Yongshuo H. Fu

Declining global warming effects on the phenology of spring leaf unfolding

Earlier spring leaf unfolding is a frequently observed response of plants to climate warming. Many deciduous tree species require chilling for dormancy release, and warming-related reductions in chilling may counteract the advance of leaf unfolding in response to warming. Empirical evidence for this, however, is limited to saplings or twigs in climate-controlled chambers. Using long-term in situ observations of leaf unfolding for seven dominant European tree species at 1,245 sites, here we show that the apparent response of leaf unfolding to climate warming (ST, expressed in days advance of leaf unfolding per °C warming) has significantly decreased from 1980 to 2013 in all monitored tree species. Averaged across all species and sites, ST decreased by 40% from 4.0 ± 1.8 days °C−1 during 1980–1994 to 2.3 ± 1.6 days °C−1 during 1999–2013. The declining ST was also simulated by chilling-based phenology models, albeit with a weaker decline (24–30%) than observed in situ. The reduction in ST is likely to be partly attributable to reduced chilling. Nonetheless, other mechanisms may also have a role, such as ‘photoperiod limitation’ mechanisms that may become ultimately limiting when leaf unfolding dates occur too early in the season. Our results provide empirical evidence for a declining ST, but also suggest that the predicted strong winter warming in the future may further reduce ST and therefore result in a slowdown in the advance of tree spring phenology.

Leaf onset in the northern hemisphere triggered by daytime temperature

Recent warming significantly advanced leaf onset in the northern hemisphere. This signal cannot be accurately reproduced by current models parameterized by daily mean temperature (Tmean). Here using in situ observations of leaf unfolding dates (LUDs) in Europe and the United States, we show that the interannual anomalies of LUD during 1982–2011 are triggered by daytime (Tmax) more than by nighttime temperature (Tmin). Furthermore, an increase of 1 °C in Tmax would advance LUD by 4.7 days in Europe and 4.3 days in the United States, more than the conventional temperature sensitivity estimated from Tmean. The triggering role of Tmax, rather than the Tmin or Tmean variable, is also supported by analysis of the large-scale patterns of satellite-derived vegetation green-up in spring in the northern hemisphere (>30°N). Our results suggest a new conceptual framework of leaf onset using daytime temperature to improve the performance of phenology modules in current Earth system models.

Variation in leaf flushing date influences autumnal senescence and next year’s flushing date in two temperate tree species

Significance Leaf phenology of temperate ecosystems is shifting in response to global warming. This affects surface albedo, ecosystem carbon balance, and evapotranspiration, and the response of leaf phenology to climatic drivers has therefore received particular interest. However, despite considerable effort, models have failed to accurately reproduce phenology patterns, likely because mechanistic understanding is incomplete. Here, we show that earlier leaf flushing in response to a warm winter translated into earlier leaf senescence and even earlier leaf flushing in the following year. This legacy effect of winter warming on leaf phenology has important implications for understanding and modelling leaf phenology and its impact on ecosystem functioning, especially in relation to global warming, and is likely to open new research lines. Recent temperature increases have elicited strong phenological shifts in temperate tree species, with subsequent effects on photosynthesis. Here, we assess the impact of advanced leaf flushing in a winter warming experiment on the current year’s senescence and next year’s leaf flushing dates in two common tree species: Quercus robur L. and Fagus sylvatica L. Results suggest that earlier leaf flushing translated into earlier senescence, thereby partially offsetting the lengthening of the growing season. Moreover, saplings that were warmed in winter–spring 2009–2010 still exhibited earlier leaf flushing in 2011, even though the saplings had been exposed to similar ambient conditions for almost 1 y. Interestingly, for both species similar trends were found in mature trees using a long-term series of phenological records gathered from various locations in Europe. We hypothesize that this long-term legacy effect is related to an advancement of the endormancy phase (chilling phase) in response to the earlier autumnal senescence. Given the importance of phenology in plant and ecosystem functioning, and the prediction of more frequent extremely warm winters, our observations and postulated underlying mechanisms should be tested in other species.

The Impact of Winter and Spring Temperatures on Temperate Tree Budburst Dates: Results from an Experimental Climate Manipulation

Budburst phenology is a key driver of ecosystem structure and functioning, and it is sensitive to global change. Both cold winter temperatures (chilling) and spring warming (forcing) are important for budburst. Future climate warming is expected to have a contrasting effect on chilling and forcing, and subsequently to have a non-linear effect on budburst timing. To clarify the different effects of warming during chilling and forcing phases of budburst phenology in deciduous trees, (i) we conducted a temperature manipulation experiment, with separate winter and spring warming treatments on well irrigated and fertilized saplings of beech, birch and oak, and (ii) we analyzed the observations with five temperature-based budburst models (Thermal Time model, Parallel model, Sequential model, Alternating model, and Unified model). The results show that both winter warming and spring warming significantly advanced budburst date, with the combination of winter plus spring warming accelerating budburst most. As expected, all three species were more sensitive to spring warming than to winter warming. Although the different chilling requirement, the warming sensitivity was not significantly different among the studied species. Model evaluation showed that both one- and two- phase models (without and with chilling, respectively) are able to accurately predict budburst. For beech, the Sequential model reproduced budburst dates best. For oak and birch, both Sequential model and the Thermal Time model yielded good fit with the data but the latter was slightly better in case of high parameter uncertainty. However, for late-flushing species, the Sequential model is likely be the most appropriate to predict budburst data in a future warmer climate.

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

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

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

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

Global warming leads to more uniform spring phenology across elevations

Significance A famous American entomologist, Andrew D. Hopkins, estimated in 1920 the progressive delay in tree leaf-out with increasing latitude, longitude, and elevation, a phenomenon referred to as “Hopkins’ bioclimatic law.” Here, based on massive ground observations in the European Alps, we show that global warming has altered this law. In the early 1960s, the elevation-induced phenological shift (EPS) was approximately 34 days’ delay for every 1,000-m increase in elevation, conforming to Hopkins’ bioclimatic law, whereas, nowadays, this shift has reduced by 35% to 22 d⋅1,000 m−1. Winter warming is likely to be responsible for this strong reduction in the EPS and future climate warming may strengthen this trend. Important consequences for the functioning of mountain ecosystems are thus anticipated. One hundred years ago, Andrew D. Hopkins estimated the progressive delay in tree leaf-out with increasing latitude, longitude, and elevation, referred to as “Hopkins’ bioclimatic law.” What if global warming is altering this well-known law? Here, based on ∼20,000 observations of the leaf-out date of four common temperate tree species located in 128 sites at various elevations in the European Alps, we found that the elevation-induced phenological shift (EPS) has significantly declined from 34 d⋅1,000 m−1 conforming to Hopkins’ bioclimatic law in 1960, to 22 d⋅1,000 m−1 in 2016, i.e., −35%. The stronger phenological advance at higher elevations, responsible for the reduction in EPS, is most likely to be connected to stronger warming during late spring as well as to warmer winter temperatures. Indeed, under similar spring temperatures, we found that the EPS was substantially reduced in years when the previous winter was warmer. Our results provide empirical evidence for a declining EPS over the last six decades. Future climate warming may further reduce the EPS with consequences for the structure and function of mountain forest ecosystems, in particular through changes in plant–animal interactions, but the actual impact of such ongoing change is today largely unknown.

Arbuscular mycorrhizal fungi may mitigate the influence of a joint rise of temperature and atmospheric CO2 on soil respiration in grasslands.

We investigated the effects of mycorrhizal colonization and future climate on roots and soil respiration (Rsoil) in model grassland ecosystems. We exposed artificial grassland communities on pasteurized soil (no living arbuscular mycorrhizal fungi (AMF) present) and on pasteurized soil subsequently inoculated with AMF to ambient conditions and to a combination of elevated CO2 and temperature (future climate scenario). After one growing season, the inoculated soil revealed a positive climate effect on AMF root colonization and this elicited a significant AMF x climate scenario interaction on root biomass. Whereas the future climate scenario tended to increase root biomass in the noninoculated soil, the inoculated soil revealed a 30% reduction of root biomass under warming at elevated CO2 (albeit not significant). This resulted in a diminished response of Rsoil to simulated climatic change, suggesting that AMF may contribute to an attenuated stimulation of Rsoil in a warmer, high CO2 world.

Extension of the growing season increases vegetation exposure to frost

While climate warming reduces the occurrence of frost events, the warming-induced lengthening of the growing season of plants in the Northern Hemisphere may actually induce more frequent frost days during the growing season (GSFDs, days with minimum temperature < 0 °C). Direct evidence of this hypothesis, however, is limited. Here we investigate the change in the number of GSFDs at latitudes greater than 30° N using remotely-sensed and in situ phenological records and three minimum temperature (Tmin) data sets from 1982 to 2012. While decreased GSFDs are found in northern Siberia, the Tibetan Plateau, and northwestern North America (mainly in autumn), ~43% of the hemisphere, especially in Europe, experienced a significant increase in GSFDs between 1982 and 2012 (mainly during spring). Overall, regions with larger increases in growing season length exhibit larger increases in GSFDs. Climate warming thus reduces the total number of frost days per year, but GSFDs nonetheless increase in many areas.Plant growing season increases under a warming climate, but it is not known whether this will alter plant exposure to frost days. Here Liu et al. investigate trends in the Northern Hemisphere over 30 years and find increased exposure to frost days in regions that have longer growing seasons.

Simulating the onset of spring vegetation growth across the Northern Hemisphere

Changes in the spring onset of vegetation growth in response to climate change can profoundly impact climate-biosphere interactions. Thus, robust simulation of spring onset is essential to accurately predict ecosystem responses and feedback to ongoing climate change. To date, the ability of vegetation phenology models to reproduce spatiotemporal patterns of spring onset at larger scales has not been thoroughly investigated. In this study, we took advantage of phenology observations via remote sensing to calibrate and evaluated six models, including both one-phase (considering only forcing temperatures) and two-phase (involving forcing, chilling, and photoperiod) models across the Northern Hemisphere between 1982 and 2012. Overall, we found that the model that integrated the photoperiod effect performed best at capturing spatiotemporal patterns of spring phenology in boreal and temperate forests. By contrast, all of the models performed poorly in simulating the onset of growth in grasslands. These results suggest that the photoperiod plays a role in controlling the onset of growth in most Northern Hemisphere forests, whereas other environmental factors (e.g., precipitation) should be considered when simulating the onset of growth in grasslands. We also found that the one-phase model performed as well as the two-phase models in boreal forests, which implies that the chilling requirement is probably fulfilled across most of the boreal zone. Conversely, two-phase models performed better in temperate forests than the one-phase model, suggesting that photoperiod and chilling play important roles in these temperate forests. Our results highlight the significance of including chilling and photoperiod effects in models of the spring onset of forest growth at large scales, and indicate that the consideration of additional drivers may be required for grasslands.