dormancy depth. Overall, freezing resistance and its hardening and dehardening potential dramatically decreased during the progress of ecodormancy and became almost nil during budburst.
Our results suggest that extreme cold events in winter are not critical for trees, as freezing resistance can be largely enhanced during this period. By contrast, the timing of budburst is a critical component of tree fitness. Our results provide quantitative values of the freezing resistance dynamics during ecodormancy, particularly valuable in process‐based species distribution models.
Robust evidence exists that certain extreme weather and climate events, especially daily temperature and precipitation extremes, have changed in regard to intensity and frequency over recent decades. These changes have been linked to human-induced climate change, while the degree to which climate change impacts an individual extreme climate event (ECE) is more difficult to quantify. Rapid progress in event attribution has recently been made through improved understanding of observed and simulated climate variability, methods for event attribution and advances in numerical modelling. Attribution for extreme temperature events is stronger compared with other event types, notably those related to the hydrological cycle. Recent advances in the understanding of ECEs, both in observations and their representation in state-of-the-art climate models, open new opportunities for assessing their effect on human and natural systems. Improved spatial resolution in global climate models and advances in statistical and dynamical downscaling now provide climatic information at appropriate spatial and temporal scales. Together with the continued development of Earth System Models that simulate biogeochemical cycles and interactions with the biosphere at increasing complexity, these make it possible to develop a mechanistic understanding of how ECEs affect biological processes, ecosystem functioning and adaptation capabilities. Limitations in the observational network, both for physical climate system parameters and even more so for long-term ecological monitoring, have hampered progress in understanding bio-physical interactions across a range of scales. New opportunities for assessing how ECEs modulate ecosystem structure and functioning arise from better scientific understanding of ECEs coupled with technological advances in observing systems and instrumentation. This article is part of the themed issue ‘Behavioural, ecological and evolutionary responses to extreme climatic events’. © 2017 The Author(s) Published by the Royal Society. All rights reserved.
We created a new dataset of spatially interpolated monthly climate data for global land areas at a very high spatial resolution (approximately 1 km 2). We included monthly temperature (minimum, maximum and average), precipitation, solar radiation, vapour pressure and wind speed, aggregated across a target temporal range of 1970–2000, using data from between 9000 and 60 000 weather stations. Weather station data were interpolated using thin-plate splines with covariates including elevation, distance to the coast and three satellite-derived covariates: maximum and minimum land surface temperature as well as cloud cover, obtained with the MODIS satellite platform. Interpolation was done for 23 regions of varying size depending on station density. Satellite data improved prediction accuracy for temperature variables 5–15% (0.07–0.17 ∘ C), particularly for areas with a low station density, although prediction error remained high in such regions for all climate variables. Contributions of satellite covariates were mostly negligible for the other variables, although their importance varied by region. In contrast to the common approach to use a single model formulation for the entire world, we constructed the final product by selecting the best performing model for each region and variable. Global cross-validation correlations were ≥ 0.99 for temperature and humidity, 0.86 for precipitation and 0.76 for wind speed. The fact that most of our climate surface estimates were only marginally improved by use of satellite covariates highlights the importance having a dense, high-quality network of climate station data.
Key message
European beech showed low resistance but high resilience in radial growth after an extreme late frost event. Site-specific growth reductions correlated with absolute minimum temperature in May.
Abstract
Late spring frost events occurring after the early leaf unfolding (“false spring”) can result in severe leaf damages in deciduous trees. With climate warming, such damages may occur more frequently due to an earlier start of the growing season. While affected, mature trees usually survive, but radial and height growth after the late frost has rarely been quantified in relation to the magnitude of the frost events. The effects of a severe late frost event in the early May 2011, following a warm spring and early bud break, was quantified for European beech (Fagus sylvatica L.) at 7 forest stands in Bavaria, Germany. Resistance and resilience of tree growth were quantified based on tree-ring widths of 135 trees. Resistance to the late frost event (comparing tree-ring width in the frost year with the previous 5 years) was on average reduced by 46%. Resistance was positively correlated with May minimum temperature at the study sites, indicating a relationship between growth reduction and frost severity. Partial least-square linear models based on monthly climate data (precipitation, temperature, potential evapotranspiration, and the Standardized Precipitation Evapotranspiration Index) could not explain the growth reduction in 2011, thereby providing evidence for the importance of frost damages on annual growth. F. sylvatica showed high resilience after the frost year, with tree-ring widths in the subsequent years being comparable to the previous years. This study suggests that frost events may strongly reduce growth of F. sylvatica in the event year, but that carry-over effects on the radial growth of subsequent years are not likely.
Global biodiversity and productivity
The relationship between biodiversity and ecosystem productivity has been explored in detail in herbaceous vegetation, but patterns in forests are far less well understood. Liang et al. have amassed a global forest data set from >770,000 sample plots in 44 countries. A positive and consistent relationship can be discerned between tree diversity and ecosystem productivity at landscape, country, and ecoregion scales. On average, a 10% loss in biodiversity leads to a 3% loss in productivity. This means that the economic value of maintaining biodiversity for the sake of global forest productivity is more than fivefold greater than global conservation costs.
Science , this issue p. 196
Monitoring and understanding climate-induced changes in the boreal and arctic vegetation is critical to aid in prognosticating their future. We used a 33 year (1982–2014) long record of satellite observations to robustly assess changes in metrics of growing season (onset: SOS, end: EOS and length: LOS) and seasonal total gross primary productivity. Particular attention was paid to evaluating the accuracy of these metrics by comparing them to multiple independent direct and indirect growing season and productivity measures. These comparisons reveal that the derived metrics capture the spatio-temporal variations and trends with acceptable significance level (generally p
Aim: Cold events determine the distributional range limits of woody species. Despite global warming, the magnitude of late frost events in boreal and temperate regions is not expected to change. Hence, the risk for late spring frost damage of woody species may increase with an earlier onset of the growing season. Here, we investigated biogeographical, phenological and phylogenetic effects on late frost sensitivity. Location: Ecological-Botanical Gardens Bayreuth, Germany (49°55′45″N, 11°35′10″E). Methods: We inspected 170 woody species in the Ecological-Botanical Gardens from across the entire Northern Hemisphere for frost damage after an extreme late frost event in May 2011 (air temperature -4.3 °C after leaf unfolding of all species). Distribution range characteristics, climatic parameters of place of origin and phenological strategy were linked to sensitivity to the late frost event. Results: The northern distribution limit and the range in continentality across the distributional ranges correlated negatively with a taxon's late frost sensitivity (pseudo-R2=0.42, pseudo-R2=0.33, respectively). Sensitivity to the late frost event was well explained by the climatic conditions within species' native ranges (boosted regression trees; receiver operating characteristic 0.737). Average (1950-2000) May minimum temperature in species' native ranges was the main explanatory variable of late frost sensitivity (51.7% of explained variance). Phylogenetic relatedness explained additional variance in sensitivity to the late frost event. Sensitivity to the late frost event further correlates well with species phenological strategy. Frost-tolerant species flushed on average 2 weeks earlier than frost-sensitive species. Main conclusions: Range characteristics and the prevalent climatic parameters across species native ranges are strongly related to their susceptibility to late spring frost damage. Further, more late frost-sensitive species unfolded their leaves later than more tolerant species and late frost tolerance is phylogenetically conserved. Thus, late frost sensitivity may challenge natural and human-assisted migration of woody species under global warming.
Attempts at explaining range limits of temperate tree species still rest on correlations with climatic data that lack a physiological justification. Here, we present a synthesis of a multidisciplinary project that offers mechanistic explanations. Employing climatology, biogeography, dendrology, population and reproduction biology, stress physiology and phenology, we combine results from in situ elevational (Swiss Alps) and latitudinal (Alps vs. Scandinavia) comparisons, from reciprocal common garden and phytotron studies for eight European broadleaf tree species.
We show that unlike for low‐stature plants, tree canopy temperatures can be predicted from weather station data, and that low‐temperature extremes in winter do not explain range limits. At the current low‐temperature range limit, all species recruit well. Transplants revealed that the local environment rather than elevation of seed origin dominates growth and phenology. Tree ring width at the range limit is not related to season length, but to growing season temperature, with no evidence of carbon shortage. Bud break and leaf emergence in adults trees are timed in such a way that the probability of freezing damage is almost zero, with a uniform safety margin across elevations and taxa. More freezing‐resistant species flush earlier than less resistant species.
Synthesis : we conclude that the range limits of the examined tree species are set by the interactive influence of freezing resistance in spring, phenology settings, and the time required to mature tissue. Microevolution of spring phenology compromises between demands set by freezing resistance of young, immature tissue and season length requirements related to autumnal tissue maturation.
Within the same forest stand, temperate deciduous trees generally exhibit a distinct pattern in leaf-out timing, with some species flushing earlier than other species. This study aimed to explain the timing of leaf-out of various temperate tree species in relation to the risk of freezing damage to leaves.
We combined long-term series of leaf-out date (14–32 years) of five temperate tree species located in both low and high elevations in Switzerland, daily minimum temperatures recorded on the same sites and species-specific freezing resistance (LT50) of emerging leaves. We calculated temperature safety margins (the temperature difference between absolute minimum temperature during leaf-out and species-specific LT50 values), and date safety margins (time lag between the last day when temperature falls below species-specific LT50 values and the date of leaf-out).
The timing of leaf-out occurred when the probability to encounter freezing damage approaches zero, irrespective of climatic conditions (low vs. high elevation) and species (early and late flushing species). In other words, trees leaf-out precisely at the beginning of the probabilistically safe period. Interestingly, the temperature safety margins did not differ significantly between low and high elevation. Yet, the date safety margin was smaller at high elevation, presumably due to a faster increase of temperature during the leaf-out period at high elevation.
When species-specific freezing resistance is taken into account, the time of leaf-out converges among species towards a marginal risk of freezing damage. Thus, leaf-out time has likely evolved in a way that the risk of freezing damage is minimized over a large spectrum of climatic conditions. Species with a small safety margin against freezing temperature, like Fagus sylvatica, appear to employ photoperiod co-control of spring phenology, whereas species with a large safety margin depend largely on temperature for the right timing of leaf-out.
Our results offer a new avenue to explain the differences in leaf-out timing among co-occurring tree species. They further suggest that in a warming climate, tree species can expand their distribution range to the extent their phenology matches the stochasticity of freezing temperatures in spring.
Earlier spring leaf unfolding is a frequently observed response of plants to climate warming. Many deciduous tree species require chilling for dormancy release, and warming-related reductions in chilling may counteract the advance of leaf unfolding in response to warming. Empirical evidence for this, however, is limited to saplings or twigs in climate-controlled chambers. Using long-term in situ observations of leaf unfolding for seven dominant European tree species at 1,245 sites, here we show that the apparent response of leaf unfolding to climate warming (ST, expressed in days advance of leaf unfolding per °C warming) has significantly decreased from 1980 to 2013 in all monitored tree species. Averaged across all species and sites, ST decreased by 40% from 4.0 ± 1.8 days °C(-1) during 1980-1994 to 2.3 ± 1.6 days °C(-1) during 1999-2013. The declining ST was also simulated by chilling-based phenology models, albeit with a weaker decline (24-30%) than observed in situ. The reduction in ST is likely to be partly attributable to reduced chilling. Nonetheless, other mechanisms may also have a role, such as 'photoperiod limitation' mechanisms that may become ultimately limiting when leaf unfolding dates occur too early in the season. Our results provide empirical evidence for a declining ST, but also suggest that the predicted strong winter warming in the future may further reduce ST and therefore result in a slowdown in the advance of tree spring phenology.
Recent advances in the implementation of spatial econometrics model estimation techniques have made it desirable to compare results, which should correspond between implementations across software applications for the same data. These model estimation techniques are associated with methods for estimating impacts (emanating effects), which are also presented and compared. This review constitutes an up-to-date comparison of generalized method of moments and maximum likelihood implementations now available. The comparison uses the cross-sectional US county data set provided by Drukker, Prucha, and Raciborski (2013d). The comparisons will be cast in the context of alternatives using the MATLAB Spatial Econometrics toolbox, Stata's user-written sppack commands, Python with PySAL and R packages including spdep, sphet and McSpatial.
The objective of this study is the analysis of dam-
aging frost events in agriculture, by examining the relation-
ship between the daily minimum temperature in the lower
atmosphere (at an isobaric level of 850 hPa) and crop pro-
duction losses. Furthermore, the study suggests a method-
ological approach for estimating agriculture risk due to frost
events, with the aim of estimating the short-term probability
and magnitude of frost-related financial losses for different
levels of 850 hPa temperature. Compared with near-surface
temperature forecasts, temperature forecasts at the level of
850 hPa are less influenced by varying weather conditions or
by local topographical features; thus, they constitute a more
consistent indicator of the forthcoming weather conditions.
The analysis of the daily monetary compensations for in-
sured crop losses caused by weather events in Greece shows
that, during the period 1999–2011, frost caused more dam-
age to crop production than any other meteorological phe-
nomenon. Two regions of different geographical latitudes
are examined further, to account for the differences in the
temperature ranges developed within their ecological envi-
ronment. Using a series of linear and logistic regressions,
we found that minimum temperature (at an 850 hPa level),
grouped into three categories according to its magnitude, and
seasonality, are significant variables when trying to explain
crop damage costs, as well as to predict and quantify the like-
lihood and magnitude of damaging frost events.
A revised and updated classification for the families of flowering plants is provided. Many recent studies have yielded increasingly detailed evidence for the positions of formerly unplaced families, resulting in a number of newly adopted orders, including Amborellales, Berberidopsidales, Bruniales, Buxales, Chloranthales, Escalloniales, Huerteales, Nymphaeales, Paracryphiales, Petrosaviales, Picramniales, Trochodendrales, Vitales and Zygophyllales. A number of previously unplaced genera and families are included here in orders, greatly reducing the number of unplaced taxa; these include Hydatellaceae (Nymphaeales), Haptanthaceae (Buxales), Peridiscaceae (Saxifragales), Huaceae (Oxalidales), Centroplacaceae and Rafflesiaceae (both Malpighiales), Aphloiaceae, Geissolomataceae and Strasburgeriaceae (all Crossosomatales), Picramniaceae (Picramniales), Dipentodontaceae and Gerrardinaceae (both Huerteales), Cytinaceae (Malvales), Balanophoraceae (Santalales), Mitrastemonaceae (Ericales) and Boraginaceae (now at least known to be a member of lamiid clade). Newly segregated families for genera previously understood to be in other APG-recognized families include Petermanniaceae (Liliales), Calophyllaceae (Malpighiales), Capparaceae and Cleomaceae (both Brassicales), Schoepfiaceae (Santalales), Anacampserotaceae, Limeaceae, Lophiocarpaceae, Montiaceae and Talinaceae (all Caryophyllales) and Linderniaceae and Thomandersiaceae (both Lamiales). Use of bracketed families is abandoned because of its unpopularity, and in most cases the broader circumscriptions are retained; these include Amaryllidaceae, Asparagaceace and Xanthorrheaceae (all Asparagales), Passifloraceae (Malpighiales), Primulaceae (Ericales) and several other smaller families. Separate papers in this same volume deal with a new linear order for APG, subfamilial names that can be used for more accurate communication in Amaryllidaceae s.l., Asparagaceace s.l. and Xanthorrheaceae s.l. (all Asparagales) and a formal supraordinal classification for the flowering plants.
Temperate climates are defined by distinct temperature seasonality with large and often unpredictable weather during any of the four seasons. To thrive in such climates, trees have to withstand a cold winter and the stochastic occurrence of freeze events during any time of the year. The physiological mechanisms trees adopt to escape, avoid, and tolerate freezing temperatures include a cold acclimation in autumn, a dormancy period during winter (leafless in deciduous trees), and the maintenance of a certain freezing tolerance during dehardening in early spring. The change from one phase to the next is mediated by complex interactions between temperature and photoperiod. This review aims at providing an overview of the interplay between phenology of leaves and species-specific freezing resistance. First, we address the long-term evolutionary responses that enabled temperate trees to tolerate certain low temperature extremes. We provide evidence that short term acclimation of freezing resistance plays a crucial role both in dormant and active buds, including re-acclimation to cold conditions following warm spells. This ability declines to almost zero during leaf emergence. Second, we show that the risk that native temperate trees encounter freeze injuries is low and is confined to spring and underline that this risk might be altered by climate warming depending on species-specific phenological responses to environmental cues.
The timing of phenological events exerts a strong control over ecosystem function and leads to multiple feedbacks to the climate system1. Phenology is inherently sensitive to temperature (although the exact sensitivity is disputed2) and recent warming is reported to have led