https://orcid.org/0009-0001-1078-7463
Abstract
Icerya seychellarum (Westwood, 1855) (Hemiptera: Monophlebidae) is found in most tropical and subtropical regions worldwide and is a highly polyphagous pest that affects more than 140 genera of host plants. In 2023, I. seychellarum was discovered for the first time in Seogwipo-si, Jeju Island, South Korea. The specimen was found in heavily infested Cycas revoluta. Here, we provide information regarding the associated host damage, a description of the species, and details of sampling locations. The discovery of I. seychellarum is of agricultural and quarantine importance in South Korea; therefore, this study presents an opportunity to investigate new strategies geared toward advancing efforts to detect and eliminate threats in the future.
Scale insects (Hemiptera: Sternorrhyncha: Coccoidea) are an economically important group of sap-sucking phytophages with approximately 8,000 described species worldwide (García Morales et al. 2016). Several scale insects are pests, particularly those feeding on fruit trees, woody ornamentals, and shrubs. Scale insects damage fruits and leaves by covering plants with their waxy secretions, which favor the growth of sooty molds. Visible symptoms include leaf loss and dwarfing, and heavy infestation can lead to host plant death. The economic losses caused by scale insects have been estimated to exceed 500 million USD per year in the United States (Kosztarab and Kozár 2012). In addition, some scale insects are invasive with strong adaptability to new environments and can cause serious economic damage when they colonize a new region. Among the 255 species introduced to the United States, approximately 75% are considered serious pests (Miller et al. 2005).
The genus Icerya Signoret (Monophlebidae: Monophlebinae) comprises 38 described species worldwide (García Morales et al. 2016). Some Icerya species have proliferated and become serious pests that invade new areas because of the absence of natural predators (Kondo et al. 2016). For example, Icerya purchasi Maskell is native to Australia and New Zealand and causes damage to 213 genera of host plants (García Morales et al. 2016, Kollár et al. 2016). This pest has been introduced in 150 countries and has caused enormous damage (García Morales et al. 2016). In the United States, I. purchasi was introduced to California with Acacia latifolia in 1868 and has since caused significant damage to citrus groves in the south (DeBach 1974).
Icerya seychellarum (Westwood) is a phloem-feeding, honeydew-secreting insect that is an important economic pest of several crops and ornamental plants, including grapes, mangoes, kaki, avocado, guava, citrus, palm, rose, and chestnut trees (García Morales et al. 2016). This species was described by Westwood (1855) from Seychelles and has been recorded in 69 countries (García Morales et al. 2016, Giliomee and Millar 2019, Kondo and Watson 2022). Until now, I. seychellarum was known to attack 166 host plant genera belonging to 63 families (García Morales et al. 2016). In particular, I. seychellarum is considered a serious threat to citrus (Lever 1946). Plants infested with I. seychellarum have significantly reduced growth and can die if the infestation is heavy (Newbery 1980). Because of the damage potential of I. seychellarum, this species is included in the Alert List of the North Atlantic Plant Protection Organization (NAPPO) and is listed as a potentially invasive species in the United States, the Caribbean Basin (Evans and Dooley 2013), and a quarantine insect pest in South Korea (Suh et al. 2013).
In this study, we report the detection of Icerya seychellarum on Jeju Island, South Korea. It is the largest island in Korea and is situated approximately 86 km from the Korean Peninsula. Jeju Island has subtropical climate and is therefore an important region for subtropical fruit cultivation. However, because of the different climates on the island, several invasive species in Korea are detected here first. After the initial detection of invasive species on Jeju Island, some species spread to the mainland. For example, Frankliniella occidentalis (Pergande) and Thrips palmi Karny (Thysanoptera: Thripidae) were first discovered on Jeju Island in 1993 and have now spread to most regions of Korea (Ahn et al. 1994, Woo et al. 1994, Hong et al. 1998). This suggests that I. seychellarum may also possibly spread to the Korean Peninsula and needs to be urgently controlled.
First Observation, Sample Collection, Field Survey
On 30 August 2023, Icerya seychellarum was first detected on Jeju Island, South Korea. It was collected on sago palm, Cycas revoluta, in Donghong-dong, Seogwipo-si (Site 1, GPS: 33°14’39”N, 126°34’27”E) and Hahyo-dong, Seogwipo-si (Site 2, GPS: 33°14’51”N, 126°37’05”E) (Fig. 1). Live I. seychellarum still had intact wax, which was photographically recorded (Fig. 2). Colonies of I. seychellarum are usually found on the underside of leaves or stems (Fig. 2A). Cycas revoluta at Seogwipo-si were particularly heavily infested with I. seychellarum. These pests damage plants by inserting needle-like mouthparts into plant tissues and sucking plant sap from the phloem. The direct damage caused by sap-sucking pests to C. revoluta includes leaf yellowing, general wilting, and browning (Fig. 2C and D). In addition, we surveyed several other cycad species present in the area, but no I. seychellarum was observed on these plants.
Map of collection sites in Jeju Island, South Korea, produced using QGIS v3.32.3.
A) Wide view of a heavy infestation of Icerya seychellarum on Cycas revoluta, B) adult female on Cycas leaf, and C and D) slightly infested plant, showing yellowing of needles of a Cycas leaf.
To morphologically identify these giant scales, collected samples were placed in tubes containing 90% ethyl alcohol and stored at −70 °C. The identification of scale insects was based on the morphology of slide-mounted adult females. Before making the slide-mounted specimens, samples were still in 90% ethyl alcohol punctured behind its marginal body segment with a needle or surgery scissors and were placed in 10% potassium hydroxide (KOH) solution for 30 min or 1 h at 70 °C. If body contents did not become transparent, it was gently pumped and carefully teased out the guts of insect using a spatula. The samples were then placed in distilled water for 5−10 min, and a few drops of the stain were added to distilled water and incubated for 5 min (Miller and Davidson 2005). Adult females were identified using the method described by Unruh and Gullan (2008). Permanent slides of adult females were deposited at the Institute of Agriculture Life Science, Gyeongsang National University, Jinju, South Korea.
Morphological Description of Icerya seychellarum
Field diagnostic characters: Adult females are elliptical with dark orange to almost light red bodies following clearing. Antennae, eyes, and legs are black. Its dorsum is covered with a thick layer of white and often yellowish wax, with distinct secreted wax tufts around margin (Fig. 2B), and occurs on leaves of host plants. Microscopic slide mounting characters: In slide-mounted specimens, the adult female is elliptical (Fig. 3A), its body length is 3.8−4.7 mm, width 2.6−3.2 mm, antennae 11-segmented (Fig. 3B), and mouthparts and thoracic spiracles are well developed. Abdominal spiracles are arranged in 3 pairs toward lateral areas of abdominal segments (Fig. 3D). Flagellate setae occur along the body margin, with thin ovisac bands. Three rounded cicatrices are posterior to the vulva (Fig. 3C). The vulva opening is surrounded by small multilocular pores and robust hair-like setae. Open-centered pores, each 13−18 µm in diameter, are usually present around body margin and on dorsum, and each pore has 14−16 outer loculi and small triangular cleft on inner margin (Fig. 3E). Multilocular pores, each 8−11 µm in diameter with bilocular center and 9−11 outer loculi, were irregularly scattered on the dermis.
Icerya seychellarum, stereomicroscope images (the slide accession number: GNU230830000251). A) Body, B) antennae, C) cicatrices, D) abdominal spiracle, and E) open-centered pores. Scale lines. A = 1 mm; B = 500 µm; C = 100 µm; D and E = 50 µm.
Economic Importance of Icerya seychellarum and Future Efforts
To date, Icerya seychellarum has been recorded in 69 countries in Africa, Asia, Southeast Asia, Southern Europe, South America, and Australia (García Morales et al. 2016). Recently, this species was also reported in Italy (Lo Verde et al. 2020).
Jeju Island is an area optimized for the commercial cultivation of tropical and subtropical plants, such as guava, avocado, and mango. It is also the most important area in Korea for commercial citrus production. As we found I. seychellarum on the island, this pest has great potential to be of economic importance to several crops and horticultural plants here, especially considering its polyphagous feeding habits. This species could have serious impacts on the crop-growing and horticultural industries, as well as the native flora of Jeju Island. Icerya seychellarum has been reported as a citrus pest on Vanuatu, an island in the South Pacific Ocean (Williams and Butcher 1987), suggesting that I. seychellarum could cause economic damage to citrus trees in South Korea.
The increasing number of invasive insects introduced into new geographic regions is strongly related to international trade, mainly of live plants. This is particularly true for scale insects, whose characteristics, such as size and life habits, make them difficult to detect during regular quarantine inspections of imported trees, ornamentals, and fruits. In South Korea, I. seychellarum was detected only once (from an unknown plant from China) during quarantine inspections between 2011 and 2017 (Suh et al. 2013); however, I. seychellarum were not found afterward. Here we report a fully established population of I. seychellarum in the open landscape in Korea at 2 different locations approximately 4 km apart (straight-line distance). It is currently unknown whether these insect scales were introduced only once and spread or whether 2 independent introduction events occurred. Future studies on population genetics are warranted to determine the source of introduction and whether these 2 populations are genetically identical.
In Korea, several reports have indicated that invasive pests detected on Jeju Island for the first time tend to spread to the mainland over time (e.g., F. occidentalis and T. palmi) (Ahn et al. 1994, Woo et al. 1994, Hong et al. 1998). Therefore, an integrated pest management program is required. To prevent the settlement and spread of I. seychellarum, it must be monitored on a regular basis, starting from nearby areas, to prevent further spread and potential economic and environmental damage. Currently, active monitoring and pesticide treatment are the most reliable control strategies. In addition, a biological control program can be implemented in the future. Natural enemies of I. seychellarum include Rodolia cardinalis (Mulsant), Rodolia limbata Blackburn, and R. pumila Weise (Coleoptera: Coccinellidae), Cryptochaetum iceryae (Williston) (Diptera: Cryptochetidae), and a few wasp species (Kondo et al. 2016). Among its previously reported natural enemies, R. cardinalis is currently distributed in Korea, so R. cardinalis can potentially be used as a biological control agent for I. seychellarum, although this requires further investigation through efficacy studies.
Diagnostics of scale insects are difficult and of limited use to non-experts, especially for imperfectly preserved specimens (Hardy 2013). Consequently, it is necessary to develop appropriate management strategies ahead of quarantine to assist in preventing large-scale insect invasions into uninfested regions. To solve this problem, a domestic quarantine program is necessary to prevent the further spread of I. seychellarum across the Korean Peninsula. Until now, there has been no domestic quarantine program for commodities or ornamental trees between Jeju Island and mainland Korea. The rigorous quarantine program followed in Hawaii might be a good model to prevent the introduction and spread of invasive species (Krausa and Duffy 2010). Researchers and inspectors involved in plant quarantine must conduct thorough regulatory inspections of imported plants and (sub)tropical plants to prevent the introduction of unwanted pests to the mainland.
In future studies, it will be crucial to conduct surveys to assess the current distribution, extent, and density of I. seychellarum, accompanied by thorough ecological studies examining the larval feeding habits, damage symptoms, and other potential host plants in South Korea. Furthermore, the Jeju population should be identified through a comprehensive sampling of I. seychellarum from several countries and evaluation using genetic markers.
Acknowledgments
This research was also supported by a grant from the Nakdonggang National Institute of Biological Resources (NNIBR), funded by the Ministry of Environment (MOE) of the Republic of Korea (NNIBR20241204).
Data Availability
All data analyzed and generated from this study are available upon written request from the corresponding author, Wonhoon Lee.
Author Contributions
Hyeongsu Kim (Conceptualization [equal], Data curation [equal], Formal analysis [equal], Visualization [equal], Writing—original draft [equal], Writing—review & editing [equal]), Sang-Bin Lee (Data curation [equal], Formal analysis [equal]), and Wonhoon Lee (Conceptualization [equal], Formal analysis [equal], Project administration [equal], Supervision [equal], Writing—original draft [equal], Writing—review & editing [equal])
