Journal of Asia-Pacific Entomology 22 (2019) 353–358

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Journal of Asia-Pacific Entomology

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Short communication A review of host of (Eoxenus) relictus Semenov (Coleoptera: Cerambycidae: ), a natural monument, with a new host, T Quercus aliena Blume ⁎ Seung-Gyu Leea, Cheolhak Kimb, Ik-Je Choic, Alexander V. Kuprind, Jongok Lima, a Division of Forest Biodiversity, Korea National Arboretum, Pocheon 11186, Republic of Korea b Institution of Biological Resources, Osang K-, Yesan 32426, Republic of Korea c Division of Eco-friendly Agriculture, Division of Agriculture and Stockbreeding Distribution Bureau, Governor of Gyeongsangbuk-do, Pungsan, Andong, Gyeongbuk Province, Republic of Korea d Federal Scientific Center of the East Asia Terrestrial Biodiversity, Russian Academy of Science, Vladivostok-22, 690022,

ARTICLE INFO ABSTRACT

Keywords: A comprehensive checklist identifying host plants of phytophagous are essential in protecting forest Callipogon (Eoxenus) relictus ecosystems from major insect pests. We investigated host plants of Callipogon (Eoxenus) relictus Semenov Gwangneung forest (Coleoptera: Cerambycidae: Prioninae), an insect categorized as a natural monument in . Field Host plants surveys in Gwangneung forest led us to newly recognize the oriental white oak, Quercus aliena Blume (Fagaceae), Natural monument as a host of C. (E.) relictus. Based on this result and a literature search, we provide an updated list of host Quercus aliena plants of C. (E.) relictus in the present study. In addition, we also discussed about microorganisms (mushrooms) and habitats in Gwangneung forest (South Korea) and Ussurisky Nature Reserve (Russia) that are relevant to C. (E.) relictus.

Introduction Vlasak, 2014; Doychev et al., 2017; Monné, 2017). In South Korea, Lim et al. (2014) presented 170 host plants for 181 cerambycid . Commonly known as longhorn or timber (Machado et al., The Callipogon includes eight species in four subgenera with 2012), the phytophagous family Cerambycidae (Coleoptera) comprises an interesting disjunct distribution in the Neotropical and West 35,000 species worldwide (Monné et al., 2009). Although some feed on Palearctic regions (Li et al., 2012; Monné, 2017). Seven species (re- herbaceous growths, members of the family generally attack arbor- presenting three subgenera) are known to occur in escent plants, including each species restricted to a single tree species or (Monné, 2017). The last one is C. (Eoxenus) relictus Semenov, the largest genus (Craighead, 1923). As wood borers, the cerambycids are some of in the Palearctic region (Byun et al., 2007) and the only re- the most ecologically and economically relevant insects in the world, presentative of the genus Callipogon in East Asia (Bezborodov, 2016). given their ability to damage timber already in service, as well as ser- This distribution could serve as a part of the evidence supporting the iously debilitate or kill commercially valuable trees and shrubs (Linsley, Bering land bridge theory, i.e., a terrestrial connection between Eastern 1959; Web, 1987). Palearctic and Western Nearctic regions during the early Cenozoic (An, Subfamily Prioninae have been known as a primitive group and 2010; Bezborodov, 2016). primarily consists of borers that feed on rotten wood or roots (Wang In South Korea, where the beetle is designated as a Korean natural et al., 2014). monument (No. 218), C. (E.) relictus was first recorded as Macrotoma Measures to protect forest ecosystems against phytophagous insect (Bandar) fisheri Waterhouse (Saito, 1932) without a detailed collection pests must involve generating an up-to-date checklist affected host locality, and Carpinus laxiflora (Siebold and Zucc.) Blume () plants of the pests. The life cycle and host information of Cerambycidae was newly reported as its host plant of C. (E.) relictus (Murayama, 1936) are particularly important, given their high destructive potential. in Gwangneung forest. However, the population of C. (E.) relictus has Recently, many checklists of cerambycids and new records of host not been fully investigated, because considerable effort is required for plants have been published from the world (Machado et al., 2012; its isolation and identification of this species living heartwood.

⁎ Corresponding author at: Division of Forest Biodiversity, Korea National Arboretum, Pocheon-si, Gyeonggi province 11186, Republic of Korea E-mail address: [email protected] (J. Lim). https://doi.org/10.1016/j.aspen.2019.01.016 Received 2 April 2018; Received in revised form 19 October 2018; Accepted 30 January 2019 Available online 01 February 2019 1226-8615/ © 2019 Korean Society of Applied Entomology. Published by Elsevier B.V. All rights reserved. S.-G. Lee et al. Journal of Asia-Pacific Entomology 22 (2019) 353–358

Table 1 Host plants of Semenov (*, new record; †, species distributed in Gwangneung forest) (A, Murayama, 1936;B,Cho, 1959;C,Cho, 1959;D,Ko, 1969; E, Kim et al., 1976;F,Kim, 1977;G,Lee, 1987;H,Cherepanov, 1988;I,Chung et al., 1995;J,Wang, 2003;K,Ministry of Environment, 2007;L,Shin et al., 2007;M, Kuprin and Bezborodov, 2012;N,Li et al., 2012;O,Lim et al., 2013;P,Kuprin et al., 2014;Q,Yi et al., 2018; PS, present study).

No. Host plant Literatures for each country

Family Scientific name S. Korea Russia

1 Aceraceae Maxim. H, K, M, P 2 Anacardiaceae Anacardiaceae mono Maxim. N 3 Betulaceae Trautv. K, M, P 4 Betula spp. J 5 Carpinus cordata Blume† K, PS 6 C. laxiflora (Siebold & Zucc.) Blume† A, C, D, E, I, K, L, O, PS K 7 Carpinus spp. G, PS 8 Fagaceae Quercus aliena Blume*,† PS (new host) 9 Q. mongolica Fisch.† C, D, E, F, I, K, L B, K H, K, M, P 10 Q. wutaishanica Mayr N 11 Quercus spp. G, PS J 12 Salicaceae Chosenia arbutifolia (Pall.) A. Skvorts. M, P 13 Populus maximowiczii A. Henry H, K, M, P, Q 14 Salix caprea L.† M 15 S. schwerinii E. Wolf. M 16 Tiliaceae amurensis Rupr.† H, K, M, P 17 Ulmaceae Fraxinus mandshurica Rupr. E, K K H, K, M, P 18 F. rhynchophylla Hance† E, F, I, K, L N 19 Fraxinus spp. G J 20 Ulmus davidiana var. japonica (Rehder) Nakai† KK,P,Q 21 U. laciniata (Trautv.) N 22 U. propinqua Koidz H 23 Ulmus spp. G 7 families 11 genera 17 species 7 (species level) 6 (species level) 10 (species level)

Furthermore, its life cycle spans 2–6 years (Kim et al., 1976; Wang, 2003; Li et al., 2012), requiring long-term study. The aim of the present study is to review recorded host plants of C. (E.) relictus and investigate the possibility of novel hosts in South Korea. Through field surveys, we identified one new host of the species and provided fundamental biological data on C. (E.) relictus, including its association with the surrounding habitat. This information should prove its benefit for efforts to restore or re-introduce certain trees into natural habitats.

Materials and methods

Literature survey

We reviewed 17 references (Murayama, 1936; Chen et al., 1959; Cho, 1959; Ko, 1969; Kim et al., 1976; Kim, 1977; Lee, 1987; Cherepanov, 1988; Chung et al., 1995; Wang, 2003; Ministry of Environment, 2007; Shin et al., 2007; Kuprin and Bezborodov, 2012; Li et al., 2012; Lim et al., 2013; Kuprin et al., 2014; Yi et al., 2018) di- rectly related to host plants of Callipogon (Eoxenus) relictus. The studies spanned Korea (10 references), China (three references), and far eastern Russia (four references). Scientific names of host plants follow the “Korean Plant Names Index” (Nature).

Field study in Gwangneung forest, Korea

From early April to late August since 2006, we performed annual surveys of Callipogon (Eoxenus) relictus habitats and ecological char- acters (including occurrence and host plants) in Gwangneung forest (2526.5 ha). In 2010, this site was designated as the fourth UNESCO biosphere reserve of South Korea, owing to the fact that it is a re- presentative old-growth forest protected since the 15th century (Cho Figs. 1–3. A new host plant, Quercus aliena in Gwangneung forest, South Korea. et al., 2012; Lee et al., 2016). 1, dead tree; 2, exit hole on the tree; 3, broken trunk of the tree. Located in the central Korean peninsula (37°42′36″–47′41″ N, 127°8′20″–11′58″ E; 40–620 m above sea level), the region is classified as a cool temperature forest. Mean annual precipitation and

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Figs. 4–7. Biological photographs related with Callipogon (Eoxenus) relictus. 4, splitting the tree; 5, pupal chamber in the tree; 6–7, and the gallery.

Figs. 8–9. Biological photographs related with Callipogon (Eoxenus) relictus. 8, Cross-sectional plane of the host tree; 9, female exuvium.

Figs. 10–11. Carpinus laxiflora and Fomes fomentarius in Gwangneung forest. 9, Carpinus laxiflora infected with Fomes fomentarius; 10, Fomes fomentarius infecting Carpinus laxiflora.

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Figs. 12–15. Various fungi infecting host plants in Ussurisky nature reserve, Russia. 12, Pleurotus sp.; 13–14, Fomes sp.; 15, Dacrymyces sp. temperature are 1417.9 mm and 11.7 °C, respectively (Lee et al., 2016). China. Approximately 942 taxa and 3966 insect species have In this study, we treated Fisch. (Salicaceae) from been recorded in the forest (Cho et al., 2012), or 20% of all known plant Russia (Kuprin and Bezborodov, 2012; Kuprin et al., 2014)asP. max- species in South Korea (4400 taxa; Cho et al., 2012; Lee et al., 2016) imowiczii A. Henry because the former is a junior synonym of the latter. and 28% of known insect species in the Korean Peninsula, respectively.

Field survey in Gwangneung forest Results On August 1 of our 2016 survey, we found a dead Quercus Review of host plants (Fagaceae) tree in Gwangneung forest (37°44′ 53.34″N, 127°10′2.93″E; altitude 134 m) with a large bore (240 × 350 mm) that we determined We recognized a total of 16 vascular plant species (excluding taxa to be an exit hole of Callipogon (Eoxenus) relictus (Fig. 2). The tree was recorded at the genus level) representing 11 genera in seven families identified as Q. aliena Blume (oriental white oak) and is here reported that were recorded as host plants of Callipogon (Eoxenus) relictus from as a new host of C. (E.) relictus. South Korea (6 spp.), China (6 spp.), and Far Eastern Russia (11 spp.) The tree had fallen and was approximately 250 cm from the ground (Table 1) through review of the previous literatures. Russia has the (Fig. 1). Total tree length was about 28 m, including length of the highest diversity of host species. broken trunk (Fig. 3). The exit hole was 210 cm from the ground, where In addition, of previously identified hosts recorded at the genus trunk diameter was 310 mm. The area around the hole was debarked level, we noted: Fraxinus spp. (Ulmaceae) from Korea and China (Lee, longitudinally (Figs. 1–2). 1987; Wang, 2003), Ulmus spp. (Ulmaceae) from Korea (Lee, 1987), Upon splitting the tree and exit hole, we found and measured a Betula spp. (Betulaceae) from China (Wang, 2003), Carpinus spp. (Be- larval gallery; pupal chamber (Figs. 4–5); and a large (length, 105 mm; tulaceae) from Korea (Lee, 1987), as well as Quercus spp. (Fagaceae) head width, 11.4 mm; weight, 25.8 g), living cerambycid larva within from Korea and China (Lee, 1987; Wang, 2003). the larval gallery (Fig. 6–7). An unknown species recorded as Anacardiaceae mono Maxim. was The first author identified this larva as C. (E.) relictus based on listed as a host of C. (E.) relictus in China (Li et al., 2012), but we could morphological characters (Lim et al., 2013). The larval gallery was not identify the exact species. Based on frequent reports of Acer mono 110 cm from the ground, where the trunk diameter was 36 cm (Fig. 8). Maxim. (Aceraceae) as a host plant in Korea and Russia (Cherepanov, We also found a larval exuvium in the gallery (Fig. 9), identified as 1988; Ministry of Environment, 2007; Kuprin and Bezborodov, 2012; being from a female with coiled short antenna. Kuprin et al., 2014), we assumed it to be the species reported from

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Figs. 16–19. Various fungi infecting host plants in Ussurisky nature reserve, Russia. 16, Ganoderma sp.; 17, Gymnopilus sp.; 18, Laetiporus sp. 19. Trametes sp.

Discussion (Table 1). Callipogon (Eoxenus) relictus had been observed more fre- quently from Carpinus laxiflora than other tree hosts in earlier studies, Host plants of Callipogon (Eoxenus) relictus leading to a dominant focus on C. laxiflora-dominated forests when surveying C. (E.) relictus habitats. However, our data suggest the beetle Until the current study, only the host plants of two Callipogon spe- can feed more species than previously supposed and that subsequent cies, C.(Callipogon) barbatum (Fabricius) and C.(Dendroblaptus) barbi- survey efforts should be enlarged to include broad-leaved forests. flavum (Chevrolet), were well established (Monné, 2017). Host plants of the former species include six coniferous and broad-leaved species re- presenting five genera in four families: Cordia alliodora (Ruíz and Association with fungi Pavón) Oken, C. stellifera I.M. Johnston (Boraginaceae), Brosimum ali- castrum Swartz, Ficus sp. (Moraceae), Pinus rudis Endlicher (Pinaceae), It is known that the larvae of Callipogon (Eoxenus) relictus are xy- Citrus aurantium Linné (Rutaceae). In contrast, C. (D.) barbiflavum is lomycetophages (or sapro-xylo-mycetophages) that can develop in known to occur only in a conifer, Pinus caribaea Morelet (Pinaceae) Japanese elm (Ulmus davidiana var. japonica) infested with white rot (Monné, 2017). (Kuprin and Bezborodov, 2012; Kuprin et al., 2014). A recent indoor fl In the present study, we found that C.(E.) relictus feeds on 17 de- experiment using the white oyster mushroom (Pleurotus orida (Eager); ciduous broad-leaved species representing 11 genera in seven families. Agaricales: Pleurotaceae) suggests C. (E.) relictus is primarily fungi- We updated the list of known hosts with the addition of Q. aliena Blume vorous, similar to larvae of many other wood-boring saprophagous (Fagaceae), is commonly called the oriental white oak and distributed Coleoptera that feed on fungal mycelia inside dead or decaying wood in southern East Asia, China, Japan, and the Korean peninsula (Lee (Yi et al., 2017). et al., 2009). In the Korean peninsula, this species is not forming pure In this study, we found various species of fungi from South Korea stands and is scattered in deciduous lowlands with Q. serrata Thunb. (Gwangneung forest) and Russia (Ussurisky nature reserve). In South (Global Biodiversity Information Facility, 2018). Korea, it has been known that the larvae of the species were usually fl Based on our surveys and previous research, we conclude that there found from Carpinus laxi ora with the hoof , Fomes fomentarius are eight host species of C. (E.) relictus distributed in Gwangneung (L.) J.J.Kickx (Polyporales: Polyporaceae), although there are not en- fi forest: Ulmus davidiana var. japonica Rehder, Fraxinus rhynchophylla ough scienti c reports on fungi associated with C. (E.) relictus – Hance (Ulmaceae), Salix caprea L. (Salicaceae), Carpinus cordata Blume, (Figs. 10 11). C. laxiflora (Siebold and Zucc.) Blume (Betulaceae), We observed more fungal diversity came from the Ussurisky nature Fisch., Q. aliena Blume (Fagaceae), and Rupr. (Tiliaceae) reserve, Russia. Notably, C. (E.) relictus was more frequently found in association with Pleurotus sp. (Agaricales: Pleurotaceae) (Fig. 12)

357 S.-G. Lee et al. Journal of Asia-Pacific Entomology 22 (2019) 353–358 infecting Ulmus davidiana var. japonica than other fungal species (data Cho, Y.-C., Koo, B.-Y., Shin, J.-K., Kim, S.-S., Park, K.-W., Oh, S.-H., Lee, Y.-M., Bae, G.-H., from 2015; Mr. Kuprin, per. comm.). In Ussurisky Nature Reserve, the Kim, N.-S., 2012. Changing environment and biodiversity of Gwangneung forest. In: Korea National Arboretum. Dongjin Publishing Co., Seoul. same host species also exhibited other fungi, such as Fomes sp. (Poly- Chung, Y.J., Lee, B.Y., Byun, B.H., 1995. A List of Insect Pests of Trees and Shrubs in porales: Polyporaceae), Dacrymyces sp. (Dacrymycetales: Dacrymyce- Korea. Forestry Research Institute, Seoul. taceae), Ganoderma sp. (Polyporales: Ganodermataceae), Laetiporus Craighead, F.C., 1923. North American Cerambycid Larvae: a classification and the biology of North American cerambycid larvae. Entomol. Bull. 23, 1–239. (Polyporales: Fomitopsidacae), Trametes sp. (Polyporales: Poly- Doychev, D., Topalov, P., Zaemdjikova, G., Sakalian, V., Georgiev, G., 2017. Host plant of poraceae), Gymnopilus sp. (Agaricales: Strophariaceae) (Figs. 13–19). Xylophagous longhorn beetles (Coleoptera: Cerambycidae) in Bulgaria. Acta Zool. Most mushroom taxa (Fomes, Ganoderma, Gymnopilus, Pleurotus, Tra- Bulgarica 69 (4), 511–528. metes spp.) from Ussurisky are white rot, with Laetiporus and Dacry- Global Biodiversity Information Facility: Free and Open Access to Biodiversity Data. https://www.gbif.org (assessed date: 31 January 2018). myces (brown rot) being exceptions (Worrall, 1997). Therefore, C. (E.) Kim, C.W., 1977. Distribution atlas of insects of Korea. In: Series 2. Coleoptera. Korea relictus appears capable of inhabiting host trees infected with diverse University Press, Seoul. (white or brown) lignicolous fungi. Kim, C.W., Yoon, I.B., Nam, S.H., 1976. On the habitats and habits of Callipogon relictus S. (Col. Cerambycidae). Environ. Preserv. 11, 5–16. Ko, J.H., 1969. A List of Insect Pests of Trees and Shrubs in Korea. Forestry Research Habitats Institute, Seoul. Kuprin, A.V., Bezborodov, V.G., 2012. Areal of Callipogon relictus Semenov, 1899 (Coleoptera, Cerambycidae) in the . Biol. Bull. 39 (4), 387–391. Large populations of Callipogon (Eoxenus) relictus are associated with Kuprin, A.V., Bezborodv, V.G., Yi, D.A., Kotlyar, A.K., 2014. Developmental biology and preserved nemoral forests (Bezborodov, 2016; Yi et al., 2018); thus, its ecological peculiarities of the Relictus Callipogon relictus Semenov, survival depends on conserving such regions (Bezborodov, 2016). 1899 (Coleoptera, Cerambycidae). Entomol. Rev. 94 (9), 1251–1256. Lee, S.-M., 1987. The Longicorn Beetles of Korean Peninsula. National Science Museum, The Gwangneung forest is a prime model for forest conservation and Seoul. restoration (Lee et al., 2016). 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