The Role of Aging and Wind in Inducing Death and/or Growth Reduction in Korean Fir ( Abies Koreana Wilson) on Mt. Halla, Korea

: The purpose of this study was to investigate the role of strong winds and aging in the death and/or decline in the growth of Korean ﬁr on Mt. Halla in Korea. Bangeoreum (BA-S), Jindalrebat (JD-E), and Youngsil (YS-W) on the southern, eastern, and western slopes of Mt. Halla (ca. 1600 and 1700 m a.s.l.) were selected for the study. The site chronologies were established using more than 10 living Korean ﬁrs at each site. Additionally, to date the years and seasons of death of standing/fallen dead Korean ﬁrs, 15/15, 14/15, and 10/10 trees were selected at BA-S, JD-E, and YS-W, respectively. After adjusting the age with the period of growth up to the sampling point, the oldest Korean ﬁr found among the living trees was 114 years old at JD-E and the oldest ﬁr among the dead trees was 131 years old at JD-E. Besides this, most of the trees at BA-S and JD-E were found to have died between 2008 and 2015, and at irregular intervals between 1976 and 2013 at YS-W. Also, the maximum number of trees, that is, 62.7% died between spring and summer, followed by 20.9% between summer and autumn, and 16.4% between autumn of the current year and spring of the following year. Abrupt growth reductions occurred at BA-S and JD-E, and have become more signiﬁcant in recent years, whereas at YS-W, the abrupt growth reduction and recovery occur in a cyclic order. The intensity and frequency of the typhoons increased from 2012, and this trend was in-line with the increased number of abrupt growth reductions at BA-S and JD-E. Therefore, the typhoons of 2012 are considered as the most likely inﬂuencing factor in death and/or growth reduction in Korean ﬁrs. In contrast, the decline in the growth of the Korean ﬁrs located on the windward slope (YS-W) showed a relationship with winds stronger than 25–33 m/s.


Introduction
The excellent adaptability of trees to the ever-changing regional and/or local climate has led to their wide geographical distribution [1][2][3]. Also, tree growth depends upon climate [4]. Various studies have reported that trees at high elevations face mortality and/or reduced growth due to climate changes, such as warming, drought, or unexpected natural events caused by warming [5][6][7][8]. In particular, trees in alpine and subalpine regions are highly sensitive to climatic conditions, and because of this, any shift in their range can be related to climate change [9,10].
Korean fir (Abies koreana Wilson), one of the endemic subalpine tree species in the Republic of Korea, is distributed above 1000 m a.s.l. (ca. 35 • 40 and 33 • 50 N) on Mt. Halla, Jiri, Deogyu, Gaya, Baegun, Yeongchuk, Geumwon, and Songni [11][12][13]. Due to the moisture stress caused by warming and/or additional stresses caused by strong wind and heavy snow, the number of Korean firs has decreased so markedly [14][15][16][17][18] that the  The sample trees were selected based on whether they were living, standing dead, or fallen dead ( Figure 3). A minimum of 10 Korean firs in each group were studied using tree-ring analysis ( Table 1). The size of the firs at BA-S was smaller than those at JD-E and YS-W. Considering the size differences, Korean firs thicker than 10 cm at breast height were selected at BA-S and thicker than 15 cm at JD-E and YS-W for the tree-ring analysis. The first sampling at YS-W was done in 2017, followed by JD-E in 2018 and BA-S in 2019. Two tree-ring core samples were extracted from the sample trees at breast height using an increment borer of diameter 5.12 mm. To avoid compression and reaction in the wood caused by slope [4], the tree-ring cores were collected in a parallel direction to the contour of the slope [25]. For the inclined stems, the increment cores were sampled between the upper and lower sides.    The sample trees were selected based on whether they were living, standing dead, or fallen dead (Figure 3). A minimum of 10 Korean firs in each group were studied using tree-ring analysis ( Table 1). The size of the firs at BA-S was smaller than those at JD-E and YS-W. Considering the size differences, Korean firs thicker than 10 cm at breast height  The sample trees were selected based on whether they were living, standing dead, or fallen dead ( Figure 3). A minimum of 10 Korean firs in each group were studied using tree-ring analysis ( Table 1). The size of the firs at BA-S was smaller than those at JD-E and YS-W. Considering the size differences, Korean firs thicker than 10 cm at breast height were selected at BA-S and thicker than 15 cm at JD-E and YS-W for the tree-ring analysis. The first sampling at YS-W was done in 2017, followed by JD-E in 2018 and BA-S in 2019. Two tree-ring core samples were extracted from the sample trees at breast height using an increment borer of diameter 5.12 mm. To avoid compression and reaction in the wood caused by slope [4], the tree-ring cores were collected in a parallel direction to the contour of the slope [25]. For the inclined stems, the increment cores were sampled between the upper and lower sides.

Tree-Ring Measurement and Cross-Dating
Before measuring the ring width, the increment cores were mounted with their cells vertically aligned and the cross-planes were sanded using a belt sander. The sanding began with #80 sandpaper through #120 and #360 and up to #600 until the ring boundaries were clearly visible [38]. The annual ring widths were measured to the nearest 0.01 mm using the LINTAB (Rinntech, Germany) measurement system.

Tree-Ring Measurement and Cross-Dating
Before measuring the ring width, the increment cores were mounted with their cells vertically aligned and the cross-planes were sanded using a belt sander. The sanding began with #80 sandpaper through #120 and #360 and up to #600 until the ring boundaries were clearly visible [38]. The annual ring widths were measured to the nearest 0.01 mm using the LINTAB (Rinntech, Germany) measurement system.
Cross-dating was applied to establish the site chronologies for BA-S, JD-E, and YS-W using ring-width time series from the living trees. The site chronologies were used to date the year of death of the Korean fir by testing the synchronization between the individual ring-width time series from the dead trees and the corresponding site chronologies. The success of the dating was determined by the statistical t-value (Equation (1)) and G value (Equation (2)) run in the TSAP-Win program (Rinntech, Germany) [39,40] and from their graphical synchronization [41].
where r is the correlation coefficient between the individual ring-width time series and n is the number of overlapped years. where G (x,y) is the G-value and x i and y i are the measured ring-width values for the ith year.

Death of Trees According to Season
The tree rings of conifers consist of thin-walled large-diameter tracheids (earlywood) and thick-walled small-diameter tracheids (latewood) [42]. The initiation and cessation of tree-ring formation in the Korean fir in the subalpine areas of Mt. Deogyu (35 • 51 N, 127 • 44 , 1585-1594 m a.s.l.) are early May and late September, respectively, whereas the transition from earlywood to latewoods occurs between mid-July and early August [43]. Therefore, the earlywood and latewoods in the youngest dead tree ring can be used as a criterion to determine the season in which tree death occurred. Based on the wood cells' anatomical characteristics, these seasons were determined by the following criteria: (1) if the youngest tree ring has only earlywood, the death of the tree occurred between spring and summer (image on the left in Figure 4); (2) if its latewood formation is incomplete, the tree died between summer and autumn (middle image in Figure 4); and (3) if the latewood formation is complete, the tree died between the autumn of the current year and spring of the following year (image on the right in Figure 4).
is the number of overlapped years.
is the G-value and and are the measured ring-width values for the ℎ year.

Death of Trees According to Season
The tree rings of conifers consist of thin-walled large-diameter tracheids (earlywood) and thick-walled small-diameter tracheids (latewood) [42]. The initiation and cessation of tree-ring formation in the Korean fir in the subalpine areas of Mt. Deogyu (35°51′ N, 127°44′, 1585-1594 m a.s.l.) are early May and late September, respectively, whereas the transition from earlywood to latewoods occurs between mid-July and early August [43]. Therefore, the earlywood and latewoods in the youngest dead tree ring can be used as a criterion to determine the season in which tree death occurred. Based on the wood cells' anatomical characteristics, these seasons were determined by the following criteria: (1) if the youngest tree ring has only earlywood, the death of the tree occurred between spring and summer (image on the left in Figure 4); (2) if its latewood formation is incomplete, the tree died between summer and autumn (middle image in Figure 4); and (3) if the latewood formation is complete, the tree died between the autumn of the current year and spring of the following year (image on the right in Figure 4).

Age Analysis
The increment cores with and without pith (taken at breast height) and the number of tree rings were used to estimate the age of the tree (A in Figure 5). When there was no pith in the increment cores, the pith location was first estimated using circles drawn at 1 cm radius intervals on a transparency film (B in Figure 5). Next, the number of tree rings was counted from the innermost tree ring to the bark until the sum of the ring widths reached the estimated distance from the innermost tree ring to the estimated pith location (C in Figure 5).

Age Analysis
The increment cores with and without pith (taken at breast height) and the number of tree rings were used to estimate the age of the tree ( Figure 5A). When there was no pith in the increment cores, the pith location was first estimated using circles drawn at 1 cm radius intervals on a transparency film ( Figure 5B). Next, the number of tree rings was counted from the innermost tree ring to the bark until the sum of the ring widths reached the estimated distance from the innermost tree ring to the estimated pith location ( Figure 5C).

Monitoring of Abrupt Growth Reduction
In the present study, abrupt growth reduction is signified by a marked decrease in the ring width for three years or more [44]. Such an abrupt reduction in growth observed for three consecutive years is considered to be due to natural destruction, such as mechanical injury, destruction of the foliage, land movement, or thinning [4,44]. To investigate the effect of typhoons and strong winds (a type of natural disaster), the abrupt growth

Monitoring of Abrupt Growth Reduction
In the present study, abrupt growth reduction is signified by a marked decrease in the ring width for three years or more [44]. Such an abrupt reduction in growth observed for three consecutive years is considered to be due to natural destruction, such as mechanical injury, destruction of the foliage, land movement, or thinning [4,44]. To investigate the effect of typhoons and strong winds (a type of natural disaster), the abrupt growth reduction was categorized into three classes: class I-here the ring-width growth was reduced by 40-55% for three consecutive years or more (light grey in Figure 6); class II-the ring width growth was reduced by 56-70% (dark grey in Figure 6); and class III-the ring width growth was reduced by more than 70% (black in Figure 6). Figure 5. Illustration of method used to estimate the age of Korean firs (Abies koreana). (A) Crosssection with directions to extract increment cores with pith (ⓐ) and without pith (ⓑ), (B) estimating the location of the pith, when the increment cores have no pith, and (C) estimating the number of tree rings between the innermost tree ring and the estimated location of pith (ⓒ).

Monitoring of Abrupt Growth Reduction
In the present study, abrupt growth reduction is signified by a marked decrease in the ring width for three years or more [44]. Such an abrupt reduction in growth observed for three consecutive years is considered to be due to natural destruction, such as mechanical injury, destruction of the foliage, land movement, or thinning [4,44]. To investigate the effect of typhoons and strong winds (a type of natural disaster), the abrupt growth reduction was categorized into three classes: class Ⅰ-here the ring-width growth was reduced by 40-55% for three consecutive years or more (light grey in Figure 6); class Ⅱ-the ring width growth was reduced by 56-70% (dark grey in Figure 6); and class Ⅲ-the ring width growth was reduced by more than 70% (black in Figure 6).

Site Chronologies and Their Synchronization
All living trees within the same study sites (BA-S, JD-E, and YS-W) were successfully cross-dated with each other (Figure 7). The mean t-values and G values between the individual ring-width time series and the corresponding site chronologies were higher than 8.2 and 72.3%, respectively. The longest mean chronology of 114 years was established at JD-E, followed by 107 years at YS-W and 73 years at BA-S. The highest mean number of trees rings calculated was 66.7 (44-107) at YS-W, followed by 64.9 (36-114) at JD-E and 52.4  at BA-S. The site chronology of BA-S showed higher synchronization with JD-E (t-value: Atmosphere 2021, 12, 1135 7 of 13 5.7/G value: 65%) than with YS-W (t-value: 2.1/G value: 60%). The synchronization between JD-E and YS-W was lower than the others (t-value: 0.4/G value: 63%).
All living trees within the same study sites (BA-S, JD-E, and YS-W) were successfully cross-dated with each other (Figure 7). The mean t-values and G values between the individual ring-width time series and the corresponding site chronologies were higher than 8.2 and 72.3%, respectively. The longest mean chronology of 114 years was established at JD-E, followed by 107 years at YS-W and 73 years at BA-S. The highest mean number of trees rings calculated was 66.7 (44-107) at YS-W, followed by 64.9 (36-114) at JD-E and 52.4 (33-73) at BA-S. The site chronology of BA-S showed higher synchronization with JD-E (t-value: 5.7/G value: 65%) than with YS-W (t-value: 2.1/G value: 60%). The synchronization between JD-E and YS-W was lower than the others (t-value: 0.4/G value: 63%). The inter-annual growth variation in the trees was determined by the most limiting factor for their growth [45], as well as their sensitivity to the limiting factor [46][47][48]. The The inter-annual growth variation in the trees was determined by the most limiting factor for their growth [45], as well as their sensitivity to the limiting factor [46][47][48]. The synchronization between the site chronologies reflects the similarity of the growth environment. The lapse rate of the annual mean temperature at the northern and southern slopes was −0.61 • C/100 m and −0.68 • C/100 m, respectively, and the annual solar radiation measured on the northern aspect was lower than that on the southern aspect [28]. Besides these, the literature presents several other differences between the northern and southern slopes of Mt. Hall in terms of slope, soil moisture, and annual precipitation. These site conditions at BA-S showed more similarity to those at JD-E than those at YS-W's. In other words, the site chronology of BA-S showed more synchronization with JD-E than YS-W (Figure 7).

Tree Ages
The increment cores with abnormally shaped innermost tree rings due to needles or which were decayed, were not considered for the age estimation to avoid over-or underestimation ( Table 2). For the estimation, ca. 2-10 tree rings were added to the actual number of tree rings counted in the increment cores. In living trees, the oldest mean age was estimated as 73 years old at YS-W, followed by JD-E (70 years old) and BA-S (58 years old). The oldest Korean fir among the living trees was 114 years old at JD-E. Among the dead trees, the standing dead trees were older than the fallen dead trees at BA-S (58 > 49 years old) and JD-E (80 > 61 years old); however, they were younger at YS-W (54 < 59 years old). The oldest Korean fir among the dead trees was 131 years old and was found at JD-E. Among the living Korean fir, the trees distributed at the lowest altitude (1610-1613 m a.s.l.) at YS-W were older than the other sites, followed by JD-E where trees were distributed at the second highest altitude (1672-1683 m a.s.l.) and BA-S at the highest altitude (1692-1700 m a.s.l.). The upper limitation of cold climate relict plants like the Korean fir shifts according to temperature, which is the most sensitive factor for tree growth [7,49,50]. It has been proven that the tree-lines at high altitudes of the European Alps, Indian Himalayas, and Altai Mountains shift upward due to climate warming [51][52][53]. The observed age differences among the study sites with different altitudes can also be attributed to the shift due to climate warming.
Abies species at high elevations grow very slowly when juvenile and are not able to live as long as other tree species [27,37]. It has already been proven that the annual mean growth of the Korean fir on Mt. Halla is 1.2 cm for the first 10 years [23] and Farges fir (A. fargesii Franch.) in the Qinling Mountains in China takes ca. 27 years to grow 100 cm [54]. So, the real tree ages of the Korean firs are at least ca. 27 years older than the estimated ages.
Typically, the Korean firs on Mt. Halla grow in shallow soils of volcanic bedrock, so the old trees are more vulnerable to strong winds and/or drought than the younger ones [23]. Until now, none of the past studies on Mt. Halla have found any Korean firs over 120 years old, where the age was determined from the number of tree rings at breast height [24,25]. Although the oldest Korean fir on the mainland, was reported to be 235 years old [17], most Korean firs are less than ca. 150 years old, according to the ages obtained from the increment cores at breast height [24,25,[32][33][34][35].

Year and Season of Death
The distribution of the year of death of the standing dead Korean fir at JD-E and YS-W was wider than the fallen dead Korean firs (Figure 8). On the other hand, at BA-S, the fallen dead Korean fir showed a wider distribution for the year of death than the standing dead Korean fir. Most of the deaths occurred between 2008 and 2015 at BA-S and JD-E. The deaths at YS-W happened in irregular intervals between 1976 and 2013. From the total number of dead trees (ALL-SD and ALL-FD in Figure 8), most of the standing and fallen dead Korean firs died in 2012 (thirteen trees) and 2013 (nine trees), 28.3% died in these 2 years.
Atmosphere 2021, 12, 1135 9 of 13 ural catastrophe, e.g., typhoon, insects, extreme drought, heavy precipitation or fire [59][60][61][62][63]. The majority of the studies done on other sites as well as on the current sites [17,25,33] reported that the moisture stress related to temperature warming is the principal cause of death of the Korean fir. Considering the rates of increment in the annual mean temperature and total precipitation from 1993 to 2020, viz. 0.025 °C and 8.13 mm, respectively, with a predominate warming trend, (Figure 2), the moisture stress due to warming is the most influential stress factor for the Korean fir.  Figure 8), followed by 20.9% (14/67 trees) between summer and autumn (gray bar in ALL-SD and -FD in Figure 8) and 16.4% (11/67 trees) died between autumn of the current year and spring of the following year (black bar in ALL-SD and -FD in Figure 8).
The death of the trees is actually the result of accumulated stress from competition between the trees for nutrients, water and light [55,56], climate change [57,58], and/or natural catastrophe, e.g., typhoon, insects, extreme drought, heavy precipitation or fire [59][60][61][62][63]. The majority of the studies done on other sites as well as on the current sites [17,25,33] reported that the moisture stress related to temperature warming is the principal cause of death of the Korean fir. Considering the rates of increment in the annual mean temperature and total precipitation from 1993 to 2020, viz. 0.025 • C and 8.13 mm, respectively, with a predominate warming trend, (Figure 2), the moisture stress due to warming is the most influential stress factor for the Korean fir.
Most Korean firs on Mt. Halla grow in the shallow soils of the volcanic bedrock [23]. During summer, their growth is highly affected by summer monsoons and typhoons from the Pacific Ocean [64]. Therefore, the strong wind during summer either blows the trees down or disturbs the biological activities by breaking branches, causing the leaves to drop, or separating root systems from the soils [29,30]. A study from 1975 to 2020 revealed that relatively frequent and strong typhoons occurred in 2012 (Figure 8), which might have played a significant role in blowing Korean firs down at BA-S and JD-E. Therefore, 71.4% of the total fallen dead Korean firs at BA-S and JD-E occurred in spring and summer. Moreover, the standing dead Korean firs found in 2013 could be the result of the typhoons in 2012 as well. On the contrary, the death of Korean firs at YS-W did not occur in any single year. The main wind over Mt. Halla blows from west to east [65]; therefore, the Korean firs at YS-W are usually exposed to strong winds. The moisture stress caused by temperature warming and the continuous winds are the main reasons for the death of the Korean firs in different years at YS-W. The above-mentioned two factors are also responsible for the spatial heterogeneity and various shapes and sizes of the Korean firs at YS-W. Furthermore, the deaths at YS-W occurred during the growing season. This implies that the deaths were highly correlated to disturbances in the biological process during the growing season.
Notably, the intensity of the abrupt growth reduction at BA-S and JD-E was found to be stronger in recent years, whereas the Korean firs at YS-W showed a repeated cycle of abrupt growth reduction and recovery ( Figure 6). Considering the year of death of the individual Korean firs, the abrupt growth reduction at every site was found to be the strongest in the 10 years before the trees died.
The intensity and frequency of typhoons also increased from 2012, and these trends were in line with the increase in the intensity of the abrupt growth reduction at BA-S and JD-E ( Figure 6). Except for this pattern, no other conspicuous correlations could be observed between the typhoons and the abrupt growth reduction.
The firs on Mt. Halla grow under a lot of stress, such as wet, drought, hot, cold, strong winds, insects, wildfires, and competition with neighboring plants [6,28,[66][67][68]. Trees with relatively lower vitality or that grow under harsh microsite conditions usually form narrow annual rings during periods of such stress-the stress is a limiting factor for growth [4,44]. Since the dead trees (SD and FD) exhibit a higher rate of abrupt growth reduction than the living trees (LV), it implies that Korean firs, which have low vitality and/or grow under unfavorable micro conditions, have a higher possibility of death.
On Jeju Island, strong winds blow typically from the west to east [23,65]. Therefore, the Korean fir at YS-W grows under the influence of this wind. The highest intensity of abrupt growth reduction occurred in 1946 and 2002 at YS-W-LV, in 1972 at YS-W-SD and in 1972 and 2002 at YS-W-FD. The above-mentioned years coincide with those in which typhoons stronger than 25-33 m/sec hit the sites. Since the firs were growing in shallow soils of volcanic bedrock, the roots were loosened and lifted from the soil by these strong winds, thereby causing abrupt growth reductions. This is because if the roots are lifted, the trees are not able to get water from the soil easily and adequately, resulting in a decrease in the tree growth [23]. Unlike YS-W, there was no pronounced effect of strong winds on the growth of the firs at BA-S and JD-E. There were some similar patterns in that the intensity of the abrupt growth reduction and the number of typhoons increased in parallel after 2012. Based on the large number of stand and fallen dead Korean firs at BA-S and JD-E that died in 2012 and 2013 when relatively frequent and strong typhoons occurred (Figure 8), it can be inferred that the strong winds in 2012 played a major role in the death and/or reduction in the growth of Korean firs at BA-S and JD-E. However, strong winds may not always have a direct effect on them.

Conclusions
The present study attempted to estimate the age of Korean fir trees growing on Mt. Halla and found that the oldest living Korean fir was 114 years old at JD-E and the oldest dead tree was 131 years old at JD-E, based on the 101 sample trees studied. Since no older Korean fir on Mt. Halla has been reported so far, it can be concluded that the Korean fir is not able to live more than ca. 150 years. Typhoons with an intensity of more than 25-33 m/s at the windward slope (YS-W) showed a strong positive relationship with the death and/or abrupt reduction in the growth of the trees. Additionally, Korean firs on the other slopes (BA-S and JD-E) showed a high death rate and abrupt growth reduction starting from 2012. These findings show that the wind has a direct or an indirect effect on the tree growth, depending on its flow direction. There was no significant difference between the standing and fallen dead trees in regard to the patterns of their year of death and the intensity of the abrupt growth reduction rate. Based on these findings, aging and strong winds can be considered in future research as the primary factors causing the decline in growth of the Korean firs on Mt. Halla together with climate change.  Data Availability Statement: The data will be made available at the Tree-Ring Research Center (www.dendro.kr/datasets).

Conflicts of Interest:
The authors declare no conflict of interest.