Establishment of non-native Anoplophora horsfieldii (Coleoptera: Cerambycidae) in South Korea

Abstract

The longhorned beetles (Coleoptera: Cerambycidae) contain many invasive alien species that spread through lumber, wood packing material, and ornamental plants, causing tremendous threats to agriculture and forestry in countries where they introduced (Eyre and Haack 2017, Wu et al. 2017). Among them, the genus Anoplophora is widely recognized in pest science due to 2 highly invasive alien species (IASs): the Asian longhorned beetle (ALB: Anoplophora glabripennis (Motschulsky, 1854)) and citrus longhorned beetle (CLB: Anoplophora chinensis (Forster, 1771)) (Haack et al. 2010; Eyre and Haack 2017). Both species have caused significant global economic losses after being introduced outside of their native ranges. For example, $373 million was spent from 1997 to 2008 for the eradication of ALB in the United States, while $3 million was spent from 2001 to 2008 to monitor and control CLB in Europe (Haack et al. 2010). On the other hand, other species of Anoplophora have been largely overlooked in pest science until now because of their moderate population levels in the native range and the absence of interception or establishment records. However, there has always been a considerable possibility of an outbreak or invasion of another Anoplophora congener, given that many new IAS cerambycids are emerging because of the recent increase in global trade and climate change (e.g., Aromia bungii (Faldermann, 1835) (Lee et al. 2021, Tamura and Shoda-Kagaya 2022), Trichoferus campestris (Faldermann, 1835) (Grebennikov et al. 2010, Bullas-Appleton et al. 2014)). Furthermore, many Anoplophora species generally attack living trees and are known to utilize multiple host species, with some hosts being highly susceptible to infestation (Lingafelter and Hoebeke 2002; Haack et al. 2010). Therefore, any Anoplophora species’ invasion may cause significant damage to the invaded area.

However, despite the potential significance of many Anoplophora species, their detailed biology remains poorly understood and only a few representative species have been thoroughly investigated (e.g., Haack et al. 2010). One such species is Anoplophora horsfieldii (Hope, 1843), which has a wide distribution across China and the Indochina Peninsula, including India, Laos, Taiwan, Thailand, and Vietnam (Barševskis et al. 2022). Adult beetles of A. horsfieldii are diurnal, and their peak activity has been observed during different periods across their range (May–July in Taiwan, July–August in southeast China; Lingafelter and Hoebeke 2002). Anoplophora horsfieldii attack various living trees, including Camellia oleifera Abel, 1818, Camellia sinensis (Linnaeus) Kuntze, 1887, Celtis spp., Melia azedarach Linnaeus, 1753, Quercus glauca Thunberg, 1784, and Ulmus pumila Linnaeus, 1753 (Gressit 1942, 1951, Hua et al. 1993, Lingafelter and Hoebeke 2002, Chou 2004, Tavakilian and Chevillotte 2021). These beetles are distinguishable from other species by their 4 yellow transverse bands on the elytra (Lingafelter and Hoebeke 2002).

In this study, we report the third non-native species of the genus Anoplophora based on the establishment of A. horsfieldii (Fig. 1) on Jeju Island, South Korea. Jeju Island is the largest island located in the southernmost part of South Korea, covering an area of approximately 1,800 km² (central GPS: 33°23′N, 126°34′E) (Woo et al. 2013). It is 90 km away from the Korean peninsula and was formed by volcanic eruptions during the Pleistocene epoch (Woo et al. 2013). Due to its unique subtropical climate and geographical location, Jeju Island is an ideal habitat for various tropical pests, serving as an intermediate bridge for their spread into the mainland. Several invasive insects, including Spodoptera frugiperda (Smith, 1797) (Lepidoptera: Noctuidae), Frankliniella occidentalis (Pergande, 1895) (Thysanoptera: Thripidae), and Thrips palmi Karny, 1925 (Thysanoptera: Thripidae), were first discovered on the island before spreading to the mainland (Ahn 1994, Lee et al. 2020). Additionally, in the case of the oriental fruit fly, Bactrocera dorsalis (Hendel 1912) (Diptera: Tephritidae), it has the potential to be introduced to Jeju Island from tropical regions, rather than mainland South Korea, highlighting Jeju island’s role as a hub for the influx of tropical pests (Kim and Kim 2018).

Fig. 1.

Habitus of Anoplophora horsfieldii, scale bar = 10 mm. A) Male dorsal view. B) Female dorsal view. C) Female ventral view.

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First Observation, Sample Collection, and Field Survey

Anoplophora horsfieldii was first discovered on Jeju Island in September 2019. A photograph of an A. horsfieldii collected on the road in Yongdam-dong, Jeju-si (red dot in Fig. 2A, GPS: 33°30′N, 126°30′E) was uploaded to a beetle hobbyists’ website that same month (see Supplementary Appendix S1), and the specimen was subsequently sent to the authors. Two weeks after the initial discovery, we conducted surveys near the collection site and a distant location, but we were unable to find any beetles or signs of infestation. In July 2022, another photograph of an A. horsfieldii was posted on a nonentomological online community (see Supplementary Appendix S1). We were able to find the beetles at the precise location where the photograph was taken (Yongyeon Valley, marked in yellow in Fig. 2A) and confirmed their establishment by observing multiple exit holes in Celtis sinensis Persoon, 1805. These exit holes are circular and have a diameter greater than 15 mm in living trees. Among the large woodboring beetles that inhabit Jeju Island, Chrysochroa coreana Han and Park, 2012 (Buprestidae) and Anoplophora chinensis utilize Ce. sinensis (Jung 2019). However, C. coreana produces elliptical-shaped exit holes and primarily infests dead trees (Kwon 2013), while A. chinensis creates round exit holes, but they are typically smaller than the ones we observed (Anderson et al. 2016) and tend to occur in the tree trunk or roots (Haack et al. 2010). We also surveyed 8 sites, including Yongyeon Valley, to confirm the distributional range. We evaluated the establishment by collecting multiple beetles and observing exit holes and ovipositing females on the hackberry tree Ce. sinensis. We searched for survey sites near the original discovery site using the Korean terms “팽나무 (Celtis sinensis)” and “제주도 (Jeju island)” and confirmed the presence of Ce. sinensis through Google Maps and Street View. As a result of observing all individuals exclusively on Ce. sinensis in the first field survey, our subsequent field survey was specifically focused on this species, while also encompassing a search for beetles on other tree species in the survey sites.

Fig. 2.

A) Graphical summary of field survey. The numbers correspond to “No.” in Supplementary Appendix S2. B) Female ovipositing on Celtis sinensis. C) A. horsfieldii on its host, Celtis sinensis. D) Exit holes of A. horsfieldii.

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Among the 8 surveyed sites, all 30 beetles were found over the last 3 yr only within a small district, the Yongyeon Valley, and adjacent areas. In Yongyeon Valley, exit holes were found on 32 Ce. sinensis, of which 4 were partly or totally withered, possibly due to extensive larval feeding activities that can be presumed from numerous exit holes (Fig. 2D). Other symptoms seen from the outside, such as piles of sawdust-like frass from the larval tunnel, loosened or scraped bark, sap, and frass flow from oviposition pits, and adult feeding damage to branches and shoots, are far less evident than those of A. glabripennis or A. chinensis (Haack et al. 2010). No beetles were found at sites other than the Yongyeon Valley, but we found one exit hole, which is likely to be A. horsfieldii (Fig. 2D), upstream of Yongyeon Valley (orange dot in Fig. 2A, GPS: 33°30′24′′N, 126°30′41′′E). Although a few Melia azedarach trees were present in the Yongyeon Valley, which are also recognized hosts for A. horsfieldii, our observations did not reveal any exit holes, adult beetles, or oviposition pits on these trees. Additionally, we also surveyed several other tree species present in the area, including Ailanthus altissima (Mill.) Swingle 1916 (Simaroubaceae), Morus alba Linnaeus, 1753 (Moraceae), and Zelkova serrata (Thunb.) Makino, 1903 (Ulmaceae), but did not observe any A. horsfieldii on these trees either. Detailed survey dates, surveyors, and number of beetles observed and collected, and remarks are provided in Fig. 2A and Supplementary Appendix S2.

Importance and Future Concerns

Anoplophora horsfieldii can be considered to be non-native to South Korea in that (i) the known distribution of the species is restricted to Southeast Asia, (ii) the sizable beetle has never been observed in such a famous tourist attraction, and (iii) the current distribution appears to be restricted to a small district located between the island’s largest port and airport.

Given the long life cycle of other Anoplophora congeners (generally 1–2 yr: Lingafelter and Hoebeke 2002; Haack et al. 2010), A. horsfieldii may have been established in Jeju at least a few years before the first detection to reach a population level that is high enough to be accidentally found by a random citizen, similar to ALB in the United States (see Crooks 2005, Carter et al. 2009). Based on the presence of old exit holes and observations of the numerous beetle in Yongyeon Valley, it is likely that at least 2 or more generations of the beetle have passed. Therefore, the first invasion appears to have occurred at the latest before 2015. This species appears to be in the early stages of invasion, providing an opportunity for assessment of its potential impact on the island and the development of a management plan before it disperses widely and poses tremendous damage.

There is a large possibility that the population may disperse within the island or serve as a source of colonists for remote new territories. As Ce. sinensis is abundantly distributed in the lowlands of Jeju Island (Lim 2012) and the dispersal of IAS largely depends on the presence and abundance of their host plants (Dethier 1959, Harrison 1994, Canelles et al. 2021), A. horsfieldii may disperse faster than other IAS on Jeju Island. Furthermore, the beetle may disperse to the mainland Korean Peninsula because Ce. sinensis is a common ornamental tree raised on Jeju Island and transplanted to the mainland of the Korean Peninsula. There is also a high risk that the beetle could be inadvertently introduced to the South Korean mainland peninsula through the unintentional release of collected individuals by beetle enthusiasts. All A. horsfieldii found on Jeju Island until now have been associated with Ce. sinensis, but they have also been known to infest other host plants from different families (Lingafelter and Hoebeke 2002, Chou 2004, Tavakilian and Chevillotte 2021). Among them, the plantation of C. sinensis on Jeju Island can be threatened by the dispersal of this non-native species, as the island accounts for approximately 40% of the total tea production in South Korea (MAFRA 2020).

To prevent this newly introduced non-native species from dispersing, continuous monitoring and surveillance activities are essential to guarantee rapid response actions and implement governmental measures. In future studies, it is crucial to conduct surveys that assess the current distribution, extent, and density of A. horsfieldii, accompanied by thorough ecological studies examining larval feeding habits, damage symptoms, and other potential host trees utilized in South Korea. Furthermore, the non-native origin of the Jeju population should be identified through comprehensive sampling of A. horsfieldii from various regions in Southeast Asia and using a high-resolution genetic marker, such as single-nucleotide polymorphism or microsatellite.

Acknowledgments

This study was carried out with the support of R&D Program for Forest Science Technology (Project No. FTIS2017042B10-2223-CA01), provided by Korea Forest Service (Korea Forestry Promotion Institute) and Basic Science Research Program through the National Research Foundation of Korea (NRF), funded by the Ministry of Education (NRF2020R1I1A2069484). This work was also supported by the Animal and Plant Quarantine Agency (Project No. PQ20170B013).

Author Contributions

Seunghyun Lee (Conceptualization-Equal, Data curation-Equal, Formal analysis-Equal, Investigation-Equal, Methodology-Equal, Project administration-Equal, Resources-Equal, Validation-Equal, Visualization-Equal, Writing – original draft-Equal, Writing – review & editing-Equal), Junhyeong Choi (Conceptualization-Equal, Data curation-Equal, Investigation-Equal, Resources-Equal, Writing – original draft-Equal, Writing – review & editing-Equal), Hyunkyu Jang (Conceptualization-Equal, Investigation-Equal, Resources-Equal, Visualization-Equal, Writing – original draft-Equal), Woong Choi (Conceptualization-Equal, Investigation-Equal, Resources-Equal, Visualization-Equal), Woochan Kwon (Conceptualization-Equal, Investigation-Equal, Resources-Equal, Writing – review & editing-Equal), Do-yoon Kim (Conceptualization-Equal, Investigation-Equal, Resources-Equal, Writing – review & editing-Equal), Jaedong Gim (Conceptualization-Equal, Investigation-Equal, Resources-Equal, Writing – review & editing-Equal), Jonghyun Park (Conceptualization-Equal, Investigation-Equal, Resources-Equal, Writing – review & editing-Equal), Sangwook Park (Conceptualization-Equal, Investigation-Equal, Resources-Equal, Supervision-Equal, Writing – review & editing-Equal), Sangil Kim (Resources-Equal, Writing – original draft-Equal, Writing – review & editing-Equal), Seunggwan Shin (Resources-Equal, Supervision-Equal, Writing – review & editing-Equal), Seunghwan Lee (Conceptualization-Equal, Funding acquisition-Equal, Resources-Equal, Supervision-Equal, Writing – original draft-Equal, Writing – review & editing-Equal)

References

Author notes