Current status of invasive alien plants in Ramsar wetlands on Jeju Island, Republic of Korea

Ramsar wetlands are known for their high ecological and economic value; however, in some cases, the indigenous species community is rapidly changing owing to the presence of invasive alien plants (IAPs). To address this issue, we conducted a plant survey of five Ramsar wetland sites on Jeju Island from August 2021 to August 2022 and constructed a list of IAP species. A total of 24 IAP plant species belonging to 13 families were identified. Species of the Asteraceae and Poaceae families, which have high seed production, high adaptability to damaged ecosystems, and a wide range of organisms, from annuals to perennials, were found to be abundant. The distribution of IAP species was consistent with the pattern expected during the early stages of IAP invasion in Korea. Additionally, a positive correlation was observed between the distance from residential areas and the number of IAP species. Wetlands not visited by people were found to be relatively intact, while those frequented by tourists and visitors were susceptible to IAPs. These results suggest that the introduction of IAP species into the Jeju Ramsar wetlands may have been the result of anthropogenic activities, such as tourism. Our study demonstrated that the introduction of IAPs into the Jeju Ramsar wetlands is in its early stages and is mainly attributable to human activity. Therefore, it is necessary to identify the invasion pathways, develop strategies to control or reduce invasion, and control the geographic expansion of these species. Our study highlights the threat of alien species to Jeju Ramsar wetlands, providing the basis for a strategy to protect these wetlands from the threat of invasive species.


Introduction
Wetlands are habitats for a diverse range of organisms, including animals, plants, and microorganisms.They play significant environmental, social, cultural, and economic roles, such as the removal of pollutants, flood control, climate regulation, recreation, and aesthetic functions (Gibbs 2000;Ko et al. 2014;Janse et al. 2019;Adeeyo et al. 2022).The designation of wetlands as Ramsar wetlands under the Ramsar Convention promotes the wise use of wetlands with high ecological and economic value and provides international protection for wetlands (Geijzendorffer et al. 2019;Farrier and Tucker 2000).In particular, wetlands can provide important conservation benefits and serve as the foundation of the global protected area network (Le Saout et al. 2013;Bomanowska et al. 2019).However, Ramsar wetlands face various pressures, including water abstraction, changes in the natural flood regime, land reclamation, pollution, overutilization of natural resources, and poaching (Junk et al. 2006).The most serious issue associated with anthropological activities is the spread of invasive alien plants (IAPs) (Saura-Mas and Lloret 2005; Shrestha 2016; Chu et al. 2020).
Invasive alien plants, which are not native to Korea and have been introduced into the country through various routes and pathways, pose a threat to the biodiversity, ecosystems, habitats, and human welfare of the habitats they invade (Richardson et al. 2000;Shiferaw et al. 2018).Invasive alien plants are mainly introduced into Korea unintentionally through edible or fodder grain imports (Oh et al. 2003;Cha et al. 2019).However, intentional introduction for economic purposes has also been observed, with many species establishing themselves in the local ecosystems (Kil and Kim 2014).In particular, the importation of various plant species from other countries for ornamental purposes in gardens, parks, highways, and roadside areas, including botanical gardens, is a major pathway for the spread of IAPs (Dehnen-Schmutz 2011).As of 2021, IAP species in Korea have been classified into 41 families, 203 genera, and 392 taxa (Korea National Arboretum 2021).Among these, 186 taxa of IAPs have been identified in the Jeju region (Jung 2014).Invasive alien plants can adapt to their new environments owing to their broad ecological preferences/tolerance, high competitive abilities, and adaptability to new habitats (Müller-Schärer et al. 2004;Schlaepfer et al. 2009;Gioria and Osborne 2014;Iacarella et al. 2015).Therefore, IAPs may easily adapt to climate change and spread rapidly (Huang et al. 2011).Although they generally appear in human-impacted areas, such as settlements, roads, construction sites, and landfills (Szumańska et al. 2021), their distribution has recently expanded to natural ecosystems such as forests (Jiang et al. 2011).
Invasive alien plants contribute significantly to the numerous threats affecting Ramsar wetlands (Pandey et al. 2020).To develop management strategies and long-term plans for IAPs, it is essential to understand their status, introduction pathways, and specific impacts on ecosystems (Kang et al. 2020).Updating the list of IAPs that enter wetlands is a fundamental step in this process and should be prioritized in IAP monitoring (Henderson and Wilson 2017).
This study focuses specifically on investigating IAPs in Ramsar wetlands on Jeju Island, Republic of Korea.We emphasize the novelty and authenticity of our investigation, and offer fresh insights without duplicating already existing information.By monitoring the status of IAP introduction and constructing a comprehensive list of IAP species, we aim to provide essential information for the effective management of Ramsar wetlands.
The main economic activities on Jeju Island are tourism, agriculture, and fishing (Kim 2004).The Mulyeongarioreum, Dongbaekdongsan, and 1100 Highland wetlands selected as the study areas are highly valued tourist attractions visited by approximately 200,000 people per year (https://know.tour.go.kr/stat/visitStatDis/area.do).However, owing to the entry of outsiders, they are also considered susceptible to the introduction of invasive species (Cameron et al. 2015).

Data collection
Plant surveys were conducted throughout the Ramsar wetlands, and all species found during the survey were recorded.Plants that were difficult to identify in the field were collected, taken to the laboratory, classified, and prepared as specimens.Invasive alien plants were classified based on Kang et al. (2020).Species and author names were allotted in accordance with the International Plant Names Index (IPNI) and Integrated Taxonomic Information System (ITIS).The list of Korean IAPs was compiled according to the Korean National Arboretum (2021).
The distance from each Ramsar wetland site to the nearest residential area was measured using a handheld GPS device (Garmin GPSMAP 64s; Garmin, Olathe, KS, USA) and recorded as the shortest distance between the wetland and a village-level residential area.

Data analysis
Linear regression analysis was performed to examine the correlation between the number of IAP species, altitude, and distance from residential areas across the wetlands.In addition, a one-way analysis of variance was conducted to examine the correlation between the number of IAP species and wetland type.Data were analyzed using IBM SPSS Statistics version 20.0 (IBM Corp., Armonk, NY, USA), and statistical significance was set at p < 0.05.

Results and discussion
In the Jeju Ramsar wetlands, we identified 24 taxa belonging to 13 families (22 genera) (Supplementary material Table S1).The Asteraceae was the largest family with six species, followed by Poaceae with four species.These families together comprised 41.7% of all species.The seeds of plants in the Asteraceae and Poaceae families are achenes and caryopses, respectively, which can disperse widely and rapidly, mainly via wind, rivers, animals, and other agents (Kim et al. 2010;Kim and Lee 2019;Qi et al. 2022).The frequent occurrence of these families is attributed to their characteristics, such as high seed production, high adaptability to disturbed ecosystems, various life forms from annual to perennial plants, and high seed germination rates (Kim et al. 2000).
The most frequently occurring IAPs were Hypochaeris radicata (Thunb.)Franch.& Sav. and Trifolium repens L., which appeared in three locations, followed by Sisyrinchium angustifolium Mill., Conyza canadensis (L.) Cronquist, Crassocephalum crepidioides (Benth.)S. Moore, Erigeron annuus (L.) Pers., Phytolacca americana L., Rumex acetosella L., Veronica arvensis L., and Veronica persica Poir.Among them, H. radicata and R. acetosella are classified as wild plants typical of disturbed ecosystems by the Ministry of Environment; their cultivation, importation, exportation, transplantation, storage, transportation, and distribution are prohibited (Kim et al. 2017).Furthermore, four species, namely, C. canadensis, E. annuus, H. radicata, and T. repens, are wild plants known to cause ecosystem disturbances and are classified as harmful weeds by the Animal and Plant Quarantine Agency (https://www.qia.go.kr/viewwebQiaCom.do?id=45413&type=3_14jyzk).Invasion by these alien species is typical of the early stages of IAP introduction in Korea, indicating the vulnerability of the Jeju Ramsar wetlands to invasion (Lee et al. 2011).Therefore, legal regulations and management measures to control the IAP trade should be established to prevent its introduction and spread (Kil and Kim 2014).
The highest number of species ( 22) was observed in the Dongbaekdongsan wetland, followed by the Mulyeongarioreum and 1100 Highland wetlands (five species), Muljangorioreum wetland (three species), and Sumeunmulbaengdui wetland (no IAP species present) (Figure 3).Differences in the number of species observed in each wetland may be attributed to factors such as village accessibility, human activity, and wetland type (Belcher et al. 2004;Pyšek and Richardson 2006;Chu et al. 2020).
Residential areas have the highest human activity and can be regarded as typical disturbed areas (Park et al. 2021).According to the linear regression analysis of the correlation between the number of IAP species and the distance from residential areas to wetlands, the number of invasive species increased as the distance decreased (p < 0.05) (Figure 4).These results may be attributed to human activities, such as increased pressure from tourist activities, development, and reforestation (Lee and Lee 2006).Restricted access to the Muljangorioreum and Sumeunmulbaengdui wetlands due to their protected status resulted in very few or no invasive species being observed.
According to the one-way ANOVA used to determine the difference in the number of IAP species by wetland type, there was no significant difference between freshwater reservoirs and highland wetlands; however, the lowland wetland (the Dongbaekdongsan wetland) was significantly different (p < 0.05).Lowland wetlands are closely associated with roads, which facilitate the spread of IAP species (Levine 2003).In addition, the characteristics of IAPs, where the chance of germination is increased by the removal of competing species caused by disturbance, are relatively less reflected in mountainous wetlands with natural obstacles, such as altitude and location (DeFerari and Naiman 1994).The Mulyeongarioreum and Muljangorioreum wetlands are lake-type wetlands located within the Jeju Island summit crater, whereas the Sumeunmulbaengdui and 1100 Highland wetlands are located in highaltitude mountainous areas.The Dongbaekdongsan wetland, a lowland wetland, is relatively more susceptible to the introduction and threat of invasive species than other wetlands because it allows for a high influx of such species, and the success rate of IAP adaptation is high.
Currently, the IAP invasion in the Jeju Ramsar wetlands could be considered as in early stages; therefore, there is a need to quickly identify the introduction pathways, eradicate the established species and control introductions, with the ultimate aim to develop strategies to control the geographic expansion of such alien species (Moshovane et al. 2022).
Comprehensive management measures such as continuous monitoring, establishing management systems, planting substitute plants, and promoting ecotourism should be introduced (Auld and Johnson 2014;Park and Lee 2018).
The Jeju Ramsar wetlands are high-biodiversity wetlands with excellent ecological quality, and have been designated as protected areas (Seo et al. 2015).However, this study confirmed that invasion by alien species due to various disturbances is in its early stages, and wetlands that are closer to residential areas and more frequently affected by human interference are more vulnerable to invasion by alien species (van Kleunen et al. 2018;Lim et al. 2020).Human activities and the richness of invasive species are positively correlated (van Wilgen et al. 2001;Auffret and Cousins 2013;Cameron et al. 2015;Shrestha 2016).The influx of invasive species into the Jeju Ramsar wetlands may be due to human activities such as tourism.Tourism often promotes biological invasion, contributing to the introduction and spread of alien species (Hall et al. 2011;Anderson et al. 2015).To prevent the introduction of alien species, continuous monitoring and establishment of a species list are necessary, and measures to control IAPs are required.Visitors management, quick identification of the pathways of alien species, and control of their invasion and expansion are practical approaches to resolving the problem (Nikodinoska et al. 2014;Moshovane et al. 2022).
Our study demonstrates that Jeju Ramsar wetlands are threatened by IAPs.In this study, we monitored and established a species list for IAPs in Jeju Ramsar wetlands, which can serve as baseline information for a strategy to protect the wetlands from invasive species.Proactive management of invasive species is therefore necessary for the protection of Jeju Ramsar wetlands.

Figure 2 .
Figure 2. Protected areas in Ramsar wetlands, location of invasive species (upper case letter) and landscape view of study sites (lower case letter) (A, a = Mulyeongarioreum wetland; B, b = Muljangorioreum wetland; C, c = 1100 Highland wetland; D, d = Dongbaekdongsan wetland; and E, e = Sumeunmulbaengdui wetland; red line = protected areas).The boundaries of the protected areas were referred to Conservation plan for Jeju Wetland Protected Area.

Figure 4 .
Figure 4. Relationship between distance from residential areas and the number of species.

Table 1 .
Type, restrictions on access, and distance from residential areas for each Ramsar Wetland on Jeju Island