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ISSN : 1229-3857(Print)
ISSN : 2288-131X(Online)
Korean Journal of Environment and Ecology Vol.38 No.6 pp.672-691
DOI : https://doi.org/10.13047/KJEE.2024.38.6.672

Distributional Characteristics, Population Structures and Sustainability of Korean Endemic Plant, Abeliophyllum distichum1a

Young-Chul Kim2,3*, Hyun-Hee Chae3, Do-Il Oh4, Ji-Young Jung5, Sungwon Son6
2Research Center for Natural Science, Gangneung-Wonju National University, 7, Jukheon-gil, Gangneung-si, Gangwon-do 25457, Korea
3Research Laboratory of Korean Rare and Endangered Plants, 7, Jongjimok-gil, Daegwallyeong, Pyeongchang-gun, Gangwon-do 25343, Korea
4Byeonsan Peninsula National Park Office, Korea National Park Service, Jeollabuk-do, 56337, Korea
5Division of Garden and Plant Resources, Korea National Arboretum, 509, Gwangneung Soomokwon-ro, Soheul-eup, Pocheon-si, Gyeonggi-do 11186, Korea
5Division of Research Planning and Coordination, Korea National Arboretum, 509, Gwangneung Soomokwon-ro, Soheul-eup, Pocheon-si, Gyeonggi-do 11186, Korea

a This work was supported by a grant (KNA 1-2-37, 20-4) from the Korea National Arboretum (KNA)


* Corresponding author: modemipool@hanmail.net
02/08/2024 17/11/2024 18/11/2024

Abstract


Abeliophyllum distichum Nakai is a deciduous shrub and an endemic plant of Korea, which is also considered an endangered (EN) species. The national distribution of the plant was analyzed in detail, and then the population structures were assessed based on the observed distribution patterns. In addition, the effects of vegetation and soil quality on population structure were determined. In total, 13 sub-populations of A. distichum were detected. The most stable population was located in Jincheon, Chungbuk. The species was mostly distributed at the understory of deciduous forests, while some distributions were observed in mixed coniferous and broadleaf forests. The observed areas consisted of young individuals only or mature individuals only, or a small number of mature individuals and a large number of young individuals. Most areas of distribution were in screes and steep slopes of riverbanks. Soil substrates were composed of approximately 50% gravel, with varying sizes. Complex factors including soil substrates, organic matter content, and vegetation structure influenced the population structures of different sizes of individuals observed in the areas of distribution of A. distichum. Additionally, population structure varied across different re-establishment periods. A re-assessment was conducted based on regional Red List category and criteria. Despite variations in the area of occurrence and population size, the endangered status (B2ab [iii]) of the species was maintained due to a reduction in habitat quality observed in the areas of distribution and the increased fragmentation across groups within sub-populations. Consequently, conservation management plans considering the species traits of each sub-population should be formulated and implemented.


CONSERVATION , PLANT PHENOLOGY , SPECIES TRAITS , VEGETATIVE REPRODUCTION

한국특산 미선나무(Abeliophyllum distichum Nakai)의 분포특성, 개체군구조 및 지속가능성1a

김영철2,3*, 채현희3, 오도일4, 정지영5, 손성원6
2강릉원주대학교 자연과학연구소 전임연구원
3한국희귀멸종위기식물연구소 선임연구원
4국립공원공단 변산반도사무소
5국립수목원 정원식물자원과 연구사
6국립수목원 연구기획팀 연구사

초록


미선나무는 한국특산의 낙엽관목이며 위기종(Endangered; EN)으로 평가된다. 먼저 전국적인 분포현황을 세부적으로 평가하였다. 관찰된 분포 유형에 따라 개체군구조를 평가하였다, 또한 서로 다른 개체군 구조에 미치는 식생, 토양기질을 평가하였다. 미선나무는 총 13개의 아개체군이 조사되었다. 가장 안정적인 개체군은 충청북도 진천군에 위치하였다. 주로 낙엽활엽수림의 하부에 분포하였고 침엽수, 활엽수 혼효림에 분포지가 위치하기도 하였다. 어린개체로만 구성된 경우, 큰 개체로만 구성된 경우 및 소수의 큰 개체와 크기가 작은 개체로 구성된 경우가 조사되었다. 분포지는 돌서렁(Scree) 및 하안의 급경사지에 위치하였다. 토양기질에는 서로 다른 크기의 자갈이 약 50% 포함되어 있었고 경사도는 높았다. 분포지에서 관찰된 서로 다른 크기의 개체군 구조는 토양기질, 유기물함량, 식생구조 등이 복합적으로 작용하였다. 이와 더불어 서로 다른 정착시기에 따라 서로 다른 개체군 구조를 나타내었다. 지역적색목록평가 항목과 기준을 적용하여 재평가하였다. 점유면적 및 개체수가 변동되었지만 분포지에서 관찰되는 생육지의 질적 저하와 아개체군내에 서의 집단간 파편화 증가에 따라 위기종(EN; B2ab(iii))이 유지되었다. 각각의 아개체군별로 종의 특성을 고려한 보전관리계획의 수립과 시행이 필요함을 제안하였다.


보전 , 종 특성 , 식물계절학 , 영양번식

    INTRODUCTION

    The International Union for Conservation of Nature (IUCN) compiles a Red List for species on Earth to aid biodiversity conservation (IUCN Standards and Petition Committee, 2022). The criteria and category of the assessments for the Red List are also suggested (IUCN Standards and Petition Committee, 2022). Eight categories are suggested according to the risk of extinction, including Extinct (EX), Extinct in the Wild (EW), Critically Endangered (CR), Endangered (EN), Vulnerable (VU), Near Threatened (NT), Least Concern (LC), and Date Deficient (DD) (IUCN Standards and Petition Committee, 2022). Among the categories, only the LC species have no special management requirements due to have no extinction risk based on distribution extents and large population size (IUCN Standards and Petition Committee, 2022). The criteria for establishing a Red List should be based on an adequate basic information (IUCN Standards and Petition Committee, 2022). Informations including the extent of occurrence (EOO), area of occurrence (AOO), and population size are needed during categorization (Chae et al., 2022; IUCN Standards and Petition Committee, 2022;Chae et al., 2023). Especially, vary of EOO, AOO and population size were the most important information for the assessment of IUCN Red list criteria. However, considerable manpower, time, and financial resources are required to collect such data for each species (Kim et al., 2016b; Chae et al., 2022), so that large mammals, fishes and birds tend to attract more interest than plants.

    Currently, plant with high ornamental and medicinal value, which are under serious harvesting pressure, are being investigated (Convention on Biological Diversity, 2010;Blackmore et al., 2011). In particular, if the distribution of such a plant is limited to a narrow region or specific country globally, the risk of extinction is high (IUCN Standards and Petition Committee, 2022). The area of the Korean peninsula including North and South Korea is 223,516km², accounting for a mere 0.15% of the total area of the Earth’s terrestrial surface. Hence, a Korean endemic plant is considered to have a high risk of extinction based on a global scale assessment (Chae et al., 2022). However, based on a national level assessment, conservation priority can vary between the species distributed within the national territory and for species with localized distribution (Kim et al., 2022). Regional Red Lists of IUCN criteria are applied to determine the conservation priority of individual plants (Gardenfors et al., 2001;IUCN 2012). Nevertheless, there are cases where the same species is assigned a different categorization by the Ministry of Environment (MOE) and the Korea National Arboretum (KNA) of Korea Forest Service (KFS) based on the Red List criteria (KNA 2021;National Institute of Biological Resources (NIBR), 2021). Overall, it is critical to establish adequate current status on each target plants based on the distributional characteristics, life history, population dynamics, and threats (Kim et al., 2016a;Kim et al., 2018;Chae et al., 2019;Chae et al., 2021a;2021b). Unfortunately, make sure of such information is rarely achieved (Chae et al., 2022).

    Abeliophyllum distichum Nakai is a deciduous shrub and an endemic plant of Korea (Kim and Maunder, 1998). It was first observed in Jincheon, Chungcheongbuk-do, in 1919 (Kim and Maunder, 1998;Son et al., 2016). The seeds and several plants of A. distichum were subsequently sent to the United States (U.S.) and the United Kingdom, where they were cultivated and traded under the name ‘White Forsythia’ (Kim and Maunder, 1998). The plant has been used as a gardening shrub in Europe and the U.S. due to its unique scent as well as its high ornamental value (Kim and Maunder, 1998). Since the first report of the area of A. distichum distribution in Jincheon, distribution in other areas has been continuously reported (Kim and Kim, 2008;Lim et al., 2009;Shin et al., 2010;Lee et al., 2014a). Due to the risk of extinction based on highly isolated populations, small population size, and high collection pressure, the Cultural Heritage Administration of Korea designated the distribution areas of A. distichum as Natural Monuments (NM) (Korea Protected Areas Forum, 2009). The MOE also designated and managed A. distichum as a Class II Endangered Wildlife until 2013 (MOE, 2012). As such, the value of A. distichum has long been recognized as a target species for various study fields. Although recent studies have focused on fragrance and research for natural substances, the very first study on A. distichum explored its artificial propagation (Lee et al., 2014b). This was followed by a study re-assessing its taxonomic status and reporting new ranges of distribution (Kim and Maunder, 1998), and a large body of research has investigated its genetic structure and diversity (Chung and Chung, 1999;Chung, 1999;Kang et al., 2000;Lee et al., 2022). In addition, a study has reported the areas designated as NM and National Park based on its ecological study for distribution area (You et al., 2004). Recently, to provide basic data for the evaluation of the IUCN regional red list, a population size was assessed and reported (Kim et al., 2022). However, there is a general lack of information on the overall distribution and species traits of A. distichum.

    In this study, we have investigated current distribution of A. distichum as a basic informations for conservation activities. According to the distribution study, A. distichum is distributed across a wide range of areas and not solely in the areas designated and managed as NM. Furthermore, distinct feature of growing status were observed across population in different areas of distribution (Figure 1). Based on the current observation, the following four questions were setting up and investigated: 1) What accounts for the different states of growing conditions in each habitat? 2) What are the factors influencing population sustainability? 3) Are the conservation measures currently implemented in the areas designated as NM appropriate? 4) Are the each population sustainable? The interpretation to each question were compiled, and suggested to recommend suitable management and conservation in-situ.

    MATERIALS AND METHODS

    1. Species

    A. distichum is endemic to Korea and solely distributed on the Korean peninsula globally (KNA, 2012; NIBR, 2021). In a recent study on the areas of distribution of A. distichum, Wonju of Gangwon-do; Chungju, Goesan, Jincheon, Cheongju, Okcheon and Yeongdong, of Chungcheongbuk-do; Asan of Chungcheongnam-do; Andong and Uiseong of Gyeongsangbuk-do; and Buan of Jeollabuk-do, were reported (Kim et al., 2022). Two areas reported in previous studies; Goyang and Yeoju of Gyeonggi-do, have reportedly lost natural populations of the species, with the plants distributed in Goyang being planted and those in Yeoju having been transplanted (Kim et al., 2022). Among the areas of A. distichum distribution, the following areas have been designated as NM : Chujeom and Songdeok and Yulji in Goesan, Chuncheongbuk-do; Seolgye in Yeongdong, Chuncheongbuk-do; Junggye and Cheongrimin Buan, Jeollabuk-do (Korea Protected Areas Forum, 2009). A. distichum was designated as Class II Endangered Wildlife by the MOE until 2013; however, as the areas of A. distichum distribution were designated as NM, and considering artificial cultivation is considerably easy, the status of Class II Endangered Wildlife by the MOE was discharged. In addition, the NIBR of the MOE defines A. distichum as a vulnerable (VU) (B2ab (iii, v)) based on the National Red List assessment (NIBR 2021). The IUCN red list, however, defines A. distichum as an EN (B2ab (ⅲ)) based on only nine areas of distribution with an AOO of approximately 72㎢, isolated distribution of 20 ∼ 200km between populations, and reduction of EOO and continuous reduction of population size as a result of deterioration in habitat quality in the area of distribution (Son et al., 2016;KNA, 2021).

    A. distichum is a deciduous shrub with flower shape similar to Forsythia, while the flower color is white and the fruits are fan-shaped with flat and wide winged, which distinguishes A. distichum from Forsythia (Lee et al., 2022). The stem is characteristically bent, and as it touches the ground, it may grow roots and emerge as an independent plant (Kim and Maunder, 1998). At the base of the stem, sprouts may develop to form genets (Figure 2;A, B). The height of even an aged individuals is within 2.5m, and despite variations across habitats, the mean height is 1-1.5m (Author’s observation). The flowers developed at the axilla of the stem that grew in the preceding year, and despite variations across areas of distribution, flowers precede leaves between mid-March and early April (Figure 2;A, C, D). Leaf growth begins after the flowers have faded, at which time the fruits growth also begins (Figure 2;E). The fruits are flat and spherical or elliptical with wings along the edge. The common Korean name of the species, Miseon, meaning a beautiful fan, originates from the fruit shape resembling the fan of a fairy in a myth (Figure 2;F).

    2. Current distribution and study area

    Assessing of the status to a target plant species provides basic information that for the implement of conservation activities (IUCN Standards and Petition Committee, 2022). Therefore, the first step in the present study was to review the areas of distribution designated as NM and the areas of distribution reported in previous studies. Subsequently, the areas of distribution identified by the authors through field investigations from 2012 were added. Combining the data, the sites with potential distribution among the known areas of distribution were assessed from March 2021 to April 2022, and an in-depth analysis was conducted (Figure 3). Each population was distinguished according to the area of distribution with the distance between each population at ≥ 10km. A. distichum did not exhibit continuous distribution in each population, with patches of varying sizes observed. Hence, each patch was assessed as a single sub-population. First, using GPS (Garmin GPS 64s, Garmin Ltd, Olathe, KS, USA), the coordinates and altitudes were measured and recorded at the center of distribution area. In addition, by connecting the edges of each patch, the distribution area was measured. When estimating the population size, the growth conditions observed in each area of distribution was taken into account. In the case of small individuals flat on the ground surface, the population size was set as n=10 per 1㎡. For individuals as tall as ≥ 1.5 m with well-developed stems, the population size was set as n=1 per 1㎡. The results are presented as a list (Table 1).

    The areas of A. distichum distribution observed in the preliminary distribution study were Yeoju, in Gyeonggi; Wonju, in Gangwon; Chungju, Goesan, Jincheon, Cheongju, Okcheon, and Yeongdong, in Chungbuk; Asan, in Chungnam; Andong and Uiseong, in Gyeongbuk; and Buan, in Jeollabuk (Figure 3; Table 1). The AOO estimated for each population was 104,679㎡, while the estimated population size was 154,264 individuals (Table 1). The individuals in Yeoju population, had been transplanted to construct of a road go into a recently constructed golf course, although approximately 300㎡ area of distribution were remained (Table 1). The field investigation of the area in the Bukhansan National Park in Goyang, Gyeonggi-do, which is an area of distribution reported in previous studies, showed that natural populations had disappeared and only the planted individuals were found. Therefore, the areas of Goyang was excluded from this study. The area in Asan, was also excluded following literature review and additional investigations in 2023. In the present study, the study populations of A. distichum were selected by comparison of population size and the distribution status observed in each distribution area (Table 2).

    3. Methods

    In the field study, each population and sub-populations within a population exhibited a unique growth status (Figure 1). Hence, the area of investigation was selected to ensure that the characteristics of each area of distribution with different plant growth status were incorporated (Figure 1). First, in the vegetation survey, a 25㎡ (5m × 5m) plot was established in each selected population, and extending the 25㎡ plots, 100㎡ plots were also set. Depending on the population, however, either a 25㎡ plot or a 100㎡ plot was installed in some areas. The plants observed in each plot were recorded using the phytosociological method of vegetation survey (Braun- Blanquet, 1964), and coverage was estimated. The coverage of observed species was estimated as a percentage (%). A list of observed species was made for use in the analysis of distributional characteristics through Detrended Correspondence Analysis (DCA) ordination (Lepš and Šmilauer, 2007). A table of species composition was drawn for the plants found in the 25㎡ and 100㎡ investigation plots, and the importance value (IV) was calculated using relative coverage (RC) and relative frequency (RF).

    The observed plants were identified in reference to Lee (1980), Lee (1996a;1996b), Lee (2003a;2003b), and Lee (2006a;2006b). For naturalized plants, a reference was made to Park (2009). The scientific names and Korean names were based on the National List of Species of Korea (Kim et al., 2019). For species that could not be identified based on the above literature, references were made to Grasses and Sedges of South Korea (Cho et al., 2016) and Pteridophytes of Korea: Lycophytes and Ferns (Korean Fern Society, 2005;Lee and Lee, 2018).

    Population structures were investigated based on the 25㎡ plots installed for the vegetation study. The characteristics of A. distichum were below the mean height of < 2m and sprout were developed successfully. The branches of the developed sprouts would elongate downward to the ground, and roots could emerge from them as a form of vegetative reproduction. In light of this, 35 individuals were selected within a plot in the order of size from the tallest, and height was measured. The diameter of the stem at 5cm height (D5cmH) was also measured using a Vernier Callipers (Mitutoyo, Japan). Individuals considered to be the same ramet were excluded from the height and diameter measurements. Additionally, 35 individuals were selected in Songdeok and Chujeom in Goesan, the measurements were used to compare the structures of the natural populations and the structures of the populations identified as NM and managed artificially.

    To assess the self-compatibility of A. distichum, the populations in Euntan in Jincheon-gun, were investigated. Five individuals with relatively large sizes were selected at 30-50cm intervals during the early flowering period on March 10th, 2022. Two stems with a high flower density were selected from each individual. The selected stems were marked and the respective number of flowers counted and recorded, while one of the flowers was covered with an anti-insect net (Ø 1mm) to block pollinators. At this time, the flower was in the bud-swelling phase, with incompleted pistil and stamen growth. The net was removed on April 10th, 2022, at the completion of flowering. Subsequently, the number of fruits at each selected stem was counted on June 28th, at complete growth of fruits. The measurements were used to calculate the fruition rate in proportion to the number of flowers after flowering, and estimating the presence or absence of self-compatibility in A. distichum.

    Five random points were selected in a population within the 25㎡ vegetation study plots to collect soil samples. Care was taken to ensure particles of all the different sizes constituting the soil layer were included. The collected soil was transported to the lab and dried in a shaded condition. The soil was divided into three groups based on particle size: ≤ 2 mm, 2–4.5mm, and ≥ 4.5mm, and the respective weights were measured. Using the ≤ 2mm soil, organic matter (OM) was analyzed. In the ≥ 4.5mm soil, 50 of the largest particles in terms of length were selected and the diameter measured. The measurements were used to compare stem diameter at 5cm height in populations, and the ratios of OM and soil particle sizes. No soil was collected from nature conservation areas (NM) or their surroundings or national parks. Additionally, 30 of the largest rocks observed on the ground surface in certain areas of investigation were selected and their lengths and widths recorded.

    JC36, OC2, and CJ with the highest mean diameter and 5cm height were categorized as Performance Group I (PGR1), and JC46 and YJ with the lowest mean diameter at 5cm height were categorized as Performance Group III (PGR3). The rest, including JM1, JC7, JC52, JE5, YY1, and WJ7, were categorized as Performance Group II (PGR2). Based on this categorization of three groups, the difference in height of the measured stems, OM examineed in the soil, proportion of > 2mm soil in the soil substrates collected from the plot, proportion of > 4.5mm soil (gravel) in the soil substrates, and the proportions of particles with a length of > 4.5mm (gravel), were compared.

    To examine the annual growth characteristics of A. distichum, the populations in Jincheon and Goesan were periodically visited and monitored from February 20th to December 10th, 2022. Notably, in the flowering season, visits were made at least once a week or more to monitor growth status. Each state was photographed using a digital camera (Cannon EOS6D Mark Ⅱ, Canon, Tokyo, Japan). The annual growth characteristics were described based on the monitoring logs and photos.

    4. Statistical Analysis

    The vegetation survey data collected from the 25㎡ and 100㎡ plots installed within A. distichum habitats were analyzed through DCA ordination (Canoco 4.53, Microcomputer Power, USA; Lepš and Šmilauer, 2007). A non-parametric hypothesis test (Kruskal-Wallis test, p<0.05) was used to test for variation in fruition rate across five samples in which pollinators had been blocked. A correlation analysis (Spearman rank correlation coefficients, P<0.05) was performed for the relationship between stem diameter (5cm; n=17) and height. Before comparing the diameters of the stems from each area of distribution, the test for normality was conducted (Shapiro-Wilk and Kolmogorov-Smirnov tests, p>0.05). If normality was not satisfied, a non-parametric hypothesis test was performed (Kruskal-Wallis test, p<0.05). If normality was satisfied, one-way Analysis of Variance (p<0.05) was performed. Tukey’s Honestly-Significant-Difference (HSD) test was used to test for significant differences between individual measures. In the case of samples of different size, a non-parametric hypothesis test (Kruskal-Wallis test, p<0.05) was used to compare differences. All statistical analyses were performed in SYSTAT 12 (Systat Software Inc., San Jose, CA, USA).

    RESULTS AND DISCUSSION

    1. Vegetation of habitats

    According to the DCA ordination based on the vegetation data collected from 100㎡ plots installed in the populations of A. distichum, the areas of distribution could be broadly divided into the area in Buan and other areas (Figure 4;B). The ddfference between the population in Buan and the populations in other areas was based on the species observed solely in Buan, including Orixa japonica, Meliosma myriantha, Acer pseudosieboldianum, Hepatica asiatica, Sasa borealis, Viburnum dilatatum, and Lindera erythrocarpa, and the species observed in areas other than Buan, including Euonymus alatus for. ciliatodentatus, Fraxinus rhynchophylla, Securinega suffruticosa, Viburnum carlesii, Stephanandra incisa, Deutzia uniflora, Picrasma quassioides, Weigela subsessilis, and Lonicera praeflorens, representing trees, and Lindera obtusiloba, Dictamnus dasycarpus, Calamagrostis arundinacea, Neillia uekii, Viola acuminata, Athyrium yokoscense, Parthenocissus tricuspidate, and Dioscorea nipponica, representing shrubs. In contrast, the DCA ordination based on the vegetation data collected from 25㎡ plots showed that the areas could be broadly divided into the populations in Buan (BA), Wonju (WJ), and Chungju (CJ), the populations in Jincheon (JC), Goesan (GS), Okcheon (OC) and Yeongdong (YY), and the populations in Yeoju (YJ) and Munbaek (JE, JM, Jincheon) (Figure 4;A).

    In the tree layer of 100㎡ plots, the species with the highest IV was Quercus variabilis (19.5), followed by Platycarya strobilacea (17.0), Quercus aliena (14.7), Zelkova serrata (14.2), Fraxinus rhynchophylla (12.7), Quercus acutissima (12.7), Quercus serrata (12.7), and Pinus densiflora (10.9). In the subtree layer, the species with the highest IV was F. rhynchophylla (18.6), followed by Q. serrata (17.9), Acer pictum subsp. mono (10.9), Platycarya strobilacea (9.8), Q. aliena (9.5), and Ulmus davidiana var. japonica (8.3). In the tree layer of 25㎡ plots, the species with the highest IV was P. strobilacea (28.7), followed by Q. aliena (23.0), Z. serrata (14.4), Q. variabilis (13.7), Q. serrata (13.7), Q. acutissima (12.6), F. rhynchophylla (12.3), Quercus xurticifolia (10.2) and P. densiflora (9.2). Therefore, the areas of distribution corresponded to a mixed forest of deciduous broadleaf and a mixed forest of deciduous broadleaf and evergreen coniferous. Both forests constituted vegetation types that formed at the lower part of mountainous slopes close to rivers and streams. The results are consistent with the observation that most areas of distribution (excluding GY2 and GY6) were located at mountainous slopes close to rivers.

    In the herb layer of 100㎡ plots, the species with the highest IV was A. distichum (46.9), with a highest coverage, followed by L. obtusiloba (3.4), D. dasycarpus (3.3), Akebia quinata (3.0), C. arundinacea (2.4), N. uekii (2.4), Dryopteris lacera (2.3), and Smilax sieboldii (2.3). With the exception of A. distichum, the coverage observed in the herbaceous layer did not exceed 20%, while most were only 0.5-5%. Moreover, the coverage of the shrub layer was not high, and the order of species based on IV, with the exception of A. distichum (35.5), was L. obtusiloba (9.9), L. obtusifolium (9.2), Callicarpa japonica (8.8), and Euonymus alatus for. ciliatodentatus (7.4). For the herbaceous layer in the 25㎡ plots, the species with the highest IV was A. distichum (71.6), followed by L. obtusiloba (5.5), D. dasycarpus (4.1), Dryopteris lacera (4.1), Ampelopsis heterophylla (2.9), Stephanandra incisa (2.4), Viola acuminata (2.1), Isodon excisus (2.0), and Hydrangea serrata for. acuminata (1.9). The order of species distribution in the shrub layer based on IV with the exception of A. distichum (45.6), was L. obtusiloba (11.5), E. alatus for. ciliatodentatus (7.9), C. japonica (7.6), S. incisa (7.4), and L. obtusifolium (6.5). As with the plants in 100㎡ plots, the coverage of plants in 25㎡ plots was generally low, with the exception of A. distichum. The richness in the herbaceous layer of 100㎡ plots was as follows: 19 species (JE5, JM1) and 54 species (GY6), with a mean richness of 30.38 (±9.75). This was lower than the richness for herbaceous plants observed in the areas of distribution of Abelia tyaihyonii, a shrub species with a similar level of ground cover as A. distichum (Chae et al., 2002). Notably, a Class II Endangered Wildlife designated by MOE Iris koreana was also distributed in the area of distribution of A. distichum in Buan.

    2. Population structures

    Individuals of varying sizes were distributed in A. distichum populations. Notably, A. distichum exhibited a high level of reproduction via natural layering. As a result, a form of expansion based on genets was observed, whereby the newly growing genets covered the area around the first generation. Taking that into account, 35 individuals found in the 25 ㎡ plots in the area of investigation were selected in the order of stem height, and the diameter at 5cm was measured. Population structures was analyzed using the measured data (Figure 5). There was a strong correlation between the height and stem diameter (r=0.89, p<0.0001).

    The results indicated that the observed population structures could be divided broadly into three types, including areas of distribution composed of individuals with large diameter (GY [NM], GC [NM]), small diameter (BA8-1, BA8-2, GY6, JC46, JM1, JE5, WJ7, YY1, YJ), and diameters ranging from large to small (CJ, GY2, JC7, JC36, JC52, and OC2) (Figure 5). The two areas of investigation for the population in Buan, consisted solely of short heighted individuals with small diameter. There were areas of distribution within the population in Buan that consisted of relatively tall individuals with large diameter; however, most areas had a population structure comprising individuals with small diameter consistent with the measurements. The population structures in Jincheon and Goesan varied across sub-populations (Figure 5; GY2, GY6, JC7, JC36, JC46, JC52, JM1, JE5). The population in Jincheon was a natural population without human interference, where the area of distribution and population size, as well as the size of individuals constituting each sub-populations, varied across different sub-populations (Figure 5). In the areas of investigation for the populations in Yeongdong and Okcheon, individuals with relatively large diameter and those with small diameter were distributed in the same areas (Figure 5; OC2, YY1, WJ7). The population structures in the areas constituted two to three relatively large individuals and multiple individuals with relatively small diameter (Figure 5; OC2, YY1, WJ7).

    For the population in Yeoju, most areas of distribution had damaged due to a construction project, and approximately 20% of the total population remained at the time of the study. The remaining individuals were at the edge of the areas of distribution and comprised only individuals with small diameter (Figure 5; YJ). In contrast, the populations selected for the comparison with natural populations were those designated as NM, with consequent protection and management, where most individuals had diameters ≥ 1.0cm with mean values of 2.35(±0.70)cm (GY [NM]) and 1.81 (±0.59)cm (GC [NM]) (Figure 5; GY [NM], GC [NM]). Hence, all individuals resembled those with the largest diameter observed in other populations (Figure 5).

    3. Habitats characteristics and vitality

    The altitude of the habitats of A. distichum ranged from 42m (JE5) to 212m (GY6) (Table 3). All habitats of A. distichum were located at low altitudes and none were found in high mountainous regions. The areas of distribution were in the North, Northwest, Northeast, and Southeast regions (GC [NM], JC52; 100°) (Table 3). With the exclusion of two areas, all areas of distribution were on slopes facing the North. The mean slope degree in the habitats of A. distichum was 33.03(±8.87)° (Table 3). The plot showing the lowest slope degree was GY2 (13°), followed by JC46 (18°). The plot showing the highest slope degree was JE5 (44°) (Table 3). The slope degree of the habitats around the GY2 and JC46 regions showing low slope degree was ≥ 35°; in particular, areas with the slope degree ≥ 50° were common. Such areas hampered plot establishment, vegetation surveys, diameter and height measurement, and soil collection, and were excluded from investigation. For this reason, the measured slope degree of the habitats of A. distichum were lower than the actual gradients. The mean height of the tree layer was 15.16±2.71m, and the mean coverage was 75.33±11.87%. The plot with the highest coverage was BA8-2 (95%), followed by BA8-1 (90%). The mean height of the sub-tree layer was 5.60±0.71m, with a mean coverage of 48.33±11.90% (Table 3). The mean coverage was 52.81±14.02% for the shrub layer and 63.44±12.48% for the herb layer (Table 3). In the investigated areas, shrub or herb layer coverage depended on A. distichum. Most habitats of A. distichum were located at the lower parts of mountainous slopes close to rivers; BA8-1, BA8-2, GY(NM), GC (NM), JM1, and OC2 were in screes. The mean rock size measured in the areas was 37.26±15.21cm[L] × 30.66±13.01cm[W] (Table 3). The habitats with the largest rocks was GY2 (64.8±29.30cm[L] × 55.4±27.61cm[W]), followed by OC2 (54.8±19.76cm[L] × 43.7±16.01 cm[W]) (Table 3). Other sites of A. distichum were cliffs on riverbanks (WJ7, YY1, OC2, and CJ) and cliffs formed by past river erosion (JC36, JC7, JC46, and JE5), where the substrates included relatively small rocks and gravels, unlike in screes (Table 3).

    A. distichum stem height measured in each investigated area ranged between 191.53 ±37.98cm (GY [NM]) and 0.30±0.13cm (BA8-1) or 0.30±0.10cm (BA8-2) at min. (Table 3). Notably, the area with the tallest stems was a NM under human management. In contrast, among the natural populations devoid of human disturbance, the population in Jincheon (JC36) had the tallest stems with the mean height at 151.65±28.65cm. The population in Buan (BA8-2) had the shortest stems with a mean height of 47.05±17.64cm. With the exclusion of NM, the mean stem height across the 15 populations was 107.12±34.41cm. The largest diameter among the measurements of all investigated areas, was 2.35±0.70cm, in a nature conservation area in Goesan (GY [NM]) (Table 3). The smallest D5cmH was shown by the population in Buan (Table 3). The mean stem diameter of the 17 populations was 0.84±0.55cm.

    As A. distichum exhibits sprout development from the base of stems, the number of sprouts was counted in the individuals whose height was measured. The population in Goesan (GY [NM)), which is a NM, showed the highest number of sprouts (9.50±4.29). In contrast, the lowest number of sprouts (1.70±0.80) was observed in the population in Yeongdong (YY1) (Table 3). The number of individuals with the highest number of sprouts was 23 in the NM. The number of sprouts in the individuals distributed among low height populations was mostly 1-3 (Table 3). The mean number of sprouts in natural populations was 2.26±0.62 and the highest number of sprouts was 10 in an individual found in Jincheon (JC36).

    4. Soil substrates and performance variable

    The mean stem diameter (Figure 6;A) and mean stem height (Figure 6;B) estimated for each population showed a considerable level of similarity. All populations assessed were natural populations, and excluding those in NM, all were found at the lower part of the vegetation. Accordingly, the soil in each investigated area was collected, and the OM in the soil and the sizes of the particles constituting the collected substrates were compared. For the 11 investigated areas, the proportions of ≤ 2mm soil did not exceed 53.02% (JC36) and was a mere 1.61% (JM1) at minimum (Figure 7). The percentage of soil for the substrates collected from the soil layer was 31.30±15.83% on average, and the rest were > 2mm. The OM in the soil were the highest in Jincheon (JM1) at 58.51±0.54% (Figure 7;A). The lowest content, 4.35±0.15%, on the contrary, was observed in Okcheon (OC2) (Figure 7;A). The mean OM was 15.17±14.26%.

    Across the 10 investigated areas, the sizes of rock covering the ground surface were estimated (Figure 8;A). The mean rock size was the largest in Jincheon (GY2), at 64.80±29.30cm, an area of distribution formed in screes. The next largest mean rock size, 54.80±19.76cm, was observed in Chungju (CJ). For the 10 investigated areas where rock diameters were measured, rock length varied (Figure 8;A) and the proportion of rocks also varied (Author’s observation). Notably, most substrates consisted of rocks and the habitats with rocks of large diameters was Buan (BA8-1 and BA8-2), with mean rock diameters of 27.00±8.52cm and 31.80±9.91cm, respectively. An area of distribution similar to Buan, Munbaek in Jincheon (JM1), had a mean rock diameter of 18.70±5.97cm, showing a deviation (Figure 8;A). Among the particles collected in soil, with the exclusion of large rocks, the diameter of those categorized as ≥ 4.5mm varied according to site (Figure 8;B). The area of distribution showing the largest diameter of particles, ≥ 4.5mm, was JM1, with a mean diameter of 4.70±1.14mm. In the 11 areas of distribution from which soil was collected, the mean diameter of particles categorized as ≥ 4.5mm was 3.22±0.98mm. That is, the proportion of ≤ 2mm soil was low in the habitats of A. distichum (Figure 7;B), while all areas of distribution showed higher proportions of rock and gravel (Figure 8;A, B).

    Three levels of performance variable were categorized based on the mean diameter, as shown in Figure 6;A. Here, the habitats with no soil collections from plots; Buan (BA8-1 and BA8-2) and Goesan (GY2 and GY6), were excluded. The habitats of JC36, OC2, and CJ, with the largest mean diameter, were categorized as performance group 1 (PGR1), and the habitats of JC46 and YJ, with the smallest mean diameter, were categorized as performance group 3 (PGR3). The remaining JM1, JC7, JC52, JE5, YY1, and WJ7 were categorized as performance group 2 (PGR2). As a result, a clear variation in mean diameter was observed across the three groups (Figure 9;A, Mann-Whitney U Test, p<0.001). In addition, a clear variation in height was observed across the three groups (Figure 9;A, Mann-Whitney U Test, p<0.001). Hence, the performance variable of A. distichum was shown to vary distinctly according to three categories (Figure 9).

    For the soil collected from each plot categorized in three groups, OM, proportions of soil in the collected substrates, and proportions of ≥ 4.5mm diameter particles in substrates (in the direction of the longest axis) were compared. Among the plots displaying three levels of performance variable, the proportions of ≤ 2mm soil remained constant (Figure 10;A, Mann-Whitney U Test, p>0.05). Despite the lack of significant variation, the proportions of soil tended to be higher in PGR3, for which the performance variable was observed to be the lowest. In contrast, OM in the soil was the highest in PGR2 (Figure 10;B, Mann-Whitney U Test, p<0.05). The proportions of ≥ 4.5mm particles in the collected substrates did not vary across the three levels of performance variable (Figure 10;C, Mann-Whitney U Test, p>0.05). In contrast, the diameter measured in the direction of the longest axis in ≥ 4.5mm particles was the largest in PGR2 (Figure 10;D, Mann-Whitney U Test, p<0.001).

    5. Influence of pollinators

    The number of flowers on the five branches used to blocking pollinators (≥ 1mm) was 191.40±93.14 on average (Table 4). The number of flowers on the five branches left without blocking the pollinating insects was 145.00±95.75 on average (Table 4; χ2=0.54, p=0.47). Therefore, flower number did not vary significantly across the selected branches. The number of seeds on the branches in the absence of pollinating insects was 11.40±7.54 on average. The number of seeds on the branches without blocking the pollinating insects was 12.20±9.42 on average. Hence, the number of seeds did not vary significantly between pollinating insect blocking condition and the non-blocking condition (Table 4; χ2=0.01, p=0.92). In addition, the mean fruition rate was 8.29±9.08% in the former condition and 14.30±20.05% in the latter condition. Furthermore, the fruition rate did not vary between the two conditions (Table 4; χ2=0.27, p=0.60). The results indicated self-compatibility, leading to fruit production even in the absence of pollinators. However, follow-up studies should be conducted to explore the observations that multiple white flowers with heavy scents were produced and that the net used to block insects had 1mm grids with small insects potentially passing through the net.

    6. Phenology

    In spite of the phenological differences depend on the weather condition, on March 25th 2022, A. distichum exhibited the first signs of bud swelling at the axilla (Figure 11;B, C, D). The onset of flowering was first observed in the population in Buan, on March 20, and then in ≥ 80% populations in the areas of Jincheon and Goesan, around April 5th-10th (Figure 11;E, F). The flowering period came to an end around April 15th across all populations and the leaves started to grow on the branches without flowers and in the plants without flowers. Full leaf growth was initiated at around April 20th - 25th (Figure 11;G, H), when the growth of fertilized seeds also began (Figure 11;I). Seed growth and maturation progressed rapidly from around May 10th (Figure 11;J) to achieve full development around July 20th (Figure 11;K). Seed maturation was complete in late September, although the seeds remained attached to the stems (Figure 11;N). The flower buds for the flowering in the following year began to develop around mid-October (Figure 11;L) and depending on the climate conditions, some abnormal flowering states were observed in certain individuals and populations (Figure 11;M). The mature seeds remained on the stems even after all leaves had been shed, while some even remained until the flowering period in early March (Author observation).

    7. Discussion

    The habitats of A. distichum were generally in screes and cliffs. As a result, the rocks and gravels constituting the substrates in the areas of distribution varied in size (Table 3; Figure 7;8). A. distichum is a rhizome with development at the tip of an elongating stem, where vegetative reproduction occurs (Chung and Chung, 1999; Author’s observation). Screes are site that delay the regeneration and development of plants (Connell and Slatyer, 1977). Therefore, it hypothesized that plants regenerated in screes can maintain populations for long periods without competition, as invasion by competing species is naturally limited (Harper, 1977;Rejmánek et al., 2004). Moreover, despite frequent, small-scale degradations that may prevent plant regeneration, cliffs with high slope degree also allow species such as A. distichum that are highly capable of vegetative reproduction via natural layering, to maintain populations for long periods once the first regeneration has been established (Connell and Slatyer, 1977;Rejmánek et al., 2004). Such species traits were determined to be reflected in the vegetation and population structures in the habitats of A. distichum, as observed in the present study (Figure 5). Therefore, conservation plans and management activities for the conservation of A. distichum populations should be formulated and implemented while taking into account such species traits (Elzinga et al., 1998;Crawley and Ross, 1990; Chae et al., 2022).

    The growth status of A. distichum in its areas of distribution was broadly divided into four types (Figure 4). With the exclusion of NM with human management activities (Figure 5; GY [NM], GC [NM]), the natural A. distichum had a type that was short and spreads laterally (PGR3), at type that was tall and capable of flowering and spreading laterally (PGR2), and a type as tall as ~ 2m and mostly capable of flowering (PGR1) (Figure 5;9). The different growth states were not correlated with vegetation and soil substrate characteristics in the areas of distribution (Table 3; Figure 10). Notably, the finding that groups displaying varying growth states coexisted in a local population indicated that the performance variable was not influenced by certain physical environmental factors (Figure 12;A, B). That is, A. distichum can undergo vegetative reproduction via natural layering, through characteristic growth with flat lateral spreading of stems rather than upward growth in the early phase of establishment or regeneration. As vegetative reproduction is repeatedly achieved, genets with identical genetic traits are formed within a set range (Chung and Chung, 1999). The sizes of such genets are presumed to be correlated with the number of individuals in the early generation, and the diameter across the groups with two to three individuals was approximately 5m. The population structures of A. distichum were thus considered to reflect such growth characteristics (Figure 5). On the contrary, most individuals distributed in NM had large diameters (Figure 5; GY [NM], GC [NM]) and genets had not formed via natural layering. A potential reason is the human activity of periodically removing plants growing in the vicinity of large A. distichum individuals, within the NM. The mowing operation was performed twice a year, whereby plants around A. distichum individuals were cut to a height of ~10cm. In particular, within the NM in Buan, shrub such as Lonicera harae and L. subsessilis had density and coverage characteristics similar to A. distichum and were considered to be a competitive relationship with A. distichum. Conversely, the rates of flowering and fruition were observed to be higher in NM than in the natural areas of distribution (Author’s observation). However, in 2022, only two individuals were fruited successfully in the NM in Songdeok, Janyeon. This was presumed to be due to the influence of continuous drought in spring. It is also hypothesized that the influence of invasion by competing species would increase in the long run when the periodic management of NM is discontinued. Accordingly, there is a need to re-assess potential effects of artificial changes in light (Kim et al., 2022) and soil conditions in the natural habitats of A. distichum (Lim et al., 2009). Sudden changes in light and soil conditions may not simply exert positive effects on the co-distributed A. distichum individuals but promote the invasion and growth of competing species in certain cases, to bring about local extinction due to the competition-induced pressure in the long term.

    The small A. distichum groups with varying sizes in each population exhibited patchy distribution (Kim et al., 2022; Figure 12). Notably, the habitats with the highest number of individuals over the widest range were Chopyeong and Munbaek in Jincheon, with 70 sub-populations (Table 1; Figure 12;A), followed by distribution in Buan, with 20 sub-populations (Table 1; Figure 12;B). The individuals in Jincheon, comprised groups with different population structures as well as sub-populations of highly varied sizes (Table 1; Figure 3; Figure 12;A). Therefore, we hypothesized that the areas in Jincheon, were the centers of A. distichum distribution.

    While all areas of A. distichum distribution were found at ≤ 250m altitudes, they were located to the west of the Baekdudaegan mountain range on the Korean peninsula. No range was observed on the high mountain peaks or the rocky slopes or screes of mountain ridges. Overall, most habitats of A. distichum were located close to rivers (Kim et al., 2022; Figure 12). This the need for studies on seed dispersal mechanisms as potential factors influencing the establishment of A. distichum ranges (Hampe, 2011). A. distichum genetic diversity studies have reported that high genetic diversity even though it is an endemic plant that is distributed in isolation, which minimizes genetic exchange (Kim and Maunder, 1998;Chung and Chung, 1999;Chung, 1999;Kang et al., 2000;Lee et al., 2022). In the present study, seed production was not affected by the blocking of large pollinating insects (Table 4). For the establishment and maintenance of genetic diversity in an isolated population, the distance between each area of distribution should allow the migration of pollinating insects; however, the level of isolation of A. distichum is substantially high (Kim and Maunder, 1998;Son et al., 2016; Figure 3). Therefore, current research data on A. distichum genetic diversity, distribution, species traits, and annual life history should be integrated in conservation plans and management activities (Pickett and Thompson, 1978;Crawley, 1986;Crawley and Ross, 1990;Kim et al., 2016a; Chae et al., 2022; 2023).

    A. distichum is defined as an EN (B2ab (iii)) species in the IUCN red list (Son et al., 2016), and in the present study, an AOO of ~ 72㎢ with nine known areas of distribution and severe fragmentation with each sub-population separated by 20-220km, as well as the effects of deforestation on qualitative and quantitative degradation of natural habitats support the designation. In the present study, A. distichum current distribution is assessed comprehensively (Table 1). Thirteen populations were detected even after considering areas of distribution apart by ≤ 10km as single populations (Table 1; Figure 3). The total distribution area investigated was 106,829㎡ and the population size was 155,664 (Table 1). The AOO estimated using the 4㎢ (2km × 2km) grid suggested by the IUCN was 112㎢. This study reports the highest number of populations, distribution areas, and population sizes among recent reports on areas of A. distichum distribution (Kim and Maunder, 1998;Lee et al., 2014a;Son et al., 2016, Kim et al., 2022). Shifts in population size and EOO or AOO from a certain time point could not be comparatively analyzed. Applying EOO to plants was inappropriate, as well as applying the number of mature individuals in a woody plant and highly capable of vegetative reproduction. Hence, an AOO ≤ 500㎢ and highly isolated population characteristics should be taken into account.

    Additionally, major construction works were ongoing in the vicinity of most areas of distribution, with the exception of the area in Buan, located within the Byeonsan Peninsula National Park. The population in Yeongdong, was located in an urban area, while being isolated like an island, with surrounding parks and roads. The area of distribution in Uiseong, was also surrounded by tourist sites, farms, and residential areas. In the case of the population in Jincheon, an industrial complex was constructed in the vicinity, and the extent of population isolation was increased by extended residential areas and newly constructed roads. Moreover, the area of distribution in Yeoju, had lost its original form as two thirds of the population was moved in the course of building a road leading to a recently constructed golf course. According to the results, maintenance of the EN (B2ab (iii)) status is reasonable, even based on the IUCN red list criteria. Notably, however, the threats observed in the current A. distichum areas of distribution should be clearly stated. Furthermore, the findings of this study could facilitate quantitative evaluation of shifts in EOO, AOO, and population size in future (IUCN Standards and Petition Committee, 2022).

    Acknowledgement

    This study was funded by the government of Republic of Korea (Korea Forest Service) as part of the project Population Characteristics and Conservation Management Strategies for Rare Plants (KNA 1-2-37, 20-4) at the Korea National Arboretum.

    Figure

    KJEE-38-6-672_F1.gif

    Different growth pattern of Abeliophyllum distichum Nakai observed in the habitats, A; (Performance group3(PGR3)), B; (Performance group2(PGR2)), C: (Performance group1(PGR1)) and D; GY (National Monument(NM)).

    KJEE-38-6-672_F2.gif

    Photographies of A. distichum, A; habitat (blooming in march), B; habitat (vegetative growing in May), C; blooming flower on the layering stems, D; blooming flowers, E; maturing fruits in July, F; maturing fruits in September.

    KJEE-38-6-672_F3.gif

    Map of A. distichum populations observed in Korea, ID’s are related to Table 1.

    KJEE-38-6-672_F4.gif

    The result of DCA ordination(Squareroot-transformation) used with collected on 25㎡(A) and 100㎡(B) plots, A; using the observed every species, B; using the observed every species. population ID are related to Table 2.

    KJEE-38-6-672_F5.gif

    The population structures based on the stem height(D5cmH) established in the selected 25㎡ plots. Population ID are related to Table 1.

    KJEE-38-6-672_F6.gif

    Comparison of average D5cmH(A) and stem height(B).

    KJEE-38-6-672_F7.gif

    Comparison of organic matters (OM) and particles(below 2mm(soil), between 2mm to 4.5mm and above 4.5mm).

    KJEE-38-6-672_F8.gif

    Comparison of characteristics of matrix(A; rocks and B; gravels).

    KJEE-38-6-672_F9.gif

    Comparison of three performance groups with D5cmH(A) and stem height(B).

    KJEE-38-6-672_F10.gif

    Comparison of matrix component related to three performance groups, soil(A), OM(B), gravel(> 4.5mm)(C), gravel diameter(D).

    KJEE-38-6-672_F11.gif

    The phenology of A. distichum, A; wintering individual, B, C; flower bud, D; flower bud maturing in the JE, F; flower bloom in the GS, G; leaves growing in the BA, H, I, J, K; fruit maturing, L; flower bud emerging, M; abnormal flower blooming in the GC, N; matured fruit.

    KJEE-38-6-672_F12.gif

    Distribution maps observed and calculated in the population of Jincheon-gun, Chungbuk(A), Buan-gun, Jeollabuk(B).

    Table

    The list of A. distichum populations observed in Korea

    Abbreviations : NM = Natural Monument, PL = Planted, Pop. ID = Identification of population, Sub-pop. No. = observed number of sub-population, Pop. size = Population size, N = North, E = East, Alt. = Altitude
    * GPS coordinations are confidential to prevent illegal harvesting

    The selected population list of A. distichum on this study

    Abbreviations : Pop. ID = Identification of population and sub-population number, Pop. size = Sub-population size, N = North, E = East, Alt. = Altitude, VS = Vegetation study, PF = Performance variables
    * GPS coordinations are confidential to prevent illegal harvesting

    Performance variables collected from 17 sites

    The influence of visiting pollinators to make fruits

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