Introduction

A hitchhiker organism is temporarily associated with artificial structures or objects without forming a biological host relationship (Toy & Newfield, 2010). The red imported fire ant (Solenopsis invicta), detected in sea containers entering Korea, is a globally renowned hitchhiker insect pest (Ascunce et al., 2011; YNA, 2018). In a survey conducted over two years (2018~2019), a total of 1,141 individuals (439 species across 81 families of 12 orders) were detected in international vessels entering Korea, demonstrating high diversity among hitchhiker insect pests (Kang et al., 2023a). Such invasions, when occurring in large numbers or more frequently, are more likely to become established than those occurring in smaller numbers or less frequently (Lockwood et al., 2005; Johnston et al., 2009, Toy & Newfield, 2010). For instance, Melanoplus differentialis (Acrididae, Orthoptera), native to North America, was discovered to have established itself around Onsan Port, Korea, by 2020. It is highly probable that the species has continuously invaded since its initial detection in an international vessel entering Korea in 2018 (Kang et al., 2022).

The detection pattern of hitchhiker insects indicates that over 100 species have been detected annually since the commencement of the actual survey of international vessels entering Korea in 2018. Notably, 14 species (nine families of three orders) identified as not-distributed in Korea were found in 2018, 42 species (21 families of seven orders) in 2019, 26 species (21 families of six orders) in 2021, and 38 species (22 families of six orders) in 2022 (Kang et al., 2020, 2021, 2023b, 2024). Due to an increase in detection frequency, there is a growing necessity for long-term monitoring of insect pests hitchhiking on international vessels (Kang et al., 2023a). This study provides biological and hitchhiking data on not-distributed species in Korea detected from international vessels in 2023. Thus, the objectives of this study are to report the not-distributed species detected and identified in 2023 and provide their biological information, including taxonomic details, distribution, and inanimate pathway data.

Materials and Methods

Samples were collected by visually monitoring the corridor from the bow to the stern of international vessels entering Korean ports. A total of 562 samples consisting of both living and dead individuals were collected. Species identification began with DNA barcoding, followed by morphological re-examination of each individual. The DNA barcodes of the collected insects were compared using the BLAST search method in NCBI and the Identification Engine in the BOLD system ver. 4. Species identification for each sample was conducted using a 2% cutoff rule (Altschul et al., 1990; Hebert et al., 2003, 2004; Ratnasingham & Hebert, 2007). Molecular findings were re-assessed based on morphological characteristics at the para-taxonomic level. The identification results were checked against a website, the National Species List of Korea and Biodiversity of the Korean Peninsula (National Institute of Biological Resources, Ministry of Environment, Korea), to determine whether the species are distributed in Korea (NIBR, 2011, 2019, 2023). For species notdistributed in Korea, we catalogued biological information such as taxonomic position, distribution, collection data, and more (Table 1).

Results

Integrative analyses of the 562 individuals detected from 247 international vessels originating from 27 countries revealed that 512 individuals belonged to 260 species across 66 families of eight orders, with the remaining 50 individuals classified at the family level. Of the 260 species identified, 25 species (39 individuals) were confirmed as not being distributed in Korea. The composition of taxa identified as non-distributed species in Korea showed that Lepidoptera had the highest number of detected individuals, with 13 (11 species), followed by Hemiptera with seven individuals (four species), Hymenoptera with seven individuals (three species), Neuroptera with five individuals (two species), Orthoptera with four individuals (two species), and Coleoptera with three individuals (three species) (Fig. 1). Notably, three species (five individuals) were recognized as regulated species listed by the Animal and Plant Quarantine Agency in Korea: Oryctes rhinoceros (Scarabaeidae, Coleoptera, 1 individ.), Oecophylla smaragdina (Formicidae, Hymenoptera, 2 individs.), Solenopsis invicta (Formicidae, Hymenoptera, 2 individs.) (Fig. 2, Table 1) (QIA, 2013).

Among 39 individuals of 25 species not found in Korea, 32 individuals belonging to 20 species were detected alive, and seven of these species were detected multiple times: Hieroglyphus annulicornis (Acrididae, Orthoptera, 3 individs.), Chalcopis glandulosa (Pentatomidae, Hemiptera, 3 individs.), Chrysoperla suzukii (Chrysopidae, Neuroptera, 4 individs.), Formica cunicularia (Formicidae, Hymenoptera, 3 individs.), Solenopsis invicta (Formicidae, Hymenoptera, 2 individs.), Eumorphobotys eumorphalis (Crambidae, Lepidoptera, 2 individs.), Lemyra rhodophilodes (Erebidae, Lepidoptera, 2 individs.) (Table 1). Given the multiple detections of species in a live condition, there is a need to investigate insect pests in the ports and their adjacent areas.

Discussion

The International Plant Protection Convention (IPPC) recommended a quarantine inspection plan for sea transports and containers, and introduced a monitoring method from 2016 (IPPC, 2020). In Korea, the study of hitchhiker insect pests by international vessels has been conducted by the Animal and Plant Quarantine Agency of Korea (Kang et al., 2020, 2021, 2023b, 2024). For hitchhiker alien species, the potential for establishment is likely high when entry frequency on a particular route is low, but the number of individuals per entry is large (Toy & Newfield, 2010). Through this study, 39 individuals of 25 species across 18 families and six orders not previously distributed in Korea were detected in 2023, with 32 individuals found alive (Table 1). Of these, seven species were detected with more than two individuals. Compared to a previous studies (Kang et al., 2020, 2021, 2023b, 2024), non-native species in Korea were detected as follows: 22 individuals from 14 species in nine families across three orders in 2018, 67 individuals from 42 species in 21 families across seven orders in 2019, 29 individuals from 26 species in 21 families across six orders in 2021, 71 individuals from 38 species in 22 families across six orders in 2022, and 29 individuals from 25 species in 18 families across six orders in 2023 (Fig. 3). Consequently, the detection frequency of hitchhiker insects is generally increasing.

Comparing the detection patterns of multiple species in 2023 with a previous studies (Kang et al., 2020, 2021, 2023b, 2024), of the species detected in 2022, 10 species (Patanga succinct (Acrididae, Orthoptera, 1 individ.), Cyclopelta parva (Dinidoridae, Hemiptera, 2 individs.), Oryctes rhinoceros (Scarabaeidae, Coleoptera, 1 individ.), Formica cunicularia (Formicidae, Hymenoptera, 3 individs.), Oecophylla smaragdina (Formicidae, Hymenoptera, 2 individs.), Polyphagozerra coffeae (Cossidae, Lepidoptera, 1 individ.), Eumorphobotys eumorphalis (Crambidae, Lepidoptera, 2 individs.), Lemyra rhodophilodes (Erebidae, Lepidoptera, 2 individs.), Problepsis phoebearia (Geometridae, Lepidoptera, 1 individ.), Euhampsonia serratifera (Notodontidae, Lepidoptera, 1 individ.)) were detected again in 2023, two species (Chloroclystis pyrrholopha (Geometridae, Lepidoptera, 1 individ.), E. serratifera) in 2021, four species (Chrysoperla suzukii (Chrysopidae, Neuroptera, 4 individs.), F. cunicularia, E. eumorphalis, E. serratifera) in 2019, and three species (L. rhodophilodes, Parasa pastoralis (Limacodidae, Lepidoptera, 1 individ.), E. serratifera) in 2018 (Table 1). The likelihood of colonization by alien species increases with greater inflow amounts or frequencies (Lockwood et al., 2005, Johnston et al., 2009). Therefore, for species that are repeatedly hitchhiking or continuously detected, intensive surveys such as targeted quarantine inspections at the vessels’ port of entry or continuous monitoring around the port where the vessel is anchored are necessary. This study provides biological information including taxonomic details, original distribution, and detection data on non-native species in Korea detected in 2023 to establish rapid response plans.