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Article

Chilling and Forcing Requirements of Wintersweet (Chimonanthus praecox L.) Flowering in China

by
Yulong Hao
1,2,
Junhu Dai
1,2,3,*,
Mengyao Zhu
1,
Lijuan Cao
1,2 and
Khurram Shahzad
1,4
1
Key Laboratory of Land Surface Pattern and Simulation, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China
2
University of Chinese Academy of Sciences, Beijing 100101, China
3
China-Pakistan Joint Research Center on Earth Sciences, Chinese Academy of Sciences-Higher Education Commission of Pakistan, Islamabad 45320, Pakistan
4
Nebraska Food for Health Center, Department of Food Science and Technology, University of Nebraska-Lincoln, Lincoln, NE 68588, USA
*
Author to whom correspondence should be addressed.
Forests 2024, 15(10), 1832; https://doi.org/10.3390/f15101832
Submission received: 25 August 2024 / Revised: 16 October 2024 / Accepted: 17 October 2024 / Published: 20 October 2024
(This article belongs to the Special Issue Woody Plant Phenology in a Changing Climate)
Browse Figures
Versions Notes

Abstract

:
Numerous studies have reported phenological changes and their driving mechanisms in spring flowering plants. However, there is little research on the shifts of winter flowering phenology and its response to forcing and chilling requirements. Based on the China Phenological Observation Network (CPON) ground observation data from nine sites over the past 20 years, we explored the spatial and temporal variation patterns of flowering plants and their response to chilling and forcing in wintersweet (Chimonanthus praecox L.), a common winter flowering plant species in temperate and subtropical zones of China. We used three chilling models (chilling hour, Utah, and dynamic models) and the growing degree hours (GDHs) model to calculate each site’s daily chilling and forcing. Using the partial least squares (PLSs) regression approach, we established the relationship between the first flowering date (FFD) and pre-season chilling and forcing in wintersweet, based on which we identified chilling and forcing periods and calculated chilling and forcing requirements. This study found that the FFD of wintersweet in China showed an overall advancement trend during the last 20 years. Still, there were temporal and spatial differences in the FFD of wintersweet among different sites. The PLS results showed that wintersweet also had periods of chilling and forcing, both of which co-regulated wintersweet flowering. We found the forcing and chilling requirements of wintersweet varied significantly from site to site. The higher the latitude is, the more chilling requirements are needed. The chilling requirements for wintersweet were about 6.9–34.9 Chill Portions (CPs) and 1.4–21.6 CP in the temperate and subtropical zones, respectively, with corresponding forcing requirements of 3.2–1922.9 GDH and 965.3–8482.6 GDH, respectively. In addition, we found that the temperature requirements of wintersweet were correlated by a negative exponential relationship, suggesting that chilling and forcing requirements have an antagonistic effect on initiating flowering phenology. Our results could help us understand how flowering dates of winter flowering plants respond to climate change.

1. Introduction

Temperature is one of the most important climatic factors affecting plant phenology [1,2,3,4]. Plants in most temperate deciduous forests require certain low-temperature conditions to release dormancy and the need for low temperatures is known as chilling requirements [5,6,7]. After plants have met their chilling requirements, they need a period of warmth to complete their growth processes, such as budding, leafing, or flowering. Thissubsequent need for warmth is referred to as the forcing requirement. In recent years, the impact of temperature on temperate fruit trees’ phenology has received particular attention due to the effects of global climate change [8,9,10]. Several studies of the subtropics have also revealed that chilling and forcing combine to regulate the budburst initiation [11,12], as is the case with the spring phenology of subtropical plants in China [7,13]. Therefore, the research into tree chilling and forcing requirements has been a central theme in plant phenology and horticultural research [14,15,16,17]. Further research has indicated whether warmer temperatures advanced or delayed spring phenology depended mainly on how well plants meet their chilling requirements in winter conditions [18]. For example, eight Australian apple varieties were reported to have high to moderate chilling requirements [19]. In hotter settings, the need for chilling might be a constraint [10], as warmer winters cause a phenology postponement in the spring [20]. Long-term in situ observations using 1245 sites in Europe indicated that a reduction in chilling counteracts the advance of leaf unfolding in response to spring warming [21]. Studies in the European Alps also revealed that winter warming counteracts the advancing effect of budburst and flowering in response to preseason warming [22]. Winter warming may be beneficial in reducing the risk of exposure to late spring frost; however, this would be detrimental if the chilling requirement is not sufficient to break endodormancy. According to recent research, mild winters in southern France resulted in a 32% decrease in sweet cherry yields [23]. Cold temperatures in winter are crucial in fruit production as they are necessary to release dormancy, flowering, and complete fruit set [24]. Recent research in Germany quantified the chilling requirement for apples and pears to be 43 Chill Portions and 31 Chill Portions, respectively [25]. Another study on Japanese apricots revealed that the plants need more chilling requirements for breaking dormancy and less forcing requirements for flowering [5]. Therefore, quantifying the chilling and forcing requirements of different plants is a necessary process that can help us understand and assess the effects of plant chilling and forcing requirements on phenology and predict plant responses to future regional climates.
Current research has demonstrated the role of chilling in many woody plants and revealed the co-regulatory mechanisms of chilling and forcing. However, most of the studies have focused on spring phenology and there are few cases where winter plant phenology has been studied. Moreover, research on the chilling and forcing requirements of winter flower phenology is still in its infancy due to the scarcity of winter flower species and the need for phenological observations of winter flowers. Therefore, we aim to explore the patterns of flowering phenology of winter flowering (Chimonanthus praecox L.), a representative winter flowering plant in China, in response to temperature changes in different climatic regions and to quantify the chilling and forcing requirements.
It was proved that the partial least squares (PLSs) regression method, is reliable in determining plant chilling and forcing requirements for spring phenophases in temperate and subtropical regions. It has been revealed to be effective in contributing to the study of fruit trees and woody plants, such as apples [19,24,26], apricots [5,27,28], cherries [10,23], and walnuts [14]. Given this, we collected phenological data from nine stations in the China Phenological Observation Network (CPON) from 2000 to 2020. We applied PLS regression to study the relationship between the flowering phenology and wintersweet chilling and forcing requirements. Our primary objectives of this study of flowering of wintersweet were: (1) to characterize the changes in flowering phenology of wintersweet in nine different sites over the past 20 years; (2) to compare the chilling and forcing requirements for flowering determined by the three chilling models (namely chilling hour, Utah, and dynamic models) and a forcing model (growing degree hours model); and (3) to explore the mechanism of chilling and forcing on flowering.

2. Materials and Methods

2.1. Study Sites

We selected nine sites in the China Phenological Observation Network (CPON) that recorded the phenology of wintersweet, distributed in two different climatic zones (Figure 1). Four sites (Beijing, Tai’an, Baoji, and Xi’an) are in the warm temperate zone and five sites (Chongqing, Nanchang, Changsha, Guiyang, Guilin) are in the subtropical zone. The latitude of the study area ranged from 25°04′51″ N to 39°59′23″ N, and the longitude ranged from 106°20′ E to 117°14′55″ E (Table S1).

2.2. Phenological and Meteorological Data

The first flowering date (FFD) data are obtained from CPON. Based on the CPON set criteria, three or more individuals identified were selected for observation and the mean FFD was calculated, with FFD defined as the date when a fixed individual had three flowers fully open. Among the nine stations, only Tai’an and Baoji stations have observed phenology for less than 10 years, while the remaining stations have a record of nearly 20 years (Table S1). Each station’s daily temperature data (daily maximum, minimum, and average temperature) were retrieved from the China Meteorological Science Data Center (http://data.cma.cn/, accessed on 16 October 2024). We used the ideal curve to interpolate the daily maximum and minimum temperature data into hourly temperature data to calculate hourly chilling and forcing requirements.

2.3. Chilling and Forcing Models

In this study, we used three chilling models, the chilling hour model, the Utah model, and the dynamic model, and a forcing model based on growing degree hours (GDHs) to calculate the chilling and forcing requirements of wintersweet. The chilling hour model is the most common. According to Weinberger, plants will enter the dormancy stage and accumulate chilling within the temperature range of 0–7.2 °C [29]. The number of hours counted in this temperature range is recorded as chilling hour (CH). The number of hours that meet the threshold temperature within the chilling period can be calculated.
The Utah model is also a threshold model. It assigns different weights to different temperatures from the chilling hour model. The size of the consequences corresponds to chill units (CUs), one of which is equal to about one hour of exposure at 6 °C. The equivalent contribution of the chill units with specific temperature values is as follows: when the temperature is below or above the optimal temperature, the contribution value of the chilling will be less than 1 or even 0 or negative (for equations, see [30]).
The dynamic model is based on the observation of breaking dormancy under controlled conditions. The model simulates the dynamic development process during dormancy with the assumption that the degree of dormancy completion depends on the level of a specific dormancy-breaking factor accumulated in the bud through two steps [31]. The first step is assumed to be a reversible process of formation and destruction of thermally unstable precursors. The second stage is transformed into a stabilizing precursor that starts after the accumulation of critical parts of the precursors. The second step is the irreversible transition from an unstable precursor to a stable dormancy-breaking factor.
The forcing model, the growing degree hour model (GDH), assumes that the temperature starts accumulating forcing within a specific threshold range, including the base temperature of 4 °C, the optimum temperature of 25 °C, and the critical temperature of 36 °C (for equations, see [32]).

2.4. Determining the Chilling and Forcing Periods Based on PLS

The response of FFD to preseason daily mean temperature was analyzed by partial least squares (PLSs) regression. The two key indicators of partial least squares regression output are the importance of variables in the projection (VIP) and the normalized model coefficient. VIP value is an indicator to measure the extent of the independent variable in explaining the change in the dependent variable, and the threshold of VIP is generally set at 0.8 [33]. The standardized model coefficient represents the intensity and direction of the influence of the independent variables in the PLS model. We used the R language in version 4.2.1 and the “ChillR” package for this study’s statistical analysis.

3. Results

3.1. Trends in the First Flowering Date of the Wintersweet

Among the nine sites, the earliest FFD of wintersweet appeared in Baoji on the 29th day before the end of the year (1 December) (Table S1). The latest FFD is in Beijing on the 38th day after the end of the year (7 February) (Table S1). Most of the nine sites showed an advanced trend, and four of them showed a significant advanced trend (Figure 2, Table S2). The most apparent advance trend of the FFD was in Baoji, with an advance trend of −5.5 ± 1.447 d/a and an average advance trend of −1.692 d/a (Table S2). Only Nanchang and Guiyang showed a weak postponement trend (0.265 ± 0.311 d/a and 0.041 ± 0.277 d/a, respectively) (Figure 2, Table S2).

3.2. Identification of Chilling and Forcing Periods

Taking the dynamic model as an example, we noted that each site accurately identified periods of chilling and forcing. Regarding temperate regions, in Beijing, for example, the start and the end of chilling were most likely to occur between 8 October and 26 November (Figure 3). Chilling was evident in Tai’an between early October and late November (Figure 3). The chilling period in Xi’an was between mid-October and early November (Figure 3). It is noteworthy that the Baoji area in the same temperature zone has the earliest starting date of chilling. (Figure 3). Unlike temperate zones, subtropical regions have longer periods of forcing compared with periods of chilling. Northern wintersweet has a longer chilling period. Four sites in the temperate zone (Beijing, Tai’an, Baoji, and Xi’an) had chilling periods averaging about 43 days, while the five sites in the subtropical zone (Chongqing, Nanchang, Changsha, Guiyang, and Guilin) had chilling periods averaging about 26 days. Similarly, wintersweet in the temperate zone has a more extended period of forcing than in the subtropics. The forcing periods in the temperate and subtropical zones were 39 days and 30 days, respectively.
In temperate regions, the PLS regression results of Beijing, Tai’an, and Xi’an did not show consistently continuous negative model coefficients (Figure 4). Still, there was a pronounced chilling effect during October and November. Beijing showed an apparent clear impact of chilling on phenology in early October and early-mid November (red bars in Figure 4), with a higher accumulation of chilling associated with earlier flowering during these two short periods. Discontinuous negative model coefficients were also shown in the subtropical regions where the effect of chilling was consistent with that of temperate regions. The chilling periods were mainly in November (Figure 4), except for Guiyang. Among the five subtropical observation sites, the Chongqing and Guilin regions manifested continuous chilling periods in mid-late November and mid-November (Figure 4), respectively, indicating a direct relationship between successive chilling periods and the flowering of winter flowering plants in the subtropics. The chilling period in Nanchang was in early to mid-November (Figure 4). In Changsha, chilling effects were evident in early November and early December (Figure 4). Discontinuous periods of chilling appeared in Guiyang from mid-September to early October (Figure 4). Regarding the forcing period, the temperate region had an overall shorter forcing period compared with the chilling period. Both Baoji and Xi’an showed continuous negative model coefficients in November (Figure 4). In contrast, the forcing periods in Beijing and Tai’an are not continuous. The subtropical region suggested negative model coefficients, with the exception of Guilin where forcing periods were constant.
Variations in chilling periods were identified at the same site using different chilling models. In Beijing, the chilling period identified using the Utah model was 75 days (Figure 5), which was higher than the 50 days in the dynamic model and the 47 days in the chilling hour model (Figure 4 and Figure 6). The longest chilling period of 65 days was identified using the chilling hour model in Tai’an (Figure 6). The three chilling models identified basically the same chilling periods in Xi’an. The chilling hour model identified the shortest chilling period in Baoji was 9 days (Figure 6). At the subtropical sites, the three chilling periods of the three chilling models were basically the same in Chongqing. The chilling period was identified by the chilling hour model as the longest chilling period in Nanchang, followed by the Utah model and the dynamic model (Figure 4 and Figure 5). The shortest chilling period identified by the chilling hour model in Changsha is 20 days (Figure 6), which is much less than the 46 days in the dynamic model and the 40 days in the Utah model (Figure 4 and Figure 5). Significant differences in the chilling period in Guiyang were identified using the three models, with the dynamic and Utah models identifying the onset of the chilling effect on 18 September and 10 September (Figure 4 and Figure 5), and the chilling hour model identifying it on 16 October (Figure 6), a difference of nearly one month. The dynamic model showed the shortest chilling period of 13 days in Guilin (Figure 4), lower than the 31 days in the chilling hour model and the 34 days in the Utah model (Figure 5 and Figure 6).

3.3. Quantification of Chilling and Forcing Requirements

By accumulating the daily chilling and GDH, we obtained each site’s chilling and forcing requirements. Based on the PLS regression results, exemplified by the dynamic model, we accurately determined the time points at which chilling and forcing started and ended. The chill portion (CP) of the wintersweet in the temperate regions of Beijing, Tai’an, Xi’an, and Baoji was 26.4 ± 0.1 CP, 34.9 ± 0.1 CP, 7.3 ± 0.2 CP, and 6.9 ± 0.1 CP, respectively. The forcing requirements of these areas are 227.9 ± 3.5 GDH, 3.2 ± 0.2 GDH, 1835.4 ± 26.9 GDH, and 1922.9 ± 23.8 GDH, respectively (Table 1). Compared with the Xi’an and Baoji regions in the same temperature zone, the Beijing and Tai’an regions have more chill portions but fewer forcing requirements. The chill portions of Chongqing, Nanchang, and Changsha in the subtropical region were 8.2 ± 0.2 CP, 3.2 ± 0.1 CP, and 21.6 ± 0.2 CP, respectively, and their forcing requirements were 965.3 ± 28.1 GDH, 1656.3 ± 48.6 GDH, and 1513.7 ± 28.2 GDH, respectively (Table 1). Located in the lowest latitudes, Guiyang and Guilin, have the lowest chill portions and the highest forcing requirements, and the chill portions of the wintersweet in these two regions were 1.6 ± 0.1 CP and 1.4 ± 0.2 CP, with forcing requirements of 8482.6 ± 57.3 GDH and 7613.8 ± 53.0 GDH, respectively (Table 1). Based on the PLS regression results, and using the same methodology, we further determined the chilling and forcing requirements derived from the chilling hour and Utah models for each site (Table 1).

4. Discussion

4.1. Phenological Change in Wintersweet at Different Sites

The present study showed that the FFD of wintersweet in China advanced at an average rate of 1.21 d/a, suggesting that the FFD of wintersweet phenology in China has occurred earlier during the past 20 years, which is similar to the advancement trend obtained in some studies of spring-flowering phenology [34,35], contrary to the conclusion that autumn-flowering phenology showed a delayed trend [36]. It is worth noting that the climatic changes showed large regional differences in the wintersweet phenology, with FFD showing a consistent advancing trend in temperate regions, while FFD showed no progress and even a slight delay at some sites in subtropical regions.
This suggests that the same species can exhibit phenological differences in different climatic conditions, and studies have been conducted to reach similar conclusions [10,34]. In addition, this study revealed that the spatial distribution of FFDs of wintersweet has an obvious pattern. We found that the FFD of wintersweet in China as a whole showed that the higher the latitude, the later the FFD, with a delayed trend of about 2.62 days for each 1° increase in latitude (Figure S1). Previous research using observations from five sites in China showed that the FFD of Osmanthus fragrans in autumn was significantly earlier with increasing latitude, with an advanced trend of 3.11 days/deg latitude [37]. These latitudinal patterns are consistent with previous studies that have examined a wide range of spring species along latitudinal gradients [38,39]. A similar latitudinal pattern has been detected in autumn phenology [40,41].

4.2. Response of Wintersweet FFD to Chilling and Forcing

PLS regression results indicated that the chilling and forcing requirements of wintersweet highly varied in different regions. In temperate areas, the chilling period exhibited discontinuities with short windows, generally interrupted by short periods of lower VIP values or positive model coefficients. A similar pattern we have found in previous studies suggested that the response to chilling is incomplete in the colder temperate regions of the winter, or that there is an interaction between chilling and forcing during this period [20]. We found that the earlier the date of flowering, the lower the chilling requirement in the region. Beijing, Tai’an, and Changsha all had average flowering dates after the end of the year, on the 38th (7 February), 25th (25 January), and 13th (13 January) day, respectively. Their chilling requirement was 26.4 CP, 34.9 CP, and 21.6 CP, respectively, much greater than in other regions where the flowering date was before the end of the year. Areas of flowering dates before the end of the year have a chilling requirement of no more than 10 CP. Interestingly the Changsha region had the highest chilling requirement in the subtropics, showing a clear trend of −1.8 d/a advance in the last 20 years, which was able to be explained by the fact that the chilling requirement in this region can be met in winter. This suggests that the chilling requirement has a positive effect on flowering.
Both chilling and forcing showed significant effects on the flowering of wintersweet at different latitudes, suggesting that chilling and forcing are key factors affecting the flowering of winter flowering plants. Chilling and forcing requirements vary considerably in other latitudes. The higher the latitude, the longer the period of chilling accumulation and the more chilling requirements of the wintersweet. The less chilling requirements need to be met in lower latitudes. Conversely, subtropical areas have more forcing requirements compared to temperate zones. However, there are still more days of forcing accumulation in temperate regions than in the subtropical areas, which is understandable as temperatures are lower in temperate regions in winter. It takes longer, but only a small amount of forcing is needed. In addition, the chilling period is shorter in the subtropics than in the temperate zone (Figure 4), but at the same time, more continuous, which suggests that the chilling process in winter flowering plants is rapidly completed in the subtropics within a short period (Figure 4). In addition, we also noted that the distribution of wintersweet ranges from about 25° N in the southernmost Guilin to about 40° N in the northernmost Beijing area, spanning nearly 15 latitudes. We concluded that the flowering phenology of wintersweet is subject to both chilling and forcing and that the forcing compensates for the chilling and jointly regulates winter flowering. Previous studies have also supported the view that flowering can be delayed in warm climates when the species with a chilling requirement do not obtain sufficient cold temperatures [5]. The negative exponential relationship between chilling and forcing, showing antagonistic effects, is consistent with the response pattern of spring flowering plants, which has been revealed in many established studies [42,43,44].
In our study, we also found that the chilling and forcing requirements of wintersweet conformed to a negative exponential relationship (Figure 7), suggesting that chilling and forcing have antagonistic effects on the initiation of flowering phenology in winter flowering plants. For example, of the nine sites, only Nanchang and Guiyang indicated a delayed trend in wintersweet phenology. However, over the last two decades, the accumulation of chilling in these two regions has mainly been continuous and has met the appropriate chilling requirements; therefore, the delay in these two areas can be attributed to a decrease in winter accumulation of forcing. We also noted the advanced trend in Baoji is the most pronounced. The results also revealed that the chilling and forcing periods in Baoji were the most continuous among all the sites, suggesting that the FFD of the Baoji wintersweet was significantly advanced after the chilling requirement and the forcing requirement were met (Figure 4).

4.3. Difference in Chilling and Forcing Requirements Between Sites, Species and Methods

Wintersweet can respond quickly and sensitively to autumn and winter weather or local meteorological conditions, i.e., the FFD of wintersweet is more susceptible to being controlled by short-term meteorological conditions. This increases the uncertainty of FFD in winter plants. In addition, we found zonal differences in chilling and forcing requirements of the same plant species. This is consistent with the conclusion that phenological responses of the same species are site-specificity [45]. This contradicts the common belief that climate requirements are determined by species-specific traits and genes. We hypothesize that winter meteorological and climatic conditions in the warmer regions may not meet their chilling requirements, as winter flowers require more forcing to flower in warm winter contexts. In contrast, temperate regions only need little forcing to meet their forcing requirements, as in Beijing and Tai’an. This suggests that the higher the latitude, the more pronounced the response to a warm winter. Still, winter flower phenology in these areas may vary significantly in inter-year due to their lower and easy-to-be-met forcing requirements.
Compared to common spring flower plants, winter flower plants were found that have less chilling and forcing requirements. A study of the chilling and forcing requirements of 23 Prunus cultivars showed that the chilling requirements varied from 20 to 63.4 CP and the forcing requirements varied from 4381 to 8647 GDH [17]. Another study on the Japanese apricot (Prunus mume), a species flowering in winter and spring with a chilling requirement between 24 and 82 CP and a forcing requirement between 691.9 and 2634.7 GDH [5], which seems to be the closest to wintersweet’s FFD, may provide some reference for our study. However, the results showed that it had higher chilling requirements compared to wintersweet (Chimonanthus praecox). As far as we know, there are few systematic studies on winter flowering in the northern hemisphere and even fewer on wintersweet. The main reason is the lack of observations and experimental data due to the few varieties of winter flowers. Unfortunately, therefore, our study is a valuable addition to the field of winter flower phenology.
We analyzed three chilling models using PLS regression and showed that all three models portrayed a negative correlation between chilling requirements and forcing requirements, with the dynamic model providing the best performance (Figure 7). We determined that the chilling hour model can be useful in characterizing the chilling and forcing requirements of winter flowers. However, given that winter flowers bloom when winter temperatures reach below zero degrees Celsius in some areas and that the chilling hour model considers temperatures above 0 °C to be the effective temperature for chilling, we still believe that the chilling hour model substantially underestimates chilling requirements. In temperate and even colder regions, the chilling requirement is greater than our results suggested. The Utah model was first developed as a crop model for peach flowering in Utah. By weighting temperatures above 0 °C, the model assumes that higher temperatures will offset the accumulated chilling. The effective temperature is considered to be between 1.4 and 15.9 °C, and chilling is offset at temperatures higher than 15.9 °C [46]. For subtropical winter flowering plants, the model would greatly diminish the effect of chilling on flowering phenology. We still need to develop a better model to accurately describe winter flower phenology concerning chilling and forcing. Some findings suggested slight negative temperatures, e.g., −2 °C, can be defined as effective chilling temperatures [47,48], and growing evidence showed the contribution of sub-freezing temperatures to chilling requirements [43,49,50,51]. Thresholds need to be defined and weights need to be differently assigned to the condition for temperatures below 0 °C. It will benefit winter flower plants when they are taken into account in the future evaluation of the chilling model. Therefore, there is an urgent need to construct a reasonable winter flower model universally applicable to a wide range of winter flower species. Further experimental studies are necessary to determine the effective temperature of the chilling of winter flower plants. In addition, a limitation that should not be ignored is that the validity and feasibility of using traditional spring flower models to explain winter flower phenology deserve further investigation.

5. Conclusions

Based on nearly 20 years of ground-based observations, we analyzed the temporal and spatial variation in the FFD in wintersweet through a representative Chinese winter flowering plant and have conducted a systematic study on the response of winter flowering plant phenology to chilling and forcing requirements. We showed an increasing trend in FFD for wintersweet at most sites, but the magnitude of variation in FFD varied across sites. Our study also revealed the differences and connections between the phenological response of temperate and subtropical wintersweet to chilling and forcing. The results indicated that wintersweet flowering was co-regulated by chilling and forcing. Compared to subtropical regions, wintersweet has more chilling requirements and less forcing requirements in temperate regions, yet we noted that it has longer forcing periods. This may be related to the greater daily temperature differences in the temperate areas during winter, as we found that the periods of chilling and forcing are relatively more continuous in the subtropics. Moreover, we have found that even winter flower plants have to meet a certain amount of chilling and forcing requirements in sequence to complete the flowering process, which is consistent with the pattern of spring flowering plants responding to chilling and heat requirements, i.e., chilling and forcing also conform to a negative exponential relationship. The difference is that winter flowering plants have much lower chilling and forcing requirements than the common spring flowering plants. Our study will effectively provide a reference for research on the response of winter flowering plants to climate change, especially for increasingly warm winters. We hope to draw attention to the significance of winter phenology through a case study of a representative winter flowering plant.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/f15101832/s1, Figure S1: The relationship between FFD and latitude in Chinese wintersweet; Table S1: Basic information on phenological observation sites includes the site’s name, latitude, longitude, altitude, observation period, first flowering dates, and end flowering dates; Table S2: The result of a linear fitted equation of the FFD of wintersweet at nine sites in China during the past two decades. Including Linear fitted equation, Slope, Pearson’s r, R2, and p-value.

Author Contributions

Conceptualization, J.D.; software, Y.H.; writing-original draft preparation, Y.H.; writing-review and editing, J.D.; data curation, L.C.; supervision, M.Z., and K.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the National Key Research and Development Program of China (Grant No. 2023YFF1303804) and the National Natural Science Foundation of China (Grant No. 42271062).

Data Availability Statement

The data presented in this study are available on request from the corresponding author. The data are not publicly available due to privacy.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Overview of the study sites. (a) Geographical locations of phenological observation stations in China. (b) Mean daily temperature at nine stations in China during 2000–2020.
Figure 1. Overview of the study sites. (a) Geographical locations of phenological observation stations in China. (b) Mean daily temperature at nine stations in China during 2000–2020.
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Figure 2. Trends of first flowering date (FFD) of wintersweet at nine sites in China during the past two decades.
Figure 2. Trends of first flowering date (FFD) of wintersweet at nine sites in China during the past two decades.
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Figure 3. Chilling and forcing periods of Chinese wintersweet in the last two decades were identified using the dynamic model. The blue and red dots in the figure indicate the start and end of the chilling period and the start and end of the forcing period, respectively. The dotted line in the graph indicates the last day of the year, corresponding to a DOY of 365.
Figure 3. Chilling and forcing periods of Chinese wintersweet in the last two decades were identified using the dynamic model. The blue and red dots in the figure indicate the start and end of the chilling period and the start and end of the forcing period, respectively. The dotted line in the graph indicates the last day of the year, corresponding to a DOY of 365.
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Figure 4. Model coefficients for partial least squares regression between wintersweet flowering date and chilling and forcing. Using the dynamic model and GDH model for chilling and forcing calculation. The left panel (a) indicates chilling accumulation and the right panel (b) indicates forcing accumulation. Negative and significant model coefficients are marked by red bars and positive and significant model coefficients by green bars. Blue shading and pink shading indicate chilling and forcing periods, respectively. The range of flowering dates is indicated by gray shading, and the dashed line indicates the mean flowering date.
Figure 4. Model coefficients for partial least squares regression between wintersweet flowering date and chilling and forcing. Using the dynamic model and GDH model for chilling and forcing calculation. The left panel (a) indicates chilling accumulation and the right panel (b) indicates forcing accumulation. Negative and significant model coefficients are marked by red bars and positive and significant model coefficients by green bars. Blue shading and pink shading indicate chilling and forcing periods, respectively. The range of flowering dates is indicated by gray shading, and the dashed line indicates the mean flowering date.
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Figure 5. Model coefficients for partial least squares regression between wintersweet flowering date and chilling and forcing. Chilling and forcing were calculated by using the Utah model and GDH model, respectively. (a) indicates chilling accumulation; (b) indicates forcing accumulation. See the caption of Figure 4 for details.
Figure 5. Model coefficients for partial least squares regression between wintersweet flowering date and chilling and forcing. Chilling and forcing were calculated by using the Utah model and GDH model, respectively. (a) indicates chilling accumulation; (b) indicates forcing accumulation. See the caption of Figure 4 for details.
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Figure 6. Model coefficients for partial least squares regression between wintersweet flowering date and chilling and forcing. Chilling and forcing were calculated by using the chilling hour model and GDH model, respectively. (a) indicates chilling accumulation; (b) indicates forcing accumulation. See the caption of Figure 4 for details.
Figure 6. Model coefficients for partial least squares regression between wintersweet flowering date and chilling and forcing. Chilling and forcing were calculated by using the chilling hour model and GDH model, respectively. (a) indicates chilling accumulation; (b) indicates forcing accumulation. See the caption of Figure 4 for details.
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Figure 7. The relationship between chilling requirements and forcing requirements by using three chilling models, dynamic model (a); chilling hour model (b); Utah model (c). The black dots represent the chilling and forcing requirements for each site. The red line is the fitted curve.
Figure 7. The relationship between chilling requirements and forcing requirements by using three chilling models, dynamic model (a); chilling hour model (b); Utah model (c). The black dots represent the chilling and forcing requirements for each site. The red line is the fitted curve.
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Table 1. Chilling and forcing periods and requirements (mean ± standard deviation) of the wintersweet at nine sites. We calculated chilling requirements according to the dynamic (in CP), chilling hour (in CH), and Utah (in CU) models. The growing degree hours model (in GDH) was used to estimate forcing requirements.
Table 1. Chilling and forcing periods and requirements (mean ± standard deviation) of the wintersweet at nine sites. We calculated chilling requirements according to the dynamic (in CP), chilling hour (in CH), and Utah (in CU) models. The growing degree hours model (in GDH) was used to estimate forcing requirements.
SitesChilling PeriodChilling Requirements/Mean ± sdForcing PeriodForcing Requirements/Mean ± sd
StartEndStartEnd
Beijing7 October22 November355.6 ± 2.2 (CH)15 December19 February204.5 ± 3.7 (GDH)
4 September16 November−231.0 ± 3.3 (CU)15 December21 January51.7 ± 2.0 (GDH)
8 October26 November26.4 ± 0.1 (CP)11 November5 February227.9 ± 3.5 (GDH)
Tai’an26 September30 November658.9 ± 0.8 (CH)2 December10 January6.6 ± 0.4 (GDH)
4 October26 December756.1 ± 2.7 (CU)8 December10 January3.7 ± 0.3 (GDH)
5 October26 November34.9 ± 0.1 (CP)10 December10 January3.2 ± 0.2 (GDH)
Xi’an16 October20 November153.9 ± 2.6 (CH)5 November28 November1871.4 ± 26.5 (GDH)
22 September30 October−249.2 ± 4.9 (CU)6 November 27 November1683.8 ± 26.2 (GDH)
8 October4 November7.3 ± 0.2 (CP)5 November27 November1835.4 ± 26.9 (GDH)
Baoji22 October31 October46.6 ± 2.5 (CH)26 October27 November2203.5 ± 24.7 (GDH)
9 September23 October−249.4 ± 4.5 (CU)28 October27 November1922.9 ± 23.8 (GDH)
8 September21 October6.9 ± 0.1 (CP)28 October27 November1922.9 ± 23.8 (GDH)
Chongqing10 November1 December8.6 ± 1.3 (CH)2 November15 December1006.4 ± 30.3 (GDH)
13 November1 December56.3 ± 5.9 (CU)6 December12 December829.9 ± 28.5 (GDH)
10 November3 December8.2 ± 0.2 (CP)5 December12 December965.3 ± 28.1 (GDH)
Nanchang26 September24 November26.8 ± 1.1 (CH)24 November3 December1593.3 ± 48.0 (GDH)
6 October13 November−581.6 ± 4.1 (CU)14 November3 December3766.6 ± 53.7 (GDH)
26 October20 November3.2 ± 0.1 (CP)23 November2 December1656.3 ± 48.6 (GDH)
Changsha22 November11 December123.6 ± 4.0 (CH)12 December20 January1662.6 ± 28.8 (GDH)
7 November16 December317.4 ± 5.3 (CU)15 December20 January1443.4 ± 27.9 (GDH)
4 November19 December21.6 ± 0.2 (CP)14 December20 January1513.7 ± 28.2 (GDH)
Guiyang16 October28 November124.9 ± 2.5 (CH)12 November6 December2807.5 ± 53.0 (GDH)
10 September19 October−513.9 ± 5.0 (CU)20 October44 December8203.7 ± 57.1 (GDH)
18 September15 October1.6 ± 0.1 (CP)19 October4 December8482.6 ± 57.3 (GDH)
Guilin4 November44 December21.4 ± 1.7 (CH)26 November16 January6857.9 ± 52.5 (GDH)
22 October24 November−404.6 ± 5.5 (CU)25 November15 January7018.3 ± 52.4 (GDH)
8 November20 November1.4 ± 0.2 (CP)22 November13 January7613.8 ± 53.0 (GDH)
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Hao, Y.; Dai, J.; Zhu, M.; Cao, L.; Shahzad, K. Chilling and Forcing Requirements of Wintersweet (Chimonanthus praecox L.) Flowering in China. Forests 2024, 15, 1832. https://doi.org/10.3390/f15101832

AMA Style

Hao Y, Dai J, Zhu M, Cao L, Shahzad K. Chilling and Forcing Requirements of Wintersweet (Chimonanthus praecox L.) Flowering in China. Forests. 2024; 15(10):1832. https://doi.org/10.3390/f15101832

Chicago/Turabian Style

Hao, Yulong, Junhu Dai, Mengyao Zhu, Lijuan Cao, and Khurram Shahzad. 2024. "Chilling and Forcing Requirements of Wintersweet (Chimonanthus praecox L.) Flowering in China" Forests 15, no. 10: 1832. https://doi.org/10.3390/f15101832

APA Style

Hao, Y., Dai, J., Zhu, M., Cao, L., & Shahzad, K. (2024). Chilling and Forcing Requirements of Wintersweet (Chimonanthus praecox L.) Flowering in China. Forests, 15(10), 1832. https://doi.org/10.3390/f15101832

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