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Common garden comparison of the leaf-out phenology of woody species from different native climates, combined with herbarium records, forecasts long-term change
Abstract
A well-timed phenology is essential for plant growth and reproduction, but species-specific phenological strategies are still poorly understood. Here, we use a common garden approach to compare biannual leaf-out data for 495 woody species growing outdoors in Munich, 90% of them not native to that climate regime. For three species, data were augmented by herbarium dates for 140-year-long time series. We further meta-analysed 107 temperate-zone woody species in which leaf-out cues have been studied, half of them also monitored here. Southern climate-adapted species flushed significantly later than natives, and photoperiod- and chilling- sensitive species all flushed late. The herbarium method revealed the extent of species-specific climate tracking. Our results forecast that: (1) a northward expansion of southern species due to climate warming will increase the number of late flushers in the north, counteracting documented and expected flushing time advances; and (2) photoperiod- and chilling-sensitive woody species cannot rapidly track climate warming.
Supplementary resource (1)
... Apart from phylogeny, native climate, i.e., the climate in the native range of species, also affects plant phenology. Numerous studies have shown that species originating from higher latitudes leaf out earlier than species from lower latitudes when growing under identical conditions (Zohner and Renner, 2014;Zohner et al., 2016;Desnoues et al., 2017). However, it remains to be tested whether phylogeny affects autumn phenology and the relative importance of phylogeny and native climate on autumn phenology across species needs further investigation. ...
... However, the phenology extracted from remote sensing data is at the community scale, which majorly reflects the phenology of the vegetation canopy. In addition, plants may exhibit different phenology in diverse climate conditions due to their adaptation and plasticity (Zohner and Renner, 2014). For example, the climate in high elevations in Switzerland is more severe than in our studied areas (Bigler and Vitasse, 2021), so the plants in Switzerland might have adapted strongly to the drought and cold climate. ...
... This method of categorizing the native regions is relatively coarse and might result in uncertainty in detecting the native climate of species. Based on the available data, we could only refer to the approach of Zohner and Renner (2014), using continents with the most abundant occurrence records to represent native areas. More detailed information about the native range of species and more accurate classification of native regions through field survey and document compilation would be favored for future studies. ...
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.
... Several studies have demonstrated that different functional groups of plants have different environmental triggers for bud break (i.e. the timing of bud unfolding and start of leaf emergence), with temperate-zone woody species responding mainly to air temperature (Laube et al., 2014;Thomas et al., 2003;Zohner et al., 2016;Zohner & Renner, 2014), while perennial herbs appear to respond primarily to soil temperature and snow depth (Jánosi et al., 2020). ...
... Our finding that both trees and spring-flowering forest herbs advanced their spring phenology in response to warming temperatures is consistent with previous studies and suggests that the response of plants to rising temperatures could increase the length of the growing season in temperate deciduous forests (Jacques et al., 2015;Menzel et al., 2006;Zohner & Renner, 2014; although see Zani et al., 2020). For springflowering forest herbs, earlier emergence relative to tree leaf-out could increase fitness since they produce most of their photosynthates in spring before canopy closure (Dion et al., 2017;Heberling, Cassidy, et al., 2019;Jacques et al., 2015). ...
... 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.
... Climate warming has often been associated with advanced spring phenology, not only via observations (Wesołowski and Rowiński, 2006;Wood et al., 2006;Richardson et al., 2010;Zohner and Renner, 2014), but also through experiments (Hole, 2014) and modeling studies (Luedeling et al., 2013;Lange et al., 2016). Recently, however, a slowing down of spring phenology advancement has been documented (Fu et al., 2015). ...
... At this time buds are in the ecodormancy phase, where cold temperatures have only a minor effect on further reducing bud dormancy depth and warm temperatures have a stronger ability to reduce bud dormancy depth by fulfilling the forcing requirements and thus advancing budburst (Kramer, 1994). There is also evidence that early flushing species, such as Betula pendula, require shorter chilling periods to lower their bud dormancy depth than late successional species, such as Fagus sylvatica, which often require a longer cold period before warm temperatures advance bud break (Murray et al., 1989;Zohner and Renner, 2014). Furthermore, in F. sylvatica, short photoperiod additionally prevents rapid dormancy release to a larger extent as in other tree species (Vitasse and Basler, 2013;Malyshev et al., 2018), resulting in reduced sensitivity to warming periods earlier in the year when day length is still short. ...
... The additional chilling days in the control treatment were thus likely just as effective in decreasing the still high dormancy depth in F. sylvatica as the higher number of GDD in the warming treatment. Many studies have documented the high chilling requirements required to reduce dormancy depth in F. sylvatica compared with other tree species (Murray et al., 1989;Zohner and Renner, 2014;Malyshev et al., 2018), driven additionally by short photoperiod additionally reducing the rate of dormancy decrease in the species (Heide, 1993;Vitasse and Basler, 2013;Malyshev et al., 2018). Pioneer species such as B. pendula, which require few chilling days to release their dormancy (Heide, 2003), may therefore react more sensitively to future early spring warming periods, advancing their spring phenology to a greater extent. ...
The frequency of sudden, strong warming events is projected to increase in the future. The effects of such events on spring phenology of trees might depend on their timing because spring warming has generally been shown to advance spring budburst while fall and winter warming have been shown to delay spring phenology. To understand the mechanism behind timing-specific warming effects on spring phenology, I simulated warming events during fall, midwinter and at the end of winter and quantified their effects on bud dormancy depth and subsequently on spring leaf out. The warming events were carried out in climate chambers on tree seedlings of Betula pendula and Fagus sylvatica in October, January, and February. Control seedlings were kept at photoperiod and temperature matching the daily fluctuating field conditions. Warmed seedlings were kept 10 • C warmer than the control seedlings for 10 days during the respective warming periods. Warming in October increased bud dormancy depth and decreased spring leaf-out rate only for F. sylvatica, whereas warming in February reduced bud dormancy depth and advanced spring leaf-out rate only for B. pendula. Neither bud dormancy depth nor spring leaf out rate were affected by January warming. The results indicate that warming-induced changes in bud dormancy depth may explain species-and timing-specific warming effects on spring phenology. The extent to which the timing of bud dormancy phases is species-specific will influence among-species variation in future spring leaf out times.
... Shifts in the timing of annual growth cycles in temperate and boreal trees have direct impacts on global biogeochemical cycles (Keenan et al., 2014;Richardson et al., 2010), species distribution patterns (Chuine, 2010), and ultimately feedback to the climate system by affecting the atmospheric carbon budget (Richardson et al., 2013). There is broad consensus that warming trends over the past decades have led to an earlier arrival of spring leaf emergence in Northern Hemisphere trees, a trend that is enhancing global primary productivity under climate change (Keenan et al., 2014;Menzel & Fabian, 1999;Zohner & Renner, 2014). Depending Constantin M. Zohner and Lidong Mo should be considered joint first author. ...
... Depending Constantin M. Zohner and Lidong Mo should be considered joint first author. 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). ...
... Each of these factors is therefore likely to counteract the advances in spring leaf-out under a warming climate. Specifically, as the climate warms, the accumulated warming required for leaves to emerge is expected to increase because (a) warmer autumn temperatures delay the initiation of dormancy (Fu et al., 2014;Heide, 2003); (b) warmer winters lead to reduced chilling accumulation Zohner & Renner, 2014); and (c) days when spring warming occurs are becoming shorter (Fu et al., 2019;Heide, 1993b;Vitasse & Basler, 2013;Zohner & Renner, 2015; Figure 1). ...
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.
... Common garden studies, which transplant trees from a wide variety of historic climate conditions to a new location, act as pseudo-climate change experiments. Space-for-time substitutions in common garden studies include both warming and cooling scenarios when the common garden is placed near the center of the species' range (Liang, 2016;Steiner et al., 2021;Vitasse et al., 2010;Zohner & Renner, 2014). The spatial transfer to a common garden allows researchers to study the range-wide plasticity of phenology (i.e., the scale often detected by remote sensing) at a local scale. ...
... The spatial transfer to a common garden allows researchers to study the range-wide plasticity of phenology (i.e., the scale often detected by remote sensing) at a local scale. This can be used to distinguish adaptations to seed source conditions (via thermal accumulation and/or photoperiod requirements across the species' range) that lead to variation in population-level responses to interannual temperature variability at the common garden (Ford et al., 2017;Gerst et al., 2017;Liang, 2016;Savolainen et al., 2007;Zohner & Renner, 2014). Differences in phenological sensitivity, defined here as the magnitude of shifts in phenology per unit change in environmental condition (e.g., days per degree of warming, Wolkovich et al., 2021), may indicate whether certain populations exhibit a greater range of phenotypic plasticity that can promote fitness in response to climate change. ...
In a changing climate, the future survival and productivity of species relies on individual populations to respond to shifting environmental conditions. Many tree species including northern red oak (Quercus rubra) exhibit phenotypic plasticity, the ability to respond to changes in environmental conditions at within‐generation timescales, through varying traits such as leaf phenology. Phenotypic plasticity of phenology may vary among populations within a species’ range, and it is unclear if the range of plasticity is adequate to promote fitness. Here, we used a 58‐year‐old common garden to test whether northern red oak populations differ in phenological sensitivity to changes in temperature, and whether differences in phenological sensitivity are associated with differences in productivity and survival (proxies of fitness). We recorded eight years of spring leaf emergence and autumn leaf coloration and loss in 28 distinct populations from across the species’ full range. Across the 28 populations, spring leaf out consistently advanced in warmer years, but fall phenology was less responsive to changes in temperature. Southern, warm‐adapted populations had larger shifts in phenology in response to springtime warming but had lower long‐term survival. Moreover, higher phenological sensitivity to spring warming was not strongly linked to increased productivity. Instead, fitness was more closely linked to latitudinal gradients. Although springtime phenological sensitivity to climate change is common across northern red oak populations, responses of productivity and survival, which could determine longer‐term trajectories of species abundance, are more variable across the species’ range.
... Long-term data necessary to study these dynamics are limited, though herbaria are increasingly being used to study how phenology is changing in response to climate change (Davis et al., 2015;Heberling, Prather, et al., 2019;Lang et al., 2019;Meineke et al., 2018;Reeb et al., 2020;Zohner & Renner, 2014). Recent mass digitization of herbarium specimens has enabled easy access to millions of records of plant occurrence and phenology through time (Daru et al., 2017;Heberling, Prather, et a., 2019;Panchen et al., 2019;Soltis, 2017;Yost et al., 2018). ...
... Deciduous forests are commonly invaded by shade-tolerant woody shrubs (Martin et al., 2009), which also form a canopy over wildflowers. Non-native plants that have been introduced to new regions have evolved in different climate conditions and thus may have unique sensitivities to environmental cues that differ from native plants (Zohner & Renner, 2014). For example, many non-native plant species in North America occupy different phenological niches compared with native plants (Fridley, 2012;Gallinat et al., 2018;Gallinat et al., 2020;Reeb et al., 2020), and Reeb et al. (2020) found that native and non-native species had different phenological sensitivities to temperature and precipitation in Pennsylvania, USA. ...
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.
... In addition to phylogeny, plant phenology is strongly influenced by native climate (i.e., the climate in native range of species) of plant species. Several studies have elucidated the patterns and underlying mechanisms of adaptation to native climate of plant species in different regions (Zohner and Renner, 2014;Zohner et al., 2016). It has been demonstrated that species originating from higher latitudes leaf out earlier than contemporaries from lower latitudes under the same conditions (Zohner and Renner, 2014;Zohner et al., 2016). ...
... Several studies have elucidated the patterns and underlying mechanisms of adaptation to native climate of plant species in different regions (Zohner and Renner, 2014;Zohner et al., 2016). It has been demonstrated that species originating from higher latitudes leaf out earlier than contemporaries from lower latitudes under the same conditions (Zohner and Renner, 2014;Zohner et al., 2016). Unfortunately, only a few studies have attempted to quantify the relative contributions of phylogeny and native climate in determining the phenological traits among plant species. ...
The effects of climate change on plant phenology have been widely recognized around the world. However, the effect of plant internal factors (such as phylogeny) on the variations in phenology among plant species remains unclear. In this study, we investigated the phylogenetic conservatism in spring phenological traits using phylogenetic signal and evolutionary models, including Brownian motion (BM) model, Ornstein–Uhlenbeck (OU) model and white noise (WN) model, based on the phenological data of 48 temperate plant species in Northeast China. We also explored the relative contributions of phylogeny and adaptation to native climate (i.e., the climate in native range of species) to the variations in the phenological traits among species using phylogenetic eigenvector regression and variance partitioning analysis. The results showed thatspring phenological traits conformed to the OU model, indicating thatspring traits were phylogenetically conserved. The effect of phylogeny on flowering traits was stronger than that on leaf-out traits. Additionally, the adaptation to native climate contributed more to the variations in spring phenological traits among species than phylogeny, and adaptation to native climate explained more variations in leaf-out traits than in flowering traits. Our results suggested that the spring phenological traits were constrained by both phylogeny and adaptation to native climate. However, the adaptation to native climate had a stronger effect on the variations in phenological traits than phylogeny. Therefore, the degree of similarity in spring phenological traits across closely related species depends on the degree of similarity in the environmental conditions where these close relatives are distributed.
... Supporting this, multiple studies now show that the threshold of forcing needed for budburst depends on the sum of chilling over the fall and winter and also the photoperiod experienced in the spring (e.g. Zohner & Renner, 2014;Flynn & Wolkovich, 2018). Higher forcing is generally needed, given the lower chilling (Fig. 2) and shorter photoperiods (Basler & K€ orner, 2014;Fu et al., 2019). ...
... Although a few studies estimated interaction terms (e.g. Zohner & Renner, 2014), most studies did not, likely because of the increased effort in study design. In addition to needing enough controlled environments to apply a full-factorial design, the statistical power needed to robustly estimate an interaction is much greater than a simple main effect (such as the effect of forcing or photoperiod alone)requiring a 16 times greater sample size (Gelman et al., 2020). ...
Climate change has advanced plant phenology globally 4‐6 days per °C on average. Such shifts are some of the most reported and predictable biological impacts of rising temperatures. Yet as climate change has marched on, phenological shifts have appeared muted over recent decades—failing to match simple predictions of an advancing spring with continued warming. The main hypothesis for these changing trends is that interactions between spring phenological cues—long‐documented in lab environments—are playing a greater role in natural environments due to climate change. Here we argue that accurately linking shifts observed in long‐term data to underlying phenological cues is slowed by biases in observational studies and limited integration of insights from lab studies. We synthesize seven decades of lab experiments to quantify how phenological cue‐space has been studied and how treatments compare to shifts caused by climate change. Most studies focus on one cue, limiting our ability to make accurate predictions, but some well‐studied forest species offer opportunities to advance forecasting. We outline how greater integration of controlled environment studies with long‐term data could drive a new generation of lab experiments, built on physiological insights, that would transform our fundamental understanding of phenology and improve predictions.
... The latter is often viewed as an insurance against untimely bud break that could lead to fatal consequences (for example, frost damage) during autumn and winter 43 . Nonetheless, we found that incorporation of photoperiod (Methods) into the Unified model significantly improved its performance in capturing LUD at only a few locations (Extended Data Fig. 10), even for F. sylvatica, which has been reported as being among the species most sensitive to photoperiod 44,45 , although there was a very modest decrease in model error (Extended Data Fig. 10). Besides photoperiod, some studies suggest that frosts in late winter and early spring may exert strong control over the bud phenology of several specific species [46][47][48] . ...
... The range for optimization of parameter e was set to 0-5 with a prior value of 1.56. The revised Unified model was then applied to F. sylvatica, which has been reported to be among the species most sensitive to photoperiod 44,45 . The performance of both the default and revised Unified models in capturing LUDs was evaluated using RMSE (equation (5)) and the Akaike information criterion (AIC) (equation (16)), which considers both the goodness of fit and the number of free model parameters (n param ): ...
Changes in winter and spring temperatures have been widely used to explain the diverse responses of spring phenology to climate change. However, few studies have quantified their respective effects. Using 386,320 in situ observations of leaf unfolding date (LUD) of six tree species in Europe, we show that accelerated spring thermal accumulation and changes in winter chilling explain, on average, 61% and 39%, respectively, of the advancement in LUD for the period 1951–2019. We find that winter warming may not have delayed bud dormancy release, but rather it has increased the thermal requirement in reaching leaf unfolding. This increase in thermal requirement and the decreased efficiency of spring warming for thermal accumulation partly explain the weakening response of leaf unfolding to warming. Our study stresses the need to better assess the antagonistic and heterogeneous effects of winter and spring warming on leaf phenology, which is key to projecting future vegetation–climate feedbacks.
... This is consistent with previous findings that trees from the south usually require a greater heat sum accumulation before budburst and leaf-out than trees from the north (Olson et al. 2013;Sanz-Pérez et al. 2009). This would also explain the phenomenon where species adapted to more southern climates leaf-out later than native species in a more northerly common garden, as was shown in one common garden study in the Munich Botanical Garden (Zohner and Renner 2014). There, the southern species flushed on average 15 days later than the native species, likely because they had greater forcing needs than more northern species (Zohner and Renner 2014). ...
... This would also explain the phenomenon where species adapted to more southern climates leaf-out later than native species in a more northerly common garden, as was shown in one common garden study in the Munich Botanical Garden (Zohner and Renner 2014). There, the southern species flushed on average 15 days later than the native species, likely because they had greater forcing needs than more northern species (Zohner and Renner 2014). ...
Aims
The mechanisms regulating spring phenology have been extensively studied in angiosperm species. However, given that gymnosperms and angiosperms diverged 300 million years ago, phenology may be triggered by different cues in gymnosperm species. The regulatory mechanisms of phenology in subtropical regions remain largely unknown. In combination, it remains untested whether subtropical gymnosperm species have chilling requirements and are photosensitive.
Methods
We conducted a climate chamber experiment with three chilling and three photoperiod treatments to investigate budburst during an 8-week forcing period. We tested whether budburst of eight gymnosperms species (Cryptomeria japonica, Cunninghamia lanceolata, Cupressus funebris, Ginkgo biloba, Metasequoia glyptostroboides, Pinus massoniana, Pseudolarix amabilis, and Podocarpus macrophyllus) was photoperiod sensitive or has strong chilling requirements and whether photoperiod or chilling was more important for advancing budburst.
Important Findings
Chilling advanced budburst and increased the percentage of budburst for gymnosperm species. Gymnosperm species required moderate chilling days to advance budburst. Interestingly, the forcing requirement for gymnosperm species was higher than that for angiosperms in the same forest, suggesting that gymnosperms may need more cumulative forcing to initiate budburst than do angiosperms. Compared to temperate gymnosperm species in Germany (194-600 °C days), the subtropical species studied here had a much higher forcing requirement (814-1150 °C days). The effects of photoperiod were minor, suggesting that chilling outweighs photoperiod in advancing budburst of gymnosperm species in this subtropical region. These results reveal that increased winter temperatures with continued global warming may impact not only angiosperms but also gymnosperms, leading to their delayed spring budburst.
... To summarize, in temperate tree species, BB results from the succession of two phases: i) breaking endodormancy by the fulfilment of chilling temperature requirements and ii) the accumulation of warm temperatures (forcing temperature) during the ecodormancy phase (Lang et al., 1987). The temperature requirements during the two phases are species-specific (Kramer, 1995;Chuine and Cour, 1999;Morin et al., 2009;Vitasse et al., 2009a;Basler and Körner, 2014;Schuster et al., 2014;Zohner and Renner, 2014;Dantec et al., 2014;Laube et al., 2014;Fu et al., 2015). Moreover, in some tree species like beech, photoperiod may also interact with temperature to determine bud-burst date, though the mechanisms of this interaction remain unclear (Heide, 1993;Partanen et al., 1999;Körner and Basler, 2010;Vitasse and Basler, 2013;Basler and Körner, 2014;Laube et al., 2014;Hamilton et al., 2016;Fu et al., 2019b). ...
... Finally, phenology is also controlled by complex interactions between genetic and environmental factors. Indeed, studies on beech species have shown differences in leaf phenology among populations from a large climatic gradient within the distribution area of species (Von Wuelish et al., 1995;Zohner and Renner, 2014;Harter et al., 2015;Schueler and Liesebach, 2015;Kramer et al., 2017) or along altitudinal clines (Vitasse et al., 2009a;Vitasse et al., 2009b). These results suggest that leaf phenology in beech trees is adapted to large variations in climatic conditions, and this capacity could help populations to cope with climate change. ...
Bud-burst and leaf-senescence determine the length of the growing season for deciduous trees and therefore the duration of potential carbon assimilation with consequences on biomass production. In Fagus sylvatica L., leaf phenology depends on both photoperiod and temperature. The future climate is expected to induce more frequent soil water deficits and biotic attacks (possibly resulting in severe defoliation). The aim of the study is to assess whether these constrains may alter leaf phenology. In a common garden, we sowed seeds collected from six beech forests along a small latitudinal gradient (140 km) in North-Eastern France. In 2014, after seven years growth, a rain exclusion was installed above the trees to test how recurrent soil water deficits impacted bud-burst (BB) and leaf-yellowing (LY) over three years. We also analyzed the response of leaf phenology to annual defoliation, aiming at affecting carbon and nitrogen availability in trees. Delayed BB and early LY were observed, reducing the growing season (GS) until 14 days in response to soil water deficit whereas no influence of defoliation was detected. These time lags were not in relation with leaf nitrogen content. In the control treatment, BB occurred earlier and LY later in the northernmost populations than in the southernmost without clear relationships with local climate. A significant treatment x population interaction was observed revealing a plasticity in the leaf phenology response to soil water deficit among populations. These results suggest that beech trees present a genetic differentiation of leaf phenology even within a small latitudinal gradient but that these differentiations could be disrupted by soil water deficit that is predicted to increase in the future.
... Temperature is an important driver of biodiversity at different scales. For instance, it affects the development of animals (Gillooly and Dodson, 2000) and plants (Porter and Delecolle, 1988), phenology (Zohner and Renner, 2014;MacCannell and Staples, 2021), reproductive success (Monasterio et al., 2013) and behavior (Caraco et al., 1990;Angiulli et al., 2020). These responses to temperature, in turn, influence species interactions (Kordas et al., 2011) and shape species diversity (Condamine et al., 2012;Zhou et al., 2016), composition (Macek et al., 2019) and distribution (Woodward, 1988;Repasky, 1991), which ultimately affects ecosystem functioning (García et al., 2018). ...
Forest canopies buffer the macroclimate and thus play an important role in mitigating climate-warming impacts on forest ecosystems. Despite the importance of the tree layer for understory microclimate buffering, our knowledge about the effects of forest structure, composition and their interactions with macroclimate is limited, especially in mixtures of conifers and broadleaves. Here we studied five mixed forest stands along a 1800 km latitudinal gradient covering a 7 • C span in mean annual temperature. In each of these forests we established 40 plots (200 in total), in which air and soil temperatures were measured continuously for at least one year. The plots were located across gradients of forest density and broadleaved proportions (i.e. from open to closed canopies, and from 100% conifer to 100% broadleaved tree dominance). Air minimum, mean and maximum temperature offsets (i.e. difference between macroclimate and microclimate) and soil mean temperature offsets were calculated for the coldest and warmest months. Forest structure, and especially forest density, was the key determinant of understory temperatures. However, the absolute and relative importance of the proportion of broadleaves and forest density differed largely between response variables. Forest density ranged from being independent of, to interacting with, tree species composition. The effect of these two variables was independent of the macroclimate along our latitudinal gradient. Temperature, precipitation, snow depth and wind outside forests affected understory temperature buffering. Finally, we found that the scale at which the overstory affects soil microclimate approximated 6-7 m, whereas for air microclimate this was at least 10 m. These findings have implications for biodiversity conservation and forest management in a changing climate, as they facilitate the projection of understory temperatures in scenarios where both forest structure and macroclimate are dynamic. This is especially relevant given the global importance of ongoing forest conversion from conifers to broadleaves, and vice versa.
... For example, Burton and Cumming (1995) used 3.5, 2.1, and 3.7°C as base temperatures for the above three species, respectively, although those values were inferred from very coarse species range distributions. Other studies continue to use the standard definition of "growing degree-days" with a 5°C base temperature for the accumulation of heat sums as a predictor of leaf flush (e.g., Zohner & Renner, 2014). It is further F I G U R E 1 A spring fire (April 2018) in broadleaf-dominated woodland in Prince Alberta National Park, Saskatchewan. ...
The window between snow melt and leaf flush in broadleaf trees defines a critical period of wildfire susceptibility, especially in western boreal forests. Questions remain about how a warming climate might affect those two processes that bookend the spring fire season.
... Accordingly, it is a reliable indicator of interannual and interdecadal environmental changes such as climate change (Schwartz 2003, Morin et al. 2009). For example, warming due to climate change has advanced the start of the growing season in many plant species (e.g., Rötzer et al. 2004, Menzel et al. 2006, Zohner and Renner 2014. However, an earlier budburst (spring leaf-out) can also have a negative impact on the water cycle, as it induces earlier plant transpiration and soil moisture reduction, thereby increasing the probability of water deficiency (Lian et al. 2020). ...
The current state of knowledge on bud dormancy is limited. However, expanding such knowledge is crucial in order to properly model forest responses and feedback to future climate. Recent studies have shown that warming can decrease chilling accumulation and increase dormancy depth, thereby inducing delayed budburst in European beech (Fagus sylvatica L). Whether fall warming can advance spring phenology is unclear. To investigate the effect of warming on endodormancy of deciduous trees, we tested the impact of mild elevated temperature (+ 2.5-3.5 °C; temperature on average kept at 10 °C) in mid- and late autumn on bud dormancy depth and spring phenology of beech. We studied saplings by inducing periods of warming in greenhouses during two years. Even though warming reduced chilling in both years, we observed that the response of dormancy depth and spring budburst were year-specific. We found that warming during endodormancy peak could decrease bud dormancy depth and therefore advance spring budburst. This effect appears to be modulated by factors such as the date of senescence onset and forcing intensity during endodormancy. Results from this study suggest that not only chilling, but also forcing controls bud development during endodormancy, and that extra forcing in autumn can offset reduced chilling.
... The climate calibration method introduced in this study does not require data from common gardens (Zohner & Renner 2014, Liang 2015 or controlled experiments (Hänninen et al. 2019, Zhang et al. 2022) that are often unavailable for many species. Instead, the calibration method can be applied to more widely available observational data collected through citizen science programs such as Nature's Notebook of the USA-NPN (Crimmins et al. 2021). ...
Phenological models are needed for forecasting plant and ecosystem responses to climate change. Due to a lack of considering local adaptation induced variations in climatic requirements of plant species for phenological development, traditional uniform/non-spatial models that cover broad geographic regions are susceptible to systematic prediction biases. This study presents a climate calibration method that incorporates climate adaptation patterns of plant species into a widely used Spring Index (SI) First Leaf (FL) model. Multi-year (2009-2021) phenological observation data for a most frequently observed shrub species(common lilac Syringa vulgaris) and a most frequently observed tree species(red maple Acer rubrum) in the eastern USA from the USA-National Phenology Network (USA-NPN) were used to develop and validate the calibrated models. Climatic gradients defined by latitudinal temperature variations were used to predict varied climatic requirements of the populations of each species. Prior to calibration, SI FL predictions showed consistent geographic biases and yielded large prediction errors (especially for red maple, RMSE = 30 d). Calibrated SI FL predictions yielded reduced errors (e.g. RMSE = 16 d for red maple) and were freed from significant geographic biases (α = 0.05) in all cases. The calibration method accounted for both intraspecific and interspecific variations, leading to more accurate broad-scale first leaf predictions for the species tested. The climate-calibrated SI FL allows for more accurate tracking of the onset of spring over extensive geographic areas and would support spatially explicit natural resource and environmental conservation efforts under climate change.
... To adapt to seasonal changes in climate, temperate plants have evolved specific developmental rhythms and phenology (Basler and Körner, 2014). Recent climatic changes have dramatically altered plant phenophases, such as leaf unfolding, flowering, and leaf senescence (Zohner and Renner, 2014;Ge et al., 2015;Menzel et al., 2020). With phenological change (e.g., earlier budburst), the risk of frost damage may increase accordingly (Hänninen and Tanino, 2011;Richardson et al., 2018). ...
Woody plant species in temperate regions must withstand a cold winter and freezing events through cold acclimation and dormancy in autumn and winter. However, how seasonal changes in dormancy depth and cold hardiness affect the frost risk of temperate species is unclear because few studies have assessed dormancy depth and cold hardiness simultaneously. In this study, an experiment was conducted to estimate the dormancy depth and cold hardiness of five common woody temperate plant species during the winter of 2018/2019 in Beijing, China. Twigs of each species were collected at different dates during winter and the timing of budburst was monitored under the same forcing conditions. The dormancy depth was quantified as growing degree day (GDD) requirements of spring events. Simultaneously, the cold hardiness of buds at each sampling date was determined based on the electrical conductivity of the holding solution. Two indices (chilling accumulation and cold hardiness index) were used to simulate the past dynamics of dormancy depth, spring phenology, and cold hardiness from 1952 to 2021. The maximum dormancy depth of the study species was observed between early October and early December, and thereafter decreased exponentially. The cold hardiness peaked in mid-winter (end of December) through cold acclimation and thereafter decreased in spring (deacclimation). During the past 70 years, the budburst date (first flowering date or first leaf date) of five species was estimated to have advanced significantly, and dormancy depth in early spring was predicted to have increased owing to the warming-associated decrease in chilling accumulation. However, cold hardiness has decreased because of weakened acclimation and accelerated deacclimation under a warming climate. The frost risk before and after budburst remained unchanged because of the reduction in occurrence and severity of low-temperature events and earlier late spring frosts. The present methods could be generalized to estimate and predict the seasonal changes in dormancy depth and cold hardiness of temperate species in the context of climate change.
... Herbarium collections comprise large geographical, temporal and taxonomic depth and have been used to great effect in temperate zone investigations of phenology (Davis et al., 2015;Gallinat et al., 2018;Park et al., 2019;Willis, Ellwood, et al., 2017;Willis, Law, et al., 2017;Zohner & Renner, 2014). ...
Plant phenology has been shifting dramatically in response to climate change, a shift that may have significant and widespread ecological consequences. Of particular concern are tropical biomes, which represent the most biodiverse and imperilled regions of the world. However, compared to temperate floras, we know little about phenological responses of tropical plants because long‐term observational datasets from the tropics are sparse.
Herbarium specimens have greatly increased our phenological knowledge in temperate regions, but similar data have been underutilized in the tropics and their suitability for this purpose has not been broadly validated. Here, we compare phenological estimates derived from field observational data (i.e. plot surveys) and herbarium specimens at various spatial and taxonomic scales to determine whether specimens can provide accurate estimations of reproductive timing and its spatial variation.
Here, we demonstrate that phenological estimates from field observations and herbarium specimens coincide well. Fewer than 5% of the species exhibited significant differences between flowering periods inferred from field observations versus specimens regardless of spatial aggregation. In contrast to studies based on field records, herbarium specimens sampled much larger geographic and climatic ranges, as has been documented previously for temperate plants, and effectively captured phenological responses across varied environments.
Synthesis . Herbarium specimens are verified to be a vital resource for closing the gap in our phenological knowledge of tropical systems. Tropical plant reproductive phenology inferred from herbarium records is widely congruent with field observations, suggesting that they can and should be used to investigate phenological variation and their associated environmental cues more broadly across tropical biomes.
... species. For example, Zohner and Renner 6,23 have contributed valuable insights into interspecific variation in plant phenology using woody plants growing in European botanical gardens. It is unknown, however, if the variation in woody plant phenology found in common garden experiments are also observed at large scales, for forest trees growing in their natal environment, and across long time periods 24 . ...
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.
... This may be due to the colder and less predictable winter and spring climates of the northeastern USA. Sensitive phenological tracking of temperatures early in the year can pose large risks to reproductive success, because warm periods are often followed by chilling in this area (Zohner & Renner, 2014;Park et al., 2019). By contrast, temperatures are higher, and the advent and progression of seasons are less variable, in the southern range of C. virginica, and thus a sensitive phenological response poses less of a risk. ...
Plant–pollinator mutualisms rely upon the synchrony of interacting taxa. Climate change can disrupt this synchrony as phenological responses to climate vary within and across species. However, intra‐ and interspecific variation in phenological responses is seldom considered simultaneously, limiting our understanding of climate change impacts on interactions among taxa across their ranges.
We investigated how variation in phenological sensitivity to climate can alter ecological interactions simultaneously within and among species using natural history collections and citizen science data. We focus on a unique system, comprising a wide‐ranged spring ephemeral with varying color morphs ( Claytonia virginica ) and its specialist bee pollinator ( Andrena erigeniae ).
We found strongly opposing trends in the phenological sensitivities of plants vs their pollinators. Flowering phenology was more sensitive to temperature in warmer regions, whereas bee phenology was more responsive in colder regions. Phenological sensitivity varied across flower color morphs. Temporal synchrony between flowering and pollinator activity was predicted to change heterogeneously across the species' ranges in the future.
Our work demonstrates the complexity and fragility of ecological interactions in time and the necessity of incorporating variation in phenological responses across multiple axes to understand how such interactions will change in the future.
... In Munich, Constantin ended up studying almost 500 woody species (permanently outdoors) from numerous genera, families, with 85% of them not native in Central Europe. The results revealed, for the first time, the permanent footprint that adaptation to local climate leaves on the phenology of tree species (Zohner and Renner 2014). We titled our paper 'common garden comparison of the leaf-out phenology of woody species from different native climates, combined with herbarium records, forecasts long-term change' because we realized that for longlived species, botanical gardens are equivalent to common garden experiments in giving us the power to separate genotype and phenotype, an experimental approach first developed in the 1930s by one of the fathers of the study of plant adaptation, Göte Turesson, working on bud burst and autumn leaf senescence in Sweden, and Clausen et al. (1940), working in California. ...
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.
... • C higher than 1850-1900, with greater warming of 1.59 • C over the land area (IPCC 2021). As sensitive indicators of climate change, plant phenological events, such as leaf unfolding, flowering and leaf senescence, exhibited a significant trend to a different extent and directions (Zohner and Renner 2014, Gill et al. 2015, Fu et al. 2018, characterized by a widespread advance of spring events and an inconspicuous delay in autumn events (Fu et al. 2014, Polgar et al. 2014, Ge et al. 2015, Menzel et al. 2020. These shifts in plant phenology altered the carbon uptake capacity of terrestrial ecosystems (Keenan et al. 2014, Piao et al. 2017) and affected water and energy fluxes between ecosystems and the atmosphere (Milla et al. 2004, Peñuelas et al. 2009, Richardson et al. 2013, Jin et al. 2017. ...
Temperature and photoperiod are two major environmental cues shaping the leaf senescence of temperate tree species. However, how the control of leaf senescence is split between photoperiod and temperature is unknown for many ecologically important species. Here, we conducted a growth chamber experiment to test the effects of temperature (6, 9, 18, and 21°C) and photoperiod (8 and 16h daylength) on leaf senescence of two temperate tree species (Quercus mongolica and Larix principis-rupprechtii) distributed in montane forest of China. The results showed that low temperature (LT) alone could induce leaf senescence of both species under long daylength (LD) conditions, but the leaf senescence of L. principis-rupprechtii was more sensitive to the decrease in temperature than that of Q. mongolica under the LD condition. Short daylength (SD) alone could only induce the leaf senescence of L. principis-rupprechtii, suggesting that the photoperiod sensitivity varies between species. SD could accelerate the LT-induced senescence, but the effect of SD reduced with the decrease in temperature. Based on these findings, we developed a new autumn phenology model by incorporating interspecific differences in the photoperiod sensitivity of leaf senescence. Compared with the three existing process-based autumn phenology models, the new model was more robust in simulating the experimental data. When employing these models to available long-term phenological data, our new model also performed best in reproducing the observed leaf senescence date of two closely related species (Quercus robur and Larix decidua). These results enhance our understanding of how LT and SD control leaf senescence. The prediction of the climate change impacts on forest carbon uptake could be improved by incorporating this new autumn phenological model into the terrestrial biosphere models.
... Furthermore, we found that the temperature response of leaf phenology was significantly larger than that of flowering phenology, implying that later phenophases are associated with a larger temperature sensitivity across the two studied species. This is likely related to a conservation strategy to avoid early spring frost damage due to a higher temperature variability in early spring (Vitasse and Basler, 2014;Zohner and Renner, 2014). Flowers were more sensitive to frost than leaves because perennials have evolved to invest in strategies that ensure survival and growth rather than reproduce (CaraDonna and Bain, 2016;Neuner, 2014), and thus may develop a relatively smaller temperature sensitivity than leaf to avoid more severe damage under early spring frost. ...
The timing of flowering (FL) and leaf unfolding (LU) determine plants’ reproduction and vegetative growth. Global warming has substantially advanced FL and LU of temperate and boreal plants, but their responses to warming differ, which may influence the time interval between FL and LU (ΔLU-FL), thereby impacting plant fitness and intraspecific physiological processes. Based on twigs collected from two flowering-first tree species, Populus tomentosa and Amygdalus triloba, we conducted a manipulative experiment to investigate the effects of winter chilling, spring warming and photoperiod on the ΔLU-FL. We found that photoperiod did not affect the ΔLU-FL of Amygdalus triloba, but shortened ΔLU-FL by 5.1 d of Populus tomentosa. Interestingly, spring warming and winter chilling oppositely affected the ΔLU-FL of both species. Specifically, low chilling accumulation extended the ΔLU-FL by 3.8 and 9.4 d for Populus tomentosa and Amygdalus triloba, but spring warming shortened the ΔLU-FL by 4.1 and 0.2 d °C−1. Our results indicate that climate warming will decrease or increase the ΔLU-FL depending on the warming periods, i.e., spring or winter. The shifted time interval between flowering and leaf unfolding may have ecological effects including affecting pollen transfer efficiency and alter the structure and functioning of terrestrial ecosystem.
... The gradual deformation of plant areas occurs because of global climate changes [1][2][3]. These processes are closely related to early onset [4,5] and an increase in the total duration of the growing season [6,7]. ...
The object of research was the species, varieties and forms of the genus Robinia: R. viscosa var. hartwegii (Koehne) Ashe; R. neomexicana var. rusbyi; R. neomexicana f. pale pink; R. neomexicana f. pale purple; R. pseudoacacia L.; R. pseudoacacia f. pyramidalis (Pepin) Rehd.; R. pseudoacacia f. umbraculifera (DC) Rehd. and R. pseudoacacia x R. neomexicana, growing in the dendrological collections of the Federal Research Center of Agroecology, Russian Academy of Sciences. Most of the phenological phases of representatives of the genus Robinia occur at the optimal time for the seasonal development of flowering woody plants. This genus belongs to the group of late beginners and late terminators of the growing season. The indicator of phenological atypicality (+1 - 0) is in the lower half of the normal area, and for some species and forms (R. viscosa var. Hartwegii, R. pseudoacacia f. Pyramidalis, R. pseudoacacia f. Umbraculifera) at the edge of the normal area (+ 0.8 - +1). The research area for these introduced species is the northern border of the wide range of culture and their further promotion to regions with a more severe climate is possible only in experimental plantations or as an additional assortment. The most winter-hardy were the varieties, forms and hybrids of R. neomexicana with a phenological atypicality index from +0.3 to +0.35. We can recommend these plants for widespread use even in the northern regions of the Volgograd region due to their potential winter hardiness. The study of seasonal rhythms revealed the periods of maximum decorativeness of representatives of the generic complex Robinia, and a comparative characteristic in terms of the beginning and end of flowering. The authors found that R. viscosa var hartwegii has the longest flowering period.
... A few studies in both categories have begun to investigate sources of intraspecific variation in phenological sensitivity (Matthews and Mazer 2016;Song et al. 2020). The third category is represented by studies that compare the sensitivities derived from herbarium specimen data to those derived from highresolution field observations (Robbirt et al. 2011;Davis et al. 2015;Zohner and Renner 2014) or from remotely sensed data (Park 2012) to determine the reliability of the former, which are known to include sampling biases of various kinds (taxonomic, geographic, seasonal, and temporal; Daru et al. 2017). ...
To date, most herbarium-based studies of phenological sensitivity to climate and of climate-driven phenological shifts fall into two categories: detailed species-specific studies vs. multi-species investigations designed to explain inter-specific variation in sensitivity to climate and/or the magnitude and direction of their long-term phenological shifts. Few herbarium-based studies, however, have compared the phenological responses of closely related taxa to detect: (1) phenological divergence, which may result from selection for the avoidance of heterospecific pollen transfer or competition for pollinators, or (2) phenological similarity, which may result from phylogenetic niche conservatism, parallel or convergent adaptive evolution, or genetic constraints that prevent divergence. Here, we compare two widespread Clarkia species in California with respect to: the climates that they occupy; mean flowering date, controlling for local climate; the degree and direction of climate change to which they have been exposed over the last 115 yr; the sensitivity of flowering date to inter-annual and to long-term mean maximum spring temperature and annual precipitation across their ranges; and their phenological change over time. Specimens of C. cylindrica were sampled from sites that were chronically cooler and drier than those of C. unguiculata, although their climate envelopes broadly overlapped. Clarkia cylindrica flowers 3.5 d earlier than C. unguiculata when controlling for the effects of local climatic conditions and for quantitative variation in the phenological status of specimens. However, the congeners did not differ in their sensitivities to the climatic variables examined here; cumulative annual precipitation delayed flowering and higher spring temperatures advanced flowering. In spite of significant spring warming over the sampling period, neither species exhibited a long-term phenological shift. Precipitation and spring temperature interacted to influence flowering date: the advancing effect on flowering date of high spring temperatures was greater in dry than in mesic regions, and the delaying effect of high precipitation was greater in warm than in cool regions. The similarities between these species in their phenological sensitivity and behavior are consistent with the interpretation that facilitation by pollinators and/or shared environmental conditions generate similar patterns of selection, or that limited genetic variation in flowering time prevents evolutionary divergence between these species.
... year ( (Ducousso et al., 1996), and are probably related to the higher risk of late frost in northern populations as it is the case in the French Atlantic range of maritime pine (see also, e.g., Alberto et al., 2013;Zohner & Renner, 2014). Such clines in spring phenology along climate gradients suggested local adaptation due to divergent selection, which might suffer mismatch with changing climate conditions (Alberto et al., 2013;Badeck et al., 2004;Lindner et al., 2010). ...
Forest ecosystems are increasingly challenged by extreme events, e.g. drought, storms, pest attacks and fungal pathogen outbreaks, causing severe ecological and economic losses. Understanding the genetic basis of adaptive traits in tree species is of key importance to preserve forest ecosystems, as genetic variation in a trait (i.e. heritability) determines its potential for human-mediated or evolutionary change. Maritime pine (Pinus pinaster Aiton), a conifer widely distributed in south-western Europe and north-western Africa, grows under contrasted environmental conditions promoting local adaptation. Genetic variation at adaptive phenotypes, including height, spring phenology and susceptibility to two fungal pathogens (Diplodia sapinea and Armillaria ostoyae) and an insect pest (Thaumetopoea pityocampa), were assessed in a range-wide clonal common garden of maritime pine. Broad-sense heritability was significant for height (0.219), spring phenology (0.165-0.310) and pathogen susceptibility (necrosis length caused by D. sapinea, 0.152; and by A. ostoyae, 0.021, measured on inoculated, excised branches under controlled conditions), but not for pine processionary moth incidence in the common garden. The correlations of trait variation among populations revealed contrasting trends for pathogen susceptibility to D. sapinea and A. ostoyae with respect to height. Taller trees showed longer necrosis length caused by D. sapinea while shorter trees were more affected by A. ostoyae. Moreover, maritime pine populations from areas with high summer temperatures and frequent droughts were less susceptible to D. sapinea but more susceptible to A. ostoyae. Finally, an association study using 4,227 genome-wide SNPs revealed several loci significantly associated to each trait (range of 3-26), including a possibly disease-induced translation initiation factor, eIF-5, associated to needle discoloration caused by D. sapinea. This study provides important insights to develop genetic conservation and breeding strategies integrating species responses to biotic stressors.
... In contrast, the mechanisms regulating phenology in subtropical ecoregions remains largely unknown across all seasons (Chen et al. 2017, Du et al. 2019). In such regions, temperatures rarely decline below 5°C, which is needed for temperate plants to meet their winter chilling requirements (Ghelardini et al. 2010, Vitasse and Basler 2013, Laube et al. 2014, Zohner and Renner 2014, Fu et al. 2015a, Chuine et al. 2016, Zohner et al. 2016. Thus, subtropical plants are often not exposed to the low temperatures involved in winter chilling for temperate plants. ...
Climate‐driven changes in phenology have widespread effects on ecological interactions and species' abundances. Most predictions of changes in phenology and the consequences for ecology and conservation are based on research in temperate systems. Climate‐driven changes in phenology are largely undocumented in subtropical regions, which host much of the world's biodiversity. Factors important to regulating phenology in temperate systems (e.g. winter chilling requirements) are likely weak or absent in subtropical ecosystems; plant phenology in these regions could respond to climate differently than in the temperate zone. Here we examine flowering phenology data for 105 plant species based on herbarium specimens and photographs from 1911 to 2015 in the southern subtropical Nanling region in south China. Temperatures in this region warmed 0.3°C over the 105‐year study period, and most plant species flowered earlier over time, although species varied substantially in the magnitude of phenological response to warming temperatures. Spring flowering times advanced in response to warming temperatures in late summer and early autumn and in early spring, with late summer and early autumn temperatures having almost twice as strong an effect on spring flowering times as early spring temperatures (−4.7 versus −2.5 days °C−1). This strong effect of late summer and early autumn temperatures is very different from temperate systems and has substantial implications for anticipating future changes in phenology. The temperatures in late summer and early autumn may affect spring phenology by accelerating bud formation or initial growth. Warming January temperature delayed summer flowering and advanced winter flowering. Increases in precipitation during April to June also tended to delay summer flowering. Autumn flowering species showed inconsistent responses to warming. These results highlight important differences between climate‐driven changes in phenology in temperate and subtropical areas. Understanding these differences will be important in understanding the effects of climate change on vegetation phenology and ecosystem processes.
... More recently, large-scale digitization of natural history collections [20], citizen science programs [21], and the advent of remotely sensed land surface phenology measurements via satellite [22] have facilitated research at more extensive taxonomic, spatial, and temporal scales, some of which integrates multiple methods [23][24][25]. Much of this new work suggests that phenologies and their responses to climate change are heterogeneous within communities and across landscapes, varying both within and among species [26][27][28][29][30][31]. Interpreting and synthesizing these diverse phenological patterns across taxonomic, temporal, and spatial scales is important for understanding their causes and making realistic predictions under climate change. ...
Phenology, or the timing of life history events, can be heterogeneous across biological communities and landscapes and can vary across a wide variety of spatiotemporal scales. Here, we synthesize information from landscape phenology studies across different scales of measurement around a set of core concepts. We highlight why phenology is scale dependent and identify gaps in the spatiotemporal scales of phenological observations and inferences. We discuss the consequences of these gaps and describe opportunities to address the inherent sensitivities of phenological metrics to measurement scale. Although most studies we review and discuss are focused on plants, our work provides a broadly relevant overview of the role of observation scale in landscape phenology and a general approach for measuring and reporting scale dependence.
... 3. Improved access to herbarium specimens, photographs, and other historical records Access to herbarium specimens, photographs, and historic observations is dramatically improving and researchers are identifying new ways to use them to provide data critical to climate change research, often at botanical gardens (Zohner & Renner, 2014;Willis et al., 2017;Younis et al., 2018;Pearson et al., 2020). In the past, researchers had to visit herbaria in person to examine large numbers of herbarium specimens covering broad regions. ...
Botanical gardens make unique contributions to climate change research, conservation, and public engagement. They host unique resources, including diverse collections of plant species growing in natural conditions, historical records, expert staff, and large numbers of visitors and volunteers. Networks of botanical gardens spanning biomes and continents can expand the value of these resources. Over the past decade, research at botanical gardens has advanced our understanding of climate change impacts on plant phenology, physiology, anatomy, and conservation. For example, researchers have utilized botanical garden networks to assess anatomical, and functional traits associated with phenological responses to climate change. New methods have enhanced the pace and impact of this research, including phylogenetic and comparative methods, and online databases of herbarium specimens and photographs that allow studies to expand geographically, temporally, and taxonomically in scope. Botanical gardens have grown their community and citizen science programs, informing the public about climate change and monitoring plants more intensively than possible with garden staff alone. Despite these advances, botanical gardens are still underutilized in climate change research. To address this, we review recent progress and describe promising future directions for research and public engagement at botanical gardens.
... Therefore, Chilling Hours (CH, referred to as chilling) and Growing Degree Hours (GDH, referred to as spring forcing) of different species at each site were calculated in this study. CH was calculated as the accumulated hours (0 to 5°C) from November 1st (the starting day for CH in the northern hemisphere; Fu et al., 2015;Zohner and Renner, 2014) to April 7th (the averaged LUD of all sites in this study). GDH was calculated as the accumulated hours (above 5°C) from February 1st Vitasse et al., 2018) to April 7th. ...
Temperature is the primary factor controlling plant phenology. As temperature changes with latitude, leaf phe-nology in spring always shows a significant latitudinal pattern. However, under asymmetric warming at the low and high latitudes, the variability of the spring leaf phenology with latitude is becoming unclear. Based on the 23,094 observations of the leaf unfolding date (LUD) for woody species located in eastern China within latitudes 23-49°N, we analyzed the variability of LUD and its latitudinal sensitivity (S lat , days°N −1 , expressed in delayed days per degree in latitude) during 1963-2008. The results showed an earlier LUD at the mid-(−2.2 days decade −1) and high (−2.5 days decade −1) latitude regions, while a stable LUD at the low-latitude regions during 1963-2008. However, the temperature sensitivity of LUD (S T , days°C −1 , expressed in advanced days per degree in temperature) remained stable across the latitudes although a slight decreasing trend from 1963 to 2008. As a result, the non-uniform optimal preseason warming with latitude (T lat ,°C°N −1 , expressed in the increase of temperature per degree in latitude) decreased S lat from 2.38 (days°N −1) in 1963 to 1.55 (days°N −1) in 2008. Further analyses indicated that the Growing Degree Hours (GDH) played a critical role in these processes, although the Chilling Hours (CH) showed significant variability after 1991. Our results provide evidence that the change in the balance of CH and GDH across latitude induced declining S lat over the last 40 years in eastern China. Furthermore , it may continue under the future climate warming scenarios and ultimately has important consequences on the structure and function of ecosystems.
... These include long-term observational datasets , statistical modeling (Zhao et al. 2013), climate-change experiments (Chung et al. 2013), genetic and epigenetic studies (Kudoh 2016), common garden studies, and reciprocal transplant experiments which frequently incorporate common gardens . Common gardens can either look at many accessions of one species grown together (the focus of this study), or many species of disparate origin planted in a single location (Zohner and Renner 2014); cross-species common gardens are important to understand wide phenological patterns but are not considered here. These methods sometimes have apparently contradictory results about what cueing mechanisms trigger phenological responses (Vitasse and Basler 2013) and species' sensitivity to increased temperatures (Wolkovich et al. 2012). ...
Trees are particularly susceptible to climate change due to their long lives and slow dispersal. However, trees can adjust the timing of their growing season in response to weather conditions without evolutionary change or long-distance migration. This makes understanding phenological cueing mechanisms a critical task to forecast climate change impacts on forests. Because of slow data accumulation, unconventional and repurposed information is valuable in the study of phenology. Here, I develop and use a framework to interpret what phenological patterns among provenances of a species in a common garden reveal about their leafing cues, and potential climate change responses. Species whose high elevation/latitude provenances leaf first likely have little chilling requirement, or for latitude gradients only, a critical photoperiod cue met relatively early in the season. Species with low latitude/elevation origins leafing first have stronger controls against premature leafing; I argue that these species are likely less phenologically flexible in responding to climate change. Among published studies, the low to high order is predominant among frost-sensitive ring-porous species. Narrow-xylemed species show nearly all possible patterns, sometimes with strong contrasts even within genera for both conifers and angiosperms. Some also show complex patterns, indicating multiple mechanisms at work, and a few are largely undifferentiated across broad latitude gradients, suggesting phenotypic plasticity to a warmer climate. These results provide valuable evidence on which temperate and boreal tree species are most likely to adjust in place to climate change, and provide a framework for interpreting historic or newly-planted common garden studies of phenology.
... A caveat in using a common garden approach to assess evolutionary relationships between reproductive defenses and phenological traits is that reproductive structures formed at different times throughout the growing season will form under different environmental conditions, such as temperature. However, in a common garden experiment, species should segregate by phenology relative to their behavior in native habitat in response to the temperature and photoperiod thresholds that control phenology (Premoli et al., 2007;Panchen et al., 2014;Zohner and Renner, 2014;Mason et al., 2017). Here in Cornus, flowering start date in the Arnold Arboretum was strongly positively correlated with the average native habitat maximum temperature of the warmest month (R 2 = 0.52, Appendix S10), suggesting a temperature-based control of budbreak and flowering phenology among dogwood species that has been previously demonstrated within C. florida (Reader, 1975) and C. sericea (Kobayashi and Fuchigami, 1983). ...
Premise:
Defense investment in plant reproductive structures is relatively understudied compared to the defense of vegetative organs. Here the evolution of chemical defenses in reproductive structures is examined in light of the optimal defense, apparency, and resource availability hypotheses within the genus Cornus using a phylogenetic comparative approach in relation to phenology and native habitat environmental data.
Methods:
Individuals representing 25 Cornus species were tracked for reproductive phenology over a full growing season at the Arnold Arboretum of Harvard University. Floral, fruit, and leaf tissue was sampled to quantify defensive chemistry as well as fruit nutritional traits relevant to bird dispersal. Native habitat environmental characteristics were estimated using locality data from digitized herbarium records coupled with global soil and climate data sets.
Results:
The evolution of later flowering was correlated with increased floral tannins, and the evolution of later fruiting was correlated with increased total phenolics. Leaves were found to contain the highest tannin activity, while inflorescences contained the highest total flavonoids. Multiple aspects of fruit defensive chemistry were correlated with fruit nutritional traits. Floral and fruit defensive chemistry were evolutionarily correlated with aspects of native habitat temperature, precipitation, and soil characteristics.
Conclusions:
Results provide tentative support for the apparency hypothesis with respect to both flower and fruit phenology, while relative concentrations of secondary metabolites across organs provide mixed support for the optimal defense hypothesis. The evolution of reproductive defense with native habitat provides, at best, mixed support for the resource availability hypothesis.
... Because spring temperatures vary more in North America than Europe and Asia , invasive plants in the United States are often more responsive to temperature cues than their native associates (Wolkovich and Cleland 2011). This plasticity could provide invasive plants with a fitness advantage under future climate conditions (Wolkovich and Cleland 2011;Cleland et al. 2012;Zohner and Renner 2014). The situation maybe be further exasperated because the invasive species in this study are native to warmer climates than their Minnesotan associates (Table S9 from ESM) and plants from southern latitudes often react more strongly to spring warming (Morin et al. 2007). ...
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.
... 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.
... At the other two sites, the Virginia Depot and the Botanical Garden, species diversity over the past 20 years has increased in similar proportion (Table 2). Winters in Munich have become shorter by 4 weeks over the past 100 years (Zohner and Renner 2014), and warmer springs and summers have led to a significant increase in particular plant and insect species, including fig trees, which now establish spontaneously, and various species of Mediterranean Echium. Some species of bees are currently expanding their ranges in southern Germany, including Anthidiellum strigatum, Anthophora bimaculata, Eucera nigrescens, Halictus scabiosae, Halictus subauratus, Hoplitis adunca, Osmia cornuta, and Xylocopa violacea . ...
Previous work has shown that among 428 species of bees occurring in Germany, decline or extinction over the past 40 years have been correlated with late-season emergence and restricted habitats, while other factors, such as pollen specialization, body size, nesting sites, and sociality, played no role in models that included a phylogeny of these bees. Doing best are spring-flying, city-dwelling species. Building on these results, we here investigate changes in bee diversity from the 1990s to 2018 at three protected sites within the city perimeter of Munich, focusing on the correlates of flight season (spring or summer), flight duration (in months), and number of habitats (one or two vs. three to six). Local species pools were assessed against the total species pool from 1795 onwards. Twenty years ago, 150 species were present at one or more of the sites, while in 2017/2018, this was true of 188 species, with the increase at two sites being of similar proportion. In two of the three areas, broad habitat use was positively correlated with persistence. Flight season or duration had no statistical effect. These results underscore the function of urban protected sites in bee conservation and imply that summer food shortages, which negatively affect bees in agricultural areas, play no role in urbanized regions so that late-season flight is not an extinction handicap.
... Copenhagen herbarium, C; Florence herbarium, FLO; Munich herbarium, M; Herbarium Senckenbergianum Frankfurt, F; Stockholm herbarium, S). While all specimens of these species were photographed, only specimens in the initial leaf-out stage were used for further analysis, which was defined as (a) not all leaves entirely unfolded and (b) leaves not yet full sized (Everill, Primack, Ellwood, & Melaas, 2014;Zohner & Renner, 2014). For specimens that met these criteria, we recorded species name, collection date and collection location. ...
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.
Predicting spring phenology in temperate forests is critical for forecasting important processes such as carbon storage. One major forecasting method for phenology is the growing degree day (GDD) model, which tracks heat accumulation. Forecasts using GDD models typically assume that the GDD threshold for a species is constant across diverse landscapes, but increasing evidence suggests otherwise. Shifts in climate with anthropogenic warming may change the required GDD. Variation in climate across space may also lead to variation in GDD requirements, with recent studies suggesting that fine-scale spatial variation in climate may matter to phenology. Here, we combine simulations, observations from an urban and a rural site, and Bayesian hierarchical models to assess how consistent GDD models of budburst are across species and space. We built GDD models using two different methods to measure climate data: on-site weather stations and local dataloggers. We find that estimated GDD thresholds can vary up to 20% across sites and methods. Our results suggest our studied urban site requires fewer GDDs until budburst and may have stronger microclimate effects than the studied rural site, though these effects depend on the method used to measure climate. Further, we find that GDD models are less accurate for early-active species and may become less accurate with warming. Our results suggest that local-scale forecasts based on GDD models for spring phenology should incorporate these inherent accuracy issues of GDD models, alongside the variations we found across space, species and warming. Testing whether these issues persist at larger spatial scales could improve forecasts for temperate forests.
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. Our findings reveal 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.
The relevance is due to the introduction of the subtropical fruit crop Zizyphus jujuba (unabi) to the Volgograd region. For the first time in the conditions of the Volgograd region, the material on the biochemical properties of various varieties of unabi fruits was analyzed and generalized.
The ranking of shrubs by change to conditions is based on the fixation of environmental factors and the bioecology of plant individuals based on their physiological and biochemical parameters in field and laboratory conditions.
The purpose of the research is to rank the shrubs according to the degree of resistance to stress factors.
The objects are plant genotypes of Z. jujuba: large-fruited, medium-fruited and small-fruited. Experimental plantings with their participation are cultivated at the collection site of the Federal Research Center of Agroecology of the Russian Academy of Sciences (Volgograd, Russia).
Today plants often flower earlier due to climate warming. Herbarium specimens are excellent witnesses of such long‐term changes. However, the magnitude of phenological shifts may vary geographically, and the data are often clustered. Therefore, large‐scale analyses of herbarium data are prone to pseudoreplication and geographical biases.
We studied over 6000 herbarium specimens of 20 spring‐flowering forest understory herbs from Europe to understand how their phenology had changed during the last century. We estimated phenology trends with or without taking spatial autocorrelation into account.
On average plants now flowered over 6 d earlier than at the beginning of the last century. These changes were strongly associated with warmer spring temperatures. Flowering time advanced 3.6 d per 1°C warming. Spatial modelling showed that, in some parts of Europe, plants flowered earlier or later than expected. Without accounting for this, the estimates of phenological shifts were biased and model fits were poor.
Our study indicates that forest wildflowers in Europe strongly advanced their phenology in response to climate change. However, these phenological shifts differ geographically. This shows that it is crucial to combine the analysis of herbarium data with spatial modelling when testing for long‐term phenology trends across large spatial scales.
The rate of global warming varies in magnitude between seasons, with warming being more pronounced in winter and spring than in summer and autumn at high latitudes. Winter warming can have profound effects on dormancy release and spring phenology of perennial fruit crops, but potential follow-on impacts on growth, fruit yield or quality have only rarely been investigated. We studied the effects of mild winter warming on spring phenology, current year shoot growth, cropping performance and fruit quality in four field-grown cultivars of blackcurrant with different chilling requirements. Plants were exposed to ambient or slightly elevated (+ 0.5 °C) temperatures from early October to mid-April the following year. Winter warming had few effects on spring phenology and fruit yield, but caused significant changes in berry contents of phenolic compounds and a reduction in soluble sugars. Increased vegetative growth of warmed plants likely accounts for the changes in berry quality. The results demonstrate a persistent effect of winter warming on shoot growth, which indirectly changes fruit quality.
Spring leaf phenology and its response to climate change have crucial effects on surface albedo, carbon balance, and the water cycle of terrestrial ecosystems. Based on long‐term (period 1963–2014) in situ observations of budburst date and leaf unfolding date of more than 300 deciduous woody species from 32 sites across the temperate zone in China, we conducted model‐data comparison of spatial and temporal variations for spring leaf phenology calculated using the phenology modules that were embed into 10 existing terrestrial ecosystem models. Our results suggested that ORganizing Carbon and Hydrology in Dynamic EcosystEms and Spatially Explicit Individual‐Based performed the best in reproducing the spatial patterns of spring leaf phenology, but tended to underestimate the temporal variations in responding to temperature warming, showing low interannual variability (IAV) and temperature sensitivity (ST). In contrast, the performances of Vegetation Integrated SImulator for Trace Gases were the best in modeling IAV and ST. BIOME3, Lund‐Potsdam‐Jena model, Joint UK Land Environment Simulator, BioGeochemical Cycles, Community Land Model, Integrated Biosphere Simulator, and Commonwealth Scientific and Industrial Research Organisation Atmosphere Biosphere Land Exchange Model failed to reproduce both the spatial and temporal patterns. Using temperature series (1960–2100) form Coupled Model Intercomparison Project Number 6 scenarios to force the 10 phenology modules, our results highlighted large uncertainties in predicting spring leaf phenology changes with the warming climate, and more work is required to deal with the deficiencies of phenology model parameters and algorithms.
The role of trees in city cooling has warranted much attention based on concerns over climate change and urban expansion. Simultaneously, there is an interest in introducing trees from dry habitats to cope with the increasing risks of drought under climate change, especially for roadside plantings. Some of their adaptations to drought, however, are assumed to come at the expense of biomass production and transpiration and thus their cooling capacity. This potential trade-off has been investigated in a two-year nursery experiment by measuring the water use and biomass production of six species and cultivars originating from different habitats in terms of water availability.
Spring phenology of temperate forest trees has advanced substantially over the last decades due to climate warming, but this advancement is slowing down despite continuous temperature rise. The decline in spring advancement is often attributed to winter warming, which could reduce chilling and thus delay dormancy release. However, mechanistic evidence of a phenological response to warmer winter temperatures is missing. We aimed to understand the contrasting effects of warming on plants leaf phenology and to disentangle temperature effects during different seasons. With a series of monthly experimental warming by ca. 2.4 °C from late summer until spring, we quantified phenological responses of forest tree to warming for each month separately, using seedlings of four common European tree species. To reveal the underlying mechanism, we tracked the development of dormancy depth under ambient conditions as well as directly after each experimental warming. In addition, we quantified the temperature response of leaf senescence. As expected, warmer spring temperatures led to earlier leaf-out. The advancing effect of warming started already in January and increased towards the time of flushing, reaching 2.5 days/°C. Most interestingly, however, warming in October had the opposite effect and delayed spring phenology by 2.4 days/°C on average; despite six months between the warming and the flushing. The switch between the delaying and advancing effect occurred already in December. We conclude that not warmer winters but rather the shortening of winter, i.e. warming in autumn, is a major reason for the decline in spring phenology.
Changes in winter and spring temperatures have been widely used to explain the diverse responses of spring phenology to climate change. However, our understanding of their respective roles remain incomplete. Using >300,000 in situ observations of leaf unfolding date (LUD) in Europe, we show that the advancement of LUD since 1950 is due both to accelerated spring thermal accumulation and changes in winter chilling which explain 61% and 39% of the LUD shifts, respectively. Winter warming did not substantially retard the releasing of bud dormancy, but increased the thermal requirement to reach leaf unfolding. The increase of thermal requirement and decreased efficiency of spring warming on accelerating thermal accumulation partly explained the temporally (1950s-2010s) decreasing response of LUD to warming. Our study stresses the need to better assess the antagonistic and heterogeneous effects of winter and spring warming on leaf phenology, which is key to projection of future vegetation-climate feedbacks.
Premise:
Long-term observations show that flowering phenology has shifted in many lineages in response to climate change. However, it remains unclear whether these results can be generalized to predict the presence, direction, or magnitude of responses in lineages for which we lack long time-series data. If phenological responses are phylogenetically conserved, we can extrapolate from species for which we have data to predict the responses of close relatives. While several studies have found that closely related species flower at similar times, fewer have evaluated whether phylogenetically proximal species respond to environmental change similarly.
Methods:
We paired flowering time data from 3161 manually scored herbarium specimens of 72 species of grasses (Poaceae) with historical climate data and analyzed the phylogenetic signal and phylogenetic half-life of phenological sensitivity. We also ran these analyses on a subset of species showing statistically significant sensitivities, in order to assess the role of sampling bias on phylogenetic signal.
Results:
Closely related grass species tend to flower at similar times, but flowering times respond to temperature changes in species-specific ways. We also show that only including species for which there is strong evidence of phenological shifts results in overestimating phylogenetic signal.
Conclusions:
In agreement with other recent studies, our results suggest caution in extrapolating from evidence of phylogenetic similarity to predicting shared responses in this ecologically relevant trait. Future work is needed to better understand the discrepancy between the phylogenetic signal in observed phenological shifts and absence of such signal in sensitivity.
Earlier leaf‐out and later autumn leaf senescence under climate warming have been linked to increases in plant productivity and ecosystem carbon uptake. Yet, despite the potential implications of shifting phenology for plant carbon uptake, the degree to which phenological changes affect overall plant growth and the partitioning between above‐ and below‐ground biomass remains unclear.
Here we use a 3‐year experiment to quantify changes in root and shoot growth of three woody plant species (two common European tree species, Fagus sylvatica and Quercus robur , and one shrub Lonicera xylosteum ) under spring and autumn warming.
In both tree species, the magnitude—and in Quercus even the direction—of the effects of growing‐season length on growth depends on whether the warming happened in spring or in autumn. Each day earlier leaf‐out in response to warming resulted in total biomass increases of 0.8%–2.5%, whereas delayed senescence led to reductions of 0.2%–2.1%. Advances in leaf‐out also led to increased root‐to‐shoot biomass ratios because root growth was proportionally more stimulated than shoot growth. In the shrub species, earlier leaf‐out had no effect, while delayed senescence led to increases in root, but not shoot, biomass.
Synthesis . The strong asymmetry between growth responses to spring versus autumn phenology demonstrates that growing‐season length per se is a weak indicator of individual‐level tree productivity. The results further imply that phenological shifts are reshaping the functional balance between above‐ and below‐ground growth, which is critical for quantifying forest carbon dynamics under climate change.
Premise:
Climate change is having major impacts on alpine and arctic regions, and inter-annual variations in temperature are likely to increase. How increased climate variability will impact plant reproduction is unclear.
Methods:
In a 4-year study on fruit production by an alpine plant community in northern Sweden, we applied three warming regimes: (1) a static level of warming with open-top chambers (OTC), (2) press warming, a yearly stepwise increase in warming, and (3) pulse warming, a single-year pulse event of higher warming. We analyzed the relationship between fruit production and monthly temperatures during the budding period, fruiting period, and whole fruit production period and the effect of winter and summer precipitation on fruit production.
Results:
Year and treatment had a significant effect on total fruit production by evergreen shrubs, Cassiope tetragona, and Dryas octopetala, with large variations between treatments and years. Year, but not treatment, had a significant effect on deciduous shrubs and graminoids, both of which increased fruit production over the 4 years, while forbs were negatively affected by the press warming, but not by year. Fruit production was influenced by ambient temperature during the previous-year budding period, current-year fruiting period, and whole fruit production period. Minimum and average temperatures were more important than maximum temperature. In general, fruit production was negatively correlated with increased precipitation.
Conclusions:
These results indicate that predicted increased climate variability and increased precipitation due to climate change may affect plant reproductive output and long-term community dynamics in alpine meadow communities.
Experimental warming studies in natural communities have become an
increasingly common method to estimate plant responses to global climate
change. Many of these efforts focus on plant species' phenology-a
sensitive indicator of species responses to climate-and show advances in
spring timing with increasing temperatures. To be useful, however,
results from warming experiments should match responses to climate
change observed in unmanipulated plant communities, including the
responses due to anthropogenic warming that has already occurred. Here
we present a comprehensive synthesis of phenological responses to
climate change for both experiments and long-term monitoring of natural
plant communities. By comparing 14 long-term monitoring datasets with 36
experimental warming studies spanning four continents and 1560 species,
we estimate that warming experiments underpredict, by 8.2 and 4.6X (for
flowering and leafing, respectively), plant responses to warming when
compared to long-term observations. The warming experiments also failed
to reproduce the greater temperature sensitivity observed in populations
of wild species that flower early in the spring. Further, when
considering species for which we had data from both study-types,
experiments failed to predict both the magnitude and direction of
phenological responses. Among these species, warming experiments
predicted a delay of flowering, not the well-documented advance that has
tracked recent warming in the observational records. This discrepancy
appears unrelated to study length and degree of warming, Instead a
number of known artifacts associated with warming experiments could lead
to underestimated plant sensitivities. We recommend ways in which the
design, documentation and analysis of future experimental and
observational studies can be improved to estimate and to predict more
accurately plant phenological responses to climate change.
Phylogeography posits that the sequence of speciation events within a clade should parallel the geographic migration and isolation of members of the clade through time. The primary historical features that govern migration and allopatry in land plants are changes in physical geography (e.g., oceans, mountains, and deserts) and in climate (e.g., moisture, temperature, and day length), features that are often interrelated. If we assume that living genera retain physiological stability through time, much as they retain the morphological features that allow their identification, then these environmental features of the geologic past may be used to test phylogeographic hypotheses of living genera based on phylogenetic analysis. The history of the climatic and geographic features of the Tertiary of the Northern Hemisphere agrees with many phylogenetically based phylogeographic hypotheses of living angiosperm genera but indicates that some hypotheses require reanalysis. While the parallel comparison of phylogenetic hypotheses and historical biogeographic evidence is in its infancy, the reciprocal illumination of the two approaches shows great promise for future application.
Time of spring leaf emergence varies consistently among deciduous tree species in the north temperate forests of both E North America and Eurasia. Tree species that leaf earliest have only narrow-diameter xylem vessels (diffuse-porous wood anatomy) and relatively low numbers of vessels per unit wood volume, eg most members of the genera Populus, Betula, Salix, Alnus, Ostrya, Acer, Carpinus, Prunus and Aesculus. Later-leafing trees are characterized by having distinctly larger-diameter xylem vessels produced in their early, spring wood (ring-porous wood anatomy) and/or, especially in diffuse-porous species, relatively high numbers of vessels per unit wood volume. Both these traits contribute to greater maximum potential water conduction capacity. Among diffuse-porous species earlier leafing is also associated with greater indeterminancy of shoot growth; the earliest-leafing taxa initially flush only a few early leaves followed by a series of individual morphologically distinct late leaves on some shoots through the summer (heterophylly). Cambial activity must precede leaf emergence in ring-porous species; this explains the relatively late leafing of ring-porous genera like Fraxinus, Quercus, Rhus, Ulmus, Sassafras, Morus, Maclura, Carya and Juglans. -from Author
1 The Marsham phenological data have been 'rediscovered' several times. This unique data set, spanning two centuries, consists of first dates of observation, or 'indications of spring', for 27 phenological events which relate to over 20 species of plants and animals. 2 This paper extends the 1926 appraisal of the data from 1736 to 1925 by adding the 22 years up to 1947, when publication of the record ceased. 3 The Marsham data are examined in relation to Manley's central England monthly temperature data and Craddock's annual rainfall data and are further examined for unexplained trends over time. 4 Most of the phenological variables were significantly related to climatic variables or changed through time. 5 An appraisal of the historical response of flora and fauna to climate was made and allowed us to predict changes in species performance due to climate change in the future. If commonly used climate scenarios are accurate we predict that most or all of the indications of spring noted in the Marsham record will occur earlier in the calendar year.
Premise of the study:
Numerous long-term studies in seasonal habitats have tracked interannual variation in first flowering date (FFD) in relation to climate, documenting the effect of warming on the FFD of many species. Despite these efforts, long-term phenological observations are still lacking for many species. If we could forecast responses based on taxonomic affinity, however, then we could leverage existing data to predict the climate-related phenological shifts of many taxa not yet studied.
Methods:
We examined phenological time series of 1226 species occurrences (1031 unique species in 119 families) across seven sites in North America and England to determine whether family membership (or family mean FFD) predicts the sensitivity of FFD to standardized interannual changes in temperature and precipitation during seasonal periods before flowering and whether families differ significantly in the direction of their phenological shifts.
Key results:
Patterns observed among species within and across sites are mirrored among family means across sites; early-flowering families advance their FFD in response to warming more than late-flowering families. By contrast, we found no consistent relationships among taxa between mean FFD and sensitivity to precipitation as measured here.
Conclusions:
Family membership can be used to identify taxa of high and low sensitivity to temperature within the seasonal, temperate zone plant communities analyzed here. The high sensitivity of early-flowering families (and the absence of early-flowering families not sensitive to temperature) may reflect plasticity in flowering time, which may be adaptive in environments where early-season conditions are highly variable among years.
A considerable number of studies have investigated the phenology of European beech using models, experimental controlled conditions, or descriptive surveys of patterns in situ. In spite of this interest, there is no consensus about the environmental factors controlling bud burst in beech, especially about the role of photoperiod and chilling temperature (cold temperature effective to release bud dormancy). However, recent experimental and modelling studies provide new insights into the means by which these environmental factors control beech phenology. This present contribution aims to reconcile contradictory hypotheses about the main environmental factors controlling bud burst date of European beech. First, we review the main published results on the environmental control of beech phenology both in controlled and in natural conditions. Second, supported by the findings of recent studies, we propose a new theory for the role of photoperiod during the chilling phase for explaining spatial and temporal variations in bud burst phenology of European beech. Examples using long-term data from the Swiss Alps and Germany are presented to support this theory. The possible impacts of future and ongoing climate warming on beech phenology are discussed. Finally, due to interactions between chilling, forcing temperature, and photoperiod, we assert that beech phenology follows a nonlinear trend across biogeographical gradients such as changes in elevation or latitude and that the bud burst date of beech is expected not to undergo significant changes in response to global warming, especially in warmer climates.
In a previous paper we presented an update of the highly referenced climate classification map, that of Wladimir Koppen, which was published for the first time in 1900 and updated in its latest version by Rudolf Geiger in 1961. This updated world map of Koppen-Geiger climate classification was based on temperature and precipitation observations for the period 1951-2000. Here, we present a series of digital world maps for the extended period 1901-2100 to depict global trends in observed climate and projected climate change scenarios. World maps for the observational period 1901-2002 are based on recent data sets from the Climatic Research Unit (CRU) of the University of East Anglia and the Global Precipitation Climatology Centre (GPCC) at the German Weather Service. World maps for the period 2003-2100 are based on ensemble projections of global climate models provided by the Tyndall Centre for Climate Change Research. The main results comprise an estimation of the shifts of climate zones within the 21st century by considering different IPCC scenarios. The largest shifts between the main classes of equatorial climate (A), arid climate (B), warm temperate climate (C), snow climate (D) and polar climate (E) on global land areas are estimated as 2.6-3.4 % (E to D), 2.2-4.7 % (D to C), 1.3-2.0 (C to B) and 2.1-3.2 % (C to A).
Question: How strong are climate warming-driven changes within mid-elevation forest communities? Observations of plant community change within temperate mountain forest ecosystems in response to recent warming are scarce in comparison to high-elevation alpine and nival ecosystems, perhaps reflecting the confounding influence of forest stand dynamics.Location: Jura Mountains (France and Switzerland).Methods: We assessed changes in plant community composition by surveying 154 Abies alba forest vegetation relevés (550-1,350 m a.s.l.) in 1989 and 2007. Over this period, temperatures increased while precipitation did not change. Correspondence analysis (CA) and ecological indicator values were used to measure changes in plant community composition. Relevés in even- and uneven-aged stands were analysed separately to determine the influence of forest stand dynamics. We also analysed changes in species distribution to detect shifts along the elevation gradient by focusing on the lowest, central and highest positions of lowland and mountain species altitudinal ranges.Results: We found significant shifts along the first CA axis, which reflected a change in plant community composition towards a greater frequency of lowland species. Analyses of ecological indicator values indicated increases in temperature and light availability in A. alba stands, particularly in even-aged stands. However, no major changes in overall species distribution were found.Conclusions: The community-level changes are consistent with effects of climate warming and local stand dynamics. Changes in species distribution were small in comparison to observed local temperature increases, perhaps reflecting dispersal limitation, phenotypic plasticity or microclimatic buffering by the tree canopy. Causality cannot rigorously be inferred from such a descriptive study; however, we suggest that recent warming is now driving plant community change in the climatically more moderate mid-elevation forest setting.
Warming experiments are increasingly relied on to estimate plant responses to global climate change. For experiments to provide meaningful predictions of future responses, they should reflect the empirical record of responses to temperature variability and recent warming, including advances in the timing of flowering and leafing. We compared phenology (the timing of recurring life history events) in observational studies and warming experiments spanning four continents and 1,634 plant species using a common measure of temperature sensitivity (change in days per degree Celsius). We show that warming experiments underpredict advances in the timing of flowering and leafing by 8.5-fold and 4.0-fold, respectively, compared with long-term observations. For species that were common to both study types, the experimental results did not match the observational data in sign or magnitude. The observational data also showed that species that flower earliest in the spring have the highest temperature sensitivities, but this trend was not reflected in the experimental data. These significant mismatches seem to be unrelated to the study length or to the degree of manipulated warming in experiments. The discrepancy between experiments and observations, however, could arise from complex interactions among multiple drivers in the observational data, or it could arise from remediable artefacts in the experiments that result in lower irradiance and drier soils, thus dampening the phenological responses to manipulated warming. Our results introduce uncertainty into ecosystem models that are informed solely by experiments and suggest that responses to climate change that are predicted using such models should be re-evaluated.
Consequences of climate warming on tree phenology are readily observable, but little is known about the differences in phenological sensitivity to temperature between species and between populations within a species. The aim of the present study is to compare phenological sensitivities to temperature of seven woody species between each other and within-species between two geographical areas using both altitudinal and temporal gradients (Abies alba, Acer pseudoplatanus, Carpinus betulus, Fagus sylvatica, Fraxinus excelsior, Ilex aquifolium and Quercus petraea). The timing of leaf unfolding was monitored (i) over 2 years along two altitudinal gradients in the Pyrénées mountains (six species), and (ii) over 22 years in Fontainebleau forest (four species). Three species were present in both areas which allowed us to compare their phenological sensitivity to temperature over altitudinal and temporal gradients. Along altitudinal gradients, we observed for all species an advance in leaf unfolding with decreasing elevation, ranging from 11 to 34 days 1000 m−1 for beech and oak, respectively. Across the temporal gradient, we found significant advances in leaf unfolding for oak (−0.42 days year−1) and ash (−0.78 days year−1) since 1976, whereas no significant advance was observed for beech and hornbeam. For both gradients and for all species, significant correlations were found between leaf unfolding dates and temperature, except for beech in the temporal study. Moreover, we highlighted that phenological sensitivity to temperature was very similar between the two geographically separated populations (Pyrénées and Fontainebleau forests). Thus, oak had the strongest sensitivity (−7.48 and −7.26 days °C−1 in altitudinal and temporal gradient, respectively) and beech had the lowest (−2.09 and −2.03 days °C−1). Our results suggest that population sensitivity to global warming might be stable for a given species, in spite of its possible local adaptation.
The most frequently used climate classification map is that of Wladimir Köppen, presented in its latest version 1961 by Rudolf Geiger. A huge number of climate studies and subsequent publications adopted this or a former release of the Köppen-Geiger map. While the climate
classification concept has been widely applied to a broad range of topics in climate and climate change research as well as in physical geography, hydrology, agriculture, biology and educational aspects, a well-documented update of the world climate classification map is still missing. Based
on recent data sets from the Climatic Research Unit (CRU) of the University of East Anglia and the Global Precipitation Climatology Centre (GPCC) at the German Weather Service, we present here a new digital Köppen-Geiger world map on climate classification, valid for the second half of
the 20 century.
German
Die am häufigsten verwendete Klimaklassifikationskarte ist jene von Wladimir Köppen, die in der letzten Auflage von Rudolf Geiger aus dem Jahr 1961 vorliegt. Seither bildeten viele Klimabücher und Fachartikel diese oder eine frühere Ausgabe
der Köppen-Geiger Karte ab. Obwohl das Schema der Klimaklassifikation in vielen Forschungsgebieten wie Klima und Klimaänderung aber auch physikalische Geographie, Hydrologie, Landwirtschaftsforschung, Biologie und Ausbildung zum Einsatz kommt, fehlt bis heute eine gut dokumentierte
Aktualisierung der Köppen-Geiger Klimakarte. Basierend auf neuesten Datensätzen des Climatic Research Unit (CRU) der Universität von East Anglia und des Weltzentrums für Niederschlagsklimatologie (WZN) am Deutschen Wetterdienst präsentieren wir hier eine neue digitale
Köppen-Geiger Weltkarte für die zweite Hälfte des 20. Jahrhunderts.
Museum specimens collected in the past may be a valuable source of information on the response of species to climate change. This idea was tested by comparing the flowering times during the year 2003 of 229 living plants growing at the Arnold Arboretum in Boston, Massachusetts, USA, with 372 records of flowering times from 1885 to 2002 using herbarium specimens of the same individual plants. During this period, Boston experienced a 1.5°C increase in mean annual temperature. Flowering times became progressively earlier; plants flowered 8 d earlier from 1980 to 2002 than they did from 1900 to 1920. Most of this shift toward earlier flowering times is explained by the influence of temperature, especially temperatures in the months of February, March, April, and May, on flowering time. Plants with a long flowering duration appear to be as useful for detecting responses to changing temperatures as plants with a short flowering duration. Additional studies using herbarium specimens to detect responses to climate change could examine specimens from specific, intensively collected localities, such as mountain peaks, islands, and unique habitats.
Phenological events such as bud burst, flowering, and senescence have received increased interest in the light of global warming
(1–3). Spring events at temperate latitudes have advanced by 2.5 days per decade since 1971 (4). As global warming progresses, how will it affect the arrival of spring and the length of the growing season?
Dormancy release as influenced by duration of outdoor winter chilling in Florence (Italy) was studied under different photoperiodic and temperature treatments in collected twigs of two European (Ulmus glabra Huds. and Ulmus minor Mill.) and four Asian (Ulmus pumila L., Ulmus parvifolia Jacq., Ulmus macrocarpa Hance and Ulmus villosa Brandis) elm clones. Photoperiod had no effect on dormancy release, and there was no evidence that photoperiod affected bud burst during quiescence in the studied elm clones. Thermal time (day degrees >0 degrees C) to bud burst decreased in all the clones with increasing outdoor chilling. Although all the clones exhibited a rather weak dormancy, they significantly differed from each other. Dormancy was released earlier in the Asian than in the European clones, and the clones could be ranked from the U. pumila clone (very weak and short dormancy) to the U. minor clone (relatively stronger and longer dormancy), the other clones being intermediate. In all the clones except U. minor, the observed decrement in thermal time to bud burst was efficiently explained as an inverse exponential function of the number of chill days < or =5 degrees C received outdoor in autumn and winter. Endodormancy, as measured by the single-node cuttings test, was weak and short in all the clones. The latter result suggests that correlative inhibitions were largely responsible for preventing bud burst during winter in these elm clones.
Changes in phenology (seasonal plant and animal activity driven by environmental factors) from year to year may be a sensitive and easily observable indicator of changes in the biosphere. We have analysed data from more than 30 years of observation in Europe, and found that spring events, such as leaf unfolding, have advanced by 6 days, whereas autumn events, such as leaf colouring, have been delayed by 4.8 days. This means that the average annual growing season has lengthened by 10.8 days since the early 1960s. These shifts can be attributed to changes in air temperature.
Although now over 100 years old, the classification of climate originally formulated by Wladimir Köppen and modified by his collaborators and successors, is still in widespread use. It is widely used in teaching school and undergraduate courses on climate. It is also still in regular use by researchers across a range of disciplines as a basis for climatic regionalisation of variables and for assessing the output of global climate models. Here we have produced a new global map of climate using the Köppen-Geiger system based on a large global data set of long-term monthly precipitation and temperature station time series. Climatic variables used in the Köppen-Geiger system were calculated at each station and interpolated between stations using a two-dimensional (latitude and longitude) thin-plate spline with tension onto a 0.1°×0.1° grid for each continent. We discuss some problems in dealing with sites that are not uniquely classified into one climate type by the Köppen-Geiger system and assess the outcomes on a continent by continent basis. Globally the most common climate type by land area is BWh (14.2%, Hot desert) followed by Aw (11.5%, Tropical savannah). The updated world Köppen-Geiger climate map is freely available electronically at http://www.hydrol-earth-syst-sci.net/????.
Several North American broad-leaved tree species range from the northern United States at ∼47°N to moist tropical montane forests in Mexico and Central America at 15–20°N. Along this gradient the average minimum temperatures of the coldest month (T
Jan), which characterize annual variation in temperature, increase from −10 to 12°C and tree phenology changes from deciduous to leaf-exchanging or evergreen in the southern range with a year-long growing season. Between 30 and 45°N, the time of bud break is highly correlated with T
Jan and bud break can be reliably predicted for the week in which mean minimum temperature rises to 7°C. Temperature-dependent deciduous phenology—and hence the validity of temperature-driven phenology models—terminates in southern North America near 30°N, where T
Jan>7°C enables growth of tropical trees and cultivation of frost-sensitive citrus fruits. In tropical climates most temperate broad-leaved species exchange old for new leaves within a few weeks in January-February, i.e., their phenology becomes similar to that of tropical leaf-exchanging species. Leaf buds of the southern ecotypes of these temperate species are therefore not winter-dormant and have no chilling requirement. As in many tropical trees, bud break of Celtis, Quercus and Fagus growing in warm climates is induced in early spring by increasing daylength. In tropical climates vegetative phenology is determined mainly by leaf longevity, seasonal variation in water stress and day length. As water stress during the dry season varies widely with soil water storage, climate-driven models cannot predict tree phenology in the tropics and tropical tree phenology does not constitute a useful indicator of global warming.
Bud burst and dormancy release of latitudinal ecotypes of Betula pendula Roth and B. pubescens Ehrh. from Denmark (≈ 56° N), mid-Norway (≈ 64° N) and northern Norway (≈ 69° N) were studied in controlled environments. Dormant seedlings were chilled at 0, 5 or 10 °C from October 4 onward and then, at monthly intervals from mid-November to February, batches of seedlings were held at 15 °C in an 8-h (SD) or 24-h (LD) photoperiod to permit flushing. A decline in days to bud burst occurred with increasing chilling time in all ecotypes. In November, after 44 chilling days, time to bud burst was least in plants chilled at 0 and 5 °C. The difference diminished with increasing chilling time, and in February, after 136 chilling days, bud burst was earliest in plants chilled at 10 °C. Long photoperiods during flushing significantly reduced thermal time after short chilling periods (44 and 74 days), but had no effect when the chilling requirement was fully met after 105 or more chilling days. No significant difference in these responses was found between the two species. In both species, chilling requirement decreased significantly with increasing latitude of origin. Bud burst was normal in seedlings overwintered at 12 °C, but was erratic and delayed in seedlings overwintered at 15 and especially at 21 °C, indicating that the critical overwintering temperature is between 12 and 15 °C.
We conclude that there is little risk of a chilling deficit in birch under Scandinavian winter conditions even with a climatic warming of 7–8 °C. The likely effects of a climatic warming include earlier bud burst, a longer growing season and increased risk of spring frost injury, especially in high latitude ecotypes.
1. A data set of 36 years (1954-1989) of observations on first flowering dates (FFD) of 243 species of angiosperms and gymnosperms in one locality in southern central England is presented and analysed. 2. Individual FFDs ranged from 1 January to 17 August, and species varied considerably in the standard deviation of their FFD. The most variable species were mainly annuals and there was a negative relationship between mean FFD and variability, early-flowering species being the most variable. 3. For 219 of the 243 species, it was possible to fit regression equations for FFD to some set of monthly mean temperatures of the preceding months. These fits were generally best for woody plants and geophytes. February temperature was overall the most important determinant of flowering time. Sixty per cent of species flowering between January and April were affected by temperature 1-2 months before flowering; for summer (May onwards) flowering species, temperatures up to 4 months previously were important. 4. High spring temperatures advanced flowering by a mean of 4 days per degree. In contrast, both spring- and summer-flowering species were retarded in flowering by high temperatures in the previous autumn. 5. These relationships were used to simulate the effects of climatic warming: an overall increase of 1-degree-C in each month would advance flowering in some species and retard others, by as much as 6 weeks. Retarded species were early-flowering, advanced species late-flowering. These results suggest a high degree of dependence of flowering time on temperature, and the variation between species implies that responses to climatic warming may be difficult to predict.
To elucidate climate‐driven changes in leaf‐out phenology and their implications for species invasions, we observed and experimentally manipulated leaf out of invasive and native woody plants in C oncord, M A, USA.
Using observations collected by H enry D avid T horeau (1852–1860) and our own observations (2009–2013), we analyzed changes in leaf‐out timing and sensitivity to temperature for 43 woody plant species. We experimentally tested winter chilling requirements of 50 species by exposing cut branches to warm indoor temperatures (22°C) during the winter and spring of 2013.
Woody species are now leafing out an average of 18 d earlier than they did in the 1850s, and are advancing at a rate of 5 ± 1 d °C ⁻¹ . Functional groups differ significantly in the duration of chilling they require to leaf out: invasive shrubs generally have weaker chilling requirements than native shrubs and leaf out faster in the laboratory and earlier in the field; native trees have the strongest chilling requirements.
Our results suggest that invasive shrub species will continue to have a competitive advantage as the climate warms, because native plants are slower to respond to warming spring temperatures and, in the future, may not meet their chilling requirements.
It is well known that increased spring temperatures cause earlier onset dates of leaf unfolding and flowering. However, a temperature increase in winter may be associated with delayed development when species' chilling requirements are not fulfilled. Furthermore, photosensitivity is supposed to interfere with temperature triggers. To date, neither the relative importance nor possible interactions of these three factors have been elucidated. In this study, we present a multispecies climate chamber experiment to test the effects of chilling and photoperiod on the spring phenology of 36 woody species. Several hypotheses regarding their variation with species traits (successional strategy, floristic status, climate of their native range) were tested. Long photoperiods advanced budburst for one-third of the studied species, but magnitudes of these effects were generally minor. In contrast to prior hypotheses, photosensitive responses were not restricted to climax or oceanic species. Increased chilling length advanced budburst for almost all species; its effect greatly exceeding that of photoperiod. Moreover, we suggest that photosensitivity and chilling effects have to be rigorously disentangled, as the response to photoperiod was restricted to individuals that had not been fully chilled. The results indicate that temperature requirements and successional strategy are linked, with climax species having higher chilling and forcing requirements than pioneer species. Temperature requirements of invasive species closely matched those of native species, suggesting that high phenological concordance is a prerequisite for successful establishment. Lack of chilling not only led to a considerable delay in budburst but also caused substantial changes in the chronological order of species' budburst. The results reveal that increased winter temperatures might impact forest ecosystems more than formerly assumed. Species with lower chilling requirements, such as pioneer or invasive species, might profit from warming winters, if late spring frost events would in parallel occur earlier.
The manner in which organisms adapt to climate change informs a broader understanding of the evolution of biodiversity as well as conservation and mitigation plans. We apply common garden and association mapping approaches to quantify genetic variance and identify loci affecting bud flush and bud set, traits that define a tree's season for height growth, in the boreal forest tree Populus balsamifera L. (balsam poplar). Using data from 478 genotypes grown in each of two common gardens, one near the southern edge and another near the northern edge of P. balsamifera's range, we found that broad-sense heritability for bud flush and bud set was generally high (H(2) > 0.5 in most cases), suggesting that abundant genetic variation exists for phenological response to changes in the length of the growing season. To identify the molecular genetic basis of this variation, we genotyped trees for 346 candidate single nucleotide polymorphisms (SNPs) from 27 candidate genes for the CO/FT pathway in poplar. Mixed-model analyses of variance identified SNPs in 10 genes to be associated with variation in either bud flush or bud set. Multiple SNPs within FRIGIDA were associated with bud flush, whereas multiple SNPs in LEAFY and GIGANTEA 5 were associated with bud set. Although there was strong population structure in stem phenology, the geographic distribution of multilocus association SNP genotypes was widespread except at the most northern populations, indicating that geographic regions may harbour sufficient diversity in functional genes to facilitate adaption to future climatic conditions in many sites.
To examine the potential contribution of herbarium material to the description and analysis of tropical tree phenology, flowering times and geographical distribution were graphed for 1673 flowering collections from 18 species native to Neotropical dry forests and phenological differences between species were analysed. These include the timing and duration of flowering as well as morphological differences such as flowering on leafless twigs vs flowering on shoots bearing old or new foliage. Species-specific flowering periods of herbarium collections are similar to those observed in phenological field studies, but are often longer because of the larger geographical and temporal sampling range. Conspecific collections of different geographical origin show distinct differences in flowering periodicity, which are correlated with differences in the timing and intensity of the dry season. Interspecific differences in the timing of phenology relative to the dry season indicate differences in the control of phenology by seasonal drought. Herbaria thus represent a large potential source of phenological information which can either supplement and extend phenological field studies or provide phenological information for dry forest species not studied in the field but well represented in herbarium collections.
Chilling and daylength requirements for dormancy release and budburst in dormant beech (Fagus sylvatica L.) buds have been studied in cuttings flushing in controlled environments after different durations of outdoor chilling. Non-chilled buds sampled in mid October required long days (LD) only for budburst. Buds chilled until March still required LD for normal budburst, whereas buds sampled in November and December were unable to sprout regardless of daylength conditions and would do so only after a substantial period of chilling. Four ecotypes of distant latitudinal and altitudinal origin responded very similarly with a typical quantitative photoperiodic response. In fully chilled shoots sampled in March only 13 to 40% budburst took place in 8-h SD and only after three times as long time as in continuous light. It is concluded that this dual dormancy control system ensures optimum winter stability in trees under conditions of climatic warming. In the closely related Carpinus betulus L. budburst was unaffected by daylength.