**4. Discussion**

#### *4.1. Changes in the Green-up Dates Depending on Land Use Intensity*

Land use by human activities releases greenhouse gases, and the increase in development areas and populations causes urban heat islands and changes the microclimate [6,37,72,73]. Massive urban sprawling can bring about more deforestation, habitat destruction, and greenhouse gas (GHG) or carbon emissions, and these factors can lead to local climate change [74]. In fact, in Korea, the urbanization rate and population of urban areas increased rapidly from 1971 to 2000, during which the daily minimum, maximum, and mean temperature increased [75]. Studies carried out in China showed that the UHI effect contributes to climate warming by about 30% [76,77].

Climate change affects the developmental phase of plants, and, thus, it can bring about significant changes in phenology [23]. Every 1 ◦C increase in the land surface temperature (LST) in spring and fall advanced the SOS by 9 to 11 days, and EOS was delayed by 6 to 10 days in China [78]. In eastern North America, the SOS generally advanced by three days for every 1 ◦C increase in the LST. These phenomena were the largest in the urban center and decreased exponentially as they headed toward the rural area [78]. The authors of [79] reported that the spring phenology of vegetation occurs earlier along the urban–rural gradient, and it occurs much earlier when close to the urban center because of the UHI effect. In the urban area of eastern North America, the SOS was advanced, on average, by seven days compared with the surrounding rural area, and EOS was delayed about eight days [12]. According to [80], on average, Boston's land surface temperatures were about 7 ◦C warmer, and its growing season was 18 to 22 days longer relative to the adjacent rural areas.

In this study, the observed green-up dates in the urban center, suburbs, and rural areas were earlier than the expected dates (Table 4), which is attributed to the temperature increase due to urbanization in those areas. Mts. Nam, Mido, and Umyeon, which showed the largest difference from the expected dates, are located in the urban center where the urbanization ratio is high and thus maintain a higher temperature than the surrounding areas due to the urban heat island [17]. Although Mt. Cheonggye and Mt. Buram are located in the suburbs, it is known that they are affected artificially because they are adjacent to the urban center [81]. Therefore, those sites also showed a big difference from the expected dates. Gwangneung (Mt. Sori), which is located in a rural area, has less land use intensity and population density than the urban center and suburbs, and thus the difference between the observed and expected dates of green-up is relatively small, but compared with Mt. Jeombong, a natural forest, there is an artificial influence, indicating a difference in the green-up date (Table 4). By comparing these results by landscape type according to land use intensity, this showed the biggest difference in the urban center as the difference between the observed date and the expected date of each study site was 11 days in the rural area, about 14.5 days in the suburbs, and about 16.3 days in the urban center (Table 4). According to a previous study [23], if the mean air temperature rises by 1 ◦C, the green-up date of *Q. mongolica* is advanced by 3.58 (based on MODIS image interpretation) and 4.33 (based on AGDD) days. If the results obtained from this study are translated into the air temperature based on previous research results [23], it could be deduced that the air temperature in the urban center, suburbs, and rural area rose by 3.8 to 4.6 ◦C, 3 to 4.1 ◦C, and 2.5 to 3.1 ◦C, respectively. In fact, the air temperature in the urban center of Seoul was reported to be about 5 ◦C different from the outskirt of the city [82].

According to [83], early flowering plays an important role in determining plant reproduction and pollen limitations by increasing the probability of experiencing frost damage. In addition, a delay or shortening of the flowering period can have a significant influence on the pollination process by affecting the available time of pollen and the sharing of pollen [84]. Differences in the timing of phenological events between urban and rural areas can lead to reproductive isolation, especially with plants that have a short flowering period [29]. Different responses of plant phenology between urban and rural can be blocked or restrict gene flow among meta-populations and meta-communities in rural–urban transects, and in addition, these different responses are likely to accelerate species polarization [85].

The UHI effect caused by urbanization can be confirmed through AGDD. AGDD values are highly correlated with the date of green-up and flowering and can be used as indicators of vegetation phenology [86]. The AGDD threshold for the green-up of *Q. mongolica* is about 159 ◦C [86], and this study shows that the higher the land use strength at the study site, the faster the AGDD threshold is reached (Figure 6). These results indicate that *Q. mongolica* reaches green-up faster because the AGDD value reaches the threshold earlier due to the increase in temperature from the UHI effect. Furthermore, the results prove that the green-up of plants is accelerating due to climate change caused by urbanization.

Urbanization, along with its consequence, climate change, is occurring at an unprecedented rate [87,88]. This rapid, uncontrollable acceleration of urbanization has led to worsening environmental degradation, resulting in issues such as pollution and unpredictable climate patterns, among many other indirect consequences [19–22,88–91]. The environmental change occurring in the urban world does not only affect the cities themselves—the climate impact of urbanization is spreading out on a global scale [1,2,87]. The loss of vegetation due to urbanization leads to several consequences. Not only does the area lose its richness in biodiversity but also its circulation of water, nitrogen, and other elements would be affected [2,5,8–11,92]. At the same time, as the areal size of greenery space decreases, CO2 emissions rise, which leads to further warming of the area and, consequently, the world [2,93].

In phenological research, urban areas are an important study field because they enable an assessment of the future potential impacts of climate change on plant development [17,28]. The investigation of urban phenology is important because cities with their amplified temperatures can serve as a proxy for future conditions, and thus future phenology can be estimated from current information [29]. In this respect, this study, which indicates that vegetation phenology was advanced due to the urbanization effect, provides information on how vegetation phenology changes when the temperature increases in the future.

#### *4.2. Diagnosis of Phenological Changes by Analyzing Sap Flow*

Traditionally, the study of vegetation phenology focuses on monitoring and analyses of the timing of phenological events [17,60]. Phenological observations are mainly performed through visual observation. Consequently, most phenological studies were conducted with easily observable things such as green-up, leaf bud break, first flowering, and leaf fall [6,17,43,44]. Recently, in addition to the method of checking phenological phases by observing the visual observation, a study method to confirm phenological phases through physiological responses such as photosynthesis has also been proposed [17,50,94,95].

At scales from organs to ecosystems, many processes, particularly those related to the cycling of carbon (productivity and growth), water (evapotranspiration and runoff), and nutrients (decomposition and mineralization), are directly mediated by phenology, and the seasonality of these processes is implicitly phenological [30]. Sap flow, which is well known as a harbinger of spring, is a physiological process driven by phenological change. Sap flow becomes active and increases contemporarily with leaf development, and thereby sap flow and the leaf area index denote similar early spring patterns [54]. Simultaneously with leaf development, transpiration has to progress [96] to participate in forming the leaves and the follow-up of tree radial growth. Therefore, phenology is tightly connected to the ecophysiological processes of deciduous tree species [51]. Stem volume changes and sap flow provided valuable additional information specifying the tree development during both spring and autumn phenological stages. During the leaf expansion phase, the diameter of trees decreased in the deciduous trees. There is a close relationship between the use of stem water storage and leaf phenology. Sap flow was detected in the branches and the main stem of trees without leaf transpiration. These sap flow patterns observed in branches and stems, along with changes in VWC (volumetric water content) in sapwood and in the stem diameter, may be associated with the movement of water and carbohydrates necessary for the process of developing new leaves [59].

In this study, both the green-up date and the change trajectory of the curvature K value derived from the sap flow were similar to the green-up date and the change trajectory of the curvature K value derived from the digital camera and MODIS satellite images (Table 6). These results show that vegetation phenology observed through the appearance of plants is reflected in the sap flow as a physiological reaction within the plant body. In fact, according to [54], sap flux density and leaf unfolding showed a linear relationship, and in the late stage of leaf development, a decrease in sap flow was observed due to the reduced transpirational demand.

The results of this study, which show that physiological responses in plants are similar to the vegetation phenology, can be evaluated as the results of a step forward in phenological studies, which have mainly been observed through the appearance of plants. In particular, considering that phenological events emerging in appearance may be difficult to observe accurately and precisely due to various influences [56,57], observation of phenological events through physiological responses could be used as a tool to verify the response of vegetation according to various environmental changes including climate. Furthermore, it is expected that the sap flow of plants could be used more diversely as a tool to reinforce monitoring of vegetation phenology by collecting sap flow data of plants in various spatiotemporal scales and comparing and analyzing them with seasonal data of phenology collected using remote sensing techniques.

#### *4.3. Ecosystem Management Strategy to Adapt Climate Change*

Climate change has already become a reality, and even if we try to balance greenhouse gas emissions and absorption, it seems that we will soon be in danger of being hit by greenhouse gases already emitted [97]. An IPCC-led international agreemen<sup>t</sup> system is pushing to contain the amount of greenhouse gases currently emitted as much as possible, but it is expected that the absolute volume will increase in the coming years as the emissions of developing countries such as China, India, Brazil, and Russia increase explosively [98]. Ecosystems have experienced environmental changes such as climate change in the past and have adapted to these changes [99], but the rapid climate change that is happening will be far beyond the speed at which species and ecosystems can adapt and will have a variety of effects, including the extinction of many species [98,100]. In this regard, in parallel with efforts to reduce greenhouse gas emissions, we need to find countermeasures to adapt to future climate change [100].

We have interpreted the cause of climate change with an emphasis on the increased use of fossil fuels up to date. However, as the results of this study show, the response of ecosystems is closely related to the land use intensity of the site. The observed evidence shows that the effects of urban heat islands were greater than those from climate change that greenhouse gases cause in some locations [101,102]. The concentration of CO2 is also steadily increasing at a global level, but it is showing a distinct seasonal variation that is high in winter and low in summer [8,103], which is the result of temperate forests acting as a source of absorption [104]. All environmental problems, including climate change, have sources of both emission and absorption. Therefore, we can mitigate climate change by reducing CO2 emissions, but we can also mitigate climate change by increasing absorption sources. Sound nature helps adapt to climate change by absorbing and storing carbon. Since about 20% of greenhouse gas emissions are estimated to be due to deforestation, forest conservation and restoration can store a considerable amount of carbon [105–107]. Achieving sustainable land use by preserving and restoring nature can be a climate change adaptation measure that can mitigate climate change. As the IUCN suggests, preserving and restoring nature to achieve sustainable land use can be an adaptation measure to mitigate climate change. Vegetation achieved through ecological restoration can function as a true adaptation measure by displaying ecosystem service functions such as climate control and carbon dioxide absorption. In this respect, systematic and wise land use planning is required to achieve efficient adaptation to climate change. In fact, the balance of the carbon cycle and the air temperature increase coefficient were shown to depend on the land use pattern of local areas, and the carbon budget by region also showed such trend [108].

Even at the site scale, we can use vegetation to conserve energy and create thermally pleasant environments by encouraging evapotranspirational cooling, and shading from the hot summer sun [109–111]. As we understand the ecological functions that create surface climates and the specific landscape features that alter these functions, we can make the climate favorable for us by taking advantage of natural landscape processes [109,111–118]. This is a vital theme within the land use planning field, which advocates understanding local environmental features as part of the site planning process [117,119] and creating designs that are in harmony with the environment, especially in terms of energy and water conservation [120,121]. Therefore, we recommend conservation and restoration of natural ecosystems as a strategy that enables humankind to adapt to climate change impacts [113,122,123]
