J. Acarol. Soc. Jpn., 14(1): 31-34. May 25, 2005  The Acarological Society of Japan 31

[SHORT COMMUNICATION] A Cysticercoid in Mixacarus exilis (: ) Nymph as an Intermediate Host of Anoplocephalid Cestodes

1,2† 1‡ Satoshi SHIMANO * and Kiyoshi KAMIMURA 1 Department of Biodefence Medicine, Toyama Medical and Pharmaceutical University, Toyama, 930- 0194 Japan 2 Department of Upland Farming, National Agricultural Research Center for Tohoku Region, Fukushima 960-2156 Japan (Received 9 February 2004; Accepted 23 April 2005)

Key words: cysticercoid, Enarthronota, intermediate host as nymph, Mixacarus exilis Oribatida, tapeworm

INTRODUCTION

Oribatid have been known to serve as intermediate hosts of some tapeworm , such as and Moniezia, parasites of herbivorous . Since Stunkard (1937) discovered that an oribatid , Galumna sp., are the vectors of an anoplocephalid tapeworm, , many relationships between particular oribatid mite species and various cestode groups have been examined. Kates and Runkel (1948) suggested that efficiency as intermediate host was different according to the species of mites. In subse- quent years, various studies were conducted on the host-parasite relationship between tapeworms and oribatid mites (Haq, 1988; Rajski, 1959; Sengbusch, 1977). Denegri (1993) reported a list of oribatid mites including 127 species in 27 families that can serve as intermediate hosts for 27 species in 14 genera of anoplocephalid tapeworms. In the present study, a primitive oribatid species belonging to family Lohmanniidae (cohort: Enarthronota) was newly found to be an intermediate host species. Additionally, nymphal mites have never been reported as intermediate hosts of these tapeworms previously, but we found a nymphal Mixacarus mite that was carrying a cycticercoid.

MATERIALS AND METHODS

Samples were collected from small woodland at Yokohama National University,

日本産フトツツハラダニ Mixacarus exilis から見いだされた裸頭条虫科条虫の擬嚢尾虫 1,2† 1‡ 1 2 島野 智之 *・上村 清 （ 富山医科薬科大学・医学部・感染予防医学研究室 東北農業研究セン † ター・畑地利用部 現住所： 宮城教育大学 環境教育実践研究センター，〒 980–0845 仙台市青葉区荒 ‡ 巻字青葉 149； 〒 630–0194 富山市婦負郡婦中友坂 243） *Corresponding author: e-mail: [email protected] † Present address: Environmental Education Center, Miyagi University of Education, Aramaki Aza-Aoba, Aoba-ku, Sendai, Miyagi 980–0845, Japan ‡ Present address: 243, Tomosaka, Hutyuu, Nei-gun Toyama 930–0194 Japan 32 Satoshi SHIMANO and Kiyoshi KAMIMURA

Kanagawa Prefecture, Japan in August 1995. This woodland mainly consists of chinquapin (Castanopsis cuspidata var. sieboldii Nakai), and is inhabited by various birds, raccoon dog (Nyctereutes procyonoides), dog and cat. A total of 2,500 cm2 soil and litter samples were collected from 0–5 cm depth of the woodland floor. The oribatid mites were extracted from the samples by Berlese funnels. Collected mites were fixed in 80% ethanol and mounted on slides with Hoyer’s medium. Specimens of mites were examined with light microscopy for the identification of mite species and presence of cysticercoids. Identification of oribatid species was mainly based on the descriptions published by Aoki (1970), and cysticercoids of the tapeworms were compared with the descriptions by Kates and Runkel (1948), Kassai and Mahunka (1965) and Prokopic (1962). The identification was unfortunately impossible, because the one specimen of cysticercoid was already fixed and would not be able to use to the infection study.

RESULTS AND DISCUSSION

From the soil and litter sampled, 683 oribatid mites were collected. Among them, one deutonymphal individual (body length 437 µm: Fig. A) was found to be infected with a cysticercoid (diameter 84–88 µm: Fig. B) that could be easily differentiated from the internal organs of the mite by the presence of 3 disks (Figs. B, C). Generally, these anoplocephalid tapeworms have four disks, but we could not confirm four disks. This mite was identified as Mixacarus exilis Aoki, 1970 in the primitive family Lohman- niidae by S. Shimano, one of the authors. This is the first report of a species of this family and cohort serving as a tapeworm intermediate host. The family, Lohmanniidae, was removed from Mixonomata to the primitive group of oribatid mite, Enarthronota by Norton (2001). Although this species represented almost 10% (66exs.) of the mites recovered, only one nymph was found infected. Previous precise records of oribatid intermediate hosts have been only of adult mites. To our knowledge, this is also the first record of a nymphal mite carrying a cysticercoid. Among the various papers which reported the relationship between cestodes and oribatid mites hosts in Japan, some studies confirmed the cestode infection (Isoda et al., 1966; Misaka and Ichisawa, 1977; Watanabe et al., 1957), and others were fundamental surveys of oribatid community structure and/or abundance of potential intermediate host species of oribatids in grazing land (Aoki, 1962; Nakamura, 1973; Sanada and Aoki, 1999) for the purpose of biodefence of merino , racehorses, and general livestock. Although many investigations were carried out on grazing land throughout Japan, observations of cysticer- coids in oribatid mites were reported only in three instances before our study. Eporibatula sakamorii (Aoki, 1970) is usually distributed in greenlands (Watanabe et al., 1957), moss cushions growing on city constructions and other inferior environments (Aoki, 2000). Another reported mite host was Scheloribates laevigatus (C. L. Koch, 1836) (Isoda et al., 1966). This species is distributed in greenlands also, and sometimes occupies the position of dominant species (e.g. Kates and Runkel, 1948). The remaining one instance was reported as an unidentified species (Misaka and Ichisawa, 1977). In Japan, tapeworm infection seems Cysticercoid in Mixacarus exilis Nymph 33

Fig. A deutonymph of Mixacarus exilis Aoki, 1976, with a cysticercoid in the internal body. A: Whole body: normal compound microscope observation, scale=100 µm, the arrow indicates the cysticercoid. B: Whole body of the cysticercoid: normal compound microscope observation, scale=50 µm. The black and white arrows indicate disk of cysticercoid. C: The disk of cysticercoid observed by with Nomarski differential interference contrast, scale=20 µm, the same specimen squashed. The white arrow, which is same as Fig. B, indicates disk of cysticercoid. to be less serious tapeworm problems than in other countries. Kates and Runkel (1948) suggested that species of oribatid mites varied in their efficiency as intermediate hosts of the tapeworm. Biocontrol and biodefence for cestode disease causing serious problems require exact identification of oribatid mites in order to manage environment of grazing lands. M. exilis is usually found in forest areas and sometimes in grassland. This species had better to keep the monitoring for the grazing lands with medical safeguard, and study the play an important role as a tapeworm intermediate host in forest- lands of Japan.

ACKNOWLEDGEMENTS

I thank Prof. Soichi Imai, Department of Veterinary Parasitology, Nippon Veterinary and Science University, Prof. Roy A. Norton, State University of New York, College of Environmental Science and Forestry, and Dr. Jun-ichi Aoki, President of Kanagawa Prefec- tural Museum of Natural History, for encouragement and helpful criticisms. 34 Satoshi SHIMANO and Kiyoshi KAMIMURA

REFERENCES

Aoki, J. (1962) Distribution of oribatid mites in pasture soils of Japan. Japanese Journal of Sanitary Zoology, 13: 11–15. (In Japanese with English summary) Aoki, J. (1970) The oribatid mites of the Island of Tsushima. Bulletin of National Science Museum, Tokyo, 13: 395– 442. Aoki, J. (2000) 11. Oribatula sakamorii. In: Oribatid mites in Moss Cushions Growing on City Constructions (ed., Aoki, J.), pp. 52–53, Tokai Univ. Press, Tokyo. Denegri, G. M. (1993) Review of oribatid mites as intermediate hosts of tapeworms of the . Experimental and Applied Acarolgy, 17: 567–580. Haq, M. A. (1988) An appraisal on oribatid vectors. Bicovas, 1: 93–98. Isoda, M., S. Watanabe and K. Ookubo (1966) Biology and pest control of Anoplocephala perforiata on horse. Bulletin of Livestock Hygiene Parasitological Institute, 1: 1–18. (In Japanese) Kassai, T. and S. Mahunka (1965) Studies on tapeworms in ruminants., II. Oribatids as intermediate hosts Moniezia spp. Acta Veterinaria Hungarica, 15: 227–249. Kates, K. C. and C. E. Runkel (1948) Observations on oribatid mite vector of Moniezia expansa on pastures, with a report of several new vectors from the United States. Proceedings of the Helminthological Society of Washington, 15: 18–33. Misaka, M. and T. Ichisawa (1977) A study on Anoplocephala perfoliata living in horse and intermediate host oribatid mites. Graduation thesis in Nippon Veterinary and Animal Science University. (In Japanese) Nakamura, Y. (1973) Soil in natural and artificial grasslands. Bulletin of the National Grassland Research Institute, 4: 16–23. (In Japanese with English summary) Norton, R. A. (2001) Systematic relationships of Nothrolohmanniidae, and the evolutionary plasticity of body form in Enarthronota (Acari: Oribatida). In: Acarology: Proceeding of the 10th International Congress (eds., Halliday, R. B., D. E. Walter, H. C. Proctor, R. A. Norton, and M. J. Colloff), pp. 58–75, CSIRO Publishing, Melbourne. Prokopic, J. (1962) Archipteria celeopterata (L.) (Acarina)—Intermediate host of the tape worm Rodentolepis straminea (Goeze, 1782) (Hymenolepidoidea). Folia Zoologica, 11: 183–187. (In Czech) Rajski, A. (1959) Mechowce (Acari: Oribatei) jako zywiciele posredni tasiemcow (Cestodes: Anoplocephalata) w swietle literatury. Review Zessyky nauk, Universytetu im A. Mickiewiez, Poznan, 2: 163–192. (In Polish) Sanada, Y. and J. Aoki (1999) Distribution of oribatid mites as intermediate hosts of the horse tapeworm in pasture soils of Hidaka in Japan. Journal of the Acarological Society of Japan, 8: 159–163. (In Japanese with English summary) Sengbusch, H. G. (1977) Review of oribatid mite-anoplocephalan tapeworm relationships (Acari: Oribatei: : Anoplocephalidae). In: Biology of Oribatid Mites (ed., Dindal, D.L.), pp. 87–102, SUNY, College of Environmental Science and Forestry, Syracuse, NY. Stunkard, H. W. (1937) The life cycle of Moniezia expansa. Science, 86: 312. Watanabe, S., A. Kishi and S. Iwata (1957) Studies on intermediary host of Moniezia expansa. Journal of the Japanese Veterinary Medical Association, 10: 582–585. (In Japanese)