Ticks Collected from Selected Mammalian Hosts Surveyed in the Republic of Korea During 2008-2009

Article information

Korean J Parasitol. 2011;49(3):331-335
Publication date (electronic) : 2011 September 30
doi : https://doi.org/10.3347/kjp.2011.49.3.331
15th Medical Detachment, 168th Multifunctional Medical Battalion, 65th Medical Brigade, Unit 15247, APO AP 96205-5247, USA.
2Division of Vertebrates Research, National Institute of Biological Resources, Incheon 404-708, Korea.
3Force Health Protection and Preventive Medicine, 65th Medical Brigade/U.S. Army MEDDAC-Korea, Unit 15281, APO AP 96205-5281, USA.
4Migratory Birds Center, National Park Research Institute, Korea National Park Service, Shinan-gun, Jeollanam-do 535-917, Korea.
5Conservation Genome Resource Bank for Korean Wildlife, College of Veterinary Medicine, Seoul National University, Seoul 151-742, Korea.
6Research Institute for Veterinary Science and BK21 Program for Veterinary Science,College of Veterinary Medicine, Seoul National University, Seoul 151-742, Korea.
Corresponding author (jschae@snu.ac.kr)
Received 2011 February 04; Revised 2011 May 03; Accepted 2011 June 07.

Abstract

A tick survey was conducted to determine the relative abundance and distribution of ticks associated with selected mammals in the Republic of Korea (ROK) during 2008-2009. A total of 918 ticks were collected from 76 mammals (6 families, 9 species) captured at 6 provinces and 3 Metropolitan Cities in ROK. Haemaphysalis longicornis (54.4%) was the most frequently collected tick, followed by Haemaphysalis flava (28.5%), Ixodes nipponensis (7.6%), Ixodes pomerantzevi (4.8%), Ixodes persulcatus (4.6%), and Haemaphysalis japonica (0.1%). Adults (57.0%) and nymphs (28.7%) of Ixodes and Haemaphysalis spp. were collected most frequently from medium or large mammals in this survey, while few larvae (14.3%) were collected. Hydropotes inermis was the most frequently captured mammal (52.6%), with a 16.4 tick index and 5 of 6 species of ticks collected during this survey. H. longicornis (69.7%) was the predominant tick collected from H. inermis, followed by H. flava (22.2%), I. persulcatus (6.1%), I. nipponensis (1.8%), and H. japonica (0.2%).

In the Republic of Korea (ROK), mammals and their associated ticks are hosts to a number of zoonotic pathogens, such as spotted fever group rickettsiae [1], Ehrlichia and Anaplasma spp. [2], Bartonella spp. [3], Borrelia burgdorferi [4-5], and tick-borne encephalitis virus [6-8]. Humans are incidental hosts as a result of outdoor activities, i.e., agriculture, construction, maintenance, recreation, and military training activities. New information, including retrospective febrile patient surveys, indicates that tick-borne diseases are underdiagnosed in the ROK [9-11].

Outdoor activities, including recreational hiking, agriculture, construction, and military operations, expose large sectors of human populations and their pets to all life stages of ticks, and associated pathogens of mammal [12]. Military populations are at increased risk for acquiring tick-borne infections because they often conduct training operations in unmanaged lands where small mammals (i.e., rodents, soricomorphs, rabbits, and weasels), as well as larger species (i.e., deer, wild pigs, raccoon dogs, badgers, and feral cats) and pathogen-infected ectoparasites are present.

In a large mammal tick survey, Kang (1984) reported 565 ticks to determine baseline susceptibility to selected acaricides of ticks collected from domestic livestock (cows) from 35 cities and counties and 6 provinces from 1982 to 1984. Species collected included, Haemaphysalis longicornis (87.4%), Boophilus microplus (=Rhipicephalus microplus) (8.8%), Ixodes persulcatus (3.4%), Rhipicephalus sanguineus (0.5%), Argas vespertilionis (0.2%), and 1 unidentified tick [13]. Later, Kim et al. (2008) reported 130 H. longicornis and 12 Ixodes nipponensis from 16 wild boars at Dongducheon, Gyeonggi-do (Province), for isolation and detection of tick-borne encephalitis virus [6]. Reports and studies of tick collections from wild large mammals are few, with most surveys limited to small mammals conducted as part of rodent-borne diseases surveillance programs [14-16]. The purpose of the present study was to determine the relative abundance, infestation rates, and geographical distributions of ticks associated with Hydropotes inermis (Korean water deer) and other wild mammals in the ROK.

As part of The 8th US Army, 65th Medical Brigade tick-borne disease surveillance program, the 5th Medical Detachment collaborated with 1) The Conservation Genome Resource Bank for Korean Wildlife, Seoul National University (SNU), 2) National Institute of Biological Resources (NIBR), and 3) The Migratory Birds Center located on Hong Island, National Park Research Institute (NPRI), to collect ticks from wild mammals captured for necropsy under institutional approved animal use protocols (SNU, NIBR, and the NPRI). Ticks were removed from mammals captured from 6 provinces [Gyeonggi-do (Pocheon), Gangwon-do (Chuncheon, Cheorwon, Inje), Jeollanam-do (Goheung, Gokseong, Gwangyang, Gurye, Hampyeong, Suncheon, Yeosu, Hong Island), Chungcheongbuk-do (Cheongwon), Gyeongsangbuk-do (Uljin), and Jeju-do (Jeju, Seogwipo)], and 3 Metropolitan Cities (Seoul, Daejeon, and Ulsan) in the ROK (Table 1). Ticks were carefully removed with a fine forceps from mammals, placed in 2-ml cryovials with 80% ethyl alcohol, and transported to the Entomology Section, 5th Medical Detachment, where they were identified to species and developmental stage under a dissecting microscope using standard keys and current nomenclature [17-20].

Number of ticks and collection sites for each mammal species in the Republic of Korea, 2008-2009

A total of 918 ixodid ticks belonging to 2 genera (Ixodes and Haemaphysalis) were collected from mammals (n=76; 6 families, 9 species) captured for surveillance from 6 provinces and 3 Metropolitan Cities in the ROK. H. inermis (52.6%) was the most frequently collected mammal, followed by Felis catus (feral cat, 27.6%), Capreolus pygargus (roe deer, 5.3%), Nyctereutes procyonoides (raccoon dog, 3.9%) and Tamias sibiricus (Siberian chipmunk, 3.9%) (Table 1). Only 1-2 ticks were collected from each of the remaining 4 species. Of the 6 species of ticks collected, H. longicornis (54.4%) was the most frequently collected, followed by Haemaphysalis flava (28.5%), I. nipponensis (7.6%), Ixodes pomerantzevi (4.8%), I. persulcatus (4.6%), and Haemaphysalis japonica (0.1%). The highest tick indices for selected hosts were recorded from N. procyonoides (38.0), followed by H. inermis (16.4), T. sibiricus (15.0), C. pygargus (9.0), and Meles leucurus (7.0). Tick indices for the remaining mammals were <5.0 (Table 2).

Number of mammals captured and number of ticks collected, by stage of development, for each mammal species in the Republic of Korea, 2008-2009

H. japonica (100.0%) was collected only from the Korean water deer, while accounting for 95.2% of I. persulcatus, 91.8% of H. longicornis, 55.7% of H. flava, and 17.1% of I. nipponensis. H. longicornis (69.7%) was the predominant species collected from the Korean water deer, followed by H. flava (22.2%), I. persulcatus (6.1%), I. nipponensis (1.8%), and H. japonica (0.2%) (Table 1).

Tick-borne zoonoses pose a serious health threat to US and ROK military populations throughout Korea [1-9,14-16]. Identification of arthropod ectoparasites and isolation of pathogens provide a descriptive analysis of the relative abundance of ticks, host associations, stages of development found on hosts, and relative distributions. Epidemiological data are critical to identify the prevalence, distribution, and disease risks of endemic and emerging zoonoses affecting animals and humans in the ROK. For US and ROK military populations, these data are central to the development of disease risk assessments and mitigation strategies (e.g., use of insecticide-impregnated uniforms) that reduce the impact of zoonotic diseases while increasing awareness among medical providers of potential arthropod-borne infections. H. longicornis is commonly collected on large mammals and from tall grass habitats with associated herbaceous vegetation and margins of forested hillsides and mountains (unpublished data), while H. flava larvae and nymphs are often associated with small mammals (e.g., rodents and soricomophs) and birds [17]. However, only 1 H. flava nymph was collected from 5,953 rodents and soricomorphs captured from 2004 to 2008 in Gyeonggi-do and Gangwon-do [16].

In our survey, 262 (28.5%) H. flava ticks were collected, with nymphs and adults found on a variety of small and large mammals (Table 3). I. nipponensis, larvae and nymphs, was the predominant tick (98.9%) collected from 5,953 small mammals captured (e.g., rodents and soricomorphs) in Gyeonggi-do and Gangwon-do [16]. In other reports, I. nipponensis was the most frequently collected tick from small mammals captured in Gyeonggi-do, while I. persulcatus was more commonly collected in Gangwon-do [14]. In our survey, this species was predominantly collected from F. catus at Hong Island, Jeollanam-do, and accounted for 96.0% of the total collected from feral cats. Larvae and nymphs of I. nipponensis prefers to blood feed on small mammals, while adults are more commonly found on large mammals.

Total number, percent, and stage of development for ticks collected from mammals, Republic of Korea, 2008-2009

Recent studies indicate that I. nipponensis plays an important role in the transmission of tick-borne pathogens to humans in the ROK, as human tick bites are reported more frequently for this species among patients seen at medical clinics in the ROK [21-24]. However, the number of reports may be not only due to increased propensity to bite humans, but due to greater allergenic reactions to bites by this species than others. Ixodes persulcatus was collected most frequently from H. inermis, which was associated with dense forested habitats in the Taebaek mountain range (20/42; 47.6%) and Sobaek mountain range (13; 31.0%). I. pomerantzevi is an uncommonly collected tick, with all previous collection records of this species collected from small mammals (Myodes regulus, Tscherskia triton, T. sibiricus, and Apodemus agrarius) while conducting routine rodent-borne disease surveillance [18,25,26]. In this survey, T. sibiricus was the primary host of I. pomerantzevi, with 24 larvae, 5 nymphs, and 15 female adults collected from 1 T. sibiricus collected in northern Gyeonggi-do. Only 1 male (0.1%) H. japonica was collected from a Korean water deer, and it has been infrequently recorded in other collections, e.g., tick drags, rodents, and birds.

Adults (57.0%) and nymphs (28.7%) of Ixodes and Haemaphysalis spp. were mostly collected from medium/large mammals in this survey, while larval ticks only accounted for 14.3% of all ticks collected (Table 3). In contrast, larvae (82.8%) and nymphs (17.2%) were collected from small mammals, 5,397 A. agrarius in Gyeonggi-do and Gangwon-do during 2004-2008, while adults accounted for <0.1% of all ticks collected [16].

The changing ecology, particularly reforestation, and associated increases in wildlife populations provide for increased proximal host contact associated with the wide distribution of blood-feeding ectoparasites in the ROK. Further studies of tick-host relationships are necessary to better understand tick species distributions and population dynamics, the distribution and prevalence of tick-borne pathogens, and their potential effects on human and animal health.

ACKNOWLEDGEMENTS

We thank the commanders and soldiers of the 5th Medical Detachments, 168th Multifunctional Medical Battalion, 65th Medical Brigade for their assistance in conducting tick-borne disease surveillance. Funding for this research was provided by the Armed Forces Health Surveillance Center (AFHSC), Global Emerging Infections Surveillance and Response System (GEIS), Silver Spring, MD, the National Center for Medical Intelligence, Fort Detrick, MD, and through the BK21 Program for Veterinary Science, Seoul National University, Seoul, Korea.

Notes

Disclaimer: The opinions expressed herein are those of the authors and are not to be construed as official or reflecting the views of the US Department of the Army, Department of Defense, or the US Government.

References

1. Lee JH, Park HS, Jung KD, Jang WJ, Koh SE, Kang SS, Lee IY, Lee WJ, Kim BJ, Kook YH, Park KH, Lee SH. Identification of the spotted fever group rickettsiae detected from Haemaphysalis longicornis in Korea. Microbiol Immunol 2003;47:301–304. 12801068.
2. Chae JS, Kim CM, Kim EH, Hur EJ, Klein TA, Kang TK, Lee HC, Song JW. Molecular epidemiological study for tick-borne disease (Ehrlichia and Anaplasma spp.) surveillance at selected U.S. military training sites/installations in Korea. Ann N Y Acad Sci 2003;990:118–125. 12860612.
3. Kim CM, Kim JY, Yi YH, Lee MJ, Cho MR, Shah DH, Klein TA, Kim HC, Song JW, Chong ST, O'Guinn ML, Lee JS, Lee IY, Park JH, Chae JS. Detection of Bartonella species from ticks, mites and small mammals in Korea. J Vet Sci 2005;6:327–334. 16293997.
4. Park KH, Lee SH, Won WJ, Jang WJ, Chang WH. Isolation of Borrelia burgdorferi, the causative agent of Lyme Disease, from Ixodes ticks in Korea. J Korean Soc Microbiol 1992;27:307–312.
5. Kee S, Hwang KJ, Oh HB, Kim MB, Shim JC, Ree HI, Park KS. Isolation and identification of Borrelia burgdorferi in Korea. J Korean Soc Microbiol 1994;29:301–310.
6. Kim SY, Yun SM, Han MG, Lee IY, Lee NY, Jeong YE, Lee BC, Ju YR. Isolation of tick-borne encephalitis viruses from wild rodents, South Korea. Vector borne Zoonotic Dis 2008;8:7–13. 18240970.
7. Kim SY, Jeong YE, Yun SM, Lee IY, Han MG, Ju YR. Molecular evidence for tick-borne encephalitis virus in ticks in South Korea. Med Vet Entomol 2009;23:15–20. 19239610.
8. Ko S, Kang JG, Kim SY, Klein TA, Kim HC, Chong ST, Sames WJ, Yun SM, Ju YR, Chae JS. Prevalence of tick-borne encephalitis virus in ticks from southern Korea. J Vet Sci 2010;11:197–203. 20706026.
9. Jang WJ, Kim JH, Choi YJ, Jung KD, Kim YG, Lee SH, Choi MS, Kim IS, Walker DH, Park KH. First serologic evidence of human spotted fever group rickettsiosis in Korea. J Clin Microbiol 2004;42:2310–2313. 15131221.
10. Choi YJ, Jang WJ, Kim JH, Ryu JS, Lee SH, Park KH, Paik HS, Koh YS, Choi MS, Kim IS. Spotted fever group and typhus group rickettsioses in humans, South Korea. Emerg Infect Dis 2005;11:237–244. 15752441.
11. Choi YJ, Lee SH, Park KH, Koh YS, Lee KH, Baik HS, Choi MS, Kim IS, Jang WJ. Evaluation of PCR-based assay for diagnosis of spotted fever group rickettsiosis in human serum samples. Clin Diagn Lab Immunol 2005;12:759–763. 15939751.
12. Kang JG, Ko SJ, Kim YJ, Yang HJ, Lee H, Shin NS, Choi KS, Chae JS. New genetic variants of Anaplasma phagocytophilum and Anaplasma bovis from Korean water deer (Hydropotes inermis argyropus). Vector borne Zoonotic Dis 2011;11:929–938. 21417930.
13. Kang YB. Studies on tick eradication in Korea (1982-1984). Special project for animal health. Ann Rep Inst Vet Res, Rural Develop Admin 1984;:269–305.
14. Shim JC, Yoon YH, Kim JL, Shin EH, Yang YC, Cho YB, Lee JY. Studies on the vector of Lyme disease (Borrelia burgdorferi) (I) Geographical distribution and seasonal prevalence. Rep NIH Korea 1992;29:123–130.
15. Shim JC, Yoon YH, Kim CL, Cho YB, Lee JY, Shin EH, Yang YC, Baik MK, Yu WH, Yu HS, Park KH, Kim KH. Studies on vector potential of ticks (Ixodidae) in transmitting Lyme disease (Borrelia burgdorferi) (II) Vector incrimination and seasonal occurrence of Ixodes granulatus. Rep NIH Korea 1993;30:131–136.
16. Kim HC, Chong ST, Sames WJ, Nunn PV, Wolf SP, Robbins RG, Klein TA. Tick surveillance of small mammals captured in Gyeonggi and Gangwon Provinces, Republic of Korea, 2004-2008. Sys Applied Acarol 2010;15:100–108.
17. Yamaguti N, Tipton VJ, Keegan HL, Toshioka S. Ticks of Japan, Korea and the Ryukyu Islands. Brigham Young University Science Bulletin, Biological Series 1971;15:1–226.
18. Robbins RG, Keirans JE. Systematics and Ecology of the Subgenus Ixodiopsis (Acari: Ixodidae: Ixodes). Thomas Say Foundation Monograph XIV 1992. Lanham, Maryland, USA: Entomological Society of America. p. viii + 159.
19. Horak IG, Camicas JL, Keirans JE. The Argasidae, Ixodidae and Nuttalliellidae (Acari: Ixodida): A world list of valid tick names. Exp Applied Acarol 2002;28:27–54.
20. Guglielmone AA, Richard G, Robbins , Apanaskevich DA, Petney TN, Estrada-Pena A, Horak IG, Shao R, Barker SC. The Argasidae, Ixodidae and Nuttelliellidae (Acari: Ixodida) of the world; A list of valid species names. Zootaxa 2010;(2528):1–28.
21. Lee SH, Chai JY, Kho WG, Hong SJ, Chung YD. A human case of tick bite by Ixodes nipponensis on the scalp. Korean J Parasitol 1989;27:67–69.
22. Ryu JS, Lee JU, Ahn MH, Min DY, Ree HI. A human case of tick bite Ixodes nipponensis. Korean J Parasitol 1998;36:59–41. 9529865.
23. Ko JH, Cho DY, Chung BS, Kim SI. Two human cases of tick bite caused by Ixodes nipponensis. Korean J Parasitol 2002;40:199–203. 12509106.
24. Chang SH, Park JH, Kwak JE, Joo M, Kim HS, Chi JG, Hong ST, Chai JY. A case of histologically diagnosed tick infestation on the scalp of a Korean child. Korean J Parasitol 2006;44:157–161. 16809965.
25. . List of Animals in Korea (excluding insects). The Korean Society of Systematic Zoology 1997. Seoul, Korea: Academy Press. p. 1–489.
26. Kim HC, Kim JH, Jo YS, Chong ST, Sames WJ, Klein TA, Robbins RG. Records of Ixodes pomerantzevi Serdyukova, 1941 (Acari: Ixodidae) from small mammals in northern Gyeonggi and Gangwon Provinces, Republic of Korea. Sys Applied Acarol 2009;14:129–135.

Article information Continued

Table 1.

Number of ticks and collection sites for each mammal species in the Republic of Korea, 2008-2009

Host species Number surveyed Collection sites HL HF HJ IN IPO IPE Total
Tamias sibiricus 3 Gyeonggi 0 1 0 0 44 0 45
Mogera robusta 1 Gyeonggi 0 0 0 0 0 0 0
Nyctereutes procyonoides 3 Gangwon 9 105 0 0 0 0 114
Hydropotes inermis 1 Seoul 0 5 0 0 0 0 5
9 Gangwon 92 58 0 3 0 20 173
2 Chungcheongbuk 0 3 0 0 0 4 7
1 Daejeon 25 4 0 0 0 0 29
2 Gyeongsangbuk 8 1 1 0 0 0 10
18 Ulsan 331 30 0 9 0 3 373
7 Jeollanam 2 45 0 0 0 13 60
Capreolus pygargus 2 Ulsan 19 10 0 0 0 0 29
2 Jeju 6 0 0 1 0 0 7
Prionalurus bengalensis 2 Jeollanam 0 0 0 6 0 0 6
Felis catus 21 Jeollanam 0 0 0 48 0 2 50
Mustela sibirica 1 Jeollanam 0 0 0 3 0 0 3
Meles leucurus 1 Jeollanam 7 0 0 0 0 0 7
Total 76 499 262 1 70 44 42 918

aHL, Haemaphysalis longicornis; HF, Haemaphysalis flava; HJ, Haemaphysalis japonica; IN, Ixodes nipponensis; IPO, Ixodes pomerantzevi; IPE, Ixodes persulcatus.

Table 2.

Number of mammals captured and number of ticks collected, by stage of development, for each mammal species in the Republic of Korea, 2008-2009

Family Host species Number surveyed Tick species Larvae Nymphs Adult male Adult female Total Indexa
Sciuridae Tamias sibiricus 1 Ixodes pomerantzevi 24 5 0 15 44 15.0
2 Haemaphysalis flava 0 1 0 0 1
Talpidae Mogera robusta 1 - 0 0 0 0 0 0.0
Canidae Nyctereutes procyonoides 3 Haemaphysalis longicornis 0 0 0 9 9 38.0
Haemaphysalis flava 14 43 32 16 105
Cervidae Hydropotes inermis 40 Haemaphysalis longicornis 77 179 116 86 458 16.4
Haemaphysalis flava 15 29 65 37 146
Haemaphysalis japonica 0 0 1 0 1
Ixodes persulcatus 1 0 15 24 40
Ixodes nipponensis 0 0 6 6 12
Capreolus pygargus 4 Haemaphysalis longicornis 0 7 6 12 25 9.0
Haemaphysalis flava 0 0 6 4 10
Ixodes nipponensis 0 0 0 1 1
Felidae Prionalurus bengalensis 2 Ixodes nipponensis 0 0 2 4 6 3.0
Felis catus 21 Ixodes persulcatus 0 0 0 2 2 2.4
Ixodes nipponensis 0 0 14 34 48
Mustelidae Mustela sibirica 1 Ixodes nipponensis 0 0 1 2 3 3.0
Meles leucurus 1 Haemaphysalis longicornis 0 0 1 6 7 7.0
Total 76 131 264 265 258 918 12.1
a

Index=Total numbers of tick collected/total numbers of mammals collected.

Table 3.

Total number, percent, and stage of development for ticks collected from mammals, Republic of Korea, 2008-2009

Tick species Larvae Nymph Male Female Total (%)
Haemaphysalis longicornis 77 (15.4)a 186 (37.3)a 123 (47.3)b 113 (54.4)c 499
Haemaphysalis flava 29 (11.0) 73 (27.9) 103 (61.1) 57 (28.5) 262
Haemaphysalis japonica 0 (0.0) 0 (0.0) 1 (100.0) 0 (0.1) 1
Ixodes nipponensis 0 (0.0) 0 (0.0) 23 (100.0) 47 (7.6) 70
Ixodes pomerantzevi 24 (54.5) 5 (11.4) 0 (34.1) 15 (4.8) 44
Ixodes persulcatus 1 (2.4) 0 (0.0) 15 (97.6) 26 (4.6) 42
Total 131 (14.3) 264 (28.7) 265 (57.0) 258 (100.0) 918
a

Percent of total ticks collected from mammals by species and stage of development;

b

Percent of both male and female ticks collected from mammals;

c

Percent of ticks for all stages of development and species collected from mammals.