Autumn phenology of tree species in China is associated more with climate than with spring phenology and phylogeny.

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.

Predicting the changes in suitable habitats for six common woody species in Central Asia.

Climate change over the past decades has significantly altered global hydrothermal conditions and caused an evident shift in species distribution. Predicting species distribution patterns and identifying their influencing factors will be essential in developing coping strategies to prevent species extirpation and extinction. Yet, environmental factors affecting the distribution of woody species in Central Asia remain largely unknown. Here, I used the MaxEnt model to predict the current distributions and future distribution under three SSP-RCP scenarios of six common woody species in Central Asia. The results indicated a good performance of the MaxEnt model. Precipitation of driest month and annual mean temperature were the dominant factors affecting species distribution. For the species with wide ecological niches, i.e., Acer negundo and Rosa chinensis, the suitable areas showed an evident expansion trend under future scenarios. In addition, a trend toward higher elevation was found for the species that grew at high altitudes (1600-3200 m). However, the average elevation of suitable area for A. negundo and R. chinensis firstly increased but then decreased under future scenarios. Even though the areas with high species diversity increased from 0.59% under the current situation to 0.82% and 0.81% under ssp245 in 2021-2040 and 2041-2060, respectively, species diversity showed an apparent loss in parts of the northwest and southeast areas under ssp370 and ssp585. This study can guide susceptible habitat protections under climate change.

Varying temperature sensitivity of bud-burst date at different temperature conditions.

The relationship between the rate of development (DR) of bud-burst and temperature may be nonlinear, which could lead to varying temperature sensitivity (TS) of budburst date under different climate conditions. In order to determine the functional form between DR/TS and temperature, we gathered twigs with flower buds of five woody plants (Malus halliana, Forsythia suspense, Crataegus pinnatifida, Prunus cerasifera F. atropurpurea, and Berberis thunbergii var. atropurpurea Chenault) in early spring of 2017 at Beijing, and placed them in six growth chambers at same daylength but different temperature conditions (5, 10, 15, 20, 25, and 30 °C). The proportion of bud- burst was recorded every 2 or 3 days for each species at each temperature condition. The results showed that the proportion of bud-burst followed the logistic function over time at a given temperature. Subsequently, we developed a mathematical model to simulate the proportion of bud-burst at any temperature and date. The DR and TS were parameterized using a differential method. The simulation results showed that the DR increased monotonically with the rise in temperature, but only two species could reach the maximum value at 30 °C. The TS decreased with the increase in temperature, but this effect was weak when the temperature was high enough. These findings suggested that the predicted warming in the future may result in a slowdown in the advance of spring phenology of woody plants.

Comparison of chilling and heat requirements for leaf unfolding in deciduous woody species in temperate and subtropical China.

Climate warming has advanced the spring phenology of many plant species by accelerating heat accumulation. However, delayed phenophases due to insufficient chilling have also been reported. Based on phenological observation data (1963-2010), we compared the effects of preseason chill and heat accumulation on leaf unfolding dates of four deciduous woody species (Lagerstroemia indica, Robinia pseudoacacia, Sophora japonica, and Ulmus pumila) in temperate and subtropical regions of China. Daily chill and heat accumulation were calculated by two chilling models (the Positive Utah Model and the Dynamic Model) and the Growing Degree Hour (GDH) Model. We determined the temporal trends in chill and heat accumulations for leaf unfolding of the four species. The results showed that there were shorter chilling periods in the subtropics than in temperate sites because the chilling period typically started later and ended earlier. There was no significant difference in the length of the forcing period in the different regions. The chilling requirements for leaf unfolding were higher in temperate regions (1344.9-1798.9 chilling units (CU) or 64.7-79.4 chilling portions (CP)) than in the subtropics (1145.9-1828.1 CU or 47.9-75.2 CP). Plants in the subtropics needed higher forcing temperatures (4135.8-10084.8 GDH) than those in temperate regions (3292.0-8383.6 GDH). The earlier-leafing species (e.g., U. pumila) had a lower heat requirement for leaf unfolding than the later-leafing species (e.g., L. indica). A significant increase in heat accumulation was found at all sites except Guiyang, while chill accumulation only increased in Beijing.

Variations in the temperature sensitivity of spring leaf phenology from 1978 to 2014 in Mudanjiang, China.

Continuous long-term temperature sensitivity (ST) of leaf unfolding date (LUD) and main impacting factors in spring in the period 1978-2014 for 40 plant species in Mudanjiang, Heilongjiang Province, Northeast China, were analyzed by using observation data from the China Phenological Observation Network (CPON), together with the corresponding meteorological data from the China Meteorological Data Service Center. Temperature sensitivities, slopes of the regression between LUD and mean temperature during the optimum preseason (OP), were analyzed using 15-year moving window to determine their temporal trends. Major factors impacting ST were then chosen and evaluated by applying a random sampling method. The results showed that LUD was sensitive to mean temperature in a defined period before phenophase onset for all plant species analyzed. Over the period 1978-2014, the mean ST of LUD for all plant species was - 3.2 ± 0.49 days °C-1. The moving window analysis revealed that 75% of species displayed increasing ST of LUD, with 55% showing significant increases (P < 0.05). ST for the other 25% exhibited a decreasing trend, with 17% showing significant decreases (P < 0.05). On average, ST increased by 16%, from - 2.8 ± 0.83 days °C-1 during 1980-1994 to - 3.30 ± 0.65 days °C-1 during 2000-2014. For species with later LUD and longer OP, ST tended to increase more, while species with earlier LUD and shorter OP tended to display a decreasing ST. The standard deviation of preseason temperature impacted the temporal variation in ST. Chilling conditions influenced ST for some species, but photoperiod limitation did not have significant or coherent effects on changes in ST.

Changes in flowering phenology of woody plants from 1963 to 2014 in North China.

Existing evidence demonstrates that the first flowering date (FFD) of most plant species became earlier in response to temperature increase over the past several decades. However, the studies on changes in flowering duration (FD) were limited. By using the non-parametric Theil-Sen estimator, this study investigated the temporal trends in 127 time series of FFD, end of flowering date (EFD), and FD of 97 woody plants from 1963 to 2014 at three sites (Harbin, Beijing, and Xi'an) in North China. The relationship between flowering phenophases and temperature was analyzed using two phenological models. The results showed that most of FFD and EFD time series exhibited an apparent advancing trend. Among them, trends of 52.0% (40.9%) of FFD (EFD) time series were significant (P < 0.05). FFD and EFD time series (95.3 and 89.8%, respectively) responded negatively and significantly to preseason temperature (P < 0.05). The direction of FD changes varied among sites and species. On average, a shortening trend of FD was observed at Harbin (-0.51 days decade-1), with 7.5% of species significantly. However, FD on average extended by 0.42 and 0.93 days decade-1 at Beijing (24.5% significantly) and Xi'an (28.9% significantly), respectively. The regression models could simulate the interannual changes in FFD and EFD with the mean goodness of fit (R2) ranging from 0.37 to 0.67, but fail to simulate the changes in FD accurately (R2 ranging from 0.09 to 0.18). The growing degree day model could improve the R2 for simulating FFD and EFD except for FD. Therefore, more phenological models need to be tested, and more drivers of FD need to be further investigated.

Impacts of global warming on phenology of spring leaf unfolding remain stable in the long run.

The impact of spring temperature forcing on the timing of leaf unfolding of plants (temperature sensitivity, ST) is one important indicator of how and to what degree plant species track climate change. Fu et al. (Nature 526:104-107, 2015) found that ST has significantly decreased from the 1980-1994 to the 1999-2013 period for seven mid-latitude tree species in Europe. However, long-term changes in ST over the past 60 years are still not clear. Here, using in situ observations of leaf unfolding for seven dominant European tree species, we analyze the temporal change in ST over decadal time scales extending the data series back to 1951. Our results demonstrate that ST shows no statistically significant change within shifting 30-year windows from 1951 to 2013 and remains stable between 1951-1980 and 1984-2013 (3.6 versus 3.7 days °C-1). This result suggests that the significant decrease in ST over the past 33 years could not be sustained when examining the trends of phenological responses in the long run. Therefore, we could not conclude that tree spring phenology advances will slow down in the future, and the ST changes in warming scenarios are still uncertain.

Reply to communications by Fu et al. international journal of biometeorology.

Temperature sensitivity of plant phenology (ST) is a determining factor of as to what degree climate change impacts on plant species. Fu et al . (Int J Biometeorol 60:1611-1613, 2016) claimed that long long-term linear trends mask phenological shifts. However, the decreased and increased ST was both found in warming scenarios. The conceptual scheme telling the nonlinear relationship between spring temperature and leaf unfolding date proposed by Fu et al . (Int J Biometeorol 60:1611-1613, 2016) cannot be supported by observation data across Europe. Therefore, linking declined ST to climate warming is misleading, and future ST changes are more uncertain than they suggested.

Geographical pattern in first bloom variability and its relation to temperature sensitivity in the USA and China.

Advance in spring plant phenology over the last several decades has been found in all continents of the Northern Hemisphere. Compared to the studies detecting phenological trends, the studies investigating the geographical pattern of phenological variability (including mean date and magnitude of variability) are rather limited. In this study, we analyzed spatial pattern of mean date and standard deviation (SD) of first bloom date (FBD) time series (≥15 years) for black locust (Robinia pseudoacacia) at 22 stations in China, common lilac (Syringa vulgaris) at 79 stations in the Western US and Chinese lilac (Syringa chinensis) at 45 stations in the Eastern US. Subsequently, the impact of geographical factors (latitude, longitude, and altitude) on the mean date and SD was quantified by using the multiple regression analysis method. Meanwhile, the relationship between FBD variability and temperature sensitivity of FBD was examined. Results showed that the mean FBD highly depended on geographical factors for all the three species. Compared to the mean date, the dependence of SD of FBD time series on geographical factors was weaker. The geographical factors could only explain 13 to 31 % of spatial variance in SD of FBD. The negative regression coefficients of latitude (P < 0.05 except black locust) indicated that FBD is more variable at lower latitude. At most of stations, significant and negative correlations between FBD and preseason temperature on interannual scale were found, but the temperature sensitivity varied among different stations. The magnitude of temperature sensitivity decreased with increasing latitude. In general, the locations at lower latitude had earlier and more variable spring phenophase and showed stronger phenological response to climate change than the locations at higher latitude.