Brachymna tenuis Stål, 1861 (Hemiptera: Pentatomidae), a new invasive bamboo pest in Korea with notes on insects associated with bamboos.

BACKGROUND: We report first observations of the invasive bamboo pest, Brachymna tenuis Stål, 1861 in Korea as the first species of Brachymna Stål, 1861 (Pentatomidae) reported from the country. NEW INFORMATION: Comments on its pest status and distribution are provided. General information on this bamboo-feeding insect in Korea is analysed and provided for the first time. Soojeong Ahn, WonGun Kim, Sangsu Kim, Geonho Cho.

Introduction

Bamboo grows in the tropics and subtropics and has received increasing attention because of its fast-growing nature, social usage and industrial demand, for example, foods, crafts, building material and energy resource (Kim et al. 2018). In Korea, there are 18 species of bamboos distributed mostly in the southern part of the country (Kong 1985). Amongst them, eleven dominant bamboo species either occur naturally or are planted and they occupy more than 22 thousand hectares (Kim et al. 2018). The number of insects that feed on bamboos is estimated to be more than 1200 insects in the world (Shu and Wang 2015). The numbers may vary depending on the country and province, ranging from 97 to 244 insect species feeding on bamboos in China (Huang and Liu 2006, Zhao et al. 2006, Zhang and Zuo 2015). In Korea, the review of the entire bamboo-feeding insects has never been done before.

Bamboo pest, Stål, 1861 and its synonym, Walker, 1867 were described from Hong Kong and the Chinese mainland, respectively and subsequent records were made from twelve Provinces in China (Hoffmann 1932, Hsiao and Zheng 1977, Rider et al. 2002, Aukema and Rieger 2006, Huang and Liu 2006, Zhao et al. 2006, Zhang et al. 2008, Zhang and Zuo 2015), Japan (Aukema and Rieger 2006, Ishikawa et al. 2012, Tanaka 2013, Tanaka 2014, Igasaki 2016, Igasaki 2017, Igasaki 2018, Kanetada 2017) and Taiwan (Taiwan Encyclopedia of Life 2018). Recently, the first three authors observed somewhat large, exotic, invasive, bamboo-feeding stink bugs from southern Korea, which had never been recorded. The aim of the present paper is to report new records of invasive bamboo pest from Korea, to discuss the distribution of the species and to provide, for the first time, a list of bamboo-feeding insects in Korea, based on a literature review.

Materials and methods

Surveys were conducted in natural and cultivated bamboos, located in the southern Provinces of South Korea (Gyeongsangnam-do and Jeollanam-do) in 2020. Adults and nymphs were observed by visual inspection. The specimens were morphologically identified using the reference books by Lin and Zhang (1993) and Ishikawa et al. (2012). Photographs of habitus were taken using a DSLR camera (Nikon D500, D7100, Nikon 60 mm Micro). The plant names follow The Plant List (2016). The examined specimens were deposited in the College of Agriculture and Life Science, Seoul National University (SNU), Seoul and the private collections of the authors.

Taxon treatments

Stål, 1861

D8F7725B-3CC7-521B-A965-5E3BBA631399

http://taieol.tw/data_objects/93100

PRJNA550733

Type status: Other material. Occurrence: recordedBy: S. Ahn; W.G. Kim; individualCount: 16; sex: 3 males, 3 females, 10 nymphs; lifeStage: 6 adults, 10 nymphs; establishmentMeans: invasive; occurrenceStatus: present; preparations: in 95% ethanol; disposition: in collection; Taxon: scientificName: ; order: ; family: ; genus: ; specificEpithet: ; taxonRank: species; nomenclaturalCode: ICZN; Location: higherGeography: East Asia; South Korea; country: South Korea; stateProvince: Gyeongsangnam-do; municipality: Jinju-si; locality: Gajwa-dong, San 113-1; Identification: identifiedBy: S. Ahn; W.G. Kim; S. Kim; G. Cho; dateIdentified: 2020-07; Event: samplingProtocol: visual inspection; eventDate: 2020-06-11; year: 2020; month: 6; day: 11; habitat: ; Record Level: language: en; institutionCode: SNU; basisOfRecord: PreservedSpecimen

Type status: Other material. Occurrence: recordedBy: S. Ahn; individualCount: 2; sex: 2 nymphs; lifeStage: 2 nymphs; establishmentMeans: invasive; occurrenceStatus: present; preparations: in 95% ethanol; disposition: in collection; Taxon: scientificName: ; order: ; family: ; genus: ; specificEpithet: ; taxonRank: species; nomenclaturalCode: ICZN; Location: higherGeography: East Asia; South Korea; country: South Korea; stateProvince: Gyeongsangnam-do; municipality: Haman-gun; locality: Beopsu-myeon, Jumul-ri, San 1; Identification: identifiedBy: S. Ahn; W.G. Kim; S. Kim; G. Cho; dateIdentified: 2020-07; Event: samplingProtocol: visual inspection; eventDate: 2020-06-25; year: 2020; month: 6; day: 25; habitat: ; Record Level: language: en; institutionCode: SNU; basisOfRecord: PreservedSpecimen

Type status: Other material. Occurrence: recordedBy: S. Ahn; individualCount: 3; sex: 3 nymphs; lifeStage: 3 nymphs; establishmentMeans: invasive; occurrenceStatus: present; preparations: in 95% ethanol; disposition: in collection; Taxon: scientificName: ; order: ; family: ; genus: ; specificEpithet: ; taxonRank: species; nomenclaturalCode: ICZN; Location: higherGeography: East Asia; South Korea; country: South Korea; stateProvince: Gyeongsangnam-do; municipality: Changwon-si; locality: Masanhoewon-gu, Guam-dong 669-9; Identification: identifiedBy: S. Ahn; W.G. Kim; S. Kim; G. Cho; dateIdentified: 2020-07; Event: samplingProtocol: visual inspection; eventDate: 2020-06-28; year: 2020; month: 6; day: 28; habitat: ; Record Level: language: en; institutionCode: SNU; basisOfRecord: PreservedSpecimen

Type status: Other material. Occurrence: recordedBy: S. Ahn; individualCount: 4; sex: 1 male, 3 nymphs; lifeStage: 1 adult, 3 nymphs; establishmentMeans: invasive; occurrenceStatus: present; preparations: in 95% ethanol; disposition: in collection; Taxon: scientificName: ; order: ; family: ; genus: ; specificEpithet: ; taxonRank: species; nomenclaturalCode: ICZN; Location: higherGeography: East Asia; South Korea; country: South Korea; stateProvince: Gyeongsangnam-do; municipality: Jinju-si; locality: Gajwa-dong 952-1; Identification: identifiedBy: S. Ahn; W.G. Kim; S. Kim; G. Cho; dateIdentified: 2020-07; Event: samplingProtocol: visual inspection; eventDate: 2020-07-11; year: 2020; month: 7; day: 11; habitat: ; Record Level: language: en; institutionCode: SNU; basisOfRecord: PreservedSpecimen

Type status: Other material. Occurrence: recordedBy: S. Ahn; individualCount: 1; sex: 1 nymph; lifeStage: 1 nymph; establishmentMeans: invasive; occurrenceStatus: present; preparations: in 95% ethanol; disposition: in collection; Taxon: scientificName: ; order: ; family: ; genus: ; specificEpithet: ; taxonRank: species; nomenclaturalCode: ICZN; Location: higherGeography: East Asia; South Korea; country: South Korea; stateProvince: Gyeongsangnam-do; municipality: Hadong-gun; locality: Yangbo-myeon, Jangam-ri 419; Identification: identifiedBy: S. Ahn; W.G. Kim; S. Kim; G. Cho; dateIdentified: 2020-07; Event: samplingProtocol: visual inspection; eventDate: 2020-07-15; year: 2020; month: 7; day: 15; habitat: ; Record Level: language: en; institutionCode: SNU; basisOfRecord: PreservedSpecimen

Diagnosis

According to Lin and Zhang (1993), resembles . It differs from the latter by the yellowish-brown body colour (Fig. 1a, b) (ferruginous in ) and the pygophore bearing dentate postero-lateral processes that are obtusely curved from the postero-ventral margin (Fig. 1c) (postero-lateral processes make approximately a right angle with the postero-ventral margin in ).

Figure 1a.

Adult male, dorsal view.

Figure 1b.

Adult female, dorsal view.

Figure 1c.

Apex of abdomen of male, ventral view.

Distribution

China, Japan, Taiwan and South Korea (new record).

Analysis

Provisionally, 61 species are associated with bamboos in South Korea with the majority of the insects belonging to sap-sucking (52.46%). They are mainly polyphagous and include mostly aphids and scale insects. are the second largest group, making up 31.15% of the total; these include many defoliators, leaf-rollers and one bamboo-shoot cutworm (). are the third order, with 14.75% of the species, which include deleterious bamboo borers, such as () and spp. (). The bamboo-feeding sawfly () is included in the list as the only member of (Table 1).

Table 1.

Provisional list of insect species feeding on bamboos in Korea. The species that possibly damages bamboo is marked with *.

Insect	Host plants with reference	Feeding habits with reference
COLEOPTERA
Bostrichidae
Dinoderus japonicus Lesne, 1895	Phyllostachys, Pleioblastus (Bieńkowski and Orlova-Bienkowskaja 2017)	Borer (Bieńkowski and Orlova-Bienkowskaja 2017)
Dinoderus minutus (Fabricius, 1775)	Bambusa spp., Dendrocalamus spp., Phyllostachys spp. (Watanabe et al. 2018, CABI 2020)	Borer (Mori and Arai 1979, Watanabe et al. 2018, CABI 2020)
Lyctus brunneus (Stephens, 1830)	Bamboo (Liu and Geis 2019)	Borer (Mori and Arai 1979)
Cerambycidae
Bumetopia oscitans Pascoe, 1858	Arundinaria simonii (Park 2015)	Borer (Park 2015)
Chlorophorus annularis (Fabricius, 1787)	Bamboos; Bambusa spp., Chimonobambusa tumidissinoda, Dendrocalamus strictus, Indosasa crassiflora, Phyllostachys spp., Sinobambusa gibbosa, Sinocalamus spp. (Mori and Arai 1979, Hill 2008, Lim et al. 2014, Suma and Bella 2018)	Borer (Mori and Arai 1979, Hill 2008, Suma and Bella 2018)
Purpuricenus temminckii Guerin-Meneville, 1844	Phyllostachys spp., Sasa spp. (Mori and Arai 1979, Lim et al. 2014)	Borer (Mori and Arai 1979)
Niphona furcata (Bates, 1873)	Phyllostachys, Pleioblatus, Pseudosasa japonica, Sasa spp. (Haoje et al. 2002, Lim et al. 2014)	Borer (Haoje et al. 2002)
Nitidulidae
Epuraea submicrurula Reitter, 1875	Sasa spp. (Sakata et al. 2020) (North Korea)	Florivory (Sakata et al. 2020)
Ptinidae
Oligomerus japonicus Sakai, 1982*	Unknown	Unknown
HEMIPTERA
Aclerdidae
Nipponaclerda biwakoensis (Kuwana, 1907)	Sasa borealis (García-Morales et al. 2016, Suh 2020)	Sap-sucking
Alydidae
Distachys unicolor (Scott, 1874)	Sasa borealis (Ahn et al. 2018)	Sap-sucking
Distachys vulgaris Hsiao, 1964	Sasa borealis (Ahn et al. 2018)	Sap-sucking
Asterolecaniidae
Bambusaspis bambusicola (Kuwana, 1916)	Bambusa spp., Phyllostachys spp. (García-Morales et al. 2016, Suh 2020)	Sap-sucking
Aphididae
Ceratoglyphina styracicola (Takahashi, 1921)	Bamboos (Arundinaria or Pleioblastus) (Blackman and Eastop 2020)	Sap-sucking
Ceratovacuna cerbera Aoki, Kurosu, Shin & Choe, 1999	Sasa spp. including S. borealis and S. veichii (Aoki et al. 1999, Aoki and Kurosu 2010, Blackman and Eastop 2020)	Sap-sucking
Ceratovacuna japonica (Takahashi, 1924)	Small bamboos (Arundinaria, Bambusa, Sasa sp.) (Blackman and Eastop 2020)	Sap-sucking
Melanaphis bambusae (Fullaway, 1901)	Bamboos (Arundinaria, Bambusa, Phyllostachys) (Blackman and Eastop 2020)	Sap-sucking
Paracolopha morrisoni (Baker, 1919)	Bamboos (Arundinaria, Phyllostachys, Sasa spp.) (Blackman and Eastop 2020)	Sap-sucking
Rhopalosiphum rufiabdominale (Sasaki, 1899)	Numerous species of Poaceae (Blackman and Eastop 2020)	Sap-sucking
Takecallis alba Lee, 2018	Pseudosasa sp., Sasa spp. (Lee and Lee 2018, Blackman and Eastop 2020, Rakhshani et al. 2020)	Sap-sucking
Takecallis arundicolens (Clarke, 1903)	Arundinaria spp., Bambusa spp., Phyllostachys spp., Pleioblastus chino, Pseudosasa japonica, Sasa spp., Sasaella ramosa (Lee and Lee 2018, Blackman and Eastop 2020, Rakhshani et al. 2020)	Sap-sucking
Takecallis arundinariae (Essig, 1917)	Arundinaria spp., Bambusa spp., Dendrocalamus spp., Phyllostachys spp., Pseudasasa japonica, Sasa spp., Sinoarundinaria reticulata, Sinobambusa tootsik) (Lee and Lee 2018, Blackman and Eastop 2020, Rakhshani et al. 2020)	Sap-sucking
Takecallis taiwana (Takahashi, 1926)	Arundinaria spp., Bambusa spp., Dendrocalamus asper, Phyllostachys spp., Pleioblastus spp., Sasa spp., Shibataea kumasana) (Lee and Lee 2018, Blackman and Eastop 2020, Rakhshani et al. 2020)	Sap-sucking
Blissidae
Dimorphopterus japonicus (Hidaka, 1959)	Chimonobambusa marmorea, Sasa senanensis (Sakata et al. 2020)	Florivory, sap-sucking (Sakata et al. 2020)
Cicadellidae
Scaphoideus festivus Matsumura, 1902	Bamboo (Yang et al. 2013)	Sap-sucking
Coccidae
Coccus hesperidum Linnaeus, 1759	Various plants of 346 genera in 121 families including Bambusa vulgaris (García-Morales et al. 2016, Choi and Lee 2018)	Sap-sucking
Diaspididae
Kuwanaspis hikosani (Kuwana, 1902)	Arundinaria simonii, Bambusa spp., Phyllostachys spp., Sasa sp.) (Suh and Hodges 2007, García-Morales et al. 2016, Malumphy and Salisbury 2016, Suh 2020)	Sap-sucking
Kuwanaspis howardi (Cooley, 1898)	Arundinaria, Bambusa spp., Fargesia nitida, Phyllostachys spp. (Suh and Hodges 2007, García-Morales et al. 2016, Malumphy and Salisbury 2016, Suh 2020)	Sap-sucking
Kuwanaspis pseudoleucaspis (Kuwana, 1902)	Arundinaria spp., Bambusa, Drepanostachyum, Fargesia, Himalayacalamus, Phyllostachys spp., Pleioblastus, Pseudosasa japonica, Sasa spp., Semiarundinaria, Sinobambusa spp. (Suh and Hodges 2007, García-Morales et al. 2016, Suh 2020)	Sap-sucking
Odonaspis secreta (Cockerell, 1896)	Arundinaria, Phyllostachys spp., Pseudosasa, Sasa spp. (Suh and Hodges 2007, Kang et al. 2008, Suh 2020)	Sap-sucking
Unachionaspis tenuis (Maskell, 1897)	Arundinaria simonii, Bambusa, Phyllostachys spp., Pleioblastus, Sasa, Shibataea spp. (Suh and Hodges 2007, García-Morales et al. 2016, Suh 2020)	Sap-sucking
Eriococcidae
Acanthococcus onukii (Kuwana, 1902)	Bambusa, Phyllostachys nigra, Pseudosasa, Sasa (García-Morales et al. 2016, Suh 2020)	Sap-sucking
Miridae
Erimiris tenuicornis Miyamoto & Hasegawa, 1967	Sasa sp. (Kerzhner 1988, Ahn et al. 2018)	Sap-sucking
Pentatomidae
Aenaria lewisi (Scott, 1874)	Bamboo (Yasunaga et al. 1993)	Sap-sucking
Brachymna tenuis Stål, 1861 (new record)	Bamboos (Phyllostachys, Semiarundinaria) (Huang and Liu 2006, Zhao et al. 2006, Shu and Wang 2015, Zhang and Zuo 2015)	Sap-sucking (Shu and Wang 2015)
Pseudococcidae
Antonina crawi Cockerell, 1900	Arundinaria spp., Bambusa, Indocalamus herklotsii, Phyllostachys spp., Pleioblastus, Pseudosasa spp., Sasa spp., Semiarundinaria fastuosa (García-Morales et al. 2016, Suh 2020)	Sap-sucking
Antonina nakaharai Williams & Miller, 2002	Arundinaria simonii, Phyllostachys spp. (Lee and Suh 2011, Suh 2020)	Sap-sucking
Brevennia pulveraria (Newstead, 1892)	Sasa (García-Morales et al. 2016)	Sap-sucking
Trionymus hamberdi (Borchsenius, 1949)	Various bamboos including Pseudosasa japonica (Li et al. 2014, Ülgentürk et al. 2014, García-Morales et al. 2016, Suh 2020)	Sap-sucking
Palmicultor lumpurensis (Takahashi, 1951)	Various bamboos (Li et al. 2014, Ülgentürk et al. 2014, García-Morales et al. 2016)	Sap-sucking
Pseudococcus comstocki (Kuwana, 1902)	Sasa borealis (García-Morales et al. 2016, Suh 2020)	Sap-sucking
HYMENOPTERA
Tenthredinidae
Tenthredo nigropicta (Smith, 1874)	Pleioblastus spp. (Shinohara and Ibuki 2018)	Defoliator (Shinohara and Ibuki 2018)
LEPIDOPTERA
Crambidae
Circobotys aurealis (Leech, 1889)	Bambusa spp., Phyllostachys spp., Pleioblastus spp. (Haoje et al. 2002)	Leaf-roller (Shu and Wang 2015)
Crypsiptya coclesalis (Walker, 1859) (not confirmed)	Arundinaria, Bambusa spp., Dendrocalamus spp., Kinabaluchloa wrayi, Phyllostachys spp., Schizostachyum pergracile, Thyrsostachys oliveri (Sibuea et al. 2020)	Leaf-roller (Sibuea et al. 2020)
Demobotys pervulgalis (Hampson, 1913)	Bamboo (Shu and Wang 2015)	Leaf-roller (Shu and Wang 2015)
Sinibotys butleri (South, 1901)	Phyllostachys spp. (Lee et al. 2019)	Possibly leaf-roller (not confirmed)
Sinibotys evenoralis (Walker, 1859)	Bambusa spp., Phyllostachys spp., Pleioblastus spp. (Kim and Lee 1986, Haoje et al. 2002, Robinson et al. 2010)	Leaf-roller (Kim and Lee 1986)
Erebidae
Amata germana Felder, 1862	Bamboo (Kishida 2011b)	Probably defoliator
Rivula aequialis (Walker, 1863)	Bamboo (Kononenko and Pinratana 2013)	Probably defoliator
Rivula sericealis (Scopoli, 1763)	Bamboo (Kishida 2011b)	Probably defoliator
Lasiocampidae
Euthrix albomaculata (Bremer, 1861)	Bamboo (Robinson et al. 2010, Kishida 2011a)	Probably defoliator
Noctuidae
Bambusiphila vulgaris (Butler, 1886)	Bamboos; Phyllostachys aurea, Pleioblastus hindsii (Yoshimatsu et al. 2005, Kang et al. 2008)	Bamboo-shoot cutworm (Hill 2008, Kang et al. 2008)
Triphaenopsis jezoensis Sugi, 1962	Dwarf bamboo (Keiko et al. 2012)	Florivory, larvae feeding spikelets and caryopses (Keiko et al. 2012)
Triphaenopsis lucilla Butler, 1878	Bamboo (Sugi 1987, Choi 2008)	Probably defoliator
Notodontidae
Mimopydna pallida (Butler, 1877)	Sasa (Robinson et al. 2010)	Probably defoliator
Zygaenidae
Artona martini Efetov, 1997	Bamboos (Byun et al. 2010, Marianelli et al. 2020)	Defoliator (Byun et al. 2010)
Balataea gracilis (Walker, 1865)	Bamboo (Hirowatari et al. 2013)	Probably defoliator
Balataea octomaculata (Bremer, 1861)	Bamboo (Hirowatari et al. 2013)	Probably defoliator
Fuscartona funeralis (Butler, 1879)	Bamboos (Kang et al. 2008, Hirowatari et al. 2013)	Defoliator (Kang et al. 2008)
ORTHOPTERA
Tettigoniidae
Conocephalus bambusanus Ingrisch, 1990	Pseudosasa spp. (Kim and Kim 2002)	Probably defoliator
Palaeoagraecia lutea (Matsumura & Shiraki, 1908)	Pseudosasa (Kim and Lee 2019)	Probably defoliator

The invasive stink bug was identified as Stål, 1861 (: : ) that is recorded in South Korea for the first time (Figs 1, 2). It is one of the most important pest species feeding on bamboo branch and culm. A heavy infestation may cause defoliation, wilting of young shoots and branches and even death of the culm (Shu and Wang 2015). The species is polyphagous and is reported from various bamboo species in South Korea, for example, McClure and (Rendle) T.H.Wen (). Sometimes, it feeds also on Andersson (). Numerous adults and nymphs were observed on planted bamboos in the urban areas of Korean southern provinces. The species was also observed in Busan-si, Gwangyang-si and Yeosu-si without detailed collection data (Fig. 3).

Figure 3.

Map showing the distribution of in South Korea.

Discussion

In East Asia, is widespread in many tropical and subtropical Chinese Provinces (Anhui, Fujian, Guangdong, Guizhou, Henan, Hong Kong, Hubei, Hunan, Jiangsu, Jiangxi, Sichuan, Yunnan and Zhejiang) (Hoffmann 1932, Hsiao and Zheng 1977, Rider et al. 2002, Aukema and Rieger 2006, Huang and Liu 2006, Zhao et al. 2006, Zhang et al. 2008, Zhang and Zuo 2015) and it has been reported from subtropical Japanese Prefectures (Ryukyu, Oita and Yamaguchi) (Aukema and Rieger 2006, Tanaka 2013, Tanaka 2014, Igasaki 2016, Igasaki 2017, Igasaki 2018, Kanetada 2017) and Taiwan (Taiwan Encyclopedia of Life 2018). In Japan, after the first observation of the species in 1997 (Ishikawa et al. 2012), recent range expansion to the north and abnormal outbreaks have been observed (Tanaka 2013, Tanaka 2014, Igasaki 2017, Igasaki 2018). In South Korea, it was first found in 2020 on planted bamboos in the southern provinces (present paper). Since 2010, the first three authors carried out extensive field monitoring research mainly on terrestrial , but they had not seen any species before. As the adults of the species have been found along with numerous nymphs in restricted areas, we concluded that the species was very recently introduced and established into the country. Little is known about the viability and host plant usage of the species in South Korea. More attention is required in order to limit the further spread of the pest species.