Ticks (Acari: Ixodidae) from medium-sized to large mammals in Ehime Prefecture, Japan Takeo Yamauchi, Shinji Yano, Takahito Yamamoto, Eiji Yamamoto & Taisuke Miyamoto Experimental and Applied Acarology ISSN 0168-8162 Volume 60 Number 2 Exp Appl Acarol (2013) 60:263-270 DOI 10.1007/s10493-012-9643-9
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Author's personal copy Exp Appl Acarol (2013) 60:263–270 DOI 10.1007/s10493-012-9643-9
Ticks (Acari: Ixodidae) from medium-sized to large mammals in Ehime Prefecture, Japan Takeo Yamauchi • Shinji Yano • Takahito Yamamoto Eiji Yamamoto • Taisuke Miyamoto
•
Received: 9 July 2012 / Accepted: 29 November 2012 / Published online: 15 December 2012 Ó Springer Science+Business Media Dordrecht 2012
Abstract Ixodid ticks were collected from medium-sized to large mammals in Ehime Prefecture, Shikoku, Japan. Ten species of ticks (Amblyomma testudinarium, Dermacentor taiwanensis, Haemaphysalis flava, H. formosensis, H. hystricis, H. longicornis, H. megaspinosa, Ixodes nipponensis, I. ovatus, and I. tanuki) were collected from a total of 29 mammals comprising 11 species. Haemaphysalis hystricis, a possible vector of Japanese spotted fever in Ehime prefecture, was collected from Canis lupus familiaris (domestic dog), Martes melampus melampus, and Sus scrofa leucomystax. This is a first report of H. hystricis from the domesticated dog in the endemic area of Japanese spotted fever. This suggests that it is necessary to pay attention to dogs as a host of the vector ticks for Japanese spotted fever control. Nyctereutes procyonoides and Ma. melampus are new hosts for A. testudinarium. Nyctereutes procyonoides, Mustela itatsi, and Lepus brachyurus are new hosts for H. formosensis. Martes melampus is a new host for H. hystricis.
T. Yamauchi (&) Entomological Laboratory, Faculty of Agriculture, Ehime University, Tarumi, Matsuyama, Ehime 790-8566, Japan e-mail:
[email protected] Present Address: T. Yamauchi Toyama Institute of Health, Imizu, Toyama 939–0363, Japan S. Yano Omogo Mountain Museum, Wakayama, Kumakogen, Ehime 791-1710, Japan T. Yamamoto Saijo Nature School, Oofuki, Saijo, Ehime 793-0214, Japan E. Yamamoto Yamamoto Institute of Forest Biology, Yoshinokawa, Uchiko, Ehime 791-3511, Japan T. Miyamoto Nature Kikaku Wildlife Research Office, Kakihara, Uwajima, Ehime 798-0027, Japan
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Keywords Amblyomma Dermacentor Haemaphysalis Ixodes New host Possible vector
Introduction Ticks that feed on vertebrate blood are of medical and veterinary importance because they are vectors for various diseases. The tick life cycle is closely associated with wild mammals. Knowledge of host associations is therefore essential in studying tick-borne diseases and control efforts. Japanese spotted fever (JSF), caused by infection of Rickettsia japonica, is one tickborne disease in Japan. Since the first case of JSF was reported in 1984 (Mahara et al. 1985), many cases of JSF rickettsiosis have been reported, mainly in the western part of Japan and Pacific coastal areas. Japanese spotted fever patients have been reported in Uwajima and Matsuyama Cities of Ehime Prefecture, Shikoku, Japan (Kondo et al. 2005). Inari et al. (2006) found that R. japonica was highly infected with Haemaphysalis hystricis Supino in the areas near the residence of the patient. For JSF control, it is important to study host associations of the possible vector of JSF in the endemic area of JSF and surrounding areas. However, there is not enough information on ticks collected from medium-sized to large mammals in Ehime Prefecture (Yamaguti et al. 1971; Sakai 1995; Kitaoka and Yamamoto 2000; Shimada et al. 2003a, b). Only masked palm civet Paguma larvata (C. E. H. Smith) was recorded as a host for H. hystricis in the prefecture (Kitaoka and Yamamoto 2000). In the present study, we surveyed ixodid ticks parasitized medium-sized to large mammals in Ehime Prefecture. Materials and methods From November 2002 to December 2011, ixodid ticks were collected by the washing method and/or visual inspection from alive or fresh dead- mammals found in five cities (Shikokuchuo, Niihama, Saijo, Ozu, and Uwajima) and two towns (Kumakogen and Matsuno) of Ehime Prefecture, Shikoku, Japan (Fig. 1). A total of 29 mammals consisting 11 species: Japanese red fox Vulpes vulpes japonica Gray (n = 3), raccoon dog Nyctereutes procyonoides procyonoides (Gray) (n = 4), domestic dog Canis lupus familiaris L. (n = 2), Japanese marten Martes melampus melampus (Wagner) (n = 5), Japanese weasel Mustela itatsi itatsi (Temminck) (n = 3), Japanese Badger Meles meles anakuma Temminck (n = 3), Pa. larvata (n = 1), domestic cat Felis silvestris catus (L.) (n = 1), Japanese wild boar Sus scrofa leucomystax (Temminck and Schlegel) (n = 1), sika deer Cervus nippon nippon Temminck (n = 2), and Japanese hare Lepus brachyurus brachyurus Temminck (n = 4) were surveyed (Table 1). Of these mammals, only C. lupus familiaris and F. silvestris catus were domesticated. The ticks were preserved in 70 % ethanol and morphologically identified according to Yamaguti et al. (1971) and Fujita and Takada (2007). Results In total, 386 ixodid ticks (77 larvae, 200 nymph, and 109 adults) were collected. They were morphologically classified as four genera and 10 species: Amblyomma testudinarium Koch, Dermacentor taiwanensis Sugimoto, Haemaphysalis flava Neumann, Haemaphysalis
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Fig. 1 Map of Ehime Prefecture, Shikoku, Japan. 1; Shikokuchuo City, 2; Niihama City, 3; Saijo City, 4; Kumakogen Town, 5; Ozu City, 6; Matsuno Town, 7; Uwajima City
formosensis Neumann, H. hystricis, Haemaphysalis longicornis Neumann, Haemaphysalis megaspinosa Saito, Ixodes nipponensis Kitaoka and Saito, Ixodes ovatus Neumann, and Ixodes tanuki Saito (Table 2). Haemaphysalis flava was most abundant (n = 259) and collected from nine host species: V. vulpes japonica, N. p. procyonoides, Ca. lupus familiaris, Ma. m. melampus, Mu. itatsi itatsi, M. meles anakuma, Pa. larvata, Ce. nippon nippon, and L. b. brachyurus. Haemaphysalis longicornis and H. megaspinosa were also abundant (both n = 30) and collected from four (N. p. procyonoides, Ca. lupus familiaris, Ma. m. melampus, and M. meles anakuma) and two (Ca. lupus familiaris and Ce. nippon nippon) host species, respectively. Host mammals of the remaining ticks were as follows: A. testudinarium (N. p. procyonoides, Ca. lupus familiaris, Ma. m. melampus, M. meles anakuma, and S. scrofa leucomystax), D. taiwanensis (S. scrofa leucomystax), H. formosensis (N. p. procyonoides, Ca. lupus familiaris, Mu. itatsi itatsi, and L. b. brachyurus), H. hystricis (Ca. lupus familiaris, Ma. m. melampus, and S. scrofa leucomystax), I. nipponensis (Ma. m. melampus and L. b. brachyurus), I. ovatus (V. vulpes japonica, N. p. procyonoides, Ma. m. melampus, F. silvestris catus, and L. b. brachyurus), and I. tanuki (N. p. procyonoides, Ma. m. melampus, Mu. itatsi itatsi, and M. meles anakuma). Host species yielding a rich fauna of tick species included Ma. m. melampus (eight tick species), N. p. procyonoides (six), and Ca. lupus familiaris (six). Discussion To date, 16 ixodid species have been recorded from Ehime Prefecture: A. testudinarium, D. taiwanensis, H. flava, H. formosensis, H. hystricis, Haemaphysalis kitaokai Hoogstraal,
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Table 1 Medium-sized to large mammals examined for ticks in Ehime Prefecture, Shikoku, Japan Host
Locality
Date
Vulpes vulpes japonica
Oofuki, Saijo City
15 Apr. 2009
Shimohatanokawa, Kumakogen Town
29 May 2006
Nyctereutes p. procyonoides
Canis lupus familiaris Martes m. melampus
Mustela i. itatsi
Meles meles anakuma
Nakagumi, Kumakogen Town
13 Sep. 2006
Shibukusa, Kumakogen Town
15 Mar. 2008
Ainoki, Kumakogen Town
7 Nov. 2003
Tsuchigoya, Kumakogen Town
20 Nov. 2002
Nobinono, Matsuno Town
18 Mar. 2006
Kakihara, Uwajima City
18 May 2010
Kakihara, Uwajima City
6 Jun. 2010
Nanatori, Kumakogen Town
1 Mar. 2004
Kasagata, Kumakogen Town
18 Dec. 2008
Shibukusa, Kumakogen Town
19 Dec. 2008
Fujinokawa, Ozu City
9 Oct. 2011
Yamatosaka, Hijikawa-choˆ, Ozu City
13 Jul. 2005
Yoshino, Matsuno Town Natsume-choˆ, Uwajima City
6 Dec. 2003
Kakihara, Uwajima City
13 Nov. 2005
Ishizuchi-skyline (6 km), Kumakogen Town
25 Apr. 2008
Honkumi, Kumakogen Town Yamatosaka, Hijikawa-choˆ, Ozu City
8 Oct. 2004
23 Dec. 2004
24 Jun. 2005
Paguma larvata
Nakagumi, Kumakogen Town
17 Oct. 2006
Felis silvestris catus
Urayama, Saijo City
10 Apr. 2010
Sus scrofa leucomystax
Mitsuma, Uwajima City
10 Jul. 2010
Cervus n. nippon
Kinsya-cho, Shikokuchuo City
25 Feb. 2006
Mishima, Shikokuchuo City
24 Oct. 2009
Daieizan, Niihama City
25 Jun. 2004
Lepus b. brachyurus
Kasagata, Kumakogen Town
16 Aug. 2006
Kakihara, Uwajima City
29 Dec. 2011
Kurose, Saijo City
29 Nov. 2009
H. longicornis, H. megaspinosa, Ixodes monospinosus Saito, I. nipponensis, I. ovatus, Ixodes persulcatus Schulze, Ixodes simplex simplex Neumann, I. tanuki, Ixodes turdus Nakatsudi, and Ixodes vespertilionis Koch (Kimura 1987; Kitaoka and Yamamoto 2000; Inari et al. 2006; Yamauchi 2012). All tick species collected in the present study were already reported from the prefecture. Amblyomma testudinarium is known as the vector of Rickettsia tamurae (Fournier et al. 2006). Adult ticks are especially depending on the large-sized mammals. On the other hand, immature forms are parasitized small- to medium-sized mammals, birds, reptiles, and amphibians (Yamaguti et al. 1971; Kitaoka and Suzuki 1974). Nyctereutes procyonoides and Ma. melampus are new hosts for A. testudinarium. Haemaphysalis formosensis was recorded from Ca. lupus familiaris, small Asian mongoose Herpestes javanicus (E´. Geoffroy), Amami rabbit Pentalagus furnessi (Stone), S. scrofa, Amami woodcock Scolopax mira Hartert, jungle crow Corvus macrorhynchos
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2
2 3
PL (n = 1)
1
FS (n = 1)
SS (n = 1)
1
1
I. ovatus
Ixodes nipponensis
#
$
N
#
N
L
#
1
1
1
14
1
$ 1
14
3
N
4
5 11
N
3
8
1
32
H. megaspinosa
23
1
2
22
CN (n = 2)
H. longicornis
3
#
9 5
N
H. hystricis
2
1
$
N
H. formosensis
6
# 3
3
$ 2
38
1
63
2
N
Haemaphysalis flava
L
3 1
#
1
1
MMA (n = 3)
$
10
1 4
MI (n = 3)
1
1
MMM (n = 5)
$
3
1
N
CL (n = 2)
L
NP (n = 4)
Dermacentor taiwanensis
Amblyomma testudinarium
VV (n = 3)
Table 2 Ticks obtained from medium-sized to large mammals in Ehime Prefecture, Shikoku, Japan
3
1
5
1
11
8
24
LB (n = 4)
1
5
1
1
1
5
14
2
14
30
3
9
1
14
40
20
132
67
1
3
1
6
5
Total
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123 MI (n = 3)
#
1
MMA (n = 3)
PL (n = 1)
FS (n = 1)
SS (n = 1)
CN (n = 2)
LB (n = 4)
1
8
1
Total
CL, Canis lupus familiaris ; CN, Cervus n. nippon ; FS, Felis silvestris catus ; LB, Lepus b. brachyurus ; MI, Mustela i. itatsi ; MMA, Meles meles anakuma ; MMM, Martes m. melampus ; NP, Nyctereutes p. procyonoides ; PL, Paguma larvata ; SS, Sus scrofa leucomystax ; VV, Vulpes vulpes japonica
1
1 3
MMM (n = 5)
2
2
CL (n = 2)
$
NP (n = 4)
N
VV (n = 3)
L, larvae; N, nymphs; $, adult female; #, adult male
I. tanuki
Table 2 continued
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connectens Stresemann in Japan (Yamaguti et al. 1971; Kitaoka and Suzuki 1974; Ishibashi et al. 2009). Nyctereutes procyonoides, Mu. itatsi, and L. brachyurus are new hosts for H. formosensis. Haemaphysalis hystricis is known as one of the most important vectors of R. japonica, the agent of JSF (Takada et al. 1992; Mahara 2008). The vector tick was recorded from Ca. lupus familiaris, Pa. larvata, Iriomote cat Prionailurus bengalensis iriomotensis (Imaizumi), H. javanicus, cattle Bos taurus L., S. scrofa, black rat Rattus rattus (Linnaeus), Amami spiny rat Tokudaia osimensis (Abe), Pe. furnessi in Japan (Yamaguti et al. 1971; Asanuma et al. 1977; Kitaoka and Suzuki 1981; Kakuda et al. 1989; Ishibashi et al. 2009). In the present study, H. hystricis was collected from Ca. lupus familiaris, Ma. m. melampus, and S. scrofa leucomystax. Martes melampus is new host for H. hystricis. Haemaphysalis hystricis, a possible vector of JSF in Ehime prefecture, was collected from Ca. lupus familiaris and S. scrofa leucomystax in Uwajima City, the endemic area of JSF. This is a first report of H. hystricis from the domesticated Ca. lupus familiaris in the endemic area of JSF. This suggests that it is necessary to pay attention to Ca. lupus familiaris as a host of the vector ticks for JSF control. Recently, the population of S. scrofa leucomystax, one of the main hosts of H. hystricis, has increased in Ehime Prefecture (Yamauchi et al. 2008; Miyamoto personal observation). The spread of S. scrofa leucomystax in recent years may be related to the increase in the number of JSF patients in Ehime Prefecture. Acknowledgments We are deeply indebted to Mr. Masatoshi Ishiyama (Uwajima City), Mr. Takashi Takino (Ozu City), Mr. Eiji Tsumura (Foundation of Matsuno Town Sightseeing public corporation Nijinomori-park Osakanakan), Mr. Hidetsuna Mitsuda (Kumakogen Town), Mr. Kiyokazu Hashigoe (Uwajima City), and Mr. Naohiko Togame (Kumakogen Town) for supplying the valuable host mammals. The first author is grateful to the late Mrs. Kyoko Yamauchi (Ehime Women’s College) for her assistance in the survey in Uwajima City. This study was supported in part by Grants-in-Aid for Scientific Research on Emerging and Re-emerging Infectious Diseases from the Japanese Ministry of Health, Labor, and Welfare (H21-shinkou-ippan-005, 006).
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