Exp Appl Acarol (2014) 62:557–566 DOI 10.1007/s10493-013-9748-9
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
•
Received: 5 July 2013 / Accepted: 10 October 2013 / Published online: 20 October 2013 Ó Springer Science+Business Media Dordrecht 2013
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
C.-Y. Choi S. Lee K.-H. Moon Y.-M. Yun (&) Jeju Wildlife Rescue Center, Jeju National University, Jeju City, Jeju 690-121, Republic of Korea e-mail: [email protected] Present Address: C.-Y. Choi Research Institute for Agriculture and Life Sciences, Seoul National University, Gwanak-gu, Seoul 151-921, Republic of Korea C.-W. Kang E.-M. Kim Jeju Wildlife Research Center, 589, Hawon-dong, Seogwipo, Jeju 697-340, Republic of Korea E.-M. Kim Warm-Temperate and Subtropical Forest Research Center, Korea Forest Research Institute, 1253, Sanghyo-dong, Seogwipo, Jeju 697-050, Republic of Korea S. Lee K.-H. Moon M.-R. Oh Y.-M. Yun College of Veterinary Medicine, Jeju National University, Jeju City, Jeju 690-121, Republic of Korea T. Yamauchi Toyama Institute of Health, 17-1 Nakataikoyama, Imizu, Toyama 939-0363, Japan
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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
Introduction In spite of their importance as common indicators of ecosystem health, wild birds may also harbor and carry diverse viral, bacterial, fungal and protozoan zoonotic agents (Abulreesh et al. 2007). Given that migratory birds regularly cross over ecological barriers such as oceans, such birds have been regarded as potential hosts enabling a wide range of ectoparasites and associated pathogens to disperse over a long distance (Kinsey et al. 2000; Morshed et al. 2005; Waldenstro¨m et al. 2007; Pietzsch et al. 2008). Global climate change therefore may not only affect migratory birds in numerous ways, but may also indirectly lead to the introduction of new ectoparasites and pathogens into non-endemic areas (Lindgren et al. 2000; Cumming and van Vuuren 2006) by means of the changed patterns of migration in birds (Cotton 2003; Jenni and Ke´ry 2003). Thus the surveillance of ectoparasites parasitizing wild migratory birds is required to identify potential vectors and diseases, to understand their abundance and prevalence, and to develop reference information on the possible introduction of exotic vectors into changing environments. The importance of tick surveillance on migratory birds has been emphasized to secure the health of the public and wildlife, since the blood-sucking arthropods that commonly parasitize birds may harbor exotic pathogens. As common blood-sucking ectoparsites on dispersal hosts, Ixodidae ticks on migratory birds have been studied and monitored in many areas around the world (e.g., Miyamoto et al. 1993; Ishiguro et al. 2000; Kinsey et al. 2000; Morshed et al. 2005; Waldenstro¨m et al. 2007). The Migratory Animal Pathological Survey (MAPS) conducted from 1963 to 1971 was the most comprehensive and systematic survey of tick fauna parasitizing birds in Asia in general and the Republic of Korea in particular (McClure et al. 1973). Since MAPS, many studies on ticks, their hosts, their distribution, and associated pathogens have been conducted in Korea as part of efforts to safeguard the health of domestic animals and the public (e.g., Kim 1970; Noh 1972; Sames et al. 2008; Moon et al. 2009; Oh et al. 2009; Ko et al. 2010; Choe et al. 2011). However, information on the occurrence, prevalence, and distribution of ticks on birds and their host association has been poorly documented (Kim et al. 2009). As the largest and southernmost island in Korea, Jeju Island in particular has experienced the rapid and remarkable changes in its local climate as of late and the concurrent effects of such change: increases in sea level, mean temperature, annual precipitation, and CO2 levels, groundwater exploitation, and changes in vegetation (e.g., Lee 2011; Choi and Lee 2012). The annual mean temperature in Jeju, for instance,
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increased by 1.4–2.0 °C for the past four decades (Lee et al. 2013) while the mean global temperature increased by 0.74 °C during the twentieth century due to global climate change (IPCC 2007). The island is also the first and last site of birds crossing the Yellow Sea and East China Sea during their northward and southward migrations. Therefore, Jeju Island is an important location for migratory bird and tick surveillance, and for the long-term monitoring of related trends. In this study, we provide the first quantitative data on bird tick surveillance by collecting and identifying ticks on migratory birds on Jeju Island, one of the locations in the Republic of Korea where the effects of climate change are most apparent, and where information on bird ticks is still lacking. It is hoped that such data will facilitate the future surveillance efforts on a local and national scale.
Materials and methods The study area was Jeju Island (33.367 N, 126.533 E) and its satellite islands, including Mara Island (33.120 N, 126.268 E) and Chuja Island (33.957 N, 126.297 E), which fall under the jurisdiction of the Jeju Special Self-Governing Province in the Republic of Korea. As the largest island in Korea, Jeju Island is located 80 km south of the Korean Peninsula between the Korea Strait and the East China Sea (Fig. 1). The island therefore supports unique habitats hosting approximately 70 resident and 300 non-resident avian species (Kang et al. 2010) and plays an important role as a stopover for migratory birds that regularly cross the Yellow Sea and East China Sea during their migrations between Korea, China, Russia, Japan and other southeast Asian countries. From March 2010 to October 2012, we used several mist nets (2.5 9 6.0 m, 2.5 9 12.0 m; mesh size: 2.6–3.2 mm) to capture migratory birds during daytime hours for active surveillance. The captured birds were identified and measured, and each bird was ringed with a metal band having a unique serial identification number. We carefully examined the surface of the birds using fine forceps in order to collect ticks and other ectoparasites, with the parasites collected being preserved in cryovials filled with a 70 % ethanol solution. Upon completion of the examination and ringing process, the birds were safely released. All procedures were conducted in accordance with the standards required to obtain permits issued by the local governments and related agencies. To complement the active surveillance, we also took a passive surveillance approach by examining rescued or killed migratory birds admitted to the Jeju Wildlife Rescue Center in Jeju National University. The collected ticks were identified to the species level under dissecting (Carl Zeiss Stemi DV4) or optical microscopes (Olympus CX31 and Nikon Eclipse Ci) using standard morphological keys (Yamaguti et al. 1971; Noh 1972); unidentifiable or suspicious ticks were sent to Toyama Institute of Health in Japan for confirmation. The identified ticks were kept for future destructive analysis for pathogen detection in the Jeju Wildlife Rescue Center.
Results We examined 934 migratory birds belonging to 75 species; 913 live birds of 65 species were captured and examined, and 21 carcasses/injured birds of 14 avian species kept at the rescue center were also examined. A total of 313 ticks of six Ixodidae species belonging to
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Fig. 1 Location of the study site, Jeju Island in Korea
two genera (Haemaphysalis and Ixodes) were collected from 74 individuals (7.95 % of the total examined migratory birds) across 17 avian species (Table 1). All ticks were found on or near head parts of the examined birds, with the exception of two ticks found among body feathers in the abdominal region. Only one adult tick (A) was collected while 169 were nymphs (N) and 143 were larvae (L). The most abundant species was Haemaphysalis flava Neumann (226 ticks, 72.2 % of the total; 105N and 121L) followed by Ixodes turdus Nakatsudi (54 ticks, 17.3 %; 38N and 16L). The other ticks collected were H. formosensis Neumann (14 ticks, 4.5 %; 14N), H. longicornis Neumann (12 ticks, 3.8 %; 1A, 5N, and 6L), H. concinna Koch (4 ticks, 1.3 %; 4N), and I. nipponensis Kitaoka and Saito (3 ticks, 1.0 %; 3N). Of the 17 identified host species, thrushes belonging to the genus Turdus and Zoothera accounted for 82.4 % of the infested birds and had higher infestation rates than the birds belonging to the other avian groups. Pale (Turdus pallidus; 39 birds, 52.7 %), White’s (Zoothera aurea; 11, 14.9 %), Gray-backed (Turdus hortulorum; 4, 5.4 %) and Eye-browed thrushes (Turdus obscurus; 4, 5.4 %) were the major avian hosts of the collected ticks. In particular, White’s thrushes hosted five of the six tick species found in this study. H. formosensis, a new tick species to Korea (Fig. 2), were collected from one Pale thrush (1N, 29 April 2011), one Siberian thrush (Zoothera sibirica; 2N, 16 May 2011), two White’s thrushes (9N and 1N, 9 and 14 April 2012), and one Eye-browed thrush (1N, 29 April 2012). Nymphs of H. concinna, new to the local tick fauna in Jeju Island, were collected from two Gray-backed thrushes (2N and 2N, 22 April 2012).
123
1
1
2
1
Himantopus himantopus
Cuculus canorus
Halcyon coromanda
Pitta nympha
20
9
127
Turdus cardis
Turdus hortulorum
Turdus obscurus
Turdus pallidus
74
2
2
1
39
4
4
2
11
1
1
1
1
1
1
1
1
1
No. of birds w/ticks
105
1
1
79
4
9
2
8
1
121
3
2
88
7
8
4
1
2
6
1
1
5
2
2
1
Nymph
Adult
Nymph
Larva
H. longicornis
Haemaphysalis flava
6
6
Larva
** New to Jeju Island, Korea
* New to Korea
A total of 934 migratory birds comprising 75 species were examined, but only infested birds were presented
287
33
Emberiza tristrami
Total
16
Emberiza elegans
1
10
Zoothera aurea
Periparus venustulus
4
23
Zoothera sibirica
9
Luscinia cyane
28
1
Ficedula narcissina
1
Buteo buteo
No. of examined birds
Pernis ptilorhynchus
Avian host
14
1
1
10
2
Nymph
H. formosensis*
Table 1 Ixodidae ticks collected from migratory birds and their hosts on Jeju Island, Korea from 2010 to 2012
4
4
Nymph
H. concinna**
38
5
18
1
7
1
6
Nymph
16
10
4
2
Larva
Ixodes turdus
3
2
1
Nymph
I. nipponensis
Exp Appl Acarol (2014) 62:557–566 561
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Fig. 2 A nymph of Haemaphysalis formosensis (a dorsal view, b ventral view) collected from an Eye-browed thrush (T. obscurus) on 29 April 2012 at Mara Islet, Seogwipo City on Jeju Island in the Republic of Korea. Scale bar indicates 0.5 mm
The mean number of ticks per bird (with standard deviation) in all examined birds was 0.35 ± 2.80. However, the number of ticks per infested bird ranged from 1–59 with an average of 4.5 ± 9.2 ticks per bird. Only one or two ticks were collected per bird in most cases (70.3 %; Fig. 3), but two Pale thrushes captured in November 2010 were severely infested: one with three nymphs and 47 larvae of H. flava, and the other with 56 H. flava (34N and 22L) and three I. turdus (2N and 1L) ticks.
Discussion Until now, ten Ixodidae species have been reported on Jeju Island, Korea. Haemaphysalis campanulata Warburton (Noh 1972), H. phasiana (Sames et al. 2008), H. flava (Sames et al. 2008; Moon et al. 2009), Ixodes persulcatus (Schulze) (Noh 1972), I. vespertilionis Koch (Noh 1972), I. pomeranzevi Serdyukova (Robbins and Keirans 1992), I. turdus (Sames et al. 2008), and I. nipponensis (Kim et al. 2011) have scattered and accidental records. Boophilus microplus (Canestrini) (Kim 1970; Yamaguti et al. 1971; Noh 1972; Moon and Kim 1986) and Haemaphysalis longicornis (Hoogstraal et al. 1968; Kim 1970; Yamaguti et al. 1971; Noh 1972; Moon and Kim 1986; Sames et al. 2008; Moon et al. 2009; Oh et al. 2009; Kim et al. 2011) are regarded as species common to the island, but
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563
Fig. 3 The number of ticks per tick-infested migratory bird collected from 2010 to 2012 on Jeju Island, Korea
Moon and Kim (1986) suggest that the B. microplus population on Jeju Island has declined possibly owing to active tick controls and changed vegetation management on ranches. Therefore, H. longicornis currently seems to be the most dominant and widely distributed species on Jeju Island, comprising 99.8–100 % of the local ticks collected by flag dragging (Moon et al. 2009; Oh et al. 2009). However, only 3.8 % of the total number of ticks collected in this study were H. longicornis, and the vast majority on the birds (89.5 %) were of the species H. flava and I. turdus, demonstrating a clear difference between the composition of the avian-borne and local terrestrial tick populations. We also found one species of tick that was new tick to Korea (H. formosensis) and another that was new to Jeju Island (H. concinna) on the migratory birds examined for this study. It is important to note that these two new species were collected in April and May, during the northward migration season. Since winter temperatures are an important limiting factor in tick survival and distribution, the northward expansion of exotic ticks is of special interest worldwide in terms of the effect of climate change on public and animal health concerns regarding emerging tick-borne diseases (Lindgren et al. 2000; Cumming and van Vuuren 2006). Therefore, the introduction of these exotic ticks and their potential settlement on Jeju Island become important issues to monitor given the changing climate conditions there. Ticks found on migratory birds, including the two most common species in this study, are known vectors of diverse zoonotic pathogens such as tick-borne encephalitis virus (Ko et al. 2010) and Anaplasma, Bartonella, and Borrelia species (Kang et al. 2013) in Korea. Given the occurrence of new ticks and the unique species compositions found on migratory birds, a possible influx of associate diseases, and changing local climates, our data suggests that exotic ticks and associated pathogens may be introduced to Jeju Island via migratory birds, leading to future changes in tick abundance and distribution on the island. In this study, we identified a dominant bird tick species (H. flava) and hosts (thrushes, particularly Pale thrushes). A previous tick surveillance on Hong Island, located 200 km northwest of Jeju Island, indicated that I. turdus (66.2 %) was the dominant species on migratory birds (Kim et al. 2009). In spite of the geographical proximity of the two bird stopover sites, migratory birds at each site may transport different species of ticks in different influx rates when the birds use distinct migration routes from diverse origins with unique tick density and distribution. The infestation prevalence of ticks on birds was 7.95 % in this study, which was higher than the rate of \0.5 % in the UK (Pietzsch et al. 2008), 1.4 % in the Republic of Korea
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(Kim et al. 2009), and 3.4 % in Sweden (Waldenstro¨m et al. 2007), but lower than the rate of 9.1–13.3 % (Miyamoto et al. 1993) and 10.0 % (Ishiguro et al. 2000) found in Japan, suggesting that the Jeju Island value falls within a normal range. The infestation of Turdidae thrushes was prominent possibly due to their ground feeding and dwelling habits (McClure et al. 1973, Pietzsch et al. 2008), their high abundance (as shown in Table 1), and their large body sizes and subsequent high chance of tick encounter. The infested birds were typically found to be carrying one or two ticks, but some birds were heavily infested. This may be related to the fact that birds in poor physical health tend to have heavy parasitic loads or vice versa, though contradictory evidence exists regarding this matter (Heylen and Matthysen 2008). Most of the ticks were found on or near the head because active and effective grooming of these areas using the beak is difficult (Miyamoto et al. 1993; Kim et al. 2009); the general habit of ticks to climb up may be another possible factor. Future works on how the physical condition and preening behaviors of birds affect their tick loads are required to better understand the interaction between ectoparasites and their hosts. It is also noteworthy that only one adult tick (0.32 %) was found out of 313 collected ticks, suggesting that birds harboring ticks were not definitive hosts. Compared with the tick surveillance of Korean mammals (Kim et al. 2011), adult ticks of H. flava, H. longicornis, and I. nipponensis were more common in mammalian hosts than adults of the conspecifics found in birds. This supports the hypothesis that birds may play an important role as an intermediate hosts rather than as a definitive host and therefore may disperse ticks to other sites and hosts. Yamaguti et al. (1971) also noted that immature H. flava and I. nipponensis parasitize birds while H. longicornis use diverse hosts. Human-induced climatic change has caused the recent change in migratory patterns of birds (Cotton 2003; Jenni and Ke´ry 2003), but the current status and effects of climate change on the migration of birds as well as the biology of their ectoparasites are poorly documented in East Asia. Our results demonstrate that migratory birds hosting ticks may affect existing local tick fauna by changing tick abundance and distribution. However, a detailed mechanism of tick introduction and long-distance movements through bird migration is still unclear. As social concerns about emerging diseases induced by climate change increase, more tick surveillance on birds will be required to understand the role of migratory animals in the introduction of exotic species and associated pathogens and in the life cycles of ticks at different stages in this region. 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 Abulreesh HH, Goulder R, Scott GW (2007) Wild birds and human pathogens in the context of ringing and migration. Ringing Migr 23:193–200 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 16:215–222 Choi HM, Lee JY (2012) Changes of groundwater conditions on Jeju volcanic island, Korea: implications for sustainable agriculture. Afr J Agric Res 7:647–661 Cotton PA (2003) Avian migration phenology and global climate change. PNAS 100:12219–12222 Cumming GS, van Vuuren DP (2006) Will climate change affect ectoparasite species ranges? Glob Ecol Biogeogr 15:486–497
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Heylen DJA, Matthysen E (2008) Effect of tick parasitism on the health status of a passerine bird. Funct Ecol 22:1099–1107 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 54:1197–1213 IPCC (2007) Climate change 2007: synthesis report. Intergovernmental Panel on Climate Change, Geneva 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 66:982–986 Jenni L, Ke´ry 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 270:1467–1471 Kang CW, Kang HM, Kim EM, Park CR, Ji NJ (2010) Birds in Jeju. Hangru Publishing, Jeju 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 13:215–225 Kim SH (1970) Study on the ticks of Chejudo: life cycle. Korean J Parasitol 8:51–57 (in Korean with English abstract) 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 14:3–10 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 49:331–335 Kinsey AA, Durden LA, Oliver JH (2000) Tick infestations of birds in coastal Georgia and Alabama. J Parasitol 86:251–254 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 11:197–203 Lee JY (2011) Environmental issues of groundwater in Korea: implications for sustainable use. Environ Conserv 38:64–74 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:e68512 Lindgren E, Ta¨lleklint 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 108:119–123 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., Bangkok 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 44:315–326 Moon CR, Kim SH (1986) Studies on the control of ticks and tick-borne diseases in exotic cattle in Chejudo. Livest Prod Annu Res Rep 1:31–35 (in Korean with English abstract) 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) 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 91:780–790 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) 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 39:257–267 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 155:328–332
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Robbins RG, Keirans JE (1992) Systematics and ecology of the subgenus Ixodiopsis (Acari: Ixodidae: Ixodes). Entomological Society of America, Lanham 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 13:43–50 Waldenstro¨m J, Lundkvist A, Falk KI, Garpmo U, Bergstro¨m S, Lindengren G, Sjo¨stedt A, Mejlon H, Fransson T, Haemig PD, Olsen B (2007) Migrating birds and tick-borne encephalitis virus. Emerg Infect Dis 13:1215–1218 Yamaguti N, Tipton VJ, Keegan HL, Toshioka S (1971) Ticks of Japan, Korea, and the Ryukyu Islands. Brigham Young Univ Sci Bull Biol Ser 15:1–226
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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
•
Received: 5 July 2013 / Accepted: 10 October 2013 / Published online: 20 October 2013 Ó Springer Science+Business Media Dordrecht 2013
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
C.-Y. Choi S. Lee K.-H. Moon Y.-M. Yun (&) Jeju Wildlife Rescue Center, Jeju National University, Jeju City, Jeju 690-121, Republic of Korea e-mail: [email protected] Present Address: C.-Y. Choi Research Institute for Agriculture and Life Sciences, Seoul National University, Gwanak-gu, Seoul 151-921, Republic of Korea C.-W. Kang E.-M. Kim Jeju Wildlife Research Center, 589, Hawon-dong, Seogwipo, Jeju 697-340, Republic of Korea E.-M. Kim Warm-Temperate and Subtropical Forest Research Center, Korea Forest Research Institute, 1253, Sanghyo-dong, Seogwipo, Jeju 697-050, Republic of Korea S. Lee K.-H. Moon M.-R. Oh Y.-M. Yun College of Veterinary Medicine, Jeju National University, Jeju City, Jeju 690-121, Republic of Korea T. Yamauchi Toyama Institute of Health, 17-1 Nakataikoyama, Imizu, Toyama 939-0363, Japan
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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
Introduction In spite of their importance as common indicators of ecosystem health, wild birds may also harbor and carry diverse viral, bacterial, fungal and protozoan zoonotic agents (Abulreesh et al. 2007). Given that migratory birds regularly cross over ecological barriers such as oceans, such birds have been regarded as potential hosts enabling a wide range of ectoparasites and associated pathogens to disperse over a long distance (Kinsey et al. 2000; Morshed et al. 2005; Waldenstro¨m et al. 2007; Pietzsch et al. 2008). Global climate change therefore may not only affect migratory birds in numerous ways, but may also indirectly lead to the introduction of new ectoparasites and pathogens into non-endemic areas (Lindgren et al. 2000; Cumming and van Vuuren 2006) by means of the changed patterns of migration in birds (Cotton 2003; Jenni and Ke´ry 2003). Thus the surveillance of ectoparasites parasitizing wild migratory birds is required to identify potential vectors and diseases, to understand their abundance and prevalence, and to develop reference information on the possible introduction of exotic vectors into changing environments. The importance of tick surveillance on migratory birds has been emphasized to secure the health of the public and wildlife, since the blood-sucking arthropods that commonly parasitize birds may harbor exotic pathogens. As common blood-sucking ectoparsites on dispersal hosts, Ixodidae ticks on migratory birds have been studied and monitored in many areas around the world (e.g., Miyamoto et al. 1993; Ishiguro et al. 2000; Kinsey et al. 2000; Morshed et al. 2005; Waldenstro¨m et al. 2007). The Migratory Animal Pathological Survey (MAPS) conducted from 1963 to 1971 was the most comprehensive and systematic survey of tick fauna parasitizing birds in Asia in general and the Republic of Korea in particular (McClure et al. 1973). Since MAPS, many studies on ticks, their hosts, their distribution, and associated pathogens have been conducted in Korea as part of efforts to safeguard the health of domestic animals and the public (e.g., Kim 1970; Noh 1972; Sames et al. 2008; Moon et al. 2009; Oh et al. 2009; Ko et al. 2010; Choe et al. 2011). However, information on the occurrence, prevalence, and distribution of ticks on birds and their host association has been poorly documented (Kim et al. 2009). As the largest and southernmost island in Korea, Jeju Island in particular has experienced the rapid and remarkable changes in its local climate as of late and the concurrent effects of such change: increases in sea level, mean temperature, annual precipitation, and CO2 levels, groundwater exploitation, and changes in vegetation (e.g., Lee 2011; Choi and Lee 2012). The annual mean temperature in Jeju, for instance,
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increased by 1.4–2.0 °C for the past four decades (Lee et al. 2013) while the mean global temperature increased by 0.74 °C during the twentieth century due to global climate change (IPCC 2007). The island is also the first and last site of birds crossing the Yellow Sea and East China Sea during their northward and southward migrations. Therefore, Jeju Island is an important location for migratory bird and tick surveillance, and for the long-term monitoring of related trends. In this study, we provide the first quantitative data on bird tick surveillance by collecting and identifying ticks on migratory birds on Jeju Island, one of the locations in the Republic of Korea where the effects of climate change are most apparent, and where information on bird ticks is still lacking. It is hoped that such data will facilitate the future surveillance efforts on a local and national scale.
Materials and methods The study area was Jeju Island (33.367 N, 126.533 E) and its satellite islands, including Mara Island (33.120 N, 126.268 E) and Chuja Island (33.957 N, 126.297 E), which fall under the jurisdiction of the Jeju Special Self-Governing Province in the Republic of Korea. As the largest island in Korea, Jeju Island is located 80 km south of the Korean Peninsula between the Korea Strait and the East China Sea (Fig. 1). The island therefore supports unique habitats hosting approximately 70 resident and 300 non-resident avian species (Kang et al. 2010) and plays an important role as a stopover for migratory birds that regularly cross the Yellow Sea and East China Sea during their migrations between Korea, China, Russia, Japan and other southeast Asian countries. From March 2010 to October 2012, we used several mist nets (2.5 9 6.0 m, 2.5 9 12.0 m; mesh size: 2.6–3.2 mm) to capture migratory birds during daytime hours for active surveillance. The captured birds were identified and measured, and each bird was ringed with a metal band having a unique serial identification number. We carefully examined the surface of the birds using fine forceps in order to collect ticks and other ectoparasites, with the parasites collected being preserved in cryovials filled with a 70 % ethanol solution. Upon completion of the examination and ringing process, the birds were safely released. All procedures were conducted in accordance with the standards required to obtain permits issued by the local governments and related agencies. To complement the active surveillance, we also took a passive surveillance approach by examining rescued or killed migratory birds admitted to the Jeju Wildlife Rescue Center in Jeju National University. The collected ticks were identified to the species level under dissecting (Carl Zeiss Stemi DV4) or optical microscopes (Olympus CX31 and Nikon Eclipse Ci) using standard morphological keys (Yamaguti et al. 1971; Noh 1972); unidentifiable or suspicious ticks were sent to Toyama Institute of Health in Japan for confirmation. The identified ticks were kept for future destructive analysis for pathogen detection in the Jeju Wildlife Rescue Center.
Results We examined 934 migratory birds belonging to 75 species; 913 live birds of 65 species were captured and examined, and 21 carcasses/injured birds of 14 avian species kept at the rescue center were also examined. A total of 313 ticks of six Ixodidae species belonging to
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Fig. 1 Location of the study site, Jeju Island in Korea
two genera (Haemaphysalis and Ixodes) were collected from 74 individuals (7.95 % of the total examined migratory birds) across 17 avian species (Table 1). All ticks were found on or near head parts of the examined birds, with the exception of two ticks found among body feathers in the abdominal region. Only one adult tick (A) was collected while 169 were nymphs (N) and 143 were larvae (L). The most abundant species was Haemaphysalis flava Neumann (226 ticks, 72.2 % of the total; 105N and 121L) followed by Ixodes turdus Nakatsudi (54 ticks, 17.3 %; 38N and 16L). The other ticks collected were H. formosensis Neumann (14 ticks, 4.5 %; 14N), H. longicornis Neumann (12 ticks, 3.8 %; 1A, 5N, and 6L), H. concinna Koch (4 ticks, 1.3 %; 4N), and I. nipponensis Kitaoka and Saito (3 ticks, 1.0 %; 3N). Of the 17 identified host species, thrushes belonging to the genus Turdus and Zoothera accounted for 82.4 % of the infested birds and had higher infestation rates than the birds belonging to the other avian groups. Pale (Turdus pallidus; 39 birds, 52.7 %), White’s (Zoothera aurea; 11, 14.9 %), Gray-backed (Turdus hortulorum; 4, 5.4 %) and Eye-browed thrushes (Turdus obscurus; 4, 5.4 %) were the major avian hosts of the collected ticks. In particular, White’s thrushes hosted five of the six tick species found in this study. H. formosensis, a new tick species to Korea (Fig. 2), were collected from one Pale thrush (1N, 29 April 2011), one Siberian thrush (Zoothera sibirica; 2N, 16 May 2011), two White’s thrushes (9N and 1N, 9 and 14 April 2012), and one Eye-browed thrush (1N, 29 April 2012). Nymphs of H. concinna, new to the local tick fauna in Jeju Island, were collected from two Gray-backed thrushes (2N and 2N, 22 April 2012).
123
1
1
2
1
Himantopus himantopus
Cuculus canorus
Halcyon coromanda
Pitta nympha
20
9
127
Turdus cardis
Turdus hortulorum
Turdus obscurus
Turdus pallidus
74
2
2
1
39
4
4
2
11
1
1
1
1
1
1
1
1
1
No. of birds w/ticks
105
1
1
79
4
9
2
8
1
121
3
2
88
7
8
4
1
2
6
1
1
5
2
2
1
Nymph
Adult
Nymph
Larva
H. longicornis
Haemaphysalis flava
6
6
Larva
** New to Jeju Island, Korea
* New to Korea
A total of 934 migratory birds comprising 75 species were examined, but only infested birds were presented
287
33
Emberiza tristrami
Total
16
Emberiza elegans
1
10
Zoothera aurea
Periparus venustulus
4
23
Zoothera sibirica
9
Luscinia cyane
28
1
Ficedula narcissina
1
Buteo buteo
No. of examined birds
Pernis ptilorhynchus
Avian host
14
1
1
10
2
Nymph
H. formosensis*
Table 1 Ixodidae ticks collected from migratory birds and their hosts on Jeju Island, Korea from 2010 to 2012
4
4
Nymph
H. concinna**
38
5
18
1
7
1
6
Nymph
16
10
4
2
Larva
Ixodes turdus
3
2
1
Nymph
I. nipponensis
Exp Appl Acarol (2014) 62:557–566 561
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Fig. 2 A nymph of Haemaphysalis formosensis (a dorsal view, b ventral view) collected from an Eye-browed thrush (T. obscurus) on 29 April 2012 at Mara Islet, Seogwipo City on Jeju Island in the Republic of Korea. Scale bar indicates 0.5 mm
The mean number of ticks per bird (with standard deviation) in all examined birds was 0.35 ± 2.80. However, the number of ticks per infested bird ranged from 1–59 with an average of 4.5 ± 9.2 ticks per bird. Only one or two ticks were collected per bird in most cases (70.3 %; Fig. 3), but two Pale thrushes captured in November 2010 were severely infested: one with three nymphs and 47 larvae of H. flava, and the other with 56 H. flava (34N and 22L) and three I. turdus (2N and 1L) ticks.
Discussion Until now, ten Ixodidae species have been reported on Jeju Island, Korea. Haemaphysalis campanulata Warburton (Noh 1972), H. phasiana (Sames et al. 2008), H. flava (Sames et al. 2008; Moon et al. 2009), Ixodes persulcatus (Schulze) (Noh 1972), I. vespertilionis Koch (Noh 1972), I. pomeranzevi Serdyukova (Robbins and Keirans 1992), I. turdus (Sames et al. 2008), and I. nipponensis (Kim et al. 2011) have scattered and accidental records. Boophilus microplus (Canestrini) (Kim 1970; Yamaguti et al. 1971; Noh 1972; Moon and Kim 1986) and Haemaphysalis longicornis (Hoogstraal et al. 1968; Kim 1970; Yamaguti et al. 1971; Noh 1972; Moon and Kim 1986; Sames et al. 2008; Moon et al. 2009; Oh et al. 2009; Kim et al. 2011) are regarded as species common to the island, but
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563
Fig. 3 The number of ticks per tick-infested migratory bird collected from 2010 to 2012 on Jeju Island, Korea
Moon and Kim (1986) suggest that the B. microplus population on Jeju Island has declined possibly owing to active tick controls and changed vegetation management on ranches. Therefore, H. longicornis currently seems to be the most dominant and widely distributed species on Jeju Island, comprising 99.8–100 % of the local ticks collected by flag dragging (Moon et al. 2009; Oh et al. 2009). However, only 3.8 % of the total number of ticks collected in this study were H. longicornis, and the vast majority on the birds (89.5 %) were of the species H. flava and I. turdus, demonstrating a clear difference between the composition of the avian-borne and local terrestrial tick populations. We also found one species of tick that was new tick to Korea (H. formosensis) and another that was new to Jeju Island (H. concinna) on the migratory birds examined for this study. It is important to note that these two new species were collected in April and May, during the northward migration season. Since winter temperatures are an important limiting factor in tick survival and distribution, the northward expansion of exotic ticks is of special interest worldwide in terms of the effect of climate change on public and animal health concerns regarding emerging tick-borne diseases (Lindgren et al. 2000; Cumming and van Vuuren 2006). Therefore, the introduction of these exotic ticks and their potential settlement on Jeju Island become important issues to monitor given the changing climate conditions there. Ticks found on migratory birds, including the two most common species in this study, are known vectors of diverse zoonotic pathogens such as tick-borne encephalitis virus (Ko et al. 2010) and Anaplasma, Bartonella, and Borrelia species (Kang et al. 2013) in Korea. Given the occurrence of new ticks and the unique species compositions found on migratory birds, a possible influx of associate diseases, and changing local climates, our data suggests that exotic ticks and associated pathogens may be introduced to Jeju Island via migratory birds, leading to future changes in tick abundance and distribution on the island. In this study, we identified a dominant bird tick species (H. flava) and hosts (thrushes, particularly Pale thrushes). A previous tick surveillance on Hong Island, located 200 km northwest of Jeju Island, indicated that I. turdus (66.2 %) was the dominant species on migratory birds (Kim et al. 2009). In spite of the geographical proximity of the two bird stopover sites, migratory birds at each site may transport different species of ticks in different influx rates when the birds use distinct migration routes from diverse origins with unique tick density and distribution. The infestation prevalence of ticks on birds was 7.95 % in this study, which was higher than the rate of \0.5 % in the UK (Pietzsch et al. 2008), 1.4 % in the Republic of Korea
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(Kim et al. 2009), and 3.4 % in Sweden (Waldenstro¨m et al. 2007), but lower than the rate of 9.1–13.3 % (Miyamoto et al. 1993) and 10.0 % (Ishiguro et al. 2000) found in Japan, suggesting that the Jeju Island value falls within a normal range. The infestation of Turdidae thrushes was prominent possibly due to their ground feeding and dwelling habits (McClure et al. 1973, Pietzsch et al. 2008), their high abundance (as shown in Table 1), and their large body sizes and subsequent high chance of tick encounter. The infested birds were typically found to be carrying one or two ticks, but some birds were heavily infested. This may be related to the fact that birds in poor physical health tend to have heavy parasitic loads or vice versa, though contradictory evidence exists regarding this matter (Heylen and Matthysen 2008). Most of the ticks were found on or near the head because active and effective grooming of these areas using the beak is difficult (Miyamoto et al. 1993; Kim et al. 2009); the general habit of ticks to climb up may be another possible factor. Future works on how the physical condition and preening behaviors of birds affect their tick loads are required to better understand the interaction between ectoparasites and their hosts. It is also noteworthy that only one adult tick (0.32 %) was found out of 313 collected ticks, suggesting that birds harboring ticks were not definitive hosts. Compared with the tick surveillance of Korean mammals (Kim et al. 2011), adult ticks of H. flava, H. longicornis, and I. nipponensis were more common in mammalian hosts than adults of the conspecifics found in birds. This supports the hypothesis that birds may play an important role as an intermediate hosts rather than as a definitive host and therefore may disperse ticks to other sites and hosts. Yamaguti et al. (1971) also noted that immature H. flava and I. nipponensis parasitize birds while H. longicornis use diverse hosts. Human-induced climatic change has caused the recent change in migratory patterns of birds (Cotton 2003; Jenni and Ke´ry 2003), but the current status and effects of climate change on the migration of birds as well as the biology of their ectoparasites are poorly documented in East Asia. Our results demonstrate that migratory birds hosting ticks may affect existing local tick fauna by changing tick abundance and distribution. However, a detailed mechanism of tick introduction and long-distance movements through bird migration is still unclear. As social concerns about emerging diseases induced by climate change increase, more tick surveillance on birds will be required to understand the role of migratory animals in the introduction of exotic species and associated pathogens and in the life cycles of ticks at different stages in this region. 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 Abulreesh HH, Goulder R, Scott GW (2007) Wild birds and human pathogens in the context of ringing and migration. Ringing Migr 23:193–200 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 16:215–222 Choi HM, Lee JY (2012) Changes of groundwater conditions on Jeju volcanic island, Korea: implications for sustainable agriculture. Afr J Agric Res 7:647–661 Cotton PA (2003) Avian migration phenology and global climate change. PNAS 100:12219–12222 Cumming GS, van Vuuren DP (2006) Will climate change affect ectoparasite species ranges? Glob Ecol Biogeogr 15:486–497
123
Exp Appl Acarol (2014) 62:557–566
565
Heylen DJA, Matthysen E (2008) Effect of tick parasitism on the health status of a passerine bird. Funct Ecol 22:1099–1107 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 54:1197–1213 IPCC (2007) Climate change 2007: synthesis report. Intergovernmental Panel on Climate Change, Geneva 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 66:982–986 Jenni L, Ke´ry 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 270:1467–1471 Kang CW, Kang HM, Kim EM, Park CR, Ji NJ (2010) Birds in Jeju. Hangru Publishing, Jeju 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 13:215–225 Kim SH (1970) Study on the ticks of Chejudo: life cycle. Korean J Parasitol 8:51–57 (in Korean with English abstract) 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 14:3–10 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 49:331–335 Kinsey AA, Durden LA, Oliver JH (2000) Tick infestations of birds in coastal Georgia and Alabama. J Parasitol 86:251–254 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 11:197–203 Lee JY (2011) Environmental issues of groundwater in Korea: implications for sustainable use. Environ Conserv 38:64–74 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:e68512 Lindgren E, Ta¨lleklint 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 108:119–123 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., Bangkok 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 44:315–326 Moon CR, Kim SH (1986) Studies on the control of ticks and tick-borne diseases in exotic cattle in Chejudo. Livest Prod Annu Res Rep 1:31–35 (in Korean with English abstract) 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) 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 91:780–790 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) 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 39:257–267 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 155:328–332
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566
Exp Appl Acarol (2014) 62:557–566
Robbins RG, Keirans JE (1992) Systematics and ecology of the subgenus Ixodiopsis (Acari: Ixodidae: Ixodes). Entomological Society of America, Lanham 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 13:43–50 Waldenstro¨m J, Lundkvist A, Falk KI, Garpmo U, Bergstro¨m S, Lindengren G, Sjo¨stedt A, Mejlon H, Fransson T, Haemig PD, Olsen B (2007) Migrating birds and tick-borne encephalitis virus. Emerg Infect Dis 13:1215–1218 Yamaguti N, Tipton VJ, Keegan HL, Toshioka S (1971) Ticks of Japan, Korea, and the Ryukyu Islands. Brigham Young Univ Sci Bull Biol Ser 15:1–226
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