Oribatid Mites (Acari: Oribatida) As an Intermediate Host of Anoplocephalid Cestodes in Japan
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Appl. Entomol. Zool. 39 (1): 1–6 (2004) Mini Review Oribatid mites (Acari: Oribatida) as an intermediate host of Anoplocephalid cestodes in Japan Satoshi SHIMANO* Department of Upland Farming, National Agricultural Research Center for Tohoku region; Fukushima 960–2156, Japan (Received 4 October 2002; Accepted 3 June 2003) Abstract Denegri (1993) reviewed worldwide instances of oribatid mites as an intermediate host of Anoplocephalid cestodes (tapeworm). In Japan, only four records of cysticercoids in oribatid mites have been reported, although many investi- gations have been made on grazing lands. The oribatid species as an intermediate host previously reported from Japan are Eporibatula sakamorii, Scheloribates laevigatus, Mixacarus exilis and one unidentified species. The distribution of intermediate species is discussed according to the systematic scheme of suborder Oribatida. Key words: Cysticercoid; intermediate host; Japan; Oribatida; tapeworm The author’s purpose is to provide a current con- INTRODUCTION sensus of scientific names and Japanese names of Tapeworms (cestodes) are a serious problem in oribatid mites, and to review accurate information stock-farming. By contrast, It is generally accepted of infected cases in Japan. that the oribatid mites play an important role as de- composers of plant detritus in the ecosystem of ORIBATID MITES AS A CESTODE INTER- stock firms. The life history of anoplocephalid ces- MEDIATE HOST WORLDWIDE todes was an enigmatic problem for more than fifty years before this discovery. Since Stunkard (1937) Kates and Runkel (1948) suggested that differ- first discovered that oribatid mites are the interme- ent species of oribatid mites varied in their effi- diate hosts and vectors of these tapeworms, many ciency as intermediate hosts. In subsequent years, relationships between particular oribatid mite many studies were conducted on the relationship species and various cestode groups have been between tapeworms and oribatid mites (e.g. re- found. Oribatid mites can only become infected viewed in Denegri, 1991). The worldwide interme- when the mites mechanically destroy the outer diate hosts were reviewed by Kates and Runkel shell of the tapeworm eggs (Caley, 1975), while (1948), Rajski (1959) and Sengbusch (1977), with larger mites are able to shallow tapeworm eggs correspondence tables relating cestode species to whole (Ebermann, 1976). In the former case, the oribatid mite species. Denegri (1993) expanded oncosphere moves from the alimentary tract and their lists to include 127 species in 27 families of develops as a cysticercoid larva in the oribatid oribatid mites, that can serve as intermediate hosts body cavity. In the latter case the oncosphere is not of 27 species in 14 genera of anoplocephalid tape- able to hatch and the egg passes through the ali- worms, and demonstrated that Scheloribates laevi- mentary tract of the mite. Finally, cestodes, e.g. gatus is the most frequently reported intermediate Moniezia expansa, are transmitted to grazing ani- host of all oribatid mites. The oribatid families mals such as livestock when they feed on grass that most frequently reported by Denegri (1993) were harbors mites containing cysticercoid larvae. Oribatulidae (35 species, including S. laeviga- Although Japanese parasitologists have recog- tus**), Galumnidae (22 species), and Ceratozeti- nized this host-parasite system, incorrect oribatid dae (15 species). Haq’s (1988) report of 73 species names and unknown species have sometimes been of oribatids as intermediate hosts was not included included in Japanese textbooks of parasitology. by Denegri (1993). * E-mail: [email protected] ** Scheloribatidae was included in Oribatulidae in Denegri (1993). 1 2 S. SHIMANO and Runkel, 1948; Al-Assiuty and Seif, 1995). INSTANCES IN JAPAN When oribatid mites from the forest soil and litter Papers that have reported the relationship be- in Yokohama were collected and examined in one tween cestodes and the oribatid mites as intermedi- individual was found to be infected with a cysticer- ate hosts in Japan are summarized in Table 1. A coid (Shimano and Kamimura, submitted). Al- few studies (i.e. Watanabe et al., 1957; Oota and though, to the best as the author’s knowledge other Naruse, 1979) confirmed the cestode infection of records of oribatid intermediate host refer to mites, other studies (Fukui, 1958a; Aoki, 1962; adults, this specimen was a nymph of Mixacarus Nakamura, 1973; Sanada and Aoki, 1999) were exilis (identified by S. Shimano). The remaining re- fundamental surveys of oribatid community struc- ported case of infection (Misaka and Ichisawa, un- ture and the abundance of potential intermediate publ.) involved an unidentified oribatid species. species of oribatids in grazing land. The purposes In Japan, the intermediate host problem seems to of these studies were biodefence of livestock such be less serious than in other countries. Two possi- as merino sheep and racehorses. Although some in- ble reasons are that: 1) breeding of sheep, which vestigations were carried out on grazing land are the main host of M. expansa is not widespread throughout Japan, observations of cysticercoids in in Japan, 2) most previous reports were about a dif- oribatid mites were reported only in four instances. ferent tapeworm species, the horse tapeworm, The biocontrol and the biodefence against the Anoplocephala perfoliata. serious problem of cestoidosis requires precise While average infection rates of mites with cys- identification of oribatid mites in order to manage ticercoid were reported as 0.61% (Watanabe et al., the environment of grazing lands. Early reports 1957: M. expansa) and 0.11% (Misaka and Ichi- were the source of much confusion, partly due to sawa, 1977: A. perfoliata), Watanabe et al. (1957) insufficient knowledge of the taxonomy of Japa- noted that rates changed from 1.89% in June to nese oribatid mites. The confusion was party due 0.87% in August, and the reduction continued. to the misidentification of one oribatid mite After two years from antihelmintic treatments of species, Eporibatula sakamorii. Table 2 shows the livestock, the infection was reduced to 0.2% in synonymy of this species, using the system by Ba- August (Watanabe et al., 1957). Although Trowe yartogtokh and Aoki (2000). Figures 1–6 in Fukui (1997) reported experimental data from Germany, (1958b) were compared to Figs. 35–42, Figs. showing that the infection rates of mites with cys- 43–44, and the taxonomic key on p. 1011 in Ba- ticercoids of M. expansa, M. benedeni, Paranoplo- yartogtokh and Aoki (2000). Fukui (1958b) identi- cephala mamillana, and A. perfoliata amounted to fied a host mite as Oribatula venusta Berlese, 1908 36.5%, to 37.3%, to 11.8% and to 27.2%, respec- (Japanese name: Hokuriku-sasaradani). The host tively, in Japan the infection seems much lower. mite was identified as Oriibatula sakamorii (Aoki, Isoda et al. (1966) reported on the daily behavior 1970) (Jn: Sakamori-koitadani) and Fujikawa et al. of mites having intermediate potential. Namely, (1993) alluded to the identity of O. venusta sensu oribatid mites usually repeatedly climb up on grass Fukui (non Berlese). This species, was later moved leaves, and return to the soil in a regular pattern. It to the genus Eporibatula by Bayartogtokh and was shown that they crowded on the top of leaves, Aoki (2000). E. sakamorii is usually distributed in especially coinciding with the release and feeding grasslands, moss cushions growing on city con- time of horses (Isoda et al., 1966; Sanada and structions, and in other artificial environments Aoki, 1999). (Aoki, 2000). However, this species was not in- cluded in the review of Denegri (1993). WHAT DETERMINES IF A PARTICULAR Another mite reported as a host was S. laeviga- SPECIES IS INFECTED? tus (C. L. Koch, 1836) (Jn: Hababiro-otohimedani) (Isoda et al., 1966). This identification might not The distribution of species that can serve as an be exact but it is reasonable, because this species intermediate host (Haq, 1988; Denegri, 1993) in name sometimes including a related species group. the phylogeny of Oribatida is shown schematically S. laevigatus is also distributed in grasslands, in Fig. 1. The Japanese species known as an inter- sometimes becoming dominant there (e.g. Kates mediate host are also arranged. The schematic rela- Table 1. Reports dealing with oribatid mites serving as cestode intermediate hosts in pastures of Japan Oribatid species (containing cysticercoid) Identified by Purpose of study Cestode Cestode host Watanabe et al., 1955 Proxenillus pressulus Kishida, 1934; Dr. K. Kishidab finding cysticercoid1) Moniezia expansa sheep Nadegata-sasaradania Watanabe et al., 1957 sp. 1 (ϭProxenillus pressulus) renamed in the paper the same in Watanabe et al., 1955, Oribatid MitesasCestodeIntermediate HostinJapan 3 detailed report again.1) Fukui, 1958a Oribatula sp. (Hokuriku-sasaradania) author renamed in the paper (ϭsp. 1) Fukui, 1958b Oribatula venusta Berlese, 1908c; author renamed in the paper Hokuriku-sasaradania Aoki, 1962 pasture biogeographical study Isoda et al., 1966 Scheloribates laevigatus (C. L. Koch, 1836); authors finding cysticercoid2) Anoplocephala perforiata horse Hababirootohime-danid Nakamura, 1973 pasture biogeographical study Misaka and Ichisawa, 1977 unidentified oribatid species unidentified finding cysticercoid3) Anoplocephala perforiata horse Oota and Naruse, 1979 fundamental study Sanada and Aoki, 1999 fundamental study Shimano and Kamimura Mixacarus exilis Aoki, 1970; authors finding cysticercoid4)