Hostname: page-component-76fb5796d-wq484 Total loading time: 0 Render date: 2024-04-26T05:55:47.066Z Has data issue: false hasContentIssue false
  • English
  • Français

Higher sika deer density is associated with higher local abundance of Haemaphysalis longicornis nymphs and adults but not larvae in central Japan

Published online by Cambridge University Press:  23 May 2013

Hideharu Tsukada ,
Yoshio Nakamura ,
Tsugihiko Kamio ,
Hisashi Inokuma ,
Yasuko Hanafusa ,
Naoko Matsuda ,
Tetsuya Maruyama ,
Takahiro Ohba  and
Koji Nagata
Hideharu Tsukada*
Affiliation:
NARO Institute of Livestock and Grassland Science, Shiono, Miyota, Nagano 389-0201, Japan
Yoshio Nakamura
Affiliation:
NARO Institute of Animal Health, Kannondai, Tsukuba, Ibaraki 305-0856, Japan
Tsugihiko Kamio
Affiliation:
Kyushu Research Station, NARO Institute of Animal Health, Chuzan, Kagoshima 891-0105, Japan
Hisashi Inokuma
Affiliation:
Department of Clinical Veterinary Medicine, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan
Yasuko Hanafusa
Affiliation:
NARO Institute of Animal Health, Kannondai, Tsukuba, Ibaraki 305-0856, Japan
Naoko Matsuda
Affiliation:
Tochigi Prefectural Citizen’s Park Management Office, Nagai, Yaita, Tochigi 329-2514, Japan
Tetsuya Maruyama
Affiliation:
Department of Environment and Forestry, Tochigi Prefectural Office, Tochigi 320-8501, Japan
Takahiro Ohba
Affiliation:
Shizuoka Prefecture Forestry and Forest Products Research Institute, Hamamatsu 434-0016, Japan
Koji Nagata
Affiliation:
Kanagawa Prefecture Natural Environment Conservation Center, Nanasawa, Atsugi-shi, Kanagawa 243-0121, Japan
*
*Author for correspondence Phone: +81 (0)267 32 0757 Fax: +81 (0)267 32 2318 E-mail: htsuka@affrc.go.jp
Get access Rights & Permissions [Opens in a new window]

Abstract

Haemaphysalis longicornis (Acari: Ixodidae) is one of the most common and important arthropod disease vectors in Japan, carrying Japanese spotted fever and bovine theileriosis. The recent expansion of sika deer (Cervus nippon, Artiodactyla: Cervidae) populations, the most common wild host of H. longicornis, has also caused concern about increasing the risk of vector-borne diseases in Japan. We used generalized linear mixed model analysis to determine the relative contribution of deer density and other biological and abiotic factors on the abundance of H. longicornis ticks questing at each developmental stage. A total of 6223 H. longicornis adults, nymphs, and larvae were collected from 70 sites in three regions of central Japan. The abundance of questing adult and nymphal ticks was associated with deer density and other biotic and abiotic factors. However, the abundance of questing larvae showed no association with deer density but did show an association with other biotic and abiotic factors. These findings show that a high density of deer along with other biotic and abiotic factors is associated with increased risk of vector-borne diseases through amplified local abundance of questing nymphal and adult H. longicornis. Further, questing larvae abundance is likely regulated by environmental conditions and is likely correlated with survival potential or the distribution of other host species.

Keywords

tick abundancebiological factorclimatic factorHaemaphysalis longicornissika deer
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 104 , Issue 1 , February 2014 , pp. 19 - 28
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Atwood, E.L. & Sonenshine, D.E. (1967) Activity of American dog tick Dermacentor variabilis (Acarina – Ixodidae) in relation to solar energy changes. Annals of the Entomological Society of America 60, 354–362.CrossRefGoogle ScholarPubMed
Benjamin, M.A., Zhioua, E. & Ostfeld, R.S. (2002) Laboratory and field evaluation of the entomopathogenic fungus Metarhizium anisopliae (Deuteromycetes) for controlling questing adult Ixodes scapularis (Acari: Ixodidae). Journal of Medical Entomology 39, 723–728.Google Scholar
Burnham, K.P. & Anderson, D.R. (2002) Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. New York, Springer-Verlag.Google Scholar
Chilton, N.B. & Bull, C.M. (1993) A comparison of the off-host survival times of larvae and nymphs of two species of reptile ticks. International Journal for Parasitology 23, 693–696.Google Scholar
Daniels, T.J., Fish, D. & Schwartz, I. (1993) Reduced abundance of Ixodes scapularis (Acari: Ixodidae) and Lyme disease risk by deer exclusion. Journal of Medical Entomology 30, 1043–1049.Google Scholar
Diuk-Wasser, M.A., Vourc'h, G., Cislo, P., Hoen, A.G., Melton, F., Hamer, S.A., Rowland, M., Cortinas, R., Hickling, G.J., Tsao, J.I., Barbour, A.G., Kitron, U., Piesman, J. & Fish, D. (2010) Field and climate-based model for predicting the density of host-seeking nymphal Ixodes scapularis, an important vector of tick-borne disease agents in the eastern United States. Global Ecology and Biogeography 19, 504–514.Google Scholar
Drew, M.L. & Samuel, W. (1986) Reproduction of the winter tick, Dermacentor albipictus, under field conditions in Alberta, Canada. Canadian Journal of Zoology 64, 714–721.Google Scholar
Duffy, D.C., Campbell, S.R., Clark, D., Dimotta, C. & Gurney, S. (1994) Ixodes scapularis (Acari: Ixodidae) deer tick mesoscale populations in natural areas: effects of deer, area, and location. Journal of Medical Entomology 31, 152–158.Google Scholar
Elias, S.P., Lubelczyk, C.B., Rand, P.W., Lacombe, E.H., Holman, M.S. & Smith, R.P. (2006) Deer browse resistant exotic-invasive understory: an indicator of elevated human risk of exposure to Ixodes scapularis (Acari: Ixodidae) in southern coastal Maine woodlands. Journal of Medical Entomology 43, 1142–1152.Google Scholar
Fernandes, E.K.K., Bittencourt, V.R.E.P. & Roberts, D.W. (2012) Perspectives on the potential of entomopathogenic fungi in biological control of ticks. Experimental Parasitology 130, 300–305.Google Scholar
Fujimoto, K. (1988) Ecological studies on ixodid ticks : 5. The effect of humidity on the oviposition and development of Haemaphysalis longicornis and H. flava (Acarina : Ixodidae). Japanese Journal of Sanitary Zoology 39, 27–33 (in Japanese with English summary).Google Scholar
Fujimoto, K. (1993) Tolerances of Haemaphysalis longicornis, H. flava, and Ixodes ovatus (Acari : Ixodidae) to high and low temperatures in relation to distribution patterns of these ticks in the Chichibu Mountains. Japanese Journal of Environmental Entomology and Zoology 5, 158–165.Google Scholar
Fujimoto, K. (1995) Effect of photoperiod on the host attachment and development in the tick, Haemaphysalis longicornis . Japanese Journal of Sanitary Zoology 46, 345–348.Google Scholar
Fujimoto, K. (2000) The host-feeding activity of Haemaphysalis longicornis nymphs (Acari : Ixodidae) in autumn observed under experimental conditions. Japanese Journal of Sanitary Zoology 51, 105–107.Google Scholar
Fujimoto, K. (2004) The host-feeding activity of Haemaphysalis longicornis larvae (Acari: lxodidae) in autumn observed under experimental conditions, with special reference to behavioral diapause. Bulletin of Saitama Medical School Junior College 15, 29–31.Google Scholar
Fujimoto, K. (2008) An experimental analysis on the autumn activity of the new generation of Haemaphysalis longicornis nymphs (Acari: Ixodidae) : the autumn activities of the nymphs that developed outdoors in August and September. Japanese Journal of Sanitary Zoology 59, 15–17.Google Scholar
Fujisaki, K., Kitaoka, S. & Morii, T. (1975) Effect of different combinations of temperature and humidity on the oviposition of Haemaphysalis longicornis and Boophilus microplus . Bulletin of the National Institute of Animal Health 70, 27–34.Google Scholar
Fujita, H. & Takada, N. (2007) Identification of immature ticks in Japan. pp. 53–68 in Organizing Committee of SADI (Ed.) Acari and Emerging Reemerging Infectious Disease. Tokyo, Zenkoku Noson Kyoiku Kyokai Publishing. (in Japanese).Google Scholar
Heath, A.C. (1981) The temperature and humidity preferences of Haemaphysalis longicornis, Ixodes holocyclus and Rhipicephalus sanguineus (Ixodidae): studies on engorged larvae. International Journal for Parasitology 11, 169–175.Google Scholar
Hoogstraal, H., Roberts, F.H., Kohls, G.M. & Tipton, V.J. (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). Journal of Parasitology 54, 1197–1213.Google Scholar
Igota, H., Sakuragi, M. & Uno, H. (2008) Seasonal migration of sika deer on Hokkaido Island, Japan. pp. 251–272 in McCullough, D., Kaji, K. & Takatsuki, S. (Eds) Sika Deer: Biology and Management of Native and Introduced Populations. Tokyo, Springer.Google Scholar
Inglis, G.D., Goettel, M.S., Butt, T. & Strasser, H. (2001) Use of hyphomycetous fungi for managing insect pests. pp. 23–69 in Butt, T.M., Jackson, C. & Magan, N. (Eds) Fungi as Biocontrol Agents: Progress Problems and Potential. Oxford, CAB International.Google Scholar
Inokuma, H., Fujimoto, T., Hosoi, E., Tanaka, S., Fujisaki, K., Okuda, M. & Onishi, T. (2002) Tick infestation of sika deer (Cervus nippon) in the western part of Yamaguchi Prefecture, Japan. Journal of Veterinary Medical Science 64, 615–617.Google Scholar
Inokuma, H., Tsuji, T., Kim, S.J., Fujimoto, T., Nagata, M., Hosoi, E., Arai, S., Ishihara, C., Okuda, M. (2004) Phylogenetic analysis of Theileria sp. from sika deer, Cervus nippon, in Japan. Veterinary Parasitology 120, 339–345.Google Scholar
Inokuma, H., Seino, N., Suzuki, M., Kaji, K., Takahashi, H., Igota, H. & Inoue, S. (2008) Detection of Rickettsia helvetica DNA from peripheral blood of Sika deer (Cervus nippon yesoensis) in Japan. Journal of Wildlife Diseases 44, 164–167.Google Scholar
Inokuma, Y. & Yokoyama, N. (2010) Study on factors to decrease risk for Theileria orientalis infection of cattle in pastureland in Eastern Hokkaido. Japanese Journal of Clinical Bovine Parasitology 1, 13–17 (in Japansese with English Summary).Google Scholar
Ishihara, T. (1968) Bovine piroplasmosis in Japan. Japanese Agricultural Research Quarterly 3, 23–54.Google Scholar
Iwamoto, T., Sakata, T., Nakazono, T., Kaoka, H., Ikeda, K., Nishishita, Y., Tokida, K. & Doi, T. (2000) Improvement of the pellet count method for the estimation of sika deer density. Mammalian Science 40, 1–17 (in Japanese with English summary).Google Scholar
Izumiyama, S. & Mochizuki, T. (2008) Seasonal range use of Sika deer which inhabits the sub-alpine zone in the Southern Japan Alps. Bulletin Shinshu University Alpine Field Center 30, 25–32 (in Japanese with English summary).Google Scholar
Japan Meteorological Agency (2002) Mesh Climatic Data 2000. Tokyo, Japan Meteorological Business Support Center.Google Scholar
Jensen, P. & Jespersen, J. (2005) Five decades of tick-man interaction in Denmark - an analysis. Experimental and Applied Acarology 35, 131–146.CrossRefGoogle ScholarPubMed
Johnson, J.B. & Omland, K.S. (2004) Model selection in ecology and evolution. Trends in Ecology and Evolution 19, 101–108.Google Scholar
Jouda, F., Perret, J.L. & Gern, L. (2004) Ixodes ricinus density, and distribution and prevalence of Borrelia burgdorferi sensu lato infection along an altitudinal gradient. Journal of Medical Entomology 41, 162–169.Google Scholar
Kaaya, G.P. & Hassan, S. (2000) Entomogenous fungi as promising biopesticides for tick control. Experimental and Applied Acarology 24, 913–926.CrossRefGoogle Scholar
Kamio, T., Fujisaki, K. & Minami, T. (1989) Correlation between the infection rate of the vector tick, Haemaphysalis longicornis and the parasitaemia of cattle infected with Theileria sergenti . Annals of Tropical Medicine and Parasitology 83, 77–83.Google Scholar
Kitaoka, S., Morii, T. & Fujisaki, K. (1975) Consideration on the grazing cattle-tick relationship in Japan with special reference to large wild mammals and the deer-tick ecosystem in the Tanzawa Mountains. Bulletin of the National Institute of Animal Health 70, 35–42 (in Japanese).Google Scholar
Mahara, F. (1997) Japanese spotted fever: report of 31 cases and review of the literature. Emerging infectious diseases 3, 105–111.CrossRefGoogle ScholarPubMed
Maruyama, N. & Furubayashi, K. (1983) Preliminary examination of block count method for estimating numbers of sika deer in Fukadake. Journal of the Mammalogical Society of Japan 9, 274–278.Google Scholar
McEnroe, W. (1984) The effect of snowcover on an American dog tick, Dermacentor variabilis (Say.)(Acari, Ixodidae) population under a harsh winter environment. Zeitschrift für Angewandte Entomologie 97, 481–484.Google Scholar
Mori, K. & Tsunoda, T. (1996) Migration of Larvae in the Tick, Haemaphysalis longicornis NEUMANN (Acarina, Ixodidae). Japanese Journal of Environmental Entomology and Zoology 7, 211–213 (in Japanese with English summary).Google Scholar
Mori, K., Tsunoda, T., & Fujimagari, M. (1995) Ixodid ticks on sika deer Cervus nippon Temminck in Chiba prefecture. Medical Entomology and Zoology 46, 313–316 (in Japanese with English summary).Google Scholar
Motokuni, T., Tarumi, H., Miyamura, H., Kameide, N. & Sunaga, T. (1999) Analysis of DUV values of ground arrival ultra violet radiation based on weather classification: part2 seasonal change of daily accumulations of UV-B/DUV and relation to solar radiation. pp. 677–678. in Summaries of Technical Papers of Annual Meeting Architectural Institute of Japan. D-1, Environmental Engineering I. Hiroshima, Architectural Institute of Japan (in Japanese).Google Scholar
Needham, G.R. & Teel, P.D. (1991) Off-host physiological ecology of ixodid ticks. Annual Review of Entomology 36, 659–681.Google Scholar
Ohdachi, S.D., Ishibashi, Y., Iwasa, M.A. & Saitoh, T. (2009) The Wild Mammals of Japan. Kyoto, Shoukadoh Book Sellers.Google Scholar
Okino, T., Ushirogawa, H., Matoba, K. & Hatsushika, R. (2008) Bibliographical studies on human cases of hard tick (Acarina: Ixodidae) bites in Japan (2) Cases of Haemaphysalis longicornis and H. fulava infestation. Kawasaki Medical Journal 34, 185–201 (in Japanese with English summary).Google Scholar
Oorebeek, M. & Kleindorfer, S. (2008) Climate or host availability: what determines the seasonal abundance of ticks? Parasitology Research 103, 871–875.Google Scholar
Ostfeld, R.S., Price, A., Hornbostel, V.L., Benjamin, M.A. & Keesing, F. (2006) Controlling ticks and tick-borne zoonoses with biological and chemical agents. BioScience 56, 383–394.Google Scholar
Rand, P.W., Lubelczyk, C., Lavigne, G.R., Elias, S., Holman, M.S., Lacombe, E.H. & Smith, R.P. (2003) Deer density and the abundance of Ixodes scapularis (Acari: Ixodidae). Journal of Medical Entomology 40, 179–184.Google Scholar
R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, Available online at http://www.R-project.org/.Google Scholar
Ruiz-Fons, F. & Gilbert, L. (2010) The role of deer as vehicles to move ticks, Ixodes ricinus, between contrasting habitats. International Journal for Parasitology 40, 1013–1020.Google Scholar
Shimizu, G., Yoshizawa, K., Egashira, K., Hidaka, T. & Yamamoto, T. (2006) Measurements of solar UV radiation for 1996–2009. in Pref. Yamanashi. Annual Report of the Yamanashi Institute for Public Health 50, 61–66 (in Japanese).Google Scholar
Skaug, H., Fournier, D., Nielsen, A., Magnusson, A. & Bolker, B. (2012) Generalized Linear Mixed Models using AD Model Builder. R package version 0.7.2.12. Available online at http://glmmadmb.r-forge.r-project.org.Google Scholar
Stafford, K.C., Denicola, A.J. & Kilpatrick, H.J. (2003) Reduced abundance of Ixodes scapularis (Acari : Ixodidae) and the tick parasitoid Ixodiphagus hookeri (Hymenoptera : Encyrtidae) with reduction of white-tailed deer. Journal of Medical Entomology 40, 642–652.Google Scholar
Sutherst, R. & Bourne, A. (2006) The effect of desiccation and low temperature on the viability of eggs and emerging larvae of the tick, Rhipicephalus (Boophilus) microplus (Canestrini) (Ixodidae). International Journal for Parasitology 36, 193–200.Google Scholar
Sutherst, R.W. & Bourne, A.S. (1991) Development, survival, fecundity and behaviour of Haemaphysalis (Kaiseriana) longicornis (Ixodidae) at two locations in southeast Queensland. International Journal for Parasitology 21, 661–672.Google Scholar
Tagliapietra, V., Rosà, R., Arnoldi, D., Cagnacci, F., Capelli, G., Montarsi, F., Hauffe, H. & Rizzoli, A. (2011) Saturation deficit and deer density affect questing activity and local abundance of Ixodes ricinus (Acari, Ixodidae) in Italy. Veterinary Parasitology 183, 114–124.Google Scholar
Takatsuki, S. (1992) Foot morphology and distribution of Sika deer in relation to snow depth in Japan. Ecological Research 7, 19–23.Google Scholar
Takatsuki, S. (2009) Effects of sika deer on vegetation in Japan: a review. Biological Conservation 142, 1922–1929.Google Scholar
Takatsuki, S. & Maeyama, E. (2007) What is happening in the sika deer habiat in western Tokyo: degradation of Okutama Mountains. Biological Science 59, 50–56 (in Japanese).Google Scholar
Takatsuki, S., Suzuki, K. & Higashi, H. (2000) Seasonal elevational movements of sika deer on Mt. Goyo, northern Japan. Mammal Study 2, 107–114.Google Scholar
Tsukada, H. (2011) Effect of grazing on habitat and behavior of wild mammals. Journal of Integrated Field Science 8, 49–54.Google Scholar
Tsunoda, T. (2007 a) Seasonal change in habitat use by Haemaphysalis longicornis (Acari: Ixodidae): plant, litter, and soil. Journal of Medical Entomology 44, 575–579.Google Scholar
Tsunoda, T. (2007 b) Ticks of the Tanzawa Mountains. pp. 360–362 in The Research Group of the Tanzawa Mountains (Ed.) Results of the Sceinetific Research on the Tanzawa Mountains. Sagamihara, Hiraoka Environmental Science Laboratory (in Japanese).Google Scholar
Tsunoda, T. (2007 c) Interspecific and intraspecific associations of two species of hard ticks, Haemaphysalis longicornis and Haemaphysalis megaspinosa, in relation to questing site. Journal of Parasitology 93, 531–541.Google Scholar
Tsunoda, T. (2008) Influence of aggregation and relative humidity on longevity of unfed bush tick, Haemaphysalis longicornis Neumann (Acari: Ixodidae). Journal of Parasitology 94, 990–992.Google Scholar
Tsunoda, T. & Tatsuzawa, S. (2004) Questing height of nymphs of the bush tick, Haemaphysalis longicornis, and its closely related species, H. mageshimaensis: correlation with body size of the host. Parasitology 128, 503–509.Google Scholar
Wildlife Management Office (2009) A Report on the Present Population Status of Sika Deer in Kanagawa Prefecture in 2008. Kanagawa, Wildlife Management Office (in Japanese).Google Scholar
World Health Organization (2002) Global Solar UV Index: A Practical Guide. Geneva, World Health Organization.Google Scholar
Yabe, T. & Takatsuki, S. (2009) Migratory and sedentary behavior patterns of sika deer in Honshu and Kyushu, Japan. pp. 273–283 in McCullough, D., Kaji, K. & Takatsuki, S. (Eds) Sika Deer: Biology and Management of Native and Introduced Populations. Tokyo, Springer.Google Scholar
Yamaguchi, N., Tipton, V., Keegan, H. & Toshioka, S. (1971) Ticks in Japan, Korea and Ryukyuislands. Brigham Young University Science Bulletin Biological Series 15, 1–226.Google Scholar
Yamane, I., Nishiguchi, A., Kobayashi, S. & Zeniya, Y. (2006) Cross-sectional survey of ixodid tick species on grazing cattle in Japan. Experimental and Applied Acarology 38, 67–74.Google Scholar
Yamane, I., Nakamura, Y. & Tsukada, H. (2009) A Report on National Survey for Cattle Grazing Fields. Tsukuba, National Institute of Animal Health (in Japanese).Google Scholar
Yamashiro, T. (2000) The propaties of an entomopathogenic fungus: the effects of ultraviolet and agricultural chemicals on sterillization of Beauveria bassiana . Tochigi-ken Sangyō Sentā kenkyū yōhō [Bulletin of Tochigi-ken Sericultural Center Resarch] 42, 53–56 (in Japanese).Google Scholar
Yamauchi, T., Tabara, K., Kanamori, H., Kawabata, H., Arai, S., Katayuama, T., Fujita, H., Yano, Y., Takada, N. & Itagaki, A. (2009) Tick fauna associated with sika deer density in the Shimane peninsula, Honshu, Japan. Medical Entomology and Zoology 60, 297–304.Google Scholar