4.1. The Significant Correlation between the Leaves and Increasing Leaf Size Stages and the SOS
Ground-based observations of vegetation phenology data provide important validation data for assessing phenology metrics obtained by inverting remote-sensing data. Previously, ground observations were mainly used to make coarse spatial resolution assessments at ecosystem scales [
47,
48,
49]. In this study, it was found that the onset of ground-based phenological stages at each site, as obtained using the mean ascending-scale aggregation method, was significantly correlated with the SOS derived from Sentinel-2 data. In particular, the SOS was found to be closely correlated with the leaves and increasing leaf size stages. Furthermore, the simulation based on the Weibull distribution model indicated that an LUD of 13% corresponded most closely to the SOS. The sharp increases in vegetation index values in spring are closely related to leaf unfolding and is associated with an increase in the leaf area index and chlorophyll concentration [
50]. In the study by Bórnez et al. [
51], it was found that for deciduous broadleaf forests in Europe and the United States, the RMSE between ground-based observations of the increasing leaf size and leaves stages and the satellite-derived SOS was 9 days and 11 days, respectively. During the leaves stage, the entire leaf structure emerges from the leaf buds, and the expanded leaves become visible. Both the leaf area and chlorophyll concentration increase during this stage. The remote-sensing index, NDVI, shows a significant increase during this phase, and it is commonly accepted that ground-based observations of the leaves stage correspond to the remote sensing-derived SOS. Studies have found a significant positive correlation between the remotely sensed SOS and the leaves stage, with the highest correlation being observed for broadleaf forests in the eastern United States [
17]. White et al., conducted a study comparing the relationship between the SOS and ground-based observations of phenological stages in North America. These results also indicated a significant correlation between the SOS and ground-based determination of the leaves stage [
16]. Additionally, Luo et al., conducted research in northern China, comparing four tree species, and found that the remotely sensed SOS extracted from GIMMS NDVI3g data was highly consistent with ground-based observations during the leaves stage [
52]. During the increasing leaf size stage, most leaves on the plants have not yet reached their full size and continue to grow. It is known that the leaf area continues to expand during this stage, resulting in a noticeable increase in the NDVI. Liang et al., found that there was consistency between the SOS and the duration of the increasing leaf size stage as determined by ground observations [
53]. Together, these studies confirm the high level of agreement between the occurrence of the SOS, the leaves stage, and the duration of the increasing leaf size stage. The findings of the current study are thus in line with the existing literature, further confirming the reliability of the results.
4.2. Variations in the Relationship between the LUD and SOS between Species
The phenology of plants is influenced by their genetic characteristics, as different species possess distinct biological clocks and growth habits, resulting in variations in their lifecycles. For instance, early spring flowering plants may be influenced by factors such as temperature and sunlight, whereas plants that bloom in the summer can be affected by rainfall and temperature. Even when exposed to the same conditions, there can be considerable differences in spring phenology between plants of the same type [
54,
55]. Different deciduous broadleaf tree species exhibit differences in leaf-fall and budburst timing [
56]. Inter-specific differences in spring phenology are also believed to be strongly influenced by varying species-specific requirements for warming and chilling, as well as differences in sensitivity to abiotic drivers [
57]. For example, the sensitivity to spring temperature differs significantly between oka and beech, with budburst advancing by 7.26 days and 2.03 days, respectively, for every 1 °C increase in temperature [
58]. Previous research has shown that the vegetation phenology of different species exhibits different temperature sensitivities and that this can lead to either the compression or extension of growing seasons [
59,
60,
61]. Plant species with earlier leaf-unfolding times tend to have a higher temperature sensitivity, enabling them to initiate growth earlier and gain a competitive advantage in interspecific competition as spring temperatures rise.
The physiological structures, morphological characteristics, and environmental adaptability of plant species vary greatly with ecological type. Previous studies have shown that the consistency between remote-sensing and ground-based phenology varies depending on the species and vegetation type [
62,
63,
64], and the findings of this study are consistent with previous research. We selected species from the W/HD ecological region with sample sizes exceeding 30 to investigate the variations in the differences between the SOS and the corresponding occurrence of the LUD at different simulated LUDs for different species within the same ecological zone. The results are shown in
Figure 9. The results indicate that there are differences in the LUD that correspond to the minimum difference between the SOS and the simulated LUD for different species. For red maple, the smallest difference occurs at LUD
16%, for platanus orientalis, this occurs at LUD
29%, for Northern quercus rubra, it occurs at LUD
13%, for sugar maple, the smallest difference occurs at LUD
11%, for Florida privet, it occurs at LUD
19%, and for black cherry, it occurs at LUD
27%.
Temporal variations in vegetation phenology and physiological variables are highly heterogeneous in space, within species, and between species [
21,
65]. Within the same plant community, different species may employ distinct strategies to cope with climate change, and numerous factors contribute to variations in the timing of leaf unfolding for plants of both the same and of different species. These include environmental factors such as temperature, humidity, rainfall, and CO
2 concentration [
66] as well as the genetic characteristics of the different species themselves [
67]. Influencing biotic factors include insects and fungi [
68], tree height, and canopy density. Furthermore, not all species respond to the same driving factors, such as spring temperature increase, at the same rate [
56,
69,
70,
71]. In this study, we focused on nine representative species and calculated the relevant Pearson correlation for each species to investigate the factors driving the phenology of different species (
Table 4 and
Table 5).
The above results reveal that there are variations in the response of LUD13% and SOS to the changes in the three environmental factors between the nine representative species. For LUD13%, for all species, the highest correlation is with Tmean—the correlation is negative in all cases. The strongest correlation of all is for fragrant sumac, which has a correlation coefficient of −0.801; American beech (−0.799) and red maple (−0.771) follow closely. For the other species such as Florida privet, black cherry, and sugar maple, the absolute value of the correlation coefficient is in the range 0.4 to 0.6. However, while the SOS shows a negative correlation with Tmean, there are also species whose SOS exhibits a positive correlation with Tmean. The SOS of five species—red maple, black cherry, sugar maple, American beech, and fragrant sumac — is significantly negatively correlated with Tmean, with correlation coefficients ranging from −0.48 to −0.13. In contrast, the SOS of lagerstroemia speciosa shows a significant positive correlation with Tmean, with a correlation coefficient of 0.246. Overall, for SOS, the most significant positive correlation is with srad, with all the correlation coefficients exceeding 0.8. For most species, the correlation coefficients between the time of occurrence of LUD13% and srad range from around 0.2 to 0.4, with the value for white oak being just under 0.2. For all species, the SOS shows a significant positive correlation with pre, with correlation coefficients ranging from 0.3 to 0.5. These findings suggest that there are notable differences in the response of LUD13% and remote sensing-derived phenology to different climate conditions.
4.3. Influence of the Ecological Zone on the Correlation between the LUD and SOS
Plant phenology is not only influenced by the species, but also by the growth environment, as plants respond to environmental factors by adjusting the timing of their leaves, leaf senescence, and flowering stages [
72,
73,
74]. The growth of plants relies on external environmental factors such as the temperature, as well as the availability of nutrients, water, and light; these factors vary between ecological regions and provide varying conditions for plant growth. Consequently, plants may exhibit different phenological patterns in different regions. Furthermore, there are genetic differences between the phenological responses of populations growing under different climatic conditions [
75]. Studies have shown that the degree of spring leaf unfolding is influenced by the interaction between nutrient availability and soil moisture, and that the earlier occurrence of spring phenological phases exhibits regional and interspecies variations [
76,
77]. Within a plant community, the responses of canopy trees, understory shrubs, and herbaceous plants to changes in the growth environment can affect the competition for water and soil nutrients between these functional groups [
75].
There are significant differences in leaf unfolding phenology between plant species, and even within the same species, there are differences in the timing of leaf unfolding in different habitats [
56,
78,
79]. The findings of our study confirm these observations. We calculated the proportion of sites where the SOS corresponds to the LUD at the leaves stage for the same species in different ecological regions (
Figure 10). The results indicate that for red maple, the ratio of the LUD to SOS in the W/HD and S/SD regions is similar. For fragrant sumac, this ratio of the LUD between 1% and 4% is slightly higher in the S/SD ecological region than in the W/HD ecological region, and the proportion of sites with an LUD of above 95% is also slightly higher in the S/SD region. For privet, in the S/SD ecological region, the ratio of the LUD to SOS is slightly higher than in the W/HD ecological region for an LUD between 1% and 4% but slightly lower for an LUD above 95%. For black willow, the ratio of the LUD between 1% and 4% to SOS is significantly lower in the S/D ecological region than in the W/HD region. In addition, the proportion of sites with an LUD of between 25% and 49% is lower in in the S/D ecological region than in the W/HD region but the proportion of sites with an LUD in the range 50–74% is significantly higher. For trembling willow, there is significant variation in the ratio of the LUD to SOS across the W/HD, S/D, and M/MD ecological regions. The lowest ratio (1–4%) occurs in the S/D ecological region, and the highest value occurs in the M/MD region. Furthermore, in the S/D ecological region, the proportion of sites with an LUD between 75% and 94% or above 95% is greater than in the other two ecological regions.
We also calculated the difference between the SOS and the corresponding LUD time for all species within the four ecological zones, as shown in
Figure 11. We found that there are differences in the LUD that corresponds to the minimum time difference between the SOS and simulated LUD between the different regions. In M/MD, the smallest difference is observed at LUD
10%, whereas in S/D, the smallest difference occurs at LUD
22%, and in S/SD, the smallest difference is observed at LUD
20%. In the W/HD ecological zone, the smallest difference occurs at LUD
12%. Notably, the standard deviation in the W/HD ecological zone remains at around 20 days and exhibits minimal variation as the LUD increases.
Different species exhibit varying degrees and even directions of response to environmental changes, and these differences also vary with the location. Research indicates that, over the past 40 years, the onset of leaf unfolding in temperate tree species has become significantly earlier, a trend that has been attributed to climate warming. Studies of long-term temperature sensitivity and the factors influencing spring plants have revealed a significant positive correlation between the reproductive phase of most species and temperature [
80]. Other studies conducted using modeling and remote sensing in temperate forests have also indicated that the spring leaves stage has advanced in recent decades (at a rate of 1.8–7.8 days per decade) although there are variations between species. In high-altitude and high-latitude regions, the amount of snow accumulation and the time when snow-melt occurs are two key additional factors that influence plant phenology [
81]. The availability of water can also influence phenology in temperate and boreal forests—but to a lesser extent than temperature [
82]. Changes in water availability can lead to complex phenological changes and may have profound effects on ecosystem functionality and structure. Dry and wet tropical climates are distinguished by the amount of precipitation and its seasonal variation, and differences in community phenology levels are often driven by the duration of the dry season [
83]. Previous studies have confirmed that, in tropical regions, temperature, precipitation, and radiation can interact and have complex effects on plant phenology [
84,
85,
86]. In addition to being constrained by water stress, the leaf unfolding time in tropical forests is also correlated with the annual peak radiation [
83]. Solar radiation (total sunshine duration, peak radiation, or photoperiod) is also considered a primary driving factor of tropical phenology [
87]. In most tropical grassland areas, precipitation is a driving factor of plant phenology, and the inverse relationship between radiation and phenology is consistent with the inhibition of grassland growth due to soil moisture limitations [
87]. Temperature is a key driving factor for most species, but precipitation, through its influence on soil moisture, is also important in many cases [
88]. Summer drought resulting from low precipitation is a typical characteristic of Mediterranean ecosystems, and the seasonal variation in water availability controls vegetation activity, with most plant growth occurring during the colder but wetter times of the year [
89,
90]. In semiarid and arid desert ecosystems, phenological changes resulting from climate change can be driven by both the timing and amount of precipitation, as well as the increase in temperature. Water availability appears to be a key driver of phenology in arid and semiarid ecosystems [
91], whereas temperature and humidity are the primary drivers of phenology in grassland ecosystems [
24].
To investigate the driving factors of phenology in different ecological regions, specifically temperature, precipitation, and radiation, we calculated the Pearson correlation coefficients between both the timing of LUD
13% and SOS and these three environmental factors in the M/MD, S/D, S/SD, and W/HD ecological regions (
Table 6 and
Table 7).
Table 6 reveals significant negative correlations between the timing of LUD
13% and Tmean in all four ecological regions. In some cases, there is a significant positive correlation with pre. For all four regions, the correlation coefficient between the timing of LUD
13% and Tmean is around −0.5. It is notable that the M/MD and S/SD ecological regions have similar correlation coefficients (−0.539 and −0.534, respectively) that are slightly higher than those of the other two regions. The lowest correlation occurs in the S/D region. In both the M/MD and S/D ecological regions, there is a significant correlation between the timing of LUD
13% and pre—the correlation coefficients are 0.162 and 0.207, respectively. In all four regions, the relationship between the timing of LUD
13% and srad is close to or slightly below 0.2 and is lowest in the M/MD region (0.145). Notably, in the M/MD and S/D regions, the timing of LUD
13% is significantly correlated with all three environmental variables, whereas in the S/SD and W/HD regions, there is only an association with Tmean and srad.
Table 7 indicates that there are significant correlations between the remotely sensed vegetation phenology and Tmean, pre, and srad in all four ecological regions. The correlation with srad was found to be higher than that with Tmean and pre. In all four regions, the correlation with Tmean is significantly negative: the M/MD region has the strongest negative correlation, with a coefficient of −0.337; this is followed by the S/D region with a coefficient of −0.278, then the S/SD ecological region with a coefficient of −0.229, and finally the W/HD ecological region with a coefficient of only −0.033. In contrast, in all four regions, the SOS shows a significant positive correlation with pre. The M/MD ecological region has the highest correlation with a coefficient of 0.513, and the S/D region has the lowest correlation with a coefficient of 0.261. The S/SD and W/HD regions have similar correlation coefficients of 0.366 and 0.368, respectively. In all four regions, the SOS also shows a significant positive correlation with srad. The M/MD region has the lowest correlation with a coefficient of 0.681, whereas in the S/D ecological region the correlation coefficient is 0.812. The S/SD and W/HD regions have similar correlation coefficients of 0.91 and 0.922, respectively.
4.4. Effects of Vegetation Phenology Monitoring and Modeling on the Relationship between LUD and SOS
Because of the proven reliability of vegetation spring phenology monitoring using remote-sensing indices such as the NDVI and the Enhanced Vegetation Index (EVI), particularly as applied to large geographical areas [
4,
13,
92,
93,
94], this type of monitoring has become widely used in recent years. However, it is important to acknowledge that the processes of leaf unfolding and leaf-fall occur gradually over large geographical areas. Consequently, these remote-sensing data products have certain limitations in terms of continuous observations of phenology, which leads to a lag in the detection of vegetation changes. Furthermore, there are inherent differences in the quality of information obtained from ground-based phenological observations and remote-sensing retrievals, which leads to discrepancies between them [
95,
96].
Firstly, remote-sensing observations of forests are made from a zenithal angle, capturing signals from the top of the canopy, whereas ground-based observations collected by field technicians focus on the bottom of the canopy; this results in potential discrepancies between the phenological information obtained by the two methods. To date, most studies use indirect methods to identify phenology variation based on the time series of PhenoCam images. PhenoCam involves mounting digital cameras with visible-wavelength imaging sensors above vegetation canopies to capture images throughout the day [
97]. Near-surface observations from PhenoCam provide time series of images that are ideal for tracking seasonal changes in leaf phenology, and have been used to extract leaf phenology metrics [
98] and track biodiversity [
99]. The current studies have proven that PhenoCam images carry useful information for monitoring and understanding leaf phenology. Secondly, LSP and ground-based observations are concerned with different characteristics [
95]. Ground-based observations target individual plants or species at a specific scale, while remote sensing provides aggregated information related to vegetation growth at the pixel scale [
19]. Since image pixels often contain multiple land cover types or species, the presence of heterogeneous vegetation cover can introduce errors in phenological dates obtained from remote-sensing data, as compared with ground-based observations. In addition, the pixels neighboring the pixel of interest can influence the signal received by the satellite, as the ground area corresponding to the analyzed pixel may not entirely correspond to the actual area contributing to the detected signal [
100]. Zhang [
101] also noted that the extraction of SOS results at coarse resolutions is predominantly determined by pixels where the SOS occurs earlier. However, there are also uncertainties inherent in ground-based phenological observations. For example, the phenological data collection strategy employed by the USA-NPN requires field technicians to monitor the occurrence, duration, and intensity of key phenological events and record them in discrete categories that may not fully capture the gradual transitions in leaf phenology. The Weibull distribution is increasingly used to estimate the dates of hard-to-observe phenological events, such as first and last flowering dates [
102,
103]. These contrasting results occur because of sampling biases in the raw data, which the statistical estimator corrects by providing estimates for the true statistical data. However, estimating the true onset or offset of a process may be more challenging than estimating a percentile of the phenology curve within the bounds, because it is notoriously difficult to model the tails of distributions as there are fewer data points to parameterize the model [
103]. Finally, there is no universally applicable algorithm for phenological parameter extraction [
104]. The threshold method used for SOS extraction is simple and effective, and it is widely used. However, it is subject to significant subjective factors (such as the different thresholds provided by different researchers, which can lead to noticeable variations in the length of the growing season) and does not fully take into account environmental influences (such as differences in the soil background and vegetation type) [
105]. Researchers have confirmed that the consistency between LSP and ground-based phenology varies depending on the species or vegetation type [
62,
64,
106]. On the other hand, the derivative method, although threshold-free and biologically meaningful, is more sensitive to data noise, requiring higher smoothness requirements at the data preprocessing stage [
107]. Additionally, in cases where the vegetation index curve does not exhibit abrupt changes, determining the start and end dates of the growing season becomes challenging, particularly when there is cloud contamination in the time series data of the vegetation index. The retrieval of phenology using remote sensing offers the advantage of broad spatial coverage; however, the results are influenced by various factors, including atmospheric disturbances, solar radiation effects, cloud cover, and the duration of snow cover [
108]. This limits the capability of remote-sensing data to capture species-specific phenological information.
The process of monitoring LSP is strongly influenced by ecosystem processes and vegetation types [
16,
109,
110,
111]. Previous studies have shown that LSP estimation is most reliable in deciduous forests but becomes challenging in evergreen forests [
109,
110,
112,
113,
114,
115]. We analyzed the relationship between ground-based observations and remote-sensing spring phenology retrievals at the species and ecological region levels. However, due to limitations in the available data, the species composition was relatively homogeneous, with a predominance of deciduous broadleaf species. Consequently, we did not specifically analyze the relationship between ground-based observations and the remotely sensed phenology for different vegetation types. To improve the comparability and spatiotemporal consistency of phenological parameter results obtained from different regions and time periods, further research needs to be done to develop universally applicable phenological extraction algorithms. Additionally, while this study examined the relationship between ground-based observations, remote-sensing retrievals of vegetation spring phenology, and the associated environmental driving factors under different conditions, a model that can convert ground-based observations to remotely sensed spring phenology data still needs to be developed. Future research should address this gap to enable the application of the findings from this study to the validation of remote-sensing retrievals of vegetation spring phenology. This will allow more accurate information relating to plant phenology and leaf unfolding to be obtained using remote-sensing data.