Review of ticks (families: Ixodidae and Argasidae) in the Republic of Korea

INTRODUCTION

Ticks are obligate blood-sucking arthropods distributed in tropical and temperate regions of the world [1]. The life cycle of Ixodidae and Argasidae ticks consists of egg and three active developmental stages (larva, nymph, and adult). However, Argasidae ticks have multiple nymphal instars. Most species, larvae, and nymphs find hosts, feed, detach, and molt nymphs and adults, respectively. Female Ixodidae ticks seek hosts and feed only once until they are engorged, then lay many eggs and die. However, female Argasidae ticks feed on and oviposit several times [1]. During the blood-feeding periods, ticks transmit various pathogenic agents from host to host, thus threatening livestock.

The Republic of Korea (Korea) is a Northeast Asian country and is located between the 33°N and 43°N latitudes and between the 124°E and 132°E longitudes. Geographically, more than 70% of the Korean Peninsula is covered by mountains, which are mainly located in the northern and eastern regions, whereas plains comprise the southern and southwestern regions. The climate is considered temperate to subtropical and has a heavy rainy season in the summer. Administratively, Korea is divided into eight metropolitan cities (Seoul, Sejong, Daejeon, Busan, Daegu, Gwangju, Incheon, and Ulsan) and nine provinces (Gyeonggi, Gangwon, Chungbuk [Chungcheongbuk-do], Chungnam [Chungcheongnam-do], Gyeongbuk [Gyeongsangbuk-do], Gyeongnam [Gyeongsangnam-do], Jeonbuk [Jeollabuk-do], Jeonnam [Jeollanam-do], and Jeju) [2].

Different tick species are distributed throughout the country owing to climatic conditions that are favorable to tick survival. Moreover, recent global warming has facilitated changes in the distribution patterns of ticks in Korea. Many studies on ticks have been conducted regionally by individual researchers; therefore, these studies need to be summarized. In this review, we summarize the species diversity of ticks reported in Korea.

METHODOLOGY

A literature search was conducted from 25^th October until 12^th to November 2022. Scientific research publications in English and Korean were collected by using two major databases: “PubMed” (https://www.ncbi.nlm.nih.gov/) and “Web of science” (https://www.webofknowledge.com/) with extra website including the “Korean Journal of Parasitology” (https://www.parasitol.kr/), “Google scholar” (https://scholar.google.co.kr/), and “Korea Disease Control and Prevention Agency” (https://www.kdca.go.kr/). The main keywords for searching were “tick distribution south Korea”, “tick bite cases in Korea”, “tick Korea”, “진드기 조사”, and “진드기 분포”. Furthermore, the following extra keyworks were used: “tick distribution in Korea”, “tick bite cases in Korea” “Haemaphysalis ornithophila”, and “Haemaphysalis phasiana”.

We retrieved 146 studies published from 1966 to 2022 from the databases, and excluded duplications and unrelated studies (Fig. 1). In total, 143 studies were included. The title, year of publication, study region, and tick species were extracted from the selected studies. The geographical locations for tick collection were categorized into 10 groups, including Seoul and nine provinces, and the remaining metropolitan cities were included in the nearest provinces.

Fig. 1. Flow diagram of study screening and selection.

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RESULTS

Previous studies have reported 29 tick species of Ixodidae (hard ticks) while Argasidae (soft ticks) have been represented by only five species (Table 1). Haemaphysalis longicornis, the Asian longhorned tick was the predominant species in Korea, followed by H. flava, H. japonica, H. phasiana, H. ornithophila, H. concinna, H. punctata, H. formosensis, and H. campanulata.

Sixteen species from the genus Ixodes, 16 species have been reported in Korea, including I. nipponensis, I. persulcatus, I. turdus, I. granulatus, I. tanuki, I. pomeranzevi, I. uriae, I. signatus, I. angustus, I. ovatus, I. simplex, I. vespertilionis, and I. monospinosus. Further, a few studies have identified minor tick species, including Rhipicephalus sanguineus, R. microplus, and Amblyomma testudinarium.

Conversely, limited records have been obtained on Argasidae ticks. Only Argas vespertilionis, A. boueti, Ornithodoros sawaii, Ornithodoros sp., and O. capensis were identified in the restricted regions.

DISCUSSION

Most Ixodidae ticks inhabit open environments such as grasslands, graves, forests, and mountain roads, whereas Argasidae ticks live in nests, caves, and burrows. For this reason, most studies have used dragging or flagging methods to collect ticks. H. longicornis and H. flavaare the most commonly identified and widely distributed tick species in Korea [3], whereas H. japonica is mainly collected in Gangwon Province [4]. Moreover, H. ornithophila, H. formosensis, and H. concinna have been identified in migratory birds [5], while H. campanulata, H. phasiana, and H. punctata have been reported in a few studies [6–8].

The genus Ixodes is found worldwide. In particular, I. ricinus has a wider range of distribution, covering the European Union, North Africa, and Russia [9]. Interestingly, I. nipponensis is the main Ixodes species in Korea, followed by I. persulcatus and I. granulatus [4], and I. ricinus has not yet been reported.

A. testudinarium was mainly reported in Jeonbuk Province [4]; since the first record was in Jeju in 1981, many human bites have been reported in the southern regions of Korea. Jeju and the southern regions are considered to be warmer than the other regions, which may affect the distribution of A. testudinarium [10].

Most Argasidae ticks have specific hosts for feeding, such as bats and seabirds. Migratory birds play a critical role in the introduction of novel tick species from neighboring countries to Korea during the breeding season. O. sawaii was reported in migratory birds in 2016 [11], followed by O. capensis in 2017 [12], and Ornithodoros sp. in 2020 [13]. However, A. vespertilionis and A. boueti were recorded in Korea in 1966, and no additional studies have been conducted on these species in Korea [14].

The tick distribution and abundance change from year to year depending on various factors, such as region, climate, and seasonal change. The climate in Korea has gradually changed from temperate to subtropical, which affects the density and distribution of ticks. Previous studies have shown that ticks are more active in early and late autumn. In particular, nymphs peak from April to June and larvae predominate from July to October [15]. Some Argasidae ticks depend more on migratory hosts than on seasonal patterns.

Most studies have identified tick species based on their morphological characteristics. However, morphological identification is difficult in species differentiation among close tick species. For example, the larvae of H. longicornis and H. flava are morphologically identical and are regarded as Haemaphysalis spp. [16]. Future studies should consider the use of molecular methods to identify tick species.

In conclusion, this review summarizes the distribution of ticks in Korea, published between 1966 and 2022. Studies have reported 29 species of Ixodidae ticks and five Argasidae ticks in Seoul and nine geographic provinces in Korea.