Discussion

Historically, biogeographic spaces have predominantly been delineated using the distribution of organisms according to specific knowledge (e.g., partially usable data, such as endemism or the distribution of evergreen trees), or corresponding geographical and climatic factors, rather than using actual recorded biota (Takhtajan, 1986; White, 1983). Historical definitions of vegetation-climate and floristic zones on the Korean Peninsula have used these methods (Lee and Yim, 1978; Yim and Kira, 1975). Recently, there have been attempts to review bioregions using quantitative analytical techniques, with some showing similar, and some different, results to the historical regions (Gonzalez-Orozco et al., 2014; Lenormand et al., 2019). The present study differs fundamentally from previous approaches to phytogeographic regionalization because we used high-resolution, georeferenced specimen data for the southern part of the Korean Peninsula. Although restricted to the southern regions, our results provide clearly improved phytogeographic zones through our use of SOMs and georeferenced data for recently collected plant specimens. The spatial distribution of floristic zones and the basic taxonomic composition in the southern part of the Korean Peninsula reflect a combination of repeated migrations, expansions, and reductions of species associated with climatic variation, physical and geographic factors, and human activity patterns, including the political situation (Valladares et al., 2015). In addition, we reconfirmed differences identified in historical studies in geographic and climatic conditions, which are deterministic factors in the spatial patterns of floristic assemblages (Lee and Yim, 1978; Yim and Kira, 1975). We were also able to verify the correlations between zones and the distribution of zones based on the characteristics of the floristic assemblages and the physical conditions where they are found, such as the topographic characteristics of the Korean Peninsula. In particular, we verified the importance of the topography of the Korean Peninsula (especially the connected mountainous regions and isolated mountains), which has been emphasized in recent studies (Chung et al., 2017b), and its contribution to shifts in distribution related to climate change and the process of floristic reassembly. As well as the deterministic factors for floristic assembly that have been used historically (e.g., climatic factors), more diverse ecologically important environmental factors will need to be considered at the same spatial range as the southern part of the Korean Peninsula.

Spatial characteristics of the new floristic zones

The transitional changes in the flora of the southern Korean Peninsula (from warm to cool), and the effects of physical and human activity were investigated via the derived floristic zones. The historical floristic zones of the Korean Peninsula were constructed to broadly reflect a combination of climatic factors and plant distribution patterns, and had a banded, near-planar shape (Appendix A1) (Lee and Yim, 1978). Our SOM results, revealing four statistically significant spatial clusters (Zones I–IV) representing distinct territories (detailed below), were consistent with unification (or partial inclusion) or division of the historical zones. The historical central and southern zones partially reflected the distribution patterns of some tree ecotypes, including evergreen broad-leaved trees (e.g., Citrus and Ilex ), but there was limited consideration of important biogeographic factors in small regions, such as complex mountain groups and the effects of altitude. Rather than forming a broad banded pattern, recent studies have revealed spatial patterns (at global and regional scales) that include large numbers of small, heterogeneous patches within larger biotic assemblage zones, arising from changes in the climatic and physical environment, such as quaternary glacial-interglacial oscillations, and the roles of factors such as topography (Kreft and Jetz, 2010; Lenormand et al., 2019; Médail and Diadema, 2009; Silva and Souza, 2018).
Zone I is focused around high-altitude mountains in the central Korean Peninsula (maximum altitude: 1708 m, Mt. Seoraksan) and included some high-altitude regions in the south. Among the historical zones, this partially corresponds to the central and southern zones. Zone I reflects floristic elements that moved south from the previous periglacial environment and remained in the high-altitude mountain ranges in the center of the Korean Peninsula after the periglacial environment receded. In East Asia, this region represents the southern limit of the ranges of the dwarf Siberian pine (Pinus pumila ), Korean arborvitae (Thuja koraiensis ), and Khingan fir (Abies nephrolepis ) (Kong et al., 2019; Korea National Arboretum, 2015). It is also an area with active cool-climate highland agriculture, and timber production (P. koraiensis and Larix kaempferi ).
Zone II is focused on mountainous land adjacent to Zone I, mostly consisting of inland, high-altitude mountains further south in the Korean Peninsula (1915 m, Mt. Jirisan and 1614 m, Mt. Deogyusan). Among the historical zones, this partially corresponds to the same central and southern floristic zones as Zone I. This region is the northern limit of the range of the Korean fir (A. koreana ), and the southern limit in East Asia of the range of dark-bark spruce (Picea jezoensis ) (Korea National Arboretum, 2015). Through the same historical geographical processes as Zone I, this zone shows the remnants of the influence of the periglacial environment in the southern Korean Peninsula. In addition, trees that are mostly distributed in warmer or maritime climates (e.g., Stewartia koreana and Lindera sericea ) can be found growing in the medium and high altitude areas of Zone II (Kim et al., 2014). There is almost no highland agriculture in this zone, but some timber production occurs (mostly Larix kaempferi ), and the zone is adjacent to numerous large cities.
Zone III accounts for most of the southern Korean Peninsula. Although this zone contains tall mountains and mountain ranges, it is also subject to complex effects from agricultural activity and cities with a relatively intensive level of land use. For example, the inclusion of areas in Zone III with higher latitudes than Zone I is likely because of the impact of long-term military activity in these areas. Notably, in Zone III, the plants constituting the other floristic zones (Zones I, II, and IV) remain in isolated islands. These heterogeneous patches inside Zone III are a vestige of shifts in plant diversity patterns driven by historical geographical changes, and thus are important in the heterogeneous formation of the regional floristic composition (Laliberté et al., 2014; Zobel, 1997). Recently, the function of the Korean Peninsula as a shelter for biodiversity has been emphasized, because of its topography that includes a number of core mountains (Chung et al., 2018). In-depth studies need to be conducted on the biodiversity conservation functions (e.g., provision of shelter) of these small, heterogeneous patches and on their long-term changes.
Zone IV unifies the historical floristic zones of the southern coast, Jejudo, and Ulleungdo, which have previously been more finely divided (Appendix A1), and contains a high relative abundance of Orchidaceae, Asteraceae, and Rosaceae as well as specific taxa that only appear in this zone. Although Zone IV includes some inland areas, it mostly consists of regions along the coast of the Korean Peninsula and islands that are important for biodiversity, such as the oceanic island Ulleungdo (Chang and Gil, 2014; Choi et al., 2019; Holman et al., 2017) and the volcanic island Jejudo, which contains Hallasan Mountain (1950 m). This zone ranges from the temperate zone of evergreen broad-leaf trees (e.g., Castanopsis sieboldii ) to the cool zone of polar trees (e.g., Diapensia lapponica var. obovate ). Importantly, among the four identified floristic zones, Zone IV shows relatively high diversity of specific taxa, and is a core part of the range of Orchidaceae, making it an important zone from a conservation and evolutionary perspective. Because this zone includes the volcanic islands of Ulleungdo and Jejudo, the physical conditions differ considerably from the other zones, including in parent materials (volcanic ash) and terrain (lava terraces). The north of Jejudo has acted as an agricultural and administrative center for longer than the south, which could explain the differences in the flora.

Spatial clustering and separation of floristic assemblages

In addition to plant distribution, regionalization of floristic assemblages is important for understanding the formation processes on the Korean Peninsula, including floral changes. The regional species pool is the result of numerous settlement processes caused by climatic changes, which is restricted by ecological filtration, and ultimately forms the local biotic assemblage (Ricklefs, 1987). The Korean Peninsula is composed of a network of mountain ranges along a latitudinal gradient and has witnessed interactions between the Manchurian flora region at higher latitudes, the North Chinese flora region at lower latitudes, and the Japan-Korean flora region (Takhtajan, 1986). This is the background for the current plant diversity and species composition on the peninsula (Appendix A2). Thus, through repeated historical geographical processes, such as periglacial climates, the Korean Peninsula has acted as a geographical and biological corridor, with a mixture of high- and low-latitude plants, which has produced the present-day spatial distribution of biodiversity (Chang et al., 2016; Chung et al., 2017a; Chung et al., 2017b; Kim et al., 2014; Kim et al., 2005; Kong et al., 2019).
Unlike the historical banded or homogeneous planar patterns, our revised floristic zones in the southern part of the Korean Peninsula reveal a new pattern, with Zones I and II forming central regions surrounded by a background of Zone III, with small patches of Zones I and II present within Zone III. At regional scales (e.g., the Korean Peninsula), complex physical and topographic factors can affect biotic assemblages (Lasmar et al., 2020; Tsiftsis et al., 2008; Xu et al., 2016). Across a broader area, there are also effects of climate, such as latitude (Sanders et al., 2007). The sequential settlement, expansion, contraction, and maintenance of species with historical geographic environmental oscillations are major processes involving interactions between the biota and topographic locations in a given region, which have been reported in other ecological regions (Lenormand et al., 2019; Silva and Souza, 2018). The Mt. Mudeungsan (1187 m) and Mt. Gyeryongsan (846 m) national parks in the center of the southern Korean Peninsula, the high-altitude Mt. Palgonsan (1192 m) region in the southeast Korean Peninsula, and the Youngnam Mountains (an aggregation of nine mountains over 1000 m) are important locations containing local-scale plant communities (e.g., A. koreana , Primula farinose , andCarex tenuiformis in the Youngnam mountains), which are distant from the heterogeneous flora and the central distributions of Zone III (Kim et al., 2015; Korea National Arboretum, 2014). The mountains in these regions are an important factor in the formation of heterogeneous, small-scale biological interactions (Gentili et al., 2015; Thomson, 2005) and the process of species differentiation.
Excluding the oceanic island Ulleungdo, the islands of the Korean Peninsula were last connected to the mainland before the Early Holocene, around 7,000 years ago (Kim et al., 2016). The islands have spent a long time, in terms of evolutionary biology, separated from the East Asian mainland. Among the zones defined in this study, the coastal regions and islands that constitute Zone IV (the warmest zone but with the least annual precipitation) showed especially high abundance of certain plant species (but low overall mean abundance) and specific plants (e.g., Orchidaceae and Asteraceae) were diverse. As discussed above, these results were likely because of the inclusion of the volcanic island Jejudo (1950 m above sea level) with its uniquely warm and humid maritime climate, and the oceanic island Ulleungdo (986.7 m above sea level). The Orchidaceae (71.4%)—e.g., Habenaria chejuensis —and Asteraceae (24.3%)—e.g., Artemisia hallaisanensis —that are only present in Zone IV include species that only grow on Jejudo or Ulleungdo. Orchidaceae are most abundant in warm and humid regions and show a negative correlation with the latitudinal gradient (Cribb et al., 2003; Myers et al., 2000). The family can be an index of biodiversity, since they show specialized habitat preference (Cho et al., 2019) and form associations between multiple species, including pollinators and mycorrhizal fungi (Pemberton, 2010). Spatial separation (as seen on isolated islands) is a core mechanism of species differentiation, but concomitant ecologically important environmental variables (e.g., climatic and physical conditions) also operate in combination with spatial separation to create selection pressures (Anacker and Strauss, 2014). Despite its narrow width, Zone IV is a key region in terms of ecologically important environmental characteristics, taxon diversity, and species differentiation, and thus, among the floristic zones on the Korean Peninsula, it occupies an important position from a conservation and evolutionary perspective.
Away from the coast, the mainland regions in Zone IV include Mt. Bukhansan, which is a national park close to the western coast, and Mt. Mudeungsan, which is in the southwest mainland. These regions are large mountains within Zone III and are thought to be vestiges left after the entry of coastal and island floristic features from a past environment. The slopes of Mt. Mudeungsan have many warm wind holes (Park, 2017) and contain numerous plants that can otherwise be found mostly along the coasts and in islands (e.g., Cyrtosia septentrionalis (Rchb. f.) Garay and Polypodiales) (Hong et al., 2013). Some islands to the south and west of the Korean Peninsula were categorized into Zone III., A landscape that includes grazing and crop farming predominates the islands in the south of the Korean Peninsula, and thus, there has been an active introduction of plant species from the mainland, changing the flora considerably over time (Kim et al., 2017). These ecological landscape characteristics could form the background for the high floristic connectivity of some islands within Zone III, which mostly has flora in inland developed regions and warm temperate climates.
There are research limits to explaining in detail the processes and significance of spatial clustering and separation of floristic assemblages using regional patterns alone. Detailed descriptions of the plant reassembly process after the last glacial maximum and epoch-scale studies, such as pollen analysis, are needed (Yi, 2011). In addition, in the derived floristic zones, a convergent approach to phylogenetic history and diversity would be particularly useful for analyzing historical incidents in the formation of current biodiversity patterns, and for ascertaining the historical and evolutionary relationships between zones. Nevertheless, deducing the spatial arrangements of floristic assemblages is of great importance for understanding the ecologically important environmental factors involved in forming biogeographic regions. This study provides essential background knowledge to develop precise strategies for conservation based on micro- (Fenu et al., 2010) and nano-hotspots (Grant and Samways, 2011) at the local level. Moreover, there is great potential to quantitatively calculate the rarity, endemicity, and commonness of plant species, and to improve the priority of conservation and research (Casazza et al., 2005).