Experimental and Applied Acarology

, Volume 62, Issue 4, pp 557–566 | Cite as

Ticks collected from migratory birds, including a new record of Haemaphysalis formosensis, on Jeju Island, Korea

  • Chang-Yong Choi
  • Chang-Wan Kang
  • Eun-Mi Kim
  • Sang Lee
  • Kyoung-Ha Moon
  • Mi-Rae Oh
  • Takeo Yamauchi
  • Young-Min Yun
Article

Abstract

Migratory birds may disperse parasites across ecological barriers, and recent climate change may alter the pattern of ectoparasite dispersal via changed patterns of bird migration. In order to document the parasitization of migratory birds by Ixodidae ticks on Jeju Island in Korea, we examined 934 migratory birds comprising 75 species for ticks from 2010 to 2012. In total, 313 ticks were collected from 74 migratory birds across 17 avian species and identified based on morphological keys. These ticks represented six species: Haemaphysalis flava,H. formosensis, H. longicornis, H. concinna, Ixodes turdus and I. nipponensis. Of particular note was the presence of H. formosensis, a species not previously reported to have been found in Korea, and H. concinna, which had not been previously reported on Jeju Island. The dominant tick species found were H. flava (226 ticks, 72.2 %) and I. turdus (54 ticks, 17.3 %), and ground-dwelling thrushes such as Pale thrushes (Turdus pallidus; 39 birds, 52.7 %) were the most important hosts. Although H. longicornis is the most abundant and prevalent terrestrial tick on Jeju Island, the species accounted for only 3.8 % of the total ticks collected in this study, suggesting that ticks on migratory birds may differ from the local tick fauna and that exotic ticks may be introduced via migratory birds. Therefore, long-term programs for tick and tick-borne disease surveillance are recommended to understand the role of migratory animals in the introduction of exotic species and associated pathogens and in life cycles of ticks at different stages in this region.

Keywords

Climate change Dispersal Haemaphysalis concinna Haemaphysalis flava Haemaphysalis formosensis Ixodes turdus Migratory birds Surveillance Tick 

Notes

Acknowledgments

We thank the members of the Jeju Wildlife Research Center for their dedicated assistance during our field studies. This research was funded by the Jeju Green Environment Center under the Research Development Program (Yr 2012, 12-2-70-76-1), to whom the authors would like to express much gratitude for its assistance.

References

  1. Abulreesh HH, Goulder R, Scott GW (2007) Wild birds and human pathogens in the context of ringing and migration. Ringing Migr 23:193–200CrossRefGoogle Scholar
  2. Choe HC, Fudge M, Sames WJ, Robbins RG, Lee IY, Chevalier NA, Chilcoat CD, Lee SH (2011) Tick surveillance of dogs in the Republic of Korea. Syst Appl Acarol 16:215–222Google Scholar
  3. Choi HM, Lee JY (2012) Changes of groundwater conditions on Jeju volcanic island, Korea: implications for sustainable agriculture. Afr J Agric Res 7:647–661Google Scholar
  4. Cotton PA (2003) Avian migration phenology and global climate change. PNAS 100:12219–12222PubMedCrossRefGoogle Scholar
  5. Cumming GS, van Vuuren DP (2006) Will climate change affect ectoparasite species ranges? Glob Ecol Biogeogr 15:486–497CrossRefGoogle Scholar
  6. Heylen DJA, Matthysen E (2008) Effect of tick parasitism on the health status of a passerine bird. Funct Ecol 22:1099–1107CrossRefGoogle Scholar
  7. Hoogstraal H, Roberts FHS, Kohls GM, Tipton VJ (1968) Review of Haemaphysalis (Kaiseriana) longicornis Neumann (resurrected) of Australia, New Zealand, New Caledonia, Fiji, Japan, Korea, and Northeastern China and USSR, and its parthenogenetic and bisexual populations (Ixodoidea, Ixodidae). J Parasit 54:1197–1213PubMedCrossRefGoogle Scholar
  8. IPCC (2007) Climate change 2007: synthesis report. Intergovernmental Panel on Climate Change, GenevaGoogle Scholar
  9. Ishiguro F, Takada N, Masuzawa T, Fukui T (2000) Prevalence of Lyme disease Borrelia spp. in ticks from migratory birds on the Japanese mainland. Appl Environ Microbiol 66:982–986PubMedCentralPubMedCrossRefGoogle Scholar
  10. Jenni L, Kéry M (2003) Timing of autumn bird migration under climate change: advances in long-distance migrants, delays in short-distance migrants. Proc R Soc Lond B 270:1467–1471CrossRefGoogle Scholar
  11. Kang CW, Kang HM, Kim EM, Park CR, Ji NJ (2010) Birds in Jeju. Hangru Publishing, JejuGoogle Scholar
  12. Kang JG, Kim HC, Choi CY, Nam HY, Chae HY, Chong ST, Klein TA, Ko S, Chae JS (2013) Molecular detection of Anaplasma, Bartonella, and Borrelia species in ticks collected from migratory birds from Hong-do Island, Republic of Korea. Vector Borne Zoonotic Dis 13:215–225PubMedCrossRefGoogle Scholar
  13. Kim SH (1970) Study on the ticks of Chejudo: life cycle. Korean J Parasitol 8:51–57 (in Korean with English abstract)CrossRefGoogle Scholar
  14. Kim HC, Ko SJ, Choi CY, Nam HY, Chae HY, Chong ST, Klein TA, Sames WJ, Robbins RG, Chae JS (2009) Migration bird tick surveillance, including a new record of Haemaphysalis ornitophila Hoogstraal and Kohls 1959 (Acari: Ixodidae) from Hong-do (Hong Island), Republic of Korea. Syst Appl Acarol 14:3–10Google Scholar
  15. Kim HC, Han SH, Chong ST, Klein TA, Choi CY, Nam HY, Chae HY, Lee H, Ko S, Kang JG, Chae JS (2011) Ticks collected from selected mammalian hosts surveyed in the Republic of Korea during 2008–2009. Korean J Parasitol 49:331–335PubMedCentralPubMedCrossRefGoogle Scholar
  16. Kinsey AA, Durden LA, Oliver JH (2000) Tick infestations of birds in coastal Georgia and Alabama. J Parasitol 86:251–254PubMedGoogle Scholar
  17. Ko S, Kang JG, Kim SY, Kim HC, Klein TA, Chong ST, Sames WJ, Yun SM, Ju YR, Chae JS (2010) Prevalence of tick-borne encephalitis virus in ticks from southern Korea. J Vet Sci 11:197–203PubMedCentralPubMedCrossRefGoogle Scholar
  18. Lee JY (2011) Environmental issues of groundwater in Korea: implications for sustainable use. Environ Conserv 38:64–74CrossRefGoogle Scholar
  19. Lee SH, Nam KW, Jeong JY, Yoo SJ, Koh Y-S, Lee S, Heo ST, Seong SY, Lee KH (2013) The effects of climate change and globalization on mosquito vectors: evidence from Jeju Island, South Korea on the potential for Asian Tiger Mosquito (Aedes albopictus) influxes and survival from Vietnam rather than Japan. PLoS ONE 8:e68512PubMedCentralPubMedCrossRefGoogle Scholar
  20. Lindgren E, Tälleklint L, Polfeldt T (2000) Impact of climatic change on the northern latitude limit and population density of the disease-transmitting European tick Ixodes ricinus. Environ Health Perspect 108:119–123PubMedCentralPubMedCrossRefGoogle Scholar
  21. McClure HE, Ratanaworabhan N, Emerson KC, Atyeo WT, Hoogstraal H, Maa TC, Nadchatram N, Wilson N, Kwanyuen P, Wayupong L (1973) Some ectoparasites of the birds of Asia. Jintana Printing Ltd., BangkokGoogle Scholar
  22. Miyamoto K, Nakao M, Fujita H, Sato F (1993) The ixodid ticks on migratory birds in Japan and isolation of Lyme disease spirochetes from bird-feeding ticks. Jpn J Sanit Zool 44:315–326Google Scholar
  23. Moon CR, Kim SH (1986) Studies on the control of ticks and tick-borne diseases in exotic cattle in Cheju-do. Livest Prod Annu Res Rep 1:31–35 (in Korean with English abstract)Google Scholar
  24. Moon BC, Jeong JH, Choi YJ, Kim JE, Seo HJ, Shin EH, Song BG, Lee HI, Lee SH, Park KH, Jang WJ (2009) Detection and identification of the Spotted Fever Group Rickettsial agents from Haemaphysalis ticks in Jeju Island, Korea. J Bacteriol Virol 39:317–327 (in Korean with English abstract)CrossRefGoogle Scholar
  25. Morshed MG, Scott JD, Fernando K, Beati L, Mazerolle DF, Geddes G, Durden LA (2005) Migratory songbirds disperse ticks across Canada, and first isolation of the Lyme Disease spirochete, Borrelia burgdorferi, from the avian tick, Ixodes auritulus. J Parasitol 91:780–790PubMedCrossRefGoogle Scholar
  26. Noh YT (1972) Faunal studies on the ticks in Korea. In: Kim HS (ed) Floral studies on some taxa of plants and faunal studies on some taxa of animals in Korea, R-72-82. Ministry of Science and Technology, Seoul, pp 141–160 (in Korean with English abstract)Google Scholar
  27. Oh JY, Moon BC, Bae BK, Shin EH, Ko YH, Kim YJ, Park YH, Chae JS (2009) Genetic identification and phylogenetic analysis of Anaplasma and Ehrlichia species in Haemaphysalis longicornis collected from Jeju Island, Korea. J Bacteriol Virol 39:257–267CrossRefGoogle Scholar
  28. Pietzsch ME, Mitchell R, Jameson LJ, Morgan C, Medlock JM, Collins D, Chamberlain JC, Gould EA, Hewson R, Taylor MA, Leach S (2008) Preliminary evaluation of exotic tick species and exotic pathogens imported on migratory birds into the British Isles. Vet Parasitol 155:328–332PubMedCrossRefGoogle Scholar
  29. Robbins RG, Keirans JE (1992) Systematics and ecology of the subgenus Ixodiopsis (Acari: Ixodidae: Ixodes). Entomological Society of America, LanhamGoogle Scholar
  30. Sames WJ, Kim HC, Chong ST, Lee IY, Apanaskevich DA, Robbins RG, Bast JA, Moore R, Klein TA (2008) Haemaphysalis (Ornithophysalis) phasiana (Acari: Ixodidae) in the Republic of Korea: Two province records and habitat descriptions. Syst Appl Acarol 13:43–50Google Scholar
  31. Waldenström J, Lundkvist A, Falk KI, Garpmo U, Bergström S, Lindengren G, Sjöstedt A, Mejlon H, Fransson T, Haemig PD, Olsen B (2007) Migrating birds and tick-borne encephalitis virus. Emerg Infect Dis 13:1215–1218PubMedCrossRefGoogle Scholar
  32. Yamaguti N, Tipton VJ, Keegan HL, Toshioka S (1971) Ticks of Japan, Korea, and the Ryukyu Islands. Brigham Young Univ Sci Bull Biol Ser 15:1–226Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Chang-Yong Choi
    • 1
    • 6
  • Chang-Wan Kang
    • 2
  • Eun-Mi Kim
    • 2
    • 3
  • Sang Lee
    • 1
    • 4
  • Kyoung-Ha Moon
    • 1
    • 4
  • Mi-Rae Oh
    • 4
  • Takeo Yamauchi
    • 5
  • Young-Min Yun
    • 1
    • 4
  1. 1.Jeju Wildlife Rescue CenterJeju National UniversityJeju CityRepublic of Korea
  2. 2.Jeju Wildlife Research CenterSeogwipoRepublic of Korea
  3. 3.Warm-Temperate and Subtropical Forest Research CenterKorea Forest Research InstituteSeogwipoRepublic of Korea
  4. 4.College of Veterinary MedicineJeju National UniversityJeju CityRepublic of Korea
  5. 5.Toyama Institute of HealthImizuJapan
  6. 6.Research Institute for Agriculture and Life SciencesSeoul National UniversityGwanak-gu, SeoulRepublic of Korea

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