Introduction

East Asian alder (Alnus japonica) belongs to birch family. It is a deciduous broad-leaved tree reaching up to 20 meters in height. East Asian alder mainly inhabits fertile mountain wetlands, valleys, riverside floodplains, backswamps, and alluvial lowlands (Sakio & Yamamoto, 2002). East Asian alders have been planted around the entrance of royal tombs of Joseon and their adjacent wetlands. They tend to have a strong sprouting ability and prefer good moisture-retentive soils (Kim, 2015; Korean Institute of Traditional Landscape Architecture, 2016). However, most East Asian alder forest wetlands have a small population size and face a high risk of potential extinction due to desiccation and competition from adjacent plant communities. Thus, conservation plans need to be developed promptly (Cho et al., 2020).

East Asian alders form a well-conserved community in the forest wetland of the Heonilleung because its surrounding ground has a deep layer of soil and a high groundwater table which flows from the southern part of Mt. Dae-mo. In recognition of such ecological value, the forest was designated as an Ecological Landscape Conversation Area of Seoul on November 24, 2005. Furthermore, the forest belongs to the territory of Heonilleung, which is one of 40 royal tombs of the Joseon Dynasty. Heonilleung is made of two divisions. One of them is Heolleung, the tomb of King Taejong (the third monarch of the Joseon Dynasty) and his consort Queen Won-gyeong. The other is Illeung, the tomb of King Sunjo (the 14th monarch of the Joseon Dynasty) and his consort Queen Sunwon. All royal tombs of the Joseon Dynasty including Heonilleung were registered as UNESCO World Heritage sites on June 27th, 2009. They have an outstanding historic value. Therefore, maintaining their environmental condition is highly important.

Studies on East Asian alder forest and royal tombs of the Joseon Dynasty have been conducted in various regions. Studies on East Asian alder have been conducted in places including Mt. Daemo of Seoul (Yim & Han, 1989), Mujechi Wetlands of Ulsan (Kim & Kim, 2003; Kim et al., 2005), Mt. Geumjeong of Busan (Lee & Kim, 2005), Muui Island of Incheon (Paik, 2010), Civilian Control Zone and Demilitarized Zone (Kim et al., 2010), Amgok Wetland of Gyeongju (Kim et al., 2013), and Hwasan Wetland of Gunwi (Kim et al., 2017). Studies on royal tombs of the Joseon Dynasty have been conducted in Donggureong (Lee & Chin, 2002), Seooreung (Yee & Bae, 2006), Heonilleung (Kim et al., 2010), Sareung (Lee et al., 2011a), Jangreung (Lee et al., 2011b), Yunggeolleung (Lee et al., 2011c), Samreung (Kwak et al., 2012), Hongyureung (Lee et al., 2013), Taereung (Kim et al., 2015), and Gwangreung (Oh et al., 2019). These studies were mostly focused on vegetation, while studies on flora were only performed in a sporadic manner. Although studies on vegetation of the entire Heonilleung area have already been conducted, a detailed study on the flora of East Asian alder forest wetland of Heonilleung has not been reported yet.

Thus, the objective of the present paper was to investigate vascular plant flora of the East Asian alder forest wetland of Heonilleung. Results of this study could be used as fundamental data to demonstrate botanical diversity of the study area. The outcome of this study may help us plan future conservation strategies for the wetland.

Materials and Methods

Study area

Heonilleung East Asian alder Forest Wetland is located at San 13-1, Naegokdong, Seochogu, with GPS coordinates of 37° 46’ N and 127° 08’ E, covering an area of 30,592.2 m2. The wetland covers the majority of space of Heonilleung area. It is at the entrance of the royal tomb (Fig. 1). The wetland lies at a lowland with altitudes of 31-60 m. It has a mixture of flatland and gentle-slope land with a gradient less than 15°. The wetland is an alluvium region. Its soil comprises silty clay loam, sandy loam, and loam, rendering the area fertile and moist. The underground water level of the area is 65.2 75 cm in average with consistency ( Dongguk University Industry Academic Cooperation Foundation, 2017). Regarding the climatic condition of the wetland, it has an average annual temperature of 13.9°C, a mean maximum temperature of 19.0°C, a mean minimum temperature of 9.2°C, an average annual precipitation of 988.0 mm, and an average w ind velocity of 1.5 m/s.

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Fig. 1.
Study area boundary (red) shown around the range of East Asian alder forest wetland of Heonilleung.
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Study methods

A field study was performed three times (in spring, summer, and autumn) from May to September of 2020. Plants occurring inside the wetland and its edge were investigated. Most of these plants were identified during the investigation. However, some plants could not be determined. They were photographed and identified by referring to databases of Kim and Kim (2011), Cho et al . (2016), and Kim et al. (2018). Arranging the order of plants and recording their scientific names were performed according to the Korean Plant Names Index (Mueller Dombois & National Arboretum, 2017) and the Engler system (Melchior, 1964). Based on results of investigation, all occurring plant species were categorized according to Raunkiaer’s life form system (Mueller Dombois & Ellenberg, 1974). List of rare plants (Korea National Arboretum, 2008), invasive alien pl ants (Kim et al ., 2018), and floristic regional indicator plants (Korea National Arboretum, 2019) of the wetland were sorted out afterwards.

Results and Discussion

Vascular plant species compositions

A total of 166 vascular plant species were identified, including 159 species, three subspecies, three varieties, and one cultivar. They represented 132 genera and 59 families (Table 1, Supplementary Table 1 ), accounting for 8.3% of 1,996 vascular plant species inhabiting Seoul. Among them, five (3%) species, f ive genera, and four families represented pteridophytes. One (0.6%) species, one genus, and one family represented gymnosperms. One hundred and twenty two (73.5%) species, 98 genera, and 48 families represented dicotyledons. Thirty eight (22.9%) species, 28 genera, and six families represented monocotyledons. In terms of species diversity, Poaceae had the highest diversity with 20 (12%) species, followed by Asteraceae with 16 (9.6%) species, Rosaceae with nine (5.4%) species, Cyperaceae with eight (4.8%) species, and Fabaceae and Lamiaceae with seven species each. Plants such as Equisetum arvense, Persicaria thunbergii, Corydalis ternata, Oenanthe javanica, Mentha canadensis, Phryma leptostachya var. asiatica, Lobelia chinensis, Juncus effusus, Murdannia kei sak, Poaacroleuca, Leersia oryzoides, Pinellia ternata, Carex dispalata>, and Scirus juncoides that could tolerate moist to wet soil were major herbaceous species inhabiting the wetland. Canopy tree species such as Salix koreensis and Alnus japonica, under story tree species such as Quercus aliena, Prunus padus, Acer ginnala, Euonymus hamiltonianus, Styrax japonicus, and Fraxinus rhynchophylla, and shrub species such as Akebia quinata, Ampelopsis glandulosa var. heterophylla, Rosa multiflora, Zanthoxylum pip eritum, Ampelopsis brevipedunculata, Eleutherococcus senticosus, Clerodendrum trichotomum, and Viburnum erosum were major woody plant species in the wetland. In addition, saplings or shrubs of plant species including Ginkgo biloba, Zelkova serrata, Magnolia denudata, Cercis chinensis, Robinia pseudoacacia, Acer palmatum, Euonymus alatus, Cornus officinalis, Callicarpa dichotoma, Sambucus canadensis, Viburnum opulus were found. They were introduced from planted trees in the neighborhood of Heonilleung Royal Tomb.

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Table 1.
Categorization of plant species in Heonilleung Wetland by taxon
Taxon Family Genus Species Subspecies Variety Cultivar subtotal
Pteridophyta 4 5 5 - - - 5
Gymnospermae 1 1 1 - - - 1
Dicotyledonae 48 98 36 - 2 - 38
Monocotyledonae 6 28 36 - 2 - 38
Total 59 132 159 3 3 1 166
Life forms of Plants

All 166 plant species of Heonilleung Wetland according to Raunkiaer’s life form system were ranked in decreasing order of species richness as follows: Therophytes (Th ), 52 (31.3%) species; Hemicryptophytes (H), 24 (14.5%) species; Nanophanerophytes (N), 19 (11.4%) species; Hydrophytes (HH), 18 (10.8%) species; Geophytes (G), 17 (10.2%) species; Megaphanerophytes (MM), 16 (9.6%) species; Microphanerophytes (M), 14 ( 8.4%) species; and Chamaephytes (Ch), six (3.6%) species (Table 2).

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Table 2.
Categorization of plant species in Heonilleung Wetland by life form
Life-form* Th G H Ch N M MM HH
Number of Species (%) 52 (31.3) 17 (10.2) 24 (14.5) 6 (3.6) 19 (11.4) 14 (8.4) 16 (9.6) 18 (10.8)

* Life-form: Th (Therophytes), G (Geophyte), H (Hemicryptophytes), Ch (Chamaephytes), N (Nanophanerophytes), M (Microphanerophytes), MM (Megaphanerophytes), HH (Hydatophytes).

Rare Plants

There was one rare plant species found in the wetland. It was Melothria japonica with a Least Concern (LC) status (Table 3). A small number of Melothria japonica were found inside the wetland. Their natural habitats need protection as a small number of the m are occasionally seen growing near reservoirs and mountains in Korea (Lee et al .,2016).

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Table 3.
Categorization of rare plant species in Heonilleung Wetland
Scientific name Grade*
Melothria japonica (Thunb.) Maxim. ex Cogn. LC

*Grade: LC (Least Concerned).

Floristic regional indicator plants

There were a total of 15 floristic regional indicator plant species. One of them, Carex accrescens, belonged to floristic grade IV. Two of them, Acer palmatum and Callicarpa dichotoma>, belonged to grade III. Four of them, Alnus japonica, Spiraea salicifolia, Scutellaria dependens, and Glyceria leptolepis, belonged to grade IV. Eight of them, Onoclea interrupta, Pyrus calleryana, Impatiens noli-tangere, Melothria japonica, Eleutherococcus sessiliflorus, Viburnum opulus, Cirsium pendulum, and Carex dispalata, belonged to grade I. Three of them belonged to floristic grades III and IV. Thus, their habitats are discontinuous and isolated to some degree (Table 4). Carex accrescens, a species with a small range, was inhabiting the interior of the wetland in small numbers. On the other hand, the presence of Acer palmatum and Callicarpa dichotoma, both of which belonged to floristic grade III, showed no particular ecological significance as those individuals were introduced from the outside.

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Table 4.
Categorization of floristic regional indicator plant species in Heonilleung Wetland
Scientific name Grade
Carex accerescens Ohwi
Acer palmatum Thunb.
Callicarpa dichotoma (Lour.) Raeusch. ex K.Koch
Alnus japonica (Thunb.) Steud.
Spiraea salicifolia L.
Scutellaria dependens Maxim.
Glyceria leptolepis Ohwi
Onoclea interrupta (Maxim.) Ching & P.C.Chiu
Pyrus calleryana Decne. var. fauriei (C.K.Schneid.) Rehder
Impatiens noli-tangere L.
Melothria japonica (Thunb.) Maxim. ex Cogn.
Eleutherococcus sessiliflorus (Rupr. & Maxim.) S.Y.Hu
Viburnum opulus L. var. calvescens (Rehder) H.Hara
Cirsium pendulum Fisch. ex DC.
Carex dispalata Boott
Invasive alien plants

A total of 19 invasive alien plant species were identified, including Phytolacca americana, Chenopodium album, Robinia pseudoacacia, Trifolium repens, Ipomoea nil, Erigeron annuus, Taraxacum officinale, and Panicum dichotomiflorum . Twelve (63 .2%) of them were of North American origin and three (15.8%) of them were of Euro African origin. One (5.3%) species was of temperate European origin. One (5.3%) species was of temperate Eurasian origin. One (5.3%) species was of temperate American origin and one (5.3%) species was of European origin. Eleven (57.9%) species were of spread rate V (widespread, WS). Four (21.1%) were of spread rate I (potential spread, PS). Two (10.5%) were of spread rate IV (serious spread, SS). One (5.3%) was of spread rate II (minor spread, MS) and one (5.3%) was of spread rate III (concerned spread, CS) (Table 5). The species with spread rate V including Stellaria media, Trifolium repens, Erigeron annuus, Conyza canadensis, Taraxacum officinale, Galinsoga ciliata were evenly distributed in and around the wetland in numbers. As for non invasive alien species, there were a few individuals of Ginkgo biloba, Magnolia denudata, Cercis chinensis, Ailanthus altissima, Perilla frutescens, Solanum nigrum, and Sambucus canadensis inside the wetland.

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Table 5.
Categorization of invasive alien plant species in Heonilleung Wetland
Scientific Origin* Introduction time** Spread rate***
Phytolacca americana L. AM 3 5
Stellaria media (L.) Vill. TEM, EA, AM 1 5
Cerastium glomeratum Thuill. EU, AF 3 2
Chenopodium album L. TEM, EU 2 3
Robinia pseudoacacia L. AM 1 5
Trifolium repens L. EU, AF 1 5
Oxalis dillenii Jacq. AM 3 1
Veronica peregrina L. AM 1 1
Lindernia dubia (L.) Pennell AM 3 1
Veronica arvensis L. EU, AF 2 5
Erigeron annuus (L.) Pers. AM 1 5
Conyza canadensis (L.) Cronquist AM 1 5
Bidens frondosa L. AM 3 5
Erechtites hieraciifolius (L.) Raf. ex DC. AM 2 5
Ageratina altissima (L.) R.M.King & H.Rob. AM 3 1
Taraxacum officinale F.H.Wigg. EU 2 5
Galinsoga ciliata (Raf.) S.F.Blake AM 3 5
Panicum dichotomiflorum Michx. AM 3 4
Poa pratensis L. TEM 2 4

* Origin: AF (Africa), AM (America), EA (Eurasia), EU (Europe), TEM (Temperate).

** Introduced time: 1 (1500-1931), 2 (1932-1961), 3 (1962-present).

*** Spread rate: 1 (Potential Spread), 2 (Minor Spread), 3 (Concemed Spread), 4 (Serious Spread), 5 (Wide Spread).

Conclusion

This study obtained fundamental data about the biodiversity of vegetation in East Asian alder forest wetland of Heonilleung Royal Tombs. These data could be used to develop a future plan for the conservation of the wetland. Results of this study indicated that constant invasive plant species control and restoration of the water regime of the wetland are needed to conserve the wetland. Study results are summarized as follows:

1) A total of 166 vascular plant species were found, accounting for 8.3% of 1,996 vascular plant species inhabiting Seoul.

2) Therophyte was the most common plant life form in Heonilleung Wetland. Arrangement of life forms of plants in Heonilleung Wetland according to Raunkiaer’s life form system ranked in decreasing order of species r ichness is as follows: Hemicryptophytes > Nanophanerophytes > Hydrophytes > Geophytes > Megaphanerophytes > Microphanerophytes > Chamaephytes.

3) Only one rare plant species was found in the wetland. However, 15 floristic regional indicator plant species were found in the wetland, including one belonging to floristic grade IV, two belonging to grade III, four belonging to grade IV, eight belonging to grade I, and three belonging to floristic grades III and IV, indicating that their habitats were isolated to some degree.

4) There were 19 invasive alien plant species found in the wetland. Most of them were introduced from North America after the year 1964 with a spread rate of V. As for non invasive alien species, Ginkgo biloba, Magnolia denudata, Cercis chi nensis, Ailanthus altissima, Perilla frutescens, Solanum nigrum, Sambucus canadensis were identified which were introduced from the outside.

5) The surrounding ground of Heonilleung East Asian alder forest wetland has a deep layer of soil and a stable groundwater table, which provides habitats for a number of plants tolerant of moist soil, all of which are rarely seen in Seoul. However, most of them were found to grow in small quantity. Their populations are expected to either rapidly diminish or get wiped out from the wetland if their habitat becomes desiccated or if ruderal species, invasive alien species, and cultivated plant species are kept being introduced from other areas. Therefore, detailed monitoring accompanying time series analysis and ecological management on ruderal species, alien species (including invasive alien species), and cultivated plant species should be conducted.

Conflict of Interest

The authors declare that they have no competing interests.

Acknowledgments

This study was financially supported by Seocho-gu Office of Seoul Metropolitan City for the purpose of monitoring the ecological landscape conservation area.

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