The introduction of foreign pests into a country can disturb the biological ecosystem and cause damage to the native plants economically. It will impose a tremendous amount of time and cost for monitoring, control and management of the imported pest. Except for the northern side and land borders with China and Russia, the Korean peninsula is surrounded on all three sides by sea. This geographic location has caused the sharing of numerous indigenous insect species between Korea and neighboring areas for some time. However, until the beginning of the Greater Korean Empire Era in 1897, the introduction of alien insects from other regions was restricted. Since then, international trade with other continents has increased dramatically (Hong et al., 2012). Countries all over the world are enforcing quarantine to prevent pests from spreading through imported plants. Plant quarantine aims to reduce the economic impact of alien pests invaded from other countries on the agricultural and forestry industries. In December 1961, the Korean government enacted the Plant Protection Act, which was later revised in December 1995 in accordance with the WTO/SPS Agreement (Hong et al., 2012). Quarantine system of Korea, alien insect species are categorized into 3 groups: non-quarantine pests, provisional regulated pests, and regulated pests, which are divided into two groups: quarantine and nonquarantine regulated pests. Quarantine regulated pests are also included in the prohibited and managed pests (Fig. 1A).

According to the Plant Protection Act, plant quarantine regulations have become stricter in Korea. Nevertheless, alien species continue to enter Korea via different routes and intrude on Korea's insect fauna (Hong et al., 2012). In recent decades, the world has entered a new phase in terms of the amount and diversity of biological invasions due to economic growth and improved transportation (Hulme, 2009). Biological invasion is becoming more likely as demand for foreign fresh foods (fruits and vegetables) and ornamental products (cut flowers and plants for planting) increases. While most alien mammals, reptiles and fishes have been deliberately introduced into Korea (Park et al., 1998), alien insects except for intentionally introduced natural enemies, have been introduced accidentally or unintentionally. Many alien insect species are thought to be unintentionally introduced into Korea via seaports, airports, imported cargo, and inanimate pathways (Toy and Newfiel, 2010), such as passenger baggage, containers, used vehicles, or ships, since the Korean economy is strongly sustained by international trade. Pest invasions and interceptions from imported agricultural commodities have increased considerably each year (Lee et al., 2016).

In Korea, the annual rate of pest invasion and pest interceptions from imported agricultural items has risen dramatically (Lee et al., 2016). An alien species is an individual or population, at any life stage, or a viable part of an organism which is not indigenous to an area and has entered into that area by human interference. An invasive alien species is one that has become injurious to plants, or is potentially harmful to plants based on risk analysis (FAO, 2010). In other words, when the abundance and distribution of a nonnative organism exceeds a defined and accepted environmental criterion, resulting in a net negative effect on social welfare, the term invasive alien species is used. One of the most serious threats to the environment and food production is invasive alien species (Cook et al., 2010). Kiritani (2003) identified three factors that exacerbate the problem of invading alien species: first, changes in environmental factors are occurring at a rate and scale that has never been seen before. Second, the effects of biological invasions are extremely difficult to predict. Finally, biological invasions result in faunal homogeneity and biodiversity loss. Invasive species have also been identified as a serious danger to biological diversity across the world, with the potential to disrupt ecological systems, homogenize biota, and even lead to extinction (SCOPE, 1996). Until 2011, a total of 170 insect species were considered exotic insect pests in Korea, with alien being defined as a species imported to Korea after the commencement of the Greater Korean Empire Era when Korea opened its doors to foreign countries (Hong et al., 2012). Until the 1990s, the majority of exotic insect pests were first discovered in Japan, then found in Korea, but this pattern reversed in the 2000s (Hong et al., 2012). Identifying the possible risk of exotic insect pests entering and establishing in a region is an important part of biosecurity risk assessments and emergency preparedness (Caley et al., 2015).

In this study, we focused on the insects belonging to different orders, which were detected in imported cut flowers at the Korean borders over the last 25 years (1996 to 2020). Based on available literature and the Pest Information System (PIS) database compiled by the Animal and Plant Quarantine Agency, a total of 13,757 detection records (467 species) containing insects, mites and mollusks were reported in Korea during 1996 to 2020. Over this period, 78 recorded species have been reported and confirmed as managed quarantine regulated pests in Korea. We analyzed the detection datasets according to orders, items and years and discussed the efficiency of the Korean plant quarantine systems in protecting against exotic insect pests entered in Korea by imported cut flowers.

Materials and Methods

The plant quarantine data on imported cut flowers was obtained from the PIS database, which is operated by the Animal and Plant Quarantine Agency in Korea and not to public (Fig. 1B). The PIS database contains that all records of detected pest species under the plant quarantine inspection on imported cut flowers during 1996 to 2020. We analyzed the PIS data by detected insect species, cut flower items, and exported countries. All insect data were transported and visualized in Excel 2010 program (Microsoft Korea, Seoul, Korea) with detection number of insects by cut flower items, by exporting countries, or by importing periods.

Results

Based on the PIS data, 147,160 cut flowers (159 items) are imported to Korea from 69 countries during 1996-2020 (25 years). Netherlands, Thailand, China, Columbia, South Africa, Japan, Australia, New Zealand, Malaysia and USA are the top ten source countries of imported cut flowers to Korea (Fig. 2A, Supplementary Table 1). During this period, Bigleaf hydrangea, Dendrobium, Canation, Tulip, Hyacinth, Amalis, Calla, Astilbe and Moskara orchid were the most popular imported cut flowers to Korea (Fig. 2B, Supplementary Table 2) and the highest number of cut flowers to detected pests in every 5 years (Fig. 3A).

A total of 467 species of insects have been detected in all imported cut flowers to Korea, with a total number of 13,757 detections for last 25 years. The majority of detected species were provisional regulated pests, and the greatest number of detections belonged to non-quarantine pests. 78 species with a total number of detections of 1,170 were categorized as managed pests (Table 1). Among the managed pests, ten species are more typically found in imported cut flowers from different countries. In other words, the species with a detection of less than ten times were ignored. Bemisia tabaci as the most detected a managed pest was found in imported Chrysanthemum, Gerbera, Sedum (Kirin-cho), Solidago (Goldenrod), Clematis, Rose, Lilium, Salal, Hydrangea, Euphorbia, Jasmine, and Trachelium, which came from China, Vietnam, Netherlands, Canada, Colombia, Japan, Israel, South Africa, Kenya, and New Zealand with a total number of detections of 841 (Table 2) and the most detected pests in imported cut flower items to Korea every 5 years (Fig. 3B). Fig. 4 shows the number of species intercepted in each of the 25 years, sort it by quarantine category. Non-quarantine pests had a peak during the early years of 1996 to 2020. Managed pests increased in number during 2003 to 2004, but rapidly decreased, and then increased again. The number of detected provisional regulated pests has consistently fluctuated over the years (Fig. 4). Fig. 5 reveals that Thysanopteran and Hemipteran species are major order, which are most detected under plant quarantine inspection during last 25 years. Total number of detections in Thysanoptera and Hemipteran are accounted for 6,800 as 49.4% and 4,631 as 33.6%, respectively. However, other insect orders including Lepidoptera, Coleoptera, Hymenoptera, and Diptera are relatively lower than two major orders. As a result, Thysanopteran and Hemipteran represented more than 80% of the major insect under plant quarantine inspection during last 25 years in Korea.

Discussion

According to the PIS, the source types of commodities are categorized into two groups: seeds, bulbs, and seedlings are classified as “planting materials,” whereas grains, fruits, vegetables, cut flowers, forage, medicinal herbs and spices, and woods are classified as “non-planting materials.” Lee et al. (2016) revealed that three commodities of seedlings, cut flowers, and forage were the primary pathways of invasion by exotic insect pests in Korea during 1996-2014. Pests detected in imported cut flowers during the years 1996-2020 were the subject of this investigation. Overall, during this period, 13,757 interception records belonging to 467 species and ten orders of Thysanoptera, Hemiptera, Lepidoptera, Coleoptera, Diptera, Hymenoptera, Orthoptera, Psocoptera, Collembola and Dermaptera were collected on imported cut flowers. From 1996 to 2020, Thysanoptera dominated, with the highest number of interceptions, 6,800, and Dermaptera revealed the lowest record of 1 interception. So far, the most common orders found on cut flowers in Korean quarantine borders have been Thysanoptera and Hemiptera. Bigleaf hydrangea, Tropical orchid and Dendrobium were the top host cut flowers for imported insects, according to the reported data. According to Hong et al. (2012), till 2011, a total of 170 insect species were proposed as invasive into Korea. These species belonged to ten orders of Blattaria, Embiidina, Isoptera, Psocoptera, Thysanoptera, Hemiptera, Coleoptera, Hymenoptera, Diptera, and Lepidoptera.

In this study, we found that ten most frequently intercepted species, Frankliniella schultzei (Trybom), F. fusca, F. williamsi Hood, Thrips australis, and Echinothrips americanus Morgan in Thysanoptera, Bemisia tabaci, Dysmicoccus brevipes, Pseudococcus longispinus, and Aspidiotus nerii, in Hemiptera and Tapinoma melanocephalum in Hymenoptera, which are categorized as quarantine pest in Korea. As a result, it should be noted that these imported pest species have the potential to establish in Korea, and most alien insect species now in Korea are known to have caused indirect and/or direct damage to agricultural crops such as Spodoptera frugiperda, Metcalfa pruinose, and Lycorma delicatula.

According to Lee et al. (2016), two factors can influence the capacity to establish in new habitats, which impacts the success rate of invasion. First, a unique agricultural environment (known as “greenhouse cultivation”) may offer greenhouse pests with an ecological island prone to invasion because of a lack of natural enemies. During the winter, the combination of short-day length and increased temperature provided in greenhouses provides ideal conditions for non-diapausing insects. Second, a single parthenogenetic female may successfully establish a colony in a newly invaded area without the need to find mates or suffer from inbreeding.

During the early years of 1996 to 2020, non-quarantine pests were the most commonly detected pests in imported cut flowers. However, as the number of non-quarantine pests reduced, some provisional regulated pests and also managed pests were detected in imported cut flowers. Increasing commerce combined with increased awareness, efficacy, skills, and detection effort by border officials can explain the trend (Nairn et al., 1996;Levine and D’Antonio, 2003;Waage and Mumford, 2008).

In this study, the Thysanopteran and Hemipteran had the largest number of interceptions among the ten orders. These species have cryptic life stages that require live plant material, which is a common feature of these orders. As a result, it is reasonable to assume that these species were the most often introduced pests using fresh plant materials. Live plant importation is a primary conduit for the introduction of exotic insect pests into the United States and Europe (Liebhold et al., 2012;Kenis et al., 2007). According to Lee et al. (2016), the detection ratio of insect pests in planting materials (especially seedlings) was substantially greater than in other items. As a conclusion, the findings of this study have proven the necessity of continual review of the efficacy and performance evaluation of inspection programs designed to prevent the introduction of exotic insect pests into Korea. We must consider how inspection data and accurate insect identification are essential and important in predicting the incursion risk by invasive species.