Spring leaf unfolding has been occurring earlier in the year because of rising temperatures; however, long-term evidence in the field from 7 European tree species studied in 1,245 sites shows that this early unfolding effect is being reduced in recent years, possibly because the reducing chilling and/or insolation render trees less responsive to warming. Spring leaf unfolding has been occurring earlier in the year because of rising temperatures, but some experimental evidence has suggested that the effect is becoming less marked because trees are not receiving the necessary chilling required to trigger leaf unfolding. Shilong Piao and colleagues present evidence based on long-term field observations of seven European tree species studied in 1,245 locations across Europe confirming that a weakening of temperature sensitivity of leaf unfolding is indeed occurring. The authors provide model-based evidence that the chilling effect is at least partially responsible. Earlier spring leaf unfolding is a frequently observed response of plants to climate warming1,2,3,4. Many deciduous tree species require chilling for dormancy release, and warming-related reductions in chilling may counteract the advance of leaf unfolding in response to warming5,6. Empirical evidence for this, however, is limited to saplings or twigs in climate-controlled chambers7,8. Using long-term in situ observations of leaf unfolding for seven dominant European tree species at 1,245 sites, here we show that the apparent response of leaf unfolding to climate warming (ST, expressed in days advance of leaf unfolding per °C warming) has significantly decreased from 1980 to 2013 in all monitored tree species. Averaged across all species and sites, ST decreased by 40% from 4.0 ± 1.8 days °C−1 during 1980–1994 to 2.3 ± 1.6 days °C−1 during 1999–2013. The declining ST was also simulated by chilling-based phenology models, albeit with a weaker decline (24–30%) than observed in situ. The reduction in ST is likely to be partly attributable to reduced chilling. Nonetheless, other mechanisms may also have a role, such as ‘photoperiod limitation’ mechanisms that may become ultimately limiting when leaf unfolding dates occur too early in the season. Our results provide empirical evidence for a declining ST, but also suggest that the predicted strong winter warming in the future may further reduce ST and therefore result in a slowdown in the advance of tree spring phenology.

/pdf/declining-global-warming-effects-on-the-phenology-of-spring-2l08hbljr1.pdf

Declining global warming effects on the phenology of spring leaf unfolding.

Increasing temperatures should facilitate the poleward movement of species distributions through a variety of processes, including increasing the growing season length. However, in temperate and boreal latitudes, temperature is not the only cue used by trees to determine seasonality, as changes in photoperiod provide a more consistent, reliable annual signal of seasonality than temperature. Here, we discuss how day length may limit the ability of tree species to respond to climate warming in situ, focusing on the implications of photoperiodic sensing for extending the growing season and affecting plant phenology and growth, as well as the potential role of photoperiod in controlling carbon uptake and water fluxes in forests. We also review whether there are patterns across plant functional types (based on successional strategy, xylem anatomy and leaf morphology) in their sensitivity to photoperiod that we can use to predict which species or groups might be more successful in migrating as the climate warms, or may be more successfully used for forestry and agriculture through assisted migration schemes.

https://www.onlinelibrary.wiley.com/doi/pdf/10.1111/pce.12431

Photoperiod constraints on tree phenology, performance and migration in a warming world

Shifts in vegetation phenology are a key example of the biological effects of climate change1–3. However, there is substantial uncertainty about whether these temperature-driven trends will continue, or whether other factors—for example, photoperiod—will become more important as warming exceeds the bounds of historical variability4,5. Here we use phenological transition dates derived from digital repeat photography6 to show that experimental whole-ecosystem warming treatments7 of up to +9 °C linearly correlate with a delayed autumn green-down and advanced spring green-up of the dominant woody species in a boreal Picea–Sphagnum bog. Results were confirmed by direct observation of both vegetative and reproductive phenology of these and other bog plant species, and by multiple years of observations. There was little evidence that the observed responses were constrained by photoperiod. Our results indicate a likely extension of the period of vegetation activity by 1–2 weeks under a ‘CO2 stabilization’ climate scenario (+2.6 ± 0.7 °C), and 3–6 weeks under a ‘high-CO2 emission’ scenario (+5.9 ± 1.1 °C), by the end of the twenty-first century. We also observed severe tissue mortality in the warmest enclosures after a severe spring frost event. Failure to cue to photoperiod resulted in precocious green-up and a premature loss of frost hardiness8, which suggests that vulnerability to spring frost damage will increase in a warmer world9,10. Vegetation strategies that have evolved to balance tradeoffs associated with phenological temperature tracking may be optimal under historical climates, but these strategies may not be optimized for future climate regimes. These in situ experimental results are of particular importance because boreal forests have both a circumpolar distribution and a key role in the global carbon cycle11. Experimental whole-ecosystem warming treatments of a Picea–Sphagnum peat bog reveal the likely phenological consequences of future temperature increases that exceed those of historical climate regimes.

Ecosystem warming extends vegetation activity but heightens vulnerability to cold temperatures

Temperate climates are defined by distinct temperature seasonality with large and often unpredictable weather during any of the four seasons. To thrive in such climates, trees have to withstand a cold winter and the stochastic occurrence of freeze events during any time of the year. The physiological mechanisms trees adopt to escape, avoid, and tolerate freezing temperatures include a cold acclimation in autumn, a dormancy period during winter (leafless in deciduous trees), and the maintenance of a certain freezing tolerance during dehardening in early spring. The change from one phase to the next is mediated by complex interactions between temperature and photoperiod. This review aims at providing an overview of the interplay between phenology of leaves and species-specific freezing resistance. First, we address the long-term evolutionary responses that enabled temperate trees to tolerate certain low temperature extremes. We provide evidence that short term acclimation of freezing resistance plays a crucial role both in dormant and active buds, including re-acclimation to cold conditions following warm spells. This ability declines to almost zero during leaf emergence. Second, we show that the risk that native temperate trees encounter freeze injuries is low and is confined to spring and underline that this risk might be altered by climate warming depending on species-specific phenological responses to environmental cues.

/pdf/the-interaction-between-freezing-tolerance-and-phenology-in-bv5biit97q.pdf

The interaction between freezing tolerance and phenology in temperate deciduous trees.

Light pollution is a driver of insect declines

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.

Chilling outweighs photoperiod in preventing precocious spring development.

Phenology ranks among the best ecosystem processes for fingerprinting climate change since temperature explains a high percentage of the interannual or spatial variation in phenological onset dates. However, roles of other environmental variables, such as foliar nutrient concentrations, are far from adequately understood. This observational study examined the effects of air temperature and 11 nutrients on spring phenology of Betula pendula Roth (birch) along an urban–rural gradient in Munich, Germany, during the years 2010/2011. Moreover, the influence of temperature, nutrients, and air pollutants (NO2 and O3) on the amounts of pollen and catkin biomass in 2010 was evaluated. In addition to the influence of higher temperatures advancing phenological onset dates, higher foliar concentrations of potassium, boron, zinc, and calcium were statistically significantly linked to earlier onset dates. Since flushing of leaves is a turgor-driven process and all the influential nutrients are involved in cell extension, membrane function, and stability, there might be a reasonable physiological interpretation of the observed association. The amounts of pollen were negatively correlated with temperature, atmospheric NO2, and foliar iron concentration, suggesting that these variables restrict pollen production. The results of this study suggested an influence of nutritional status on both phenology and pollen production. The interaction of urbanization and climate change should be considered in the assessment of the impact of global warming on ecosystems and human health.

/pdf/nutrient-status-a-missing-factor-in-phenological-and-pollen-46b3yl7f0b.pdf

Nutrient status: a missing factor in phenological and pollen research?

Process-orientated, unmanaged forest remnants are not sufficient for halting the loss of forest biodiversity. Thus, integrated biodiversity-promoting management for forest inhabitants is needed. Microhabitats, such as tree cavities or bark pockets, are essential for the preservation of saproxylic species and of critical importance for endangered ones. This study investigates (1) which factors trigger the formation of microhabitats at both the individual tree and aggregated plot level, and (2) whether the co-occurrence of microhabitats differs between managed (=logged) and unmanaged forests. Relationships between the occurrence of 17 microhabitat types and individual tree features (e.g. light availability, and tree vitality) and plot characteristics (e.g. stand density index and stand age) in 398 plots dominated by Fagus sylvatica or Pseudotsuga menziesii in Germany and the USA were studied using random-effects logistic and normal regression modelling. Separate analyses were performed for German beech forests, German Douglas-fir forests, and the US Douglas-fir forests. Our results show that (1) tree diameter in breast height (DBH), tree vitality and branchiness or epicormic branches are highly related with the occurrence of one or more microhabitats on individual trees in managed and unmanaged beech and US Douglas-fir forests. In managed German Douglas-fir forests, vitality is not a predictor for the occurrence of microhabitats on a tree, but tree density and the maximum age of trees in a stand in addition to DBH and branchiness have an effect. Time since last management is not a statistically significant predictor for the presence of microhabitats at the tree level, but it is for German beech at the plot level. In Douglas-fir-dominated forests both in Germany and in the USA, the stand density index was the only common predictor at the plot level. (2) Unmanaged German beech and Douglas-fir forests exhibit more statistically significant and positive correlations with microhabitat groups than managed stands, implying that the presence of one microhabitat group on a tree is associated with the presence of other microhabitat groups. We finally conclude that measures for supporting microhabitat inhabitants in managed forests are scale and species dependent (tree versus plot level; beech versus Douglas-fir-dominated forests). Trees that carry microhabitats seem to have similar features independently of forest management. At the plot level, density management may trigger the accumulation of microhabitats. Our results indicate that in forest management, it is possible to consider the factors influencing the formation of microhabitats and implement adequate forest practices to advance their formation.

Association of tree and plot characteristics with microhabitat formation in European beech and Douglas-fir forests

Nutrient status : a missing factor in phenological and pollen research? Journal of Experimental Botany

This randomized clinical trial evaluates matching efficacy, safety, and immunogenicity between biosimilar natalizumab and reference natalizumab in patients with relapsing-remitting multiple sclerosis.

/pdf/efficacy-and-safety-of-proposed-biosimilar-natalizumab-pb006-8ztzypig.pdf

Josef Höfler

Papers

Chilling outweighs photoperiod in preventing precocious spring development.

Nutrient status: a missing factor in phenological and pollen research?

Association of tree and plot characteristics with microhabitat formation in European beech and Douglas-fir forests

Nutrient status : a missing factor in phenological and pollen research? Journal of Experimental Botany

Efficacy and Safety of Proposed Biosimilar Natalizumab (PB006) in Patients With Relapsing-Remitting Multiple Sclerosis