Integrating continental mainland and islands in temperate East Asia: liverworts and hornworts of the Korean Peninsula

Abstract The liverwort and hornwort flora of the Korean Peninsula possesses some unique traits arising from the geographic position of the Peninsula, where the mainland flora meets insular flora. This flora is still not exhaustively studied, due not only to political reasons, but also because much less attention has been paid than to adjacent lands by hepaticologists. A checklist presented is based on a study of ca. 15,500 specimens collected by the authors and a review of relevant literature. This study provides the checklist of liverworts and hornworts known from Korea and the geographical distribution of each species within the peninsula. The liverworts and hornworts in Korean flora include 346 taxa (326 species, 16 subspecies and four varieties) in 112 genera and 50 families. Since 2007, 75 taxa of liverworts and four taxa of hornworts are reported as new to the Korean Peninsula, with a number of the new records arising following application of new taxonomic concepts that have become apparent over the last few decades. While compiling the checklist, 42 species, previously reported to Korea, are excluded from the Korean liverwort flora.


Introduction
The Korean Peninsula is situated on the easternmost temperate edge of the Pacific Asia mainland. It belongs to the East Asiatic floristic region and it has close floristic relationships with Manchuria (in the broad sense of this term) and Japan (Takhtajan 1986). Korea shows a remarkable variation in climatic conditions regarding temperature and precipitation. In addition, the complex mountain system that covers nearly 70% of the total area and ca. 3,400 islands along the west and south coast create a great diversity of habitats throughout the area. The flora, therefore, shows high diversity, caused by the range of communities from warm temperate, merging subtropical in the southern part to cold temperate and alpine types in the northern and high mountain regions.
The first reports of liverworts for the Korean Peninsula were those by Stephani (1909) -an incidental result obtained in the course of study of Japanese flora by U. Faurie (Bakalin and Katagiri 2014). Since then, Japanese botanists, starting with Nakai (1918), have studied liverworts and hornworts in Korea. Hong (1960a) and Choe (1975) were the first Koreans who revised liverworts and hornworts in Korea (see Taxonomic History below). Since the 1990s, studies on liverworts and hornworts in Korea were generally accomplished by reviews of literature data Yamada and Choe 1997;Park and Choi 2007). In some cases, as authors simply provided the lists of taxa without any references even to published papers, the origin of some reports could not be determined. Therefore, despite the existence of many publications dealing with Korean liverworts, the distribution of taxa within the Peninsula and even the certain presence of some species remain questionable. This is in stark contrast to the obvious progress in knowledge of vascular plants over the last several decades as exemplified by several monographic treatments and even some illustrated guidebooks (Lee 1980;Lee 1996;Lee 2006;Park 2007). Previously, the illustrated Flora and Fauna of Korea 24 and Korean Spore Plant 8  attempted to fill this gap, but actually they provided only poor data, based on limited amount of collected material and could hardly be regarded as sufficient and satisfactory in the current time. Hence, we attempt a full revision of all available collections, including those newly collected within the past 12 years and literature sources. We provide original information on the distribution of taxa within the Peninsula and arrange them in accordance with the currently accepted taxonomy, supported by recent advances in molecular-genetic research. We stress that the liverwort and hornwort flora, due to unique geological, environmental, and geographical factors, is far from a simple 'incomplete copy' of Japanese or North-East China floras (Choi et al. 2010(Choi et al. , 2012a(Choi et al. , b, c, 2020aBakalin et al. 2020a). Moreover, Korean flora possesses many unique geological, environmental, and geographical factors caused by the Peninsula being situated between continental mainland and islands on the migration route of inter-exchanges within various regions in East Asia and even within East and Northeast Asia in the broader context.

Historical background
The history of knowledge about liverworts and hornworts in Korea can be divided into four stages, based on botanists involved at the different time periods (Table 1). The first stage  is the starting stage, the second stage  includes studies conducted mainly by Japanese botanists, the third stage  includes studies by the first Korean professional bryologists Drs. W.H. Hong, D.-M. Choe and Y.H Kim and the last stage (2008-present) includes studies by various botanists in both North and South Korea.
Third stage  The first Korean botanist who studied and published on liverworts and hornworts was Won Shic Hong (1919Hong ( -20141960a, b, c, 1962a, b, c, d, 1966. He reported 149 taxa in 53 genera and 24 families, based on a study of ca. 5,000 herbarium specimens . Additionally,  markedly expanded his list that counts 259 taxa belonging to 76 genera in 37 families on the basis of personal collections and literature records, including those for North Korea (Gao and Cao 1983;Gao and Chang 1983a, b;Koponen et al. 1983;Huneck et al. 1987). Hong also provided identification keys to 263 known or expected taxa in the Korean Peninsula .  was the first who compiled the manual for the Korean liverworts, published in English. Hong's follower, Du Moon Choe (1925-2014, conducted bryofloristic research studies in South Korea. He published a manual of Korean bryophytes in the Korean language, which includes 201 liverwort taxa in 66 genera . Later, in collaboration with the Japanese hepaticologist Kohsaku Yamada, 236 taxa of Hepaticae were assembled in a special checklist providing information on distributions of species within administrative provinces of both countries on the Korean Peninsula (Choe and Yamada 1979, 1998, 2000Yamada and Choe 1997). In North Korea, Gao and Cao (1983) compiled the list of bryophytes of Mt. Baekdu, including 85 liverworts.  provided description and identification keys to 207 known taxa on the Korean Peninsula. Yamada (2006, 2009a, b) examined the hepatic flora of Jeju Island, Mt. Jiri and Mt. Gaya. Kwang Woo Park and Kyeong Choi (2007) published a list of bryophytes for the Korean Peninsula, based on literature data. The list includes 281 taxa belonging in 81 genera.

Fourth stage (2008-present)
Our own studies on Korean liverworts and hornworts started in 2008 and revealed many new species, including those new to science. As was found previously, the Korean liverwort flora was still poorly understood and peculiar traits of flora of this Peninsula were simply overlooked. Bakalin et al. (2009Bakalin et al. ( , 2020a described Tritomaria koreana and Solenostoma jirisanense from Mt. Jiri as new to science. Choi et al. (2010Choi et al. ( , 2011Choi et al. ( , 2012aChoi et al. ( , b, c, 2020a continuously reported unrecorded species from the Korean hepatic flora. Concurrently with our research, Lee et al. (2011) published the National List of Species of Korea, including 277 liverworts and eight hornworts, based on literature sources. After , the number of genera and species of liverworts and hornworts in Korea, based on literature, has been listed in Table 2.
Taking into account that checklists commonly become outdated every 10 years and many new additions have been obtained within the last stage of Korean bryophyte flora recognition, the present checklist marks the new 'frontier' in the knowledge of Korean bryophytes that, at the same time, is the starting point for new achievements in this field.

Materials and methods
Materials for this study, which include approximately 15,500 specimens, were collected mostly by Choi, with a short participation in the field research by Bakalin between October 2007 and May 2020 at various sites in Korea (Table 3, Figure 1). All the specimens are kept in Jeonbuk National University Herbarium (JNU) and Herbarium of the Botanical Garden-Institute (VBGI). The unsurveyed areas in the present study were investigated by a review of relevant reliable literature Yamada and Choe 1997) and herbarium specimens (G, HIRO, NICH, PE, VLA, VBGI). The analysis of the distribution pattern was based on floristic elements (latitudinal type) and area type (longitudinal types) identified for each occurring species in Bakalin (2010). Nomenclature mostly follows Söderström et al. (2016) with some updates from recent literature (Solenostomataceae , Apopellia (Schütz et al. 2016) etc.). The Pseudolophozia concept was followed after Konstantinova and Vilnet (2009) Park and Choi (2007) on an unclear basis (no references to literature were provided at all). Since we were not able to find the location of vouchers and the original sources for these reports, we exclude them from the flora. Lopholejeunea subfusca (Nees) Schiffn. was reported by  from Mt. Jiri. The distribution of L. subfusca covers tropical and subtropical areas, so its occurrence in Mt. Jirisan is doubtful. The plants most probably belong to Acanthocoleus yoshinaganus (S.Hatt.) Mizut., which is relatively common on Mt. Jiri, but it was not recorded by . Porella pinnata L., Lejeunea cavifolia Steph. and Riccardia incurvata Lindb. were reported by  from the northern part of Korea. However, the distribution of these three species is European-North American and hardly occurred in East Asia. The first one probably belongs to Porella grandiloba, whereas the second may belong to Lejeunea japonica and the last may belong to any Riccardia species (most probably R. multifida). See excluded and doubtful records below for the rest of the details.

Cephalozia hamatiloba
Steph. -This species was recorded for Korea , however, we were not able to find the references to literature and the location of vouchers; we exclude this species from the checklist. Also, this species is a southerly distributed taxon stretching to Indochina.
Cololejeunea latilobula (Herzog) Tixier. -This species was recorded for Korea ], however, we were not able to find the references to literature and the location of vouchers; we exclude this species from the checklist.

Delavayella serrata
Steph. -This species was recorded for Korea , however, we were not able to find the references to literature and the location of vouchers; we exclude this species from the checklist.
Lepidozia filamentosa (Lehm. et Lindenb.) Lehm. et Lindenb. -This species was recorded for GW ], however, if the narrow species treatment would be adopted in the group, this name should be referred to L. subtransversa in East Asia, whereas 'true' L. filamentosa occurs in western North America Lopholejeunea subfusca (Nees) Schiffn. -This species was recorded for JN ], Korea , however, the distribution of L. subfusca covers tropical and subtropical areas, so its occurrence in Mt. Jiri of Jeollanam-do province is doubtful. The plants most probably belong to Acanthocoleus yoshinagana (S. Hatt.) Mizut., which is relatively common on Mt. Jiri, but it was not recorded by .

Marchantia pinnata
Steph. -This species was recorded for Korea , however, we were not able to find the references to literature and the location of vouchers; we exclude this species from the checklist.
Marsupella emarginata (Ehrh.) Dumort. -This species was recorded for PB , HN , HB , however, the records from Korea are erroneous and probably belong to Marsupella tubulosa Steph.
Metalejeunea cucullata (Reinw., Blume et Nees) Grolle -This species was recorded for Korea , however, we were not able to find the references to literature and the location of vouchers; we exclude this species from the checklist.

Odontoschisma grosseverrucosum
Steph. -This species was recorded for GW , however, the record from Korea is erroneous and probably belongs to Odontoschisma pseudogrosseverrucosum Gradst., Aranda et Vanderp.

Plaiochila delavayi
Steph. -This species was recorded for Korea [Reimers 1931, Park and, however, the records from Korea and Japan are doubtful and probably belong to Plagiochila ovalifolia Mitt. (Hattori 1949;So 2001).
Porella pinnata L. -This species was recorded for GW , JG , HN , however, the distribution of this species is European and hardly occurred in East Asia.

Radula chinensis
Steph. -This species was recorded for Korea , however, we were not able to find the references to literature and the location of vouchers; we exclude this species from the checklist.

Riccardia incurvata
Lindb. -This species was recorded for HWN , HB , however the distribution of these three species is European-North American and hardly occurred in East Asia.

Riccia frostii
Austin -This species was recorded for Korea [Amnokgang River: Park and Choi 2007], however, we were not able to find the references to literature and the location of vouchers; we exclude this species from the checklist.
Riccia nipponica S.Hatt. -This species was recorded for Korea , however, we were not able to find the references to literature and the location of vouchers; we exclude this species from the checklist.
Sandeothallus japonicus (Inoue) Crand.-Stotl. et Stotler -This species was recorded for Korea  as Moerckia japonica Inoue], however, we were not able to find the references to literature and the location of vouchers; we exclude this species from the checklist.

Discussion
The infra-regional differences inside Korea are quite significant, the richest liverwort flora being found in Jeju-do Province that houses 223 taxa. Although other provinces are less rich taxonomically, they commonly house some unique species not occurring in other administrative subunits in Korea. This is strongly evident in Gangwon Province which houses several calciphilous taxa not found in other Provinces, including Mannia androgyna, M. fragrans, Mesoptychia ussuriensis, Lejeunea neelgherriana, Porella stephaniana etc. Some observations could be made in the course of comparison of Korean flora with the flora of adjacent lands, including Japan, the Russian Far East and China. The differences are most significant with the Russian Far East flora and reflect the far more northern position of the Russian Far East in comparison with the Korean Peninsula. The differences with other adjacent countries are smaller. The defined series of taxa of temperate and subtropical distribution known in Korea are absent in the Russian Far East: Acrobolbus ciliatus, Acrolejeunea pusilla, Anastrepta orcadensis etc. Some taxa, present in Korean peninsula, but absent in the Russian Far East, belong to the broadly Sino-Himalayan element, including Gymnomitrion revolutum (although the occurrence of this species in Korea is uncertain). Certain taxa, like Mannia gracilis and Bazzania manczurica, are known in all compared flora, with the exception of China. However, such taxa should likely be found in China in further studies. The differences with Japanese flora are minor and include some northern elements present in Korea, but absent in Japan, like Biantheridion undulifolium and Cephalozia ambigua (this report may be doubted), recorded in Chanbai Mt. in the northernmost North Korea or even southwards, like Cephaloziella hampeana, C. varians, Isopaches bicrenatus and Scapania sphaerifera (the latter three taxa are also not known in China). Cephalozia lacinulata -a rare boreal species is also known in the China mainland and Korea, but not known in Japan. Porella chinensis is another 'continental' species not known in Japan, although present in other adjacent flora. The temperate Pacific Cavicularia densa is not known, either in China and the Russian Far East, but is present in Korea and Japan. Radula brunnea, Japanese-Korean-Kuril Island-British Columbia taxon is not known in China. Syzygiella nipponica, a mainly Japanese species, is not known in China, although present in the Russian Far East and Korea.
Therefore, Korean hepatic flora includes several species present westwards and, for those, the Korean Peninsula is the most eastern outpost. The opposite situation occurs with some 'Japanese' taxa and for those, Korea is the western most outpost. Besides, some taxa, occurring northwards in the Russian Far East, penetrate the Korean Peninsula, but were not present (at least were never recorded) in Japan and China. Despite the relatively small size of the Peninsula, it houses two narrow endemic taxa of liverworts hitherto not known outside Korea. These facts show the great value of the Korean Peninsula for the conservation of natural resources and genetic potential of East Asian biota.