Perspectives of Host-Parasite Relationships Between Rodents and Nematodes in Japan

Mammal Study 30: S95–S99 (2005) © the Mammalogical Society of Japan

Perspectives of host-parasite relationships between rodents and nematodes in Japan

Mitsuhiko Asakawa

Department of Pathobiology, School of Veterinary Medicine, Rakuno Gakuen University, Ebetsu, Hokkkaido 069-8501, Japan

Abstract. I am investigating alien rodents that occur within Japanese Islands for their parasitic nematodes, because some alien nematodes derived from such alien hosts could become highly pathogenic agents to human and livestock, and because the parasites potentially could switch their hosts to and having a negative impact on native host-parasite relationships that have evolved as a result of adaptive radiation or co-speciation between the native rodents and parasitic nematodes. I am generalizing the patterns of host-parasite associations, and providing 4 types: alien rodents and alien nematodes such as Callosciurus erythraeus and Brevistriata callosciuri, and Myocastor coypus and Strongyloides myopotami; alien rodents and native nematodes such as Rattus rattus and Heligmosomoides kurilensis shifted from Apodemus speciosus; native rodents and alien nematodes such as Apodemus argenteus and Heligmosomoides polygyrus shifted from Mus musculus; native rodents and native nematodes such as Apodemus spp. and Heligmosomoides spp. Hence, aberrant host-parasite relationships due to the presence of alien rodents and/or nematodes comprise the 1st, 2nd and 3rd groups. These relationships should be discriminated from the native host-parasite relationships within Japanese natural ecosystem. Some potential strategies including monitoring survey for reduction of risk affected by the aberrant relationships were discussed.

Key words: alien parasitic nematodes, alien rodents, Japan, natural ecosystems, zoogeography.

Since an understanding of the ecology and/or zoo- Rodent fauna of the Japanese Islands geography of the parasitic helminths that are present in terrestrial vertebrates is one of the essential conservation A total of 29 rodent species, including 8 alien species, biological and medical tools for maintaining healthy have been recorded within the Japanese territory (Table host-parasite relationships as a part of the Japanese 1) (Abe 2005). However, those deemed as accidental natural ecosystem, we have been investigating helminth cases of exotic rodents derived immediately from pet fauna since 1981. Further, during this time we have been animals (e.g., Cynomys sp.) are excluded here because able to observe some aberrant cases of host-parasite rela- they have not yet been recognized as naturalized in tionships provoked by the presence of alien hosts and/or Japan, although they could become tentative hosts for parasites. parasitic nematodes. All of the native rodents are divid- In the present paper, using cases of rodent hosts and ed into 3 groups with respect to their locality: the 1) their some parasitic nematodes (Nematoda) due to the Endemic species group, including Sciurus lis, Pteromys presence of much data derived from not only our investi- momonga, Petaurista leucogenys, Eothenomys spp., gations but also those of other authors, we aim to provide Microtus montebelli, Apodemus speciosus, A. argenteus, an overview and generalized discussion of host-parasite and Glirulus japonicus; the 2) Eurasian species group, relationships in the Japanese Islands. Moreover, poten- including Tamias sibiricus, Pteromys volans, Clethri- tial strategies for the reduction of risk affected by aber- onomys spp., Apodemus peninsulae, A. agrarius, and rant relationships will be discussed. Micromys minutus; and the 3) Ryukyu species group, including Diplothrix legata, Tokudaia spp., and Mus calori.

E-mail: [email protected] S96 Mammal Study 30 (2005)

Table 1. Checklist of rodent species in Japan (from Abe 2005). been obtained from S. vulgaris in the Shiretoko Penin- Sciuridae sula located in the north-eastern part of the island (Ono *Pallas’s squirrel, Callosciurus erythraeus (Pallas) et al. 2005). On the other hand, there have been 2 [*]Eurasian red squirrel, Sciurus vulgaris (Linneaus) oxyurid species, Citellina petrovi from P. volans, and Japanese squirrel, S. lis (Temminck) Sypharista kamegaii from Petaurista leucogenys ob- [*]Siberian chipmunk, Tamias sibiricus (Laxmann) tained in Honshu Island, but there is no nematode record Eurasian flying squirrel, Pteromys volans (Linneaus) from Sciurus lis. Japanese flying squirrel, P. momonga (Temminck) Although S. vulgaris and T. sibiricus are native to Japanese giant flying squirrel, Petaurista leucogenys (Temminck) Hokkaido Island, both sciurids have become an alien Muridae species on the Japanese Islands including Hokkaido northern red-backed vole, Clethrionomys rutilus (Pallas) Island due to the pet trade. Up to now, these sciurids gray red-backed vole, C. rufocanus (Sundevall) have not been investigated, although C. erythraeus, king red-backed vole, C. rex (Imaizumi) which appears on Izu-Ohshima and Fukue-jima Islands, Smith’s red-backed vole, Eothenomys smithii (Thomas) has been examined helminthologically, and Brevistriata Anderson’s red-backed vole, E. andersoni (Thomas) callosciuri, Gongylonema neoplasticum, and Strongy- Japanese grass vole, Microtus montebelli (Milne-Edwards) loides cf. robustus have been recorded (Matsudate et al. *muskrat, Ondatra zibethicus (Linnaeus) 2003; Shingaki et al. 2004). large Japanese field mouse, Apodemus speciosus (Temminck) Korean field mouse, A. peninsulae (Thomas) small Japanese field mouse, A. argenteus (Temminck) (b) Muridae striped field mouse, A. agrarius (Pallas) Among the species described, redescribed, or newly harvest mouse, Micromys minutus (Pallas) recorded from Japan since the 1960s, three nematode *house mouse, Mus musculus (Linnaeus) families of zoogeographical interest are mentioned herein: Ryukyu mouse, M. calori (Bonhote) Heligmosomidae, Heligmonellidae, and Oxyuridae. Fur- *roof rat, Rattus rattus (Temminck) ther, slightly different nematode compositions exist with *Norway rat, R. norvegicus (Berkenhout) the parasite genus or species level with respect to the *Polynesian rat, R. exulans (Peale) host subfamily level (Microtinae and Murinae). How- Ryukyu long-furred rat, Diplothrix legata (Thomas) ever, it should be noted here that there are exceptions. Amami spiny rat, Tokudaia osimensis (Abe) For example, Mammanidula hokkaidensis (Heligmonel- Okinawa spiny rat, T. muenninki (Johnson) lidae), which inhabits the mammary gland and Cowper’s Gliridae gland of host individuals and shows a broad host range, Japanese dormouse, Glirulus japonicus (Schinz) has been recorded from Clethrionomys spp., Apodemus Myocastoridae spp., and Sorex spp. (Insectivora). *nutria, Myocastor coypus (Molina) Most of the nematodes recorded from native Japanese *: alien species in Japan. microtins belonging to the genera Eothenomys and [*]: native species in Hokkiado Island, but escaped or released pet ani- Microtus are endemic species to the Japanese Islands. mals found in Japan. Meanwhile, the nematodes recorded of the genus Clethrionomys that are restricted to Hokkaido Island Nematode records from Japanese rodents within the Japanese Islands are also shared by the con- tinental vole population. For example, Heligmosomum Using the previous references (Hasegawa and Asakawa (Paraheligmosomum) yamagutii (Heligmosomidae) have 2003) and our own data, here we present relatively recent been found not only from Clethrionomys spp. in nematode records and investigations that have been per- Hokkaido Island, but also from C. rufocanus in the formed since the 1960s. Scandinavia Peninsula. From C. rutilus mikado, H. (P.) mixtum (Heligmosomidae) and Syphacia petrusewiczi (a) Sciuridae (Oyuridae) have been recorded. Yatinema japonicum In Hokkaido Island, Dirofilaria formasciurorum from (Heligmonellidae) was described as a new genus, and S. vulgaris and Brevistriata skrjabini (syn. B. bergerardi) a new species, Heligmosomum (Paraheligmosomum) from T. sibiricus have been recorded in the 1980s. More hasegawai (Heligmosomidae), has been described. recently, B. skrjabini and Strongyloides robustus have They are host-specific to two species of the Japanese Asakawa, Rodent host/parasitic nematode relationship S97

Eothenomys. Morganiella cricetuli (Heligmonellidae), parasitic helminthes from two bodies of dormice carried recorded from E. smithii in Shikoku Island, is of special to an animal hospital in Tochigi Prefecture. geographical interest because it had been previously recorded only from the striped hamster (Cricetulus (d) Myocastoridae barabensis) in China. Heligmosomoides protobullosus On Honshu Island, there have been recordings of (Heligmosomidae), Heligmosomum (Heligmosomum) Strongyloides myopotami from coypus, Myocastor coy- halli, and Carolinensis minutus (Heligmonellidae) have pus, captured in Gifu and Okayama Prefectures and of been recorded from Microtus montebelli, and H. pro- Calodium hepaticum in Hiroshima Prefecture (Matsudate tobullosus seems to be endemic to Japan. Among the et al. 2003). More detailed monitoring surveys should be microtins occuring in the Japanese Islands, Ondatra required, however, because both are known as zoonotic zibethicus is the only alien microtin. However, no agents. helminthological investigation of O. zibethicus has been performed up to now. Nematode zoogeography and aberrant Japanese native murins consist of all species belong- host-parasite relationships ing to the genera Micromys, Apodemus, Diplothrix, Tokudaia, and Mus caroli. Syphacia vandenbrueli, Changes in the global political framework since the which had previously been known as the pinworm of mid 1980s have enabled Japanese parasitologists to study Micromys minutus in Europe, was recorded from the the helminths on the Eurasian continent, and at present Japanese population of the mice in Honshu Island as several international cooperative research projects are well. Among over 20 nematode species recorded from progressing. Through such projects, studies on the origin the Japanese Apodemus, Heligmosomoides kurilensis, H. and speciation of the Japanese helminths that parasitize desportesi, H. neopolygyrus, Heligmonoides speciosus, rodents are becoming more intense and focused. Native Syphacia emileromani, S. frederici, and S. agraria are murids offer many advantages with regard to the study known as biomarkers of zoogeographical epidemiology of host-parasite relationships and zoogeography. For and environmental states. On the Ryukyu Islands, there example, their geographical distribution is rarely influ- have been records of Heligmonoides ikeharai from T. enced by human activity, and they are easily collected. osimensis and of Heligmonoides ryukyensis and Syphacia Moreover, much taxonomical, zoogeographical, phylo- ohtaorum from M. caroli. Although Globocephalus genic, and ecological information on these murids has longemucronatus, a common parasitic nematode of the been accumulated. wild boar (Sus scrofa), has been obtained from D. legata, Hence, as a part of a zoogeographical research project, there is no record of a host specific nematode from the an analysis was made on the parasite fauna of the Japa- native rat. nese Microtinae and Murinae, and several endemic host- There have been many reports and medical/veterinary parasite relationships were been detected (Hasegawa publications on these parasites that include nematodes and Asakawa 2003). However, some aberrant host- from alien murins (Rattus norvegicus, R. rattus, and parasite relationships between Japanese munins and the Mus musculus) because they harbor many zoonotic heligmosomids have been observed in accidental cases helminths. Orientostrongylus ezoensis (Heligmonellidae), of Heligmosomoides kurilensis from Rattus rattus on Nippostrongylus braziliensis (Heligmonellidae), and Oki Islands (Sakata et al. 2005) and H. polygyrus from Sypacia muris have been found from Rattus spp. captured Apodemus argenteus on Hokkaido Island (Asakawa et al. in wild conditions. Further, Heligmosomoides polygyrus 1994). and Syphacia obverata are host specific to M. musculus. Four types of host-parasite relationships between (c) Gliridae rodents and nematodes Glirulus japonicus is an endangered species endemic to Honshu, Shikoku, Kyushu, and Doh-go Islands. Al- According to the rodent fauna found in Japan (Table though Acanthatrium ovatum (Trematoda) was obtained 1), there are alien and native host species (abbreviated from the small intestine of G. japonicus captured at Mt. as “H1” and “H2”, respectively) (Table 2). Further, the Ontake, there has to date been no nematode recorded. parasitic nematodes are also divided into alien and Recently, the present author could also not obtain any native types (abbreviated as “P1” and “P2”, respectively) S98 Mammal Study 30 (2005)

Table 2. Abbreviations of native/alien rodents and parasitic nematodes. Table 3. Four types of host-parasite relationships between rodents and parasitc nematodes and their some examples accorded with each Host rodents (H)/Parasitic nematodes (P) type of the relationship. alien (H1) alien (P1) Host-Parasie relationships (Abbreviations of Table 2) native (H2) native (P2) H1-P1 Callosciurus erythraeus — Brevistriata callosciuri (Table 2). Consequently, the host-parasite relationships Myocastor coypus — Strongyloides myopotami can be summarized into four patterns (Table 3), namely Rattus norvegicus — Orientostrongylus ezoensis 1) relationships between alien rodents and alien para- R. norvegicus — Nippostrongylus braziliensis sitic nematodes (abbreviated as “H1-P1”, respectively), Mus musculus — Heligmosomoides polygyrus 2) relationships between alien rodents and native para- H1-P2 sitic nematodes (abbreviated as “H1-P2”, respectively), Rattus rattus — Heligmosomoides kurilensis 3) relationships between native rodents and alien parasit- H2-P1 ic nematodes (abbreviated as “H2-P1”, respectively), and Apodemus argenteus — H. polygyrus 4) relationships between native rodents and native para- H2-P2 sitic nematodes (abbreviated as “H2-P2”, respectively). Eothenomys andersoni — Yatinema japonicum In addition, some examples of these according to each Microtus montebelli — Heligmosomoides protobullosus type of relationship in Japan are presented in Table 3. Apodemus specuosus — H. kurilensis A. argenteus — Heligmosomoides desportesi A. peninsulae — Heligmosomoides neopolygyrus Probable impacts for endemic host-parasite etc relationships caused by the presence of alien hosts and/or helminths are native species which comprise part of the natural 1) H1-P1 type ecosystem in Japan. However, because coypus use small The first cases of relationships between alien ro- waterways (vacant niches for Japanese endemic rodents) dents and alien parasitic nematodes (e.g., Callosciurus and transport these native nematodes to new sites, there erythraeus-Brevistriata callosciuri, Myocastor coypus- seems to be the possibility that a new public or wild Strongyloides myopotami, Rattus norvegicus-Orien- animal health problem will be provoked. Hence, even tostrongylus ezoensis, R. norvegicus-Nippostrongyrus native nematodes could be pathogenic agents using alien braziliensis, Mus musculus-Heligmosomoides polygyrus) hosts as new “vehicles.” indicated that intimate relationships in the places of origin (e.g., South-east Asia, South America) shifted 3) H2-P1 type directly into Japan and have been preserved constantly. An example of this type could be obtained from our Up to now, these alien nematodes have not been survey, in a case in which A. argenteus (H2) had known to parasitize Japanese native rodents (H2). How- Heligmosomoides polygyrus (P1) in Hokkaido Island ever, a constant monitoring survey and an experimental (Asakawa et al. 1994). This nematode species is a infection in a laboratory with the nematodes to the native common parasite of M. musculus, which is an old alien rodents should be performed in the future in order to rodent in Japan, and the nematode is well known to be observe whether or not the intimate host-parasite rela- pathogenic to wild and/or captive rodent hosts. In the tionship shifts to the H1-P2 or H2-P1 types and/or is UK, the nematode species has been obtained from the newly formed. small intestine of two captive common dormice (Muscardinus avellanarius) (Asakawa et al. 2006). The 2) H1-P2 type total numbers of nematode was ca. 600 to 900 in each The accidental case of Heligmosomoides kurilensis animal. It was surmised that the dormice became infected (P2) obtained from Rattus rattus (P1) (Sakata et al. 2005) through the intake of diet contaminated with infective belongs to this type. Recently, after the immigration of larvae likely derived from the feces of house mice. coypus (H1), alien rodent nematode (Calodium hepati- Hence, some host-shifts to type H2-P1 could be danger- cum) (P2) that was likely native or old parasitized to ous to wild animal health. coypus in Japan (type H1-P2). These helminths (P2) Asakawa, Rodent host/parasitic nematode relationship S99

4) H2-P2 type presence of alien rodents and/or nematodes in Japan Except for accidental cases caused by artificial distur- comprise groups 1), 2) and 3), and, further, potential bances to the essential habitat of the host species, the H2- strategies for the reduction of risk affected by these P2 type belongs to the natural ecosystem formed by the relationships should be performed for each group. evolutionary process in Japan. Further, this type of host- parasite relationship should be regarded as an aim of Acknowledgments: The present survey was supported conservation biology, and a top priority to be considered in part by a Grant-in-Aid (No. 14560271) and High when designing potential strategies is recognition that Technological Research Center (Rakuno Gakuen Univ.) an endemic host-parasite relationship creates one type from the Ministry of the Education, Science and Culture of natural biodiversity. of Japan. 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