1. Introduction
Global climate change has been analyzed using long-term meteorological and oceanographic data. Over the period from 1880 to 2012, globally averaged combined land and ocean surface temperatures followed a linear trend, increasing by 0.85 °C [
1]. At the end of the 21st century (2081–2100), the change in the global surface temperature relative to 1850–1900 is projected with high confidence to exceed 1.5 °C under RCP (Representative Concentration Pathway) 4.5, RCP6.0, and RCP8.5 scenarios [
1]. Breeding and species selection in agriculture have had to adapt to global warming, and the spread of infectious plant diseases associated with global warming has become a major problem [
2]. In addition, glacial retreat has had considerable effects on ecosystems [
3] and on the distribution of organisms in both polar regions [
4] and alpine zones [
5]. The movement of plant communities to the north has been confirmed in polar regions in the Northern Hemisphere, and the early arrival of spring has caused a mismatch in plant pollination, even in temperate regions [
6]. Plant communities have also been spreading upwards in alpine zones [
7]. Long-term monitoring is needed to confirm whether these changes are temporary or permanent, and to verify whether the simulations based on past data are correct. Long-term monitoring research is ongoing worldwide [
8]. In Japan, long-term monitoring observations have been conducted in forests, grasslands, lakes, marshes, and oceans nationwide since 2003 through the “Monitoring Site 1000” project of the Ministry of the Environment [
9]. Because a 20-year period is too short to capture the effects of global warming on long-term changes in natural ecosystems, these projects are expected to continue in the future.
The alpine timberline is a forefront of struggle for tree survival [
10]. In this zone, the timberline migrates upwards or downwards in response to plant-limiting factors, such as low air temperature, frost damage, carbon limitation, winter desiccation, and strong wind [
11]. In particular, the area called the “kampfzone” is the place with the most dynamic changes in the timberline ecosystem [
10]. This kampfzone is characterized by extreme ecological conditions for survival, growth, and competition [
12], and is very sensitive to changing climatic conditions. Long-term observation of ecosystem changes in such places is therefore considered useful for clearly understanding the effects of global climate change on ecosystems.
Mt. Fuji is the highest mountain with a timberline in Japan. Timberline zones of most high mountains in Japan are dominated by
Pinus pumila communities [
13,
14]. In Europe and North America, coniferous trees in the upper part of the timberline exhibit a high degree of phenotypic plasticity in reaction to environmental factors in the kampfzone [
10], and the forest structure around the timberline in these regions is clearly different from that of Japan. Unlike other high mountains in Japan, Mt. Fuji lacks
P. pumila and has a forest structure similar to the timberlines of Europe and North America. Conducting a survey on Mt. Fuji is important to allow comparisons of timberline dynamics in mid-latitude Japan with those in Europe [
15,
16,
17,
18,
19,
20] and North America, and to analyze their relationship with global warming. In many locations in Europe, humans have had a long-term impact on the timberline, especially in the 17th to 19th centuries when high mountain meadows were extensively used for grazing and haymaking [
21,
22,
23]. However, the timberline on Mt. Fuji has always been maintained in a natural state, with the exception of some low-impact activities such as mountain climbing. For these reasons, investigating the timberline of Mt. Fuji is especially important compared with other high mountains in Japan.
Many research reports have appeared on forest vegetation on Mt. Fuji, and the upward movement of the timberline has been pointed out in previous studies [
24,
25,
26]. Oka [
26] confirmed this phenomenon based on field surveys and an annual ring analysis, and Maruta and Masuyama [
25] reported similar observations from a time series analysis using aerial photographs. These studies were short term, however, and did not clarify the mechanism and dynamics of forest change. No long-term detailed studies of the timberline of Mt. Fuji had thus been conducted. In 1978, we installed a permanent quadrat at the timberline of Mt. Fuji and have been continuously tracking the dynamics and mechanisms of the forest vegetation [
27,
28]. In the early years of our study, we found that the timberline had expanded upwards considerably between 1978 and 1999 [
28], possibly because of climate change.
The purpose of this study was to clarify how vegetation at the timberline of Mt. Fuji changed during the 40 years from 1978 to 2018. In particular, we aimed to determine (1) whether the observed upward movement of the timberline of Mt. Fuji is continuing and (2) whether the forest structure of the timberline has changed over this period. Our results may be useful for predicting how the recent temperature rise will affect vegetation in the timberline of Mt. Fuji and how global warming will impact forest vegetation in extreme environments.
3. Discussion
According to our earlier findings, the timberline of Mt. Fuji moved upwards between 1978, when the research site was set up, and 1999 [
27,
28]. In the present study, we found that the timberline of Mt. Fuji continued to considerably advance upwards until by 2018.
The vegetation around the Mt. Fuji timberline varies according to elevation, with the change in vegetation type from upper to lower elevations following this order: herbaceous plant patches, deciduous shrubs (
S. reinii,
L. kaempferi, and
A. alnobetula subsp. maximowiczii), deciduous
L. kaempferi forests, and evergreen coniferous forests of
A. veitchii and
P. jezoensis var.
hondoensis [
27]. The most striking change over the 40 studied years was that of the upper timberline vegetation (plots 2–6) above the deciduous shrubs (
Figure 2 and
Figure 3). In plot 1, at the top, no change was observed in vegetation cover over 40 years, whereas vegetation cover in plots 2–5 increased considerably, especially that due to woody plants (
Figure 7). This change was the result of an increase in the number of
S. reinii and
L. kaempferi individuals. Both species have pioneering properties and can invade bare land, but they have different life forms.
S. reinii is a bush with multiple stems and a maximum height of 3 m. In contrast,
L. kaempferi can form forests more than 10 m high below the timberline (
Figure 4) and shade out
S. reinii individuals during growth. Although
S. reinii was able to invade the upper timberline and increase in height (
Figure 4), this species was suppressed below the timberline by
L. kaempferi, and the population therefore decreased sharply (
Figure 3 and
Figure 5). Conversely,
L. kaempferi did not decrease in population size after invading and establishing itself at higher elevations, and its BA increased with increasing tree height (
Figure 4 and
Figure 5). In our earlier study,
L. kaempferi seedlings were found to be established very close to the edges of vegetation patches [
28]. Patches of
S. reinii may play an important role in the establishment of
L. kaempferi at the krummholz limit on Mt. Fuji [
29,
30] and shrubs provide safe sites through creating a more favorable microclimate [
31,
32].
S. reinii may also contribute to tree succession by providing adjacent late colonizers (
L. kaempferi) with compatible ectomycorrhizal (ECM) symbionts [
33].
In contrast to
S. reinii,
A. alnobetula subsp
. maximowiczii markedly decreased, both in terms of population size and BA, over the 40 years without invading upper elevations (
Figure 3 and
Figure 5). Previous studies have shown that individuals of
A. alnobetula subsp
. maximowiczii on Mt. Fuji have a high production rate because of their high photosynthetic rate [
34] and the high nitrogen content of leaf litter [
35]. In one study, in addition, the amount of annual nitrogen fixation by nodules was found to be almost the same as that of nitrogen used for annual growth [
36]. This species has therefore been considered to contribute to the upward movement in nitrogen supply at the timberline of Mt. Fuji [
28]. The rapid decline of
A. alnobetula subsp.
maximowiczii dwarf forests over the past 40 years, however, suggests that factors other than improvements in soil nitrogen have had a major effect on the advance of the timberline on Mt. Fuji.
In the case of evergreen conifers, seedlings of
A. veitchii and
P. jezoensis var.
hondoensis were present in the upper part of the timberline in 1999. By 2018, some individuals with a height of approximately 2 m were observed at this higher elevation (plots 3–6). These individuals had developed from the seedlings established in 1999 (
Figure 3).
Seedling establishment is an important factor in the expansion of plant and forest distributions. Many seedlings of species such as
L. kaempferi,
A. veitchii, and
P. jezoensis var.
hondoensis were found at the upper timberline (plots 3–6) between 1978 and 1999 [
28]. In particular,
L. kaempferi invasion and establishment was extensive, with a total of 196 seedlings found in 1999 in plots 2–8 (
Table 1). By 2018, however, many seedlings had died as a result of an increase in the vegetation cover at the upper timberline (plots 3–6). Although 12 new seedlings were established between 1999 and 2018 (
Table 1), the overall population decreased to 49 in 2018 (
Figure 7). The seedling population continued to increase in the uppermost areas (plots 1 and 2), however, as
L. kaempferi was first established in plot 1 and doubled in plot 2 in 1999 (
Figure 7). The sizes of
L. kaempferi individuals established between 1978–1999 and 1999–2018 were clearly larger in the latter period in plot 2 (
Table 1). As described above, seedlings of
L. kaempferi were steadily advancing above the timberline, which is considered to be a more severe environment.
Seedlings of
A. veitchii, which has a higher shade tolerance than
L. kaempferi, were found to be distributed throughout the timberline ecotone (plots 3–9), and the number of
A. veitchii seedlings had increased in 2018 compared with 1999 (
Figure 7). The number of individuals established between 1999 and 2018 was almost the same as between 1978 and 1999 (
Table 2). In other words,
A. veitchii is a recent invader of locations of previous
L. kaempferi invasion and growth.
L. kaempferi thus acts as a facilitator for
A. veitchii, as the former has deeper roots than the latter and can avoid desiccation [
37,
38].
Tree forms are shaped by physical forces, such as strong wind and heavy snow, under severe environments [
10,
21,
39,
40,
41]. The area around the timberline is strongly affected by strong winds in winter. Life forms with highly variable physiognomy predominate among woody plants, ranging from bushes with “flagged” leaders to cushions of krummholz pressed close to the ground (table shape) [
10]. Prostrate
L. kaempferi at the upper timberline in 1978 (plots 3 and 4) are shown in
Figure 8A, while
Figure 8B shows prostrate
L. kaempferi with erect stems and an estimated age of 150 years (plot 5) at that time. In 2018, however, a different landscape of tree shapes was evident (
Figure 8C). In particular,
L. kaempferi that had newly invaded the upper portion of the krummholz limit were growing with erect trunks without dwarfing (plots 2 and 3;
Figure 8C). Maruta and Masuyama [
25] have reported that the first step in advancing timberline is the establishment of the dwarf type of
L. kaempferi, which contrasts with individuals at lower elevations that gradually form erect trunks. The conflict between the results of their study and our findings may be due to differences in topography between the respective research sites as well as factors related to climate change, such as an increase in temperature.
Air temperature and CO
2 concentration are important determinants of plant growth. Global warming has recently become a problem [
1]. The significant warming occurring in recent years may have changed timberline ecosystems in Europe [
7,
42,
43,
44], China [
45], and Japan [
28]. During the last 40 years, the average maximum temperature has continued to rise during the plant growth period on Mt. Fuji (
Figure 9). Higher temperatures will extend the plant growth period and elevate photosynthetic rates. As the photosynthetic period lengthens and the photosynthetic rate increases, the annual growth rate may increase, and shoots may be formed that can better withstand the winter environment. In addition to air temperature, the CO
2 concentration is rising. The mean CO
2 concentration at the summit of Mt. Fuji was approximately 335 ppm in August 1981 [
46], 388 ppm in 2010 [
47], and above 400 ppm in 2015 [
48]. The saturation limit for CO
2 assimilation in
L. kaempferi is at an intercellular CO
2 concentration of 600 ppm, regardless of mineral nutrient supply [
49]. The photosynthetic rate may therefore continue to rise. As mentioned above, the temperature rise and the increase in CO
2 concentration are considered to be factors that increase the biomass production of trees at the timberline. As a result, the annual growth of
L. kaempferi may have increased, and erect shoots may be able to survive, even in the severe winter environment, without unusual phenotypic response.
The mechanism responsible for timberline rise on Mt. Fuji has been thought to entail the invasion of deciduous shrub trees, such as S. reinii and A. alnobetula subsp. maximowiczii, into herbaceous patches to form shrub forests, with L. kaempferi also invading to form a table-shaped shrub forest that eventually stands upright. However, L. kaempferi has invaded the upper part of the timberline and continued to grow upright without forming dwarf shrubs with a prostrate form. This phenomenon is thought to be due to changes in external factors in addition to natural succession occurring after the eruption in 1707. One such external factor is an increase in annual growth due to temperature rise. This temperature increase promotes an increase in photosynthetic rate and an expansion in the photosynthetic period. In addition to the rise in air temperature, the increase in CO2 concentration accelerates the growth rate.
Previous studies have pointed out the consequences of the imbalance between rapid climate change and slow biological responses. Even among the most mobile species such as butterflies, these pollinators have been unable to extend their ranges as fast as required to keep pace with climate change [
50,
51]. On the other hand, results of our research over forty years and global warming forecasts [
1], has suggested that the timberline of Mt. Fuji will continue to advance upwards. These results may indicate that monitoring of the alpine ecosystems may be effective in capturing the sensitive impact of climate change on forests. The “Monitoring site 1000” project of the Ministry of the Environment in Japan, which began in 2003, has yielded results for many forests, but its impact on rapid climate change in recent years has been less apparent. Therefore, long-term monitoring in various climate zones, including alpine ecosystems, will be necessary to assess the effects of global warming on organisms.