Stable water isotopes reveal the onset of bud dormancy in temperate trees, whereas water content is a better proxy for dormancy release.

Earlier spring growth onset in temperate forests is a visible effect of global warming that alters global water and carbon cycling. Consequently, it becomes crucial to accurately predict the future spring phenological shifts in vegetation under different climate warming scenarios. However, current phenological models suffer from a lack of physiological insights of tree dormancy and are rarely experimentally validated. Here, we sampled twig cuttings of five deciduous tree species at two climatically different locations (270 and 750 m a.s.l., ~ 2.3 °C difference) throughout the winter of 2019-20. Twig budburst success, thermal time to budburst, bud water content and short-term 2H-labelled water uptake into buds were quantified to link bud dormancy status with vascular water transport efficacy, with the objective of establishing connections between the dormancy status of buds and their effectiveness in vascular water transport. We found large differences in the dormancy status between species throughout the entire investigation period, likely reflecting species-specific environmental requirements to initiate and release dormancy, whereas only small differences in the dormancy status were found between the two studied sites. We found strong 2H-labelled water uptake into buds during leaf senescence, followed by a sharp decrease, which we ascribed to the initiation of endodormancy. However, surprisingly, we did not find a progressive increase in 2H-labelled water uptake into buds as winter advanced. Nonetheless, all examined tree species exhibited a consistent relationship between bud water content and dormancy status. Our results suggest that short-term 2H-labelled water uptake may not be a robust indicator of dormancy release, yet it holds promise as a method for tracking the induction of dormancy in deciduous trees. By contrast, bud water content emerges as a cost-effective and more reliable indicator of dormancy release.

Feasting on the ordinary or starving for the exceptional in a warming climate: Phenological synchrony between spongy moth (Lymantria dispar) and budburst of six European tree species.

Global warming is affecting the phenological cycles of plants and animals, altering the complex synchronization that has co-evolved over thousands of years between interacting species and trophic levels. Here, we examined how warmer winter conditions affect the timing of budburst in six common European trees and the hatching of a generalist leaf-feeding insect, the spongy moth Lymantria dispar, whose fitness depends on the synchrony between egg hatch and leaf emergence of the host tree. We applied four different temperature treatments to L. dispar eggs and twig cuttings, that mimicked warmer winters and reduced chilling temperatures that are necessary for insect diapause and bud dormancy release, using heated open-top chambers (ambient or +3.5°C), and heated greenhouses (maintained at >6°C or >10°C). In addition, we conducted preference and performance tests to determine which tree species the larvae prefer and benefit from the most. Budburst success and twig survival were highest for all tree species at ambient temperature conditions, whereas it declined under elevated winter temperature for Tilia cordata and Acer pseudoplatanus, likely due to a lack of chilling. While L. dispar egg hatch coincided with budburst in most tree species within 10 days under ambient conditions, it coincided with budburst only in Quercus robur, Carpinus betulus, and, to a lesser extent, Ulmus glabra under warmer conditions. With further warming, we, therefore, expect an increasing mismatch in trees with high chilling requirements, such as Fagus sylvatica and A. pseudoplatanus, but still good synchronization with trees having low chilling requirements, such as Q. robur and C. betulus. Surprisingly, first instar larvae preferred and gained weight faster when fed with leaves of F. sylvatica, while Q. robur ranked second. Our results suggest that spongy moth outbreaks are likely to persist in oak and hornbeam forests in western and central Europe.

Chronic warming and dry soils limit carbon uptake and growth despite a longer growing season in beech and oak.

Progressively warmer and drier climatic conditions impact tree phenology and carbon cycling with large consequences for forest carbon balance. However, it remains unclear how individual impacts of warming and drier soils differ from their combined effects and how species interactions modulate tree responses. Using mesocosms, we assessed the multiyear impact of continuous air warming and lower soil moisture alone or in combination on phenology, leaf-level photosynthesis, nonstructural carbohydrate concentrations, and aboveground growth of young European beech (Fagus sylvatica L.) and Downy oak (Quercus pubescens Willd.) trees. We further tested how species interactions (in monocultures and in mixtures) modulated these effects. Warming prolonged the growing season of both species but reduced growth in oak. In contrast, lower moisture did not impact phenology but reduced carbon assimilation and growth in both species. Combined impacts of warming and drier soils did not differ from their single effects. Under warmer and drier conditions, performances of both species were enhanced in mixtures compared to monocultures. Our work revealed that higher temperature and lower soil moisture have contrasting impacts on phenology vs. leaf-level assimilation and growth, with the former being driven by temperature and the latter by moisture. Furthermore, we showed a compensation in the negative impacts of chronic heat and drought by tree species interactions.

Effect of climate warming on the timing of autumn leaf senescence reverses after the summer solstice.

Climate change is shifting the growing seasons of plants, affecting species performance and biogeochemical cycles. Yet how the timing of autumn leaf senescence in Northern Hemisphere forests will change remains uncertain. Using satellite, ground, carbon flux, and experimental data, we show that early-season and late-season warming have opposite effects on leaf senescence, with a reversal occurring after the year's longest day (the summer solstice). Across 84% of the northern forest area, increased temperature and vegetation activity before the solstice led to an earlier senescence onset of, on average, 1.9 ± 0.1 days per °C, whereas warmer post-solstice temperatures extended senescence duration by 2.6 ± 0.1 days per °C. The current trajectories toward an earlier onset and slowed progression of senescence affect Northern Hemisphere-wide trends in growing-season length and forest productivity.

Networking the forest infrastructure towards near real-time monitoring - A white paper.

Forests account for nearly 90 % of the world's terrestrial biomass in the form of carbon and they support 80 % of the global biodiversity. To understand the underlying forest dynamics, we need a long-term but also relatively high-frequency, networked monitoring system, as traditionally used in meteorology or hydrology. While there are numerous existing forest monitoring sites, particularly in temperate regions, the resulting data streams are rarely connected and do not provide information promptly, which hampers real-time assessments of forest responses to extreme climate events. The technology to build a better global forest monitoring network now exists. This white paper addresses the key structural components needed to achieve a novel meta-network. We propose to complement - rather than replace or unify - the existing heterogeneous infrastructure with standardized, quality-assured linking methods and interacting data processing centers to create an integrated forest monitoring network. These automated (research topic-dependent) linking methods in atmosphere, biosphere, and pedosphere play a key role in scaling site-specific results and processing them in a timely manner. To ensure broad participation from existing monitoring sites and to establish new sites, these linking methods must be as informative, reliable, affordable, and maintainable as possible, and should be supplemented by near real-time remote sensing data. The proposed novel meta-network will enable the detection of emergent patterns that would not be visible from isolated analyses of individual sites. In addition, the near real-time availability of data will facilitate predictions of current forest conditions (nowcasts), which are urgently needed for research and decision making in the face of rapid climate change. We call for international and interdisciplinary efforts in this direction.

Linking human impacts to community processes in terrestrial and freshwater ecosystems.

Human impacts such as habitat loss, climate change and biological invasions are radically altering biodiversity, with greater effects projected into the future. Evidence suggests human impacts may differ substantially between terrestrial and freshwater ecosystems, but the reasons for these differences are poorly understood. We propose an integrative approach to explain these differences by linking impacts to four fundamental processes that structure communities: dispersal, speciation, species-level selection and ecological drift. Our goal is to provide process-based insights into why human impacts, and responses to impacts, may differ across ecosystem types using a mechanistic, eco-evolutionary comparative framework. To enable these insights, we review and synthesise (i) how the four processes influence diversity and dynamics in terrestrial versus freshwater communities, specifically whether the relative importance of each process differs among ecosystems, and (ii) the pathways by which human impacts can produce divergent responses across ecosystems, due to differences in the strength of processes among ecosystems we identify. Finally, we highlight research gaps and next steps, and discuss how this approach can provide new insights for conservation. By focusing on the processes that shape diversity in communities, we aim to mechanistically link human impacts to ongoing and future changes in ecosystems.

Global warming is increasing the discrepancy between green (actual) and thermal (potential) seasons of temperate trees.

Over the past decades, global warming has led to a lengthening of the time window during which temperatures remain favorable for carbon assimilation and tree growth, resulting in a lengthening of the green season. The extent to which forest green seasons have tracked the lengthening of this favorable period under climate warming, however, has not been quantified to date. Here, we used remote sensing data and long-term ground observations of leaf-out and coloration for six dominant species of European trees at 1773 sites, for a total of 6060 species-site combinations, during 1980-2016 and found that actual green season extensions (GS: 3.1 ± 0.1 day decade-1 ) lag four times behind extensions of the potential thermal season (TS: 12.6 ± 0.1 day decade-1 ). Similar but less pronounced differences were obtained using satellite-derived vegetation phenology observations, that is, a lengthening of 4.4 ± 0.13 and 7.5 ± 0.13 day decade-1 for GS and TS, respectively. This difference was mainly driven by the larger advance in the onset of the thermal season compared to the actual advance of leaf-out dates (spring mismatch: 7.2 ± 0.1 day decade-1 ), but to a less extent caused by a phenological mismatch between GS and TS in autumn (2.4 ± 0.1 day decade-1 ). Our results showed that forest trees do not linearly track the new thermal window extension, indicating more complex interactions between winter and spring temperatures and photoperiod and a justification of demonstrating that using more sophisticated models that include the influence of chilling and photoperiod is needed to accurately predict spring phenological changes under warmer climate. They urge caution if such mechanisms are omitted to predict, for example, how vegetative health and growth, species distribution and crop yields will change in the future.

Number of growth days and not length of the growth period determines radial stem growth of temperate trees.

Radial stem growth dynamics at seasonal resolution are essential to understand how forests respond to climate change. We studied daily radial growth of 160 individuals of seven temperate tree species at 47 sites across Switzerland over 8 years. Growth of all species peaked in the early part of the growth season and commenced shortly before the summer solstice, but with species-specific seasonal patterns. Day length set a window of opportunity for radial growth. Within this window, the probability of daily growth was constrained particularly by air and soil moisture, resulting in intermittent growth to occur only on 29 to 77 days (30% to 80%) within the growth period. The number of days with growth largely determined annual growth, whereas the growth period length contributed less. We call for accounting for these non-linear intra-annual and species-specific growth dynamics in tree and forest models to reduce uncertainties in predictions under climate change.

Impact of microclimatic conditions and resource availability on spring and autumn phenology of temperate tree seedlings.

Microclimatic effects (light, temperature) are often neglected in phenological studies and little information is known about the impact of resource availability (nutrient and water) on tree's phenological cycles. Here we experimentally studied spring and autumn phenology in four temperate trees in response to changes in bud albedo (white-painted vs black-painted buds), light conditions (nonshaded vs c. 70% shaded), water availability (irrigated, control and reduced precipitation) and nutrients (low vs high availability). We found that higher bud albedo or shade delayed budburst (up to +12 d), indicating that temperature is sensed locally within each bud. Leaf senescence was delayed by high nutrient availability (up to +7 d) and shade conditions (up to +39 d) in all species, except oak. Autumn phenological responses to summer droughts depended on species, with a delay for cherry (+7 d) and an advance for beech (-7 d). The strong phenological effects of bud albedo and light exposure reveal an important role of microclimatic variation on phenology. In addition to the temperature and photoperiod effects, our results suggest a tight interplay between source and sink processes in regulating the end of the seasonal vegetation cycle, which can be largely influenced by resource availability (light, water and nutrients).

Post-glacial re-colonization and natural selection have shaped growth responses of silver fir across Europe.

Warmer climate and more frequent extreme droughts will pose major threats to forest ecosystems. Past demography processes due to post-glacial recolonization and adaptation to local environmental conditions are among the main contributors to genetic differentiation processes among provenances. Assessing the intra-specific variability of tree growth responses to such changes is crucial to explore a species' potential to cope with climate warming. We combined growth-related traits derived from tree-ring width series with neutral genetic information of 18 European provenances of silver fir (Abies alba Mill.) growing in two common garden experiments in Switzerland. Analyses based on neutral single nucleotide polymorphisms revealed that the studied provenances grouped into three longitudinal clusters. These three genetic clusters showed differences in growth traits (height and DBH), with the provenances from the eastern cluster exhibiting the highest growth. The Pyrenees cluster showed significantly lower recovery and resilience to the extreme drought of 2003 as well as lower values of growth autocorrelation. QST-FST and correlation analyses with climate of provenance origin suggest that the differences among provenances found in some traits result from natural selection. Our study suggests that the last post-glacial re-colonization and natural selection are the major drivers explaining the intra-specific variability in growth of silver fir across Europe. These findings highlight the importance of combining dendroecology and genetic analyses on fitness-related traits to assess the potential of a species to cope with global environmental change and provide insights to support assisted gene flow to ensure the persistence of the species in European forests.

Phenological and elevational shifts of plants, animals and fungi under climate change in the European Alps.

Mountain areas are biodiversity hotspots and provide a multitude of ecosystem services of irreplaceable socio-economic value. In the European Alps, air temperature has increased at a rate of about 0.36°C decade-1 since 1970, leading to glacier retreat and significant snowpack reduction. Due to these rapid environmental changes, this mountainous region is undergoing marked changes in spring phenology and elevational distribution of animals, plants and fungi. Long-term monitoring in the European Alps offers an excellent natural laboratory to synthetize climate-related changes in spring phenology and elevational distribution for a large array of taxonomic groups. This review assesses the climatic changes that have occurred across the European Alps during recent decades, spring phenological changes and upslope shifts of plants, animals and fungi from evidence in published papers and previously unpublished data. Our review provides evidence that spring phenology has been shifting earlier during the past four decades and distribution ranges show an upwards trend for most of the taxonomic groups for which there are sufficient data. The first observed activity of reptiles and terrestrial insects (e.g. butterflies) in spring has shifted significantly earlier, at an average rate of -5.7 and -6.0 days decade-1 , respectively. By contrast, the first observed spring activity of semi-aquatic insects (e.g. dragonflies and damselflies) and amphibians, as well as the singing activity or laying dates of resident birds, show smaller non-significant trends ranging from -1.0 to +1.3 days decade-1 . Leaf-out and flowering of woody and herbaceous plants showed intermediate trends with mean values of -2.4 and -2.8 days decade-1 , respectively. Regarding species distribution, plants, animals and fungi (N = 2133 species) shifted the elevation of maximum abundance (optimum elevation) upslope at a similar pace (on average between +18 and +25 m decade-1 ) but with substantial differences among taxa. For example, the optimum elevation shifted upward by +36.2 m decade-1 for terrestrial insects and +32.7 m decade-1 for woody plants, whereas it was estimated to range between -1.0 and +11 m decade-1 for semi-aquatic insects, ferns, birds and wood-decaying fungi. The upper range limit (leading edge) of most species also shifted upslope with a rate clearly higher for animals (from +47 to +91 m decade-1 ) than for plants (from +17 to +40 m decade-1 ), except for semi-aquatic insects (-4.7 m decade-1 ). Although regional land-use changes could partly explain some trends, the consistent upward shift found in almost all taxa all over the Alps is likely reflecting the strong warming and the receding of snow cover that has taken place across the European Alps over recent decades. However, with the possible exception of terrestrial insects, the upward shift of organisms seems currently too slow to track the pace of isotherm shifts induced by climate warming, estimated at about +62 to +71 m decade-1 since 1970. In the light of these results, species interactions are likely to change over multiple trophic levels through phenological and spatial mismatches. This nascent research field deserves greater attention to allow us to anticipate structural and functional changes better at the ecosystem level.

Chilled to be forced: the best dose to wake up buds from winter dormancy.

Over the last decades, spring leaf-out of temperate and boreal trees has substantially advanced in response to global warming, affecting terrestrial biogeochemical fluxes and the Earth's climate system. However, it remains unclear whether leaf-out will continue to advance with further warming because species' effective chilling temperatures, as well as the amount of chilling time required to break dormancy, are still largely unknown for most forest tree species. Here, we assessed the progress of winter dormancy and quantified the efficiency of different chilling temperatures in six dominant temperate European tree species by exposing 1170 twig cuttings to a range of temperatures from -2°C to 10°C for 1, 3, 6 or 12 wk. We found that freezing temperatures were most effective for half of the species or as effective as chilling temperatures up to 10°C, that is, leading to minimum thermal time to and maximum success of budburst. Interestingly, chilling duration had a much larger effect on dormancy release than absolute chilling temperature. Our experimental results challenge the common assumption that optimal chilling temperatures range c. 4-6°C, instead revealing strong sensitivity to a large range of temperatures. These findings are valuable for improving phenological models and predicting future spring phenology in a warming world.

Assessing the Effectiveness of in-situ Active Warming Combined With Open Top Chambers to Study Plant Responses to Climate Change.

Temperature manipulation experiments are an effective way for testing plant responses to future climate conditions, especially for predicting shifts in plant phenological events. While passive warming techniques are widely used to elevate temperature in low stature plant communities, active warming has been applied less frequently due to the associated resource requirements. In forest ecosystems, however, active warming is crucial to simulate projected air temperature rises of 3-5 K, especially at the warm (i.e., southern and low elevation) range edges of tree species. Moreover, the warming treatment should be applied to the complete height of the experimental plants, e.g., regenerating trees in the understory. Here, we combined open top chambers (OTCs) with active heat sources, an electric heater (OTC-EH) and warming cables (OTC-WC), and tested the effectiveness of these set-ups to maintain constant temperature differences compared to ambient temperature across 18 m2 plots. This chamber size is needed to grow tree saplings in mixture in forest gaps for 3 to 10 years. With passive warming only, an average temperature increase of approx. 0.4 K as compared to ambient conditions was achieved depending on time of the day and weather conditions. In the actively warmed chambers, average warming exceeded ambient temperatures by 2.5 to 2.8 K and was less variable over time. However, active warming also reduced air humidity by about 15%. These results underline the need to complement passive warming with active warming in order to achieve constant temperature differences appropriate for climate change simulations under all weather conditions in large OTCs. Since we observed considerable horizontal and vertical temperature variation within OTCs with temperature differences of up to 16.9 K, it is essential to measure and report within-plot temperature distribution as well as temporal temperature variation. If temperature distributions within large OTCs are well characterized, they may be incorporated in the experimental design helping to identify non-linear or threshold responses to warming.

Climate warming increases spring phenological differences among temperate trees.

Climate warming has substantially advanced spring leaf flushing, but winter chilling and photoperiod co-determine the leaf flushing process in ways that vary among species. As a result, the interspecific differences in spring phenology (IDSP) are expected to change with climate warming, which may, in turn, induce negative or positive ecological consequences. However, the temporal change of IDSP at large spatiotemporal scales remains unclear. In this study, we analyzed long-term in-situ observations (1951-2016) of six, coexisting temperate tree species from 305 sites across Central Europe and found that phenological ranking did not change when comparing the rapidly warming period 1984-2016 to the marginally warming period 1951-1983. However, the advance of leaf flushing was significantly larger in early-flushing species EFS (6.7 ± 0.3 days) than in late-flushing species LFS (5.9 ± 0.2 days) between the two periods, indicating extended IDSP. This IDSP extension could not be explained by differences in temperature sensitivity between EFS and LFS; however, climatic warming-induced heat accumulation effects on leaf flushing, which were linked to a greater heat requirement and higher photoperiod sensitivity in LFS, drove the shifts in IDSP. Continued climate warming is expected to further extend IDSP across temperate trees, with associated implications for ecosystem function.

Late-spring frost risk between 1959 and 2017 decreased in North America but increased in Europe and Asia.

Late-spring frosts (LSFs) affect the performance of plants and animals across the world's temperate and boreal zones, but despite their ecological and economic impact on agriculture and forestry, the geographic distribution and evolutionary impact of these frost events are poorly understood. Here, we analyze LSFs between 1959 and 2017 and the resistance strategies of Northern Hemisphere woody species to infer trees' adaptations for minimizing frost damage to their leaves and to forecast forest vulnerability under the ongoing changes in frost frequencies. Trait values on leaf-out and leaf-freezing resistance come from up to 1,500 temperate and boreal woody species cultivated in common gardens. We find that areas in which LSFs are common, such as eastern North America, harbor tree species with cautious (late-leafing) leaf-out strategies. Areas in which LSFs used to be unlikely, such as broad-leaved forests and shrublands in Europe and Asia, instead harbor opportunistic tree species (quickly reacting to warming air temperatures). LSFs in the latter regions are currently increasing, and given species' innate resistance strategies, we estimate that ∼35% of the European and ∼26% of the Asian temperate forest area, but only ∼10% of the North American, will experience increasing late-frost damage in the future. Our findings reveal region-specific changes in the spring-frost risk that can inform decision-making in land management, forestry, agriculture, and insurance policy.

Shifts in the temperature-sensitive periods for spring phenology in European beech and pedunculate oak clones across latitudes and over recent decades.

Spring phenology of temperate trees has advanced worldwide in response to global warming. However, increasing temperatures may not necessarily lead to further phenological advance, especially in the warmer latitudes because of insufficient chilling and/or shorter day length. Determining the start of the forcing phase, that is, when buds are able to respond to warmer temperatures in spring, is therefore crucial to predict how phenology will change in the future. In this study, we used 4,056 leaf-out date observations during the period 1969-2017 for clones of European beech (Fagus sylvatica L.) and pedunculate oak (Quercus robur L.) planted in 63 sites covering a large latitudinal gradient (from Portugal ~41°N to Norway ~63°N) at the International Phenological Gardens in order to (a) evaluate how the sensitivity periods to forcing and chilling have changed with climate warming, and (b) test whether consistent patterns occur along biogeographical gradients, that is, from colder to warmer environments. Partial least squares regressions suggest that the length of the forcing period has been extended over the recent decades with climate warming in the colder latitudes but has been shortened in the warmer latitudes for both species, with a more pronounced shift for beech. We attribute the lengthening of the forcing period in the colder latitudes to earlier opportunities with temperatures that can promote bud development. In contrast, at warmer or oceanic climates, the beginning of the forcing period has been delayed, possibly due to insufficient chilling. However, in spite of a later beginning of the forcing period, spring phenology has continued to advance at these areas due to a faster satisfaction of heat requirements induced by climate warming. Overall, our results support that ongoing climate warming will have different effects on the spring phenology of forest trees across latitudes due to the interactions between chilling, forcing and photoperiod.

Shortened temperature-relevant period of spring leaf-out in temperate-zone trees.

Temperature during a particular period prior to spring leaf-out, the temperature-relevant period (TRP), is a strong determinant of the leaf-out date in temperate-zone trees. Climatic warming has substantially advanced leaf-out dates in temperate biomes worldwide, but its effect on the beginning and length of the TRP has not yet been explored, despite its direct relevance for phenology modeling. Using 1,551 species-site combinations of long-term (1951-2016) in situ observations on six tree species (namely, Aesculus hippocastanum, Alnus glutinosa, Betula pendula, Fagus sylvatica, Fraxinus excelsior, and Quercus robur) in central Europe, we found that the advancing leaf-out was accompanied by a shortening of the TRP. On average across all species and sites, the length of the TRP significantly decreased by 23% (p < .05), from 60 ± 4 days during 1951-1965 to 47 ± 4 days during 2002-2016. Importantly, the average start date of the TRP did not vary significantly over the study period (March 2-5, DOY = 61-64), which could be explained by sufficient chilling over the study period in the regions considered. The advanced leaf-out date with unchanged beginning of the TRP can be explained by the faster accumulation of the required heat due to climatic warming, which overcompensated for the retarding effect of shortening daylength on bud development. This study shows that climate warming has not yet affected the mean TRP starting date in the study region, implying that phenology modules in global land surface models might be reliable assuming a fixed TRP starting date at least for the temperate central Europe. Field warming experiments do, however, remain necessary to test to what extent the length of TRP will continue to shorten and whether the starting date will remain stable under future climate conditions.