Journal of Asia-Pacific Biodiversity 9 (2016) 198e204
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Journal of Asia-Pacific Biodiversity
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Original article Butterfly fauna in Mount Gariwang-san, Korea
Cheol Min Lee a,*, Sung-Soo Kim b, Tae-Sung Kwon c a Forest and Climate Change Adaptation Laboratory, Center for Forest and Climate Change, National Institute of Forest Science, Seoul, Republic of Korea b Research Institute for East Asian Environment and Biology, Seoul, Republic of Korea c Division of Forest Insect Pests and Diseases, National Institute of Forest Science, Seoul, Republic of Korea article info abstract
Article history: The aim of this study is to elucidate butterfly fauna in Mt. Gariwang-san, Korea. A field survey was Received 31 December 2015 conducted from 2010 to 2015 using the line transect method. A literature survey was also conducted. A Received in revised form total of 2,037 butterflies belonging to 105 species were recorded. In the estimation of species richness of 25 February 2016 butterfly, 116 species were estimated to live in Mt. Gariwang-san. In butterfly fauna in Mt. Gariwang-san, Accepted 26 February 2016 the percentage of northern species was very high and the percentage of grassland species was relatively Available online 3 March 2016 higher than that of forest edge species and forest interior species. Sixteen red list species were found. In particular, Mimathyma nycteis was only recorded in Mt. Gariwang-san. When comparing the percentage Keywords: butterfly of northern species and southern species including those recorded in previous studies, the percentage of fi distribution pattern northern species was found to have decreased signi cantly whereas that of southern species increased. habitat type We suggest that the butterfly community, which is distributed at relatively high altitudes on Mt. red list species Gariwang-san, will gradually change in response to climate change. Mt. Gariwang-san Copyright Ó 2016, National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA). Production and hosting by Elsevier. This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/).
Introduction the function and structure of forest ecosystems (Pearce and Venier 2006; Maleque et al 2009). In particular, insects are often used to Mt. Gariwang-san is an alpine region located inland of assess the biodiversity in forest ecosystems (Kwon et al 2013; Lee Gangwon-do where natural broad-leaved forests are relatively and Kwon 2014; Lee et al 2014). Among insects, butterflies are widely developed, and the flora is diverse as soil conditions are considered a good indicator because of their high diversity, short favorable (Kim and Um 1997). In flora in Mt. Gariwang-san, Quercus generation, good movement, host preference, and sensitivity to mongolica is dominant, and coniferous forests including Pinus environment changes (Lee and Kwon 2012, 2014; Kwon et al 2014; densiflora, Abies nephrolepis, Abies holophylla, and Taxus cuspidata Lee et al 2015). Moreover, butterflies can be reliably identified using are partially dominant (Paik et al 1998). In 2006 and 2008, some the line transect method in the field (Pollard and Yates 1993). areas of Mt. Gariwang-san, covering a total of 2,462 ha, were In this study, literature (Kim 1988) and field (2010e2015) sur- designated as forest genetic resource reserves and are protected by veys were conducted to elucidate butterfly fauna in Mt. Gariwang- the Korea Forest Service (Daejeon, Korea). The National Institute of san. Species richness was evaluated, and distribution pattern, Forest Science (NIFoS; Seoul, Korea) has been conducting various habitat type, and red list species were analyzed. In addition, the forest management practices such as reforestation, forest road relationship between latitude and percentage of northern and development, thinning, and shelterwood forest (Lee et al 2014). A southern species was analyzed including those reported in previ- comprehensive study to evaluate the response of the forest ous studies. ecosystem to the effect of these forest management practices is being carried out in Mt. Gariwang-san (NiFoS Project). Materials and methods Biological indicators are widely used to assess biodiversity. These indicators can illustrate the effect of forest management on Study site
The study was carried out in Mt. Gariwang-san (1,561 m, 37 270 * Corresponding author. 0 0 0 E-mail address: [email protected] (C.M. Lee). N, 128 33 E) and Mt. Jungwang-san (1,371 m, 37 46 N, 128 56 E), Peer review under responsibility of National Science Museum of Korea (NSMK) and which are located in Gangwon-do, Korea (Figure 1). Mt. Gariwang- Korea National Arboretum (KNA). san is located on the boundary of Jeongseon-eup in Jeongseon-gun http://dx.doi.org/10.1016/j.japb.2016.02.005 pISSN2287-884X eISSN2287-9544/Copyright Ó 2016, National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA). Production and hosting by Elsevier. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). CM Lee et al. / Journal of Asia-Pacific Biodiversity 9 (2016) 198e204 199
Figure 1. Map showing the location of the site. Black and dotted lines indicate forest road and line transect route, respectively.
and Jinbu-myeon in Pyeongchang-gun. Mt. Jungwang-san is in the Distribution pattern, habitat type, and red list species west of Mt. Gariwang-san. In terms of vegetation, Q. mongolica is dominant and Betula costata, Acer mono, and Ulmus laciniata are The butterfly species were classified with their distribution partially dominant (Lee et al 2009). The average annual tempera- pattern, habitat type, and red list species. The distribution pattern ture and rainfall in Mt. Gariwang-san are 9.7 and 1,761.4 mm, was determined based on the local distributions in Korea, Japan, respectively (Byeon et al 2012). and East Asia. Distribution pattern was classified into three types: northern species (hereafter N species), southern species (S species), and miscellaneous species (M species). Habitat type was classified Survey method based on the habitat of butterfly larva. The butterfly species were classified into three types: grassland (GL), forest edge (FE), and In terms of survey methods, a literature survey (Kim 1988) and forest interior (FI) species. If a species occupied more than one CM Lee’s2012e2013 field data and SS Kim’s2010e2015 field data habitat, the habitat recorded for it was the more frequently used were used. Kim (1988) collected butterflies, and Lee and Kim used habitat. Distribution pattern and habitat type based on all butterfly the line transect method (Pollard and Yates 1993). The line transect species in South Korea were reported by Kim et al (2012). The method was carried out by steadily walking along the survey routes classification of red list species was based on the red data book of and recording the butterflies observed within a 10 m width along endangered insects in Korea I (National Institute of Biological the routes. The butterflies that we could not identify by sight were Resources 2012). Red list species were classified as critically en- caught using sweep nets and then released after identification. dangered (CR), endangered (EN), vulnerable (VU), or near- Kim’s (1988) survey was conducted on July 24e26, 1987, whereas threatened species (NT). CM Lee’s survey was conducted on June 4e6, 2012 (Haanmi-rielog cabin on the ridgeeJangjeon Valley) and July 30eAugust 1, 2013 (Makdong Valleyelog cabin on the ridgeeSukam-ri). SS Kim con- Data analysis ducted a series of surveys at forest roads from May to August in 2010 and 2011 (once a month), and at forest roads and mountain The species richness of butterflies was estimated using Estimate roads from May to October in 2012e2015 (once a month). These S(Colwell 2005) based on four algorithms of ACE (Chao et al 1993; surveys were conducted a total of 55 times. Chazdon et al 1998), Chao 1 (Chao 1984), Jack 1 (Burnham and 200 CM Lee et al. / Journal of Asia-Pacific Biodiversity 9 (2016) 198e204
Table 1. Butterflies recorded in Mt. Gariwang-san.
y z Species Korean name 1987 2010 2011 2012 2013 2014 2015 Total Distribution pattern* Habitat type Red list species
Papilionidae 호랑나비과 Parnassius stubbendorfii 모시나비 31217151 48 N GL Luehdorfia puziloi 애호랑나비 1315N FI Byasa alcinous 사향제비나비 112MFE Papilio xuthus 호랑나비 21317MGL Papilio machaon 산호랑나비 51 6 M GL Papilio macilentus 긴꼬리제비나비 111 2 5 S FE Papilio bianor 제비나비 711391123 M FI Papilio maackii 산제비나비 14 11 23 10 45 1 1 105 M FI Pieridae 흰나비과 Leptidea morsei 북방기생나비 22NGL Pieris napi 줄흰나비 6 38 14 54 5 117 N FE Pieris melete 큰줄흰나비 3473825M FE Pieris canidia 대만흰나비 2133 211 M FE Pieris rapae 배추흰나비 1 1 10 12 M GL Anthocharis scolymus 갈구리나비 3312 9 M FE Gonepteryx maxima 멧노랑나비 1 2 3 N FE VU Gonepteryx aspasia 각시멧노랑나비 2 4 25 2 33 M FI NT Lycaenidae 부전나비과 Ussuriana michaelis 금강산귤빛부전나비 122 5N FI Protantigius superans 깊은산부전나비 11NFIVU Japonica lutea 귤빛부전나비 11 2M FI Antigius butleri 담색긴꼬리부전나비 11NFI Chrysozephyrus smaragdinus 암붉은점녹색부전나비 11 2N FI Favonius korshunovi 깊은산녹색부전나비 224NFI Favonius taxila 산녹색부전나비 11 2N FI Rapala caerulea 범부전나비 11 2 M FE Zizeeria maha 남방부전나비 22 S GL Cupido argiades 암먹부전나비 32 5 M GL Tongeia fischeri 먹부전나비 11MGL Celastrina argiolus 푸른부전나비 12 8 40 11 35 3 5 114 M FE Celastrina sugitanii 산푸른부전나비 33NFI Scolitantides orion 작은홍띠점박이푸른부전나비 112NGL Maculinea arionides 큰점박이푸른부전나비 1179NFENT Nymphalidae 네발나비과 Libythea lepita 뿔나비 3 1 36 82 12 181 74 389 S FI Parantica sita 왕나비 21 3 24 S FE Coenonympha hero 도시처녀나비 11M GLVU Lopinga achine 눈많은그늘나비 123MFE Lopinga deidamia 뱀눈그늘나비 279MFE Kirinia epimenides 알락그늘나비 22NFE Kirinia epaminondas 황알락그늘나비 11112 6 N FE Mycalesis francisca 부처사촌나비 58619S FE Mycalesis gotama 부처나비 11SFE Lethe marginalis 먹그늘나비붙이 1 1 10 12 M FI Lethe diana 먹그늘나비 64 47 3 1 1 116 M FI Ninguta schrenckii 왕그늘나비 12 3N FE Melanargia epimede 조흰뱀눈나비 2 8 14 30 49 2 105 N GL NT Minois dryas 굴뚝나비 27425 20 N GL Ypthima argus 애물결나비 35 3 38 M GL Ypthima multistriata 물결나비 12 31 7 M GL Erebia wanga 외눈이지옥사촌나비 4 4 8 N FE VU Argynnis paphia 은줄표범나비 3 43 8 33 3 90 M FE Argynnis zenobia 산은줄표범나비 511 7 N FE Argynnis sagana 암검은표범나비 11MGL Argynnis laodice 흰줄표범나비 1 15 3 20 1 40 M GL Argynnis ruslana 큰흰줄표범나비 14 2 3 2 21 M GL Argynnis anadyomene 구름표범나비 22NFE Argynnis niobe 은점표범나비 1 1 8 10 M GL VU Argynnis vorax 긴은점표범나비 49 2 5 56 M GL Argynnis nerippe 왕은점표범나비 1 3 4 M GL VU Argynnis aglaja 풀표범나비 55NGLEN Brenthis ino 작은표범나비 22 4N GL Boloria perryi 작은은점선표범나비 11NGLVU Limenitis camilla 줄나비 2211 6M FE Limenitis doerriesi 제이줄나비 12 1 4 N FE Limenitis helmanni 제일줄나비 11 N FE Limenitis sydyi 굵은줄나비 77 N FE Limenitis moltrechti 참줄나비 11 2NFI Limenitis populi 왕줄나비 11 N FI VU Neptis sappho 애기세줄나비 3214 212 M FE Neptis philyra 세줄나비 2 391 217 N FI Neptis philyroides 참세줄나비 12 3 N FI Neptis speyeri 높은산세줄나비 11 2 4 N FI CM Lee et al. / Journal of Asia-Pacific Biodiversity 9 (2016) 198e204 201
Table 1 (continued )
y z Species Korean name 1987 2010 2011 2012 2013 2014 2015 Total Distribution pattern* Habitat type Red list species
Neptis rivularis 두줄나비 22 N FE Neptis pryeri 별박이세줄나비 3 1 3 1 11 19 M FE Neptis alwina 왕세줄나비 145MFE Neptis thisbe 황세줄나비 3711 12 N FI Neptis tshetvericovi 중국황세줄나비 33NFIVU Neptis ilos 산황세줄나비 112NFI Apatura ilia 오색나비 1 1 2 N FE VU Apatura metis 황오색나비 62 11 10 N FI Apatura iris 번개오색나비 457441 25 N FI Mimathyma schrenckii 은판나비 13141 212 N FI Mimathyma nycteis 밤오색나비 22NFEVU Chitoria ulupi 수노랑나비 11MFI Dilipa fenestra 유리창나비 11MFI Hestina assimilis 홍점알락나비 22 4S FI Sasakia charonda 왕오색나비 34 7M FI Sephisa princeps 대왕나비 1911214M FI Araschnia levana 북방거꾸로여덟팔나비 1 15 8 7 7 38 N FE Araschnia burejana 거꾸로여덟팔나비 2 4 17 20 43 N FE Vanessa cardui 작은멋쟁이나비 11 2M GL Vanessa indica 큰멋쟁이나비 1 10 1 13 1 26 M GL Polygonia c-aureum 네발나비 22 1 3 26 M GL Polygonia c-album 산네발나비 257 14N FI Nymphalis xanthomelas 들신선나비 5 4 9 N FE VU Kaniska canace 청띠신선나비 3137115M FE Hesperiidae 팔랑나비과 Lobocla bifasciata 왕팔랑나비 123MFE Satarupa nymphalis 대왕팔랑나비 23 5NFI Daimio tethys 왕자팔랑나비 21231 9 M FE Erynnis montanus 멧팔랑나비 41 5 7 53 M FE Carterocephalus silvicola 수풀알락팔랑나비 41 5 N GL Isoteinon lamprospilus 지리산팔랑나비 12 3 S FE Thymelicus leoninus 줄꼬마팔랑나비 1 1 2 13 8 25 M GL Thymelicus sylvaticus 수풀꼬마팔랑나비 13 4M GL Ochlodes ochraceus 검은테떠들썩팔랑나비 311 5N GL Ochlodes subhyalinus 유리창떠들썩팔랑나비 11MGL Parnara guttata 줄점팔랑나비 11SGL Species richness 종수 44 29 61 55 50 30 39 105 Abundance 개체수 112 102 542 377 461 262 181 2037
* Distribution pattern: M ¼ miscellaneous species; N ¼ northern species; S ¼ southern species. y Habitat type: FE ¼ forest edge species; FI ¼ forest interior species; GL ¼ grassland species. z Red list species: CR ¼ critically endangered species; EN ¼ endangered species; NT ¼ near-threatened species; VU ¼ vulnerable species.
Figure 2. Species richness of butterflies in Mt. Gariwang-san. These values were estimated by four algorithms (ACE, Chao 1, Jack 1, and Bootstrap) in Estimate S using data of butterflies recorded by Kim (1988) and field survey data (2010e2015). 202 CM Lee et al. / Journal of Asia-Pacific Biodiversity 9 (2016) 198e204
Table 2. Butterfly communities recorded at 10 sites.
y z Site Year Location Dominant species Distribution pattern* Habitat type Red list species Reference
Latitude Longitude 1st 2nd NMSGLFEFICRENVUNT
Mt. Gyeban-san 1986e1993 37 430 N 128 270 E Apatura metis (5) Mimathyma 54 43 3 35 37 28 0 5 17 3 Kim (1994) schrenckii (5)
Mt. Gariwang-san 1987, 37 270 N 128 330 E Libythea lepita (19) Pieris napi (6) 47 45 9 30 38 31 0 1 12 3 This study 2010e2015 Mt. Chiak-san 1986e1993 37 210 N 128 20 E Luehdorfia puziloi (5) Libythea lepita (5) 43 45 12 30 39 31 0 3 12 1 Sohn (1994) Mt. Pagong-san 1997e1998 36 00 N 128 410 E Pieris melete (16) Cupido 18 65 18 35 53 12 0 0 6 0 Cheong et al argiades (11) (1999)
Mt. Mudeung-san 1989e1990 35 70 N 126 590 E Minois dryas (6) Pieris melete (6) 18 62 20 45 38 17 0 1 11 2 Kim et al (1991) Mt. Unjang-san 1997e1998 35 540 N 127 210 E Ypthima argus (10) Pieris rapae (8) 13 66 22 41 53 6 0 0 3 0 Cheong et al (1999) Mt. Hwangmae-san 1997e1998 35 290 N 127 580 E Neptis sappho (12) Pieris rapae (8) 19 63 19 44 47 9 0 0 3 0 Cheong et al (1999) Mt. Naejang-san 1992e1997 35 280 N 126 530 E Libythea lepita (11) Pieris rapae (7) 24 57 19 43 34 23 1 0 9 4 Kim and Lee (1999) Mt. Jogye-san 1997e1998 35 00 N 127 180 E Pieris melete (8) Ypthima argus (5) 29 50 21 34 45 21 0 3 0 0 Cheong et al (1999) Mt. Halla-san 2007e2012 33 230 N 126 310 E Coenonympha Lethe diana (2) 23 55 23 65 23 13 0 5 13 3 Kim et al hero (8) (2013)
Is. Jeju-do 2012 33 160 N 126 280 E Ypthima Zizeeria maha (12) 3 64 33 58 28 14 0 0 2 0 Kim et al multistriata (14) (2013)
Values indicate proportion (%) of abundance (dominant species) or species richness (distribution pattern and habitat type). Values of red list species indicate the number of species. * Distribution pattern: M ¼ miscellaneous species; N ¼ northern species; S ¼ southern species. y Habitat type: FE ¼ forest edge species; FI ¼ forest interior species; GL ¼ grassland species. z Red list species: CR, critically endangered species; EN, endangered species; NT, near-threatened species; VU, vulnerable species.
Overton 1978, 1979), and Bootstrap (Smith and van Belle 1984). addition, the butterfly community in Gariwang-san was compared When conducting the estimations, the analysis was carried out according to latitude based on previous studies (Cheong et al 1999; with the unit of the sample by the number of each study (n ¼ 55). In Kim 1994; Sohn 1994; Kim and Lee 1999; Kim et al 1991; Kim et al
Figure 3. Relationship between latitude and percentage of northern and southern species. See Table 2 for latitude of each site and percentage of northern and southern species. Small letters indicate site name in Korea. CM Lee et al. / Journal of Asia-Pacific Biodiversity 9 (2016) 198e204 203
Concerning the relationship between latitude and percentage of N species and S species, the percentage of N species significantly decreased as latitude decreased (r2 ¼ 0.602, p ¼ 0.0049; Figure 3). However, the percentage of S species significantly increased as latitude increased. As for the relationship between the percentage of N species and that of S species, the percentage of S species significantly increased as the percentage of N species decreased (r2 ¼ 0.859, p < 0.001; Figure 4).
Discussion
The results showed that butterfly diversity in Mt. Gariwang-san was high, because the species richness of butterflies was estimated at 116 species. In butterfly fauna in Mt. Gariwang-san, the per- centage of N species was very high and the percentage of GL species was relatively higher than that of FE and FI species. Red list species were also abundant. In particular, Mimathyma nycteis was only recorded in Mt. Gariwang-san. This species was observed in only Figure 4. Relationship between percentages of northern and southern species. See five sites among about 500 sites in South Korea, from 1996 to 2011 Table 2 for percentage of northern and southern species. (Kim et al 2012). When comparing the relationship between lati- tude and percentage of N species and S species, the result showed significant increase and decrease. However, S species illustrated a 2013). The relationship between latitude and percentage of N more obvious explanation compared with N species. This result species and S species, and the relationship between the percentage suggests that proportion of S species is a more useful indicator than of N species and that of S species were analyzed using linear that of N species for the study of the response to the effect of regression analysis, which was performed using R software climate change. Kwon et al (2014) also emphasized that the annual (version 3.2.0; Institute for Statistics and Mathematics, Vienna northward shift of the northern margins of S species was 1.6 km for University of Economics and Business, Vienna, Austria, http://www. 60 years as a result of climate change. We expect that the structure r-project.org). of the butterfly community in Mt. Gariwang-san located in high latitudes in South Korea will be changed gradually in response to Results the effect of climate change. Various studies related to insects, such as fauna of Lepidoptera A total of 2,037 butterflies belonging to 105 species were (Kim 1988), national ecosystem survey in Ministry of Environment recorded (Table 1). Libythea lepita was the most abundant, (Ryu and Jeon 1998), fauna of Coleoptera (Lee et al 2009), effects of comprising 19% of the total number of individuals. Pieris napi, Lethe forest roads on Hemipteran diversity, Hemiptera on forest road Diana, Celastrina argiolus, Papilio maackii, and Melanargia epimede (Jung et al 2013), characteristics of Carabidae (Jung et al 2011), were also abundant. These five species comprised 27% of the total Lepidoptera in high mountains (Kim and Kwon 2013), and beetle number of individuals. In terms of estimation of species richness, diversity on forest management (Lee et al 2014), were carried out in the estimated number of species was 112 species for ACE, 110 Mt. Gariwang-san. However, there is a lack of studies focusing on species for Chao 1, 125 species for Jack 1, and 116 species for the whole forest ecosystem in Mt. Gariwang-san, wherein adequate Bootstrap (Figure 2). The average value for the four algorithms was conservation and management are carried out. Therefore, it is 116 species. All estimations were shown to be stabilized when the desirable to continue studying the butterfly community in Mt. number of samples was > 40. In the case of distribution pattern, Gariwang-san to assess how the forest ecosystem changes in species richness in N species (32 species) was higher than that in S response to climate change, and how this change impacts biotic species (9 species). For habitat type, species richness in FE (40 communities. species) and FI (33 species) was higher than that in GL (32 species). Fifteen red list species were also observed: one EN species Acknowledgments (Argynnis aglaja), 12 VU species (Gonepteryx maxima, Protantigius superans, Coenonympha hero, Erebia wanga, Argynnis niobe, Argynnis This study was conducted as part of a research project of the nerippe, Boloria perryi, Limenitis populi, Neptis tshetvericovi, Apatura National Institute of Forest Science, “Research on application plan ilia, Mimathyma nycteis, and Nymphalis xanthomelas), and three NT of long term ecological information” (Project No. FE0100-2014-02). species (Gonepteryx aspasia, Maculinea arionides, and Melanargia We thank two anonymous reviewers for their helpful suggestions. epimede). The butterfly communities were compared according to latitude References based on previous studies including those conducted in Mt. Gyeban-san, Mt. Chiak-san, Mt. Pagong-san, Mt. Mudeung-san, Mt. Burnham KP, Overton WS. 1978. Estimation of the size of a closed population when e Unjang-san, Mt. Hwangmae-san, Mt. Naejang-san, Nt. Jogye-san, capture probabilities vary among animals. Biometrika 65:623 633. Burnham KP, Overton WS. 1979. Robust estimation of population size when capture Mt. Halla-san, and Is. Jeju-do (Kim et al 1991; Kim 1994; Sohn probabilities vary among animals. Ecology 60:927e936. 1994; Cheong et al 1999; Kim and Lee 1999; Kim et al 2013). The Byeon JG, Jang JW, Yang JC, et al. 2012. The flora of Mt. Gariwangsan protected area proportion of two dominant species in Mt. Gariwang-san was for forest genetic resource, in Jeongseon-gun, Gangwon-do, Korea. Proceedings for Joint Conference of Forest Science in Spring 2012, pp 563e564. relatively higher compared with that in other sites (Table 2). The Chao A. 1984. Non-parametric estimation of the number of classes in a population. proportion of N species and FE species was substantially higher Scandinavian Journal of Statistics 11:265e270. than that in S species and GL species, respectively. Red list species Chao A, Ma MC, Yang MCK. 1993. Stopping rules and estimation for recapture debugging with unequal failure rates. Biometrika 80:193e201. were also relatively abundant. In particular, Mimathyma nycteis was Chazdon RL, Colwell RK, Denslow JS, et al. 1998. Statistical methods for estimating recorded only in Mt. Gariwang-san. species richness of woody regeneration in primary and secondary rain forests of 204 CM Lee et al. / Journal of Asia-Pacific Biodiversity 9 (2016) 198e204
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