CJap. J. Parasit., Vol. 31, No. 5, 471-478, Oct.,1982]

A New Record of Mammomonogamus auris from

the Middle Ear of the Domestic in Japan

Etsuro SUGIYAMA*, Rokuro KANO*, Noboru KAGEIt and Shigeo HAYASHIt

(Received for publication; August 25, 1982)

Key words: Mammomonogamus, Syngamidae, Nematoda, domestic , middle ear

Introduction from the of a leopard imported from Thailand. However our case is the Species belonging to the Mam first report on the genus from liv momonogamus (Syngamidae, Nematoda) ing in Japan. are known as parasites of wild and domes tic mammals, such as , buffalo, , Materials and Methods , , cat, puma, tiger, hippopotamus, elephant and okapi, and inhabit the We obtained 46 pairs of from larynx, , bronchus, nasal cavity, the middle ear of domestic cats, Felis catus middle ear and frontal sinus. Geograph Linnaeus, caught in Saitama Pref., Japan, ical distribution is world-wide, reported during the period from Aug. 1981 to Jun. from Asia, Africa, Central and South Amer 1982. Seven cats out of 124 examined were ica. Three species, M. auris, M. ierei and infected (5.6%), and one to eight pairs M. mcgaughei, have been reported from were found from one ear. Of 46 pairs, 45 the domestic cat. were gravid and one was immature. The We obtained nematodes belonging to worms were in both chambers of the mid genus Mammomonogamus from the middle dle ear and there was no unilaterality. We ear of domestic cats caught in Saitama also examined 111 cats caught in Osaka Pref., Japan, and identified them as Mam Pref. and other places but none were in momonogamus auris (Faust et Tang, fected. 1934). The worms were fixed in hot 70% ethyl- There has been only one record on alcohol and cleared with lactophenol. The Mammomonogamus species from Japan. female and the male were permanently Sakamoto et al. (1971) reported M. felis joined in copula, so some specimens were injured during separating manipulation. The summary of this paper was presented at the We measured 11 gravid females and 15 51st annual meeting of the Japanese Society of males which were separated and under Parasitology in Tokyo, Apr. 5, 1982. * Department of Medical Zoology, Faculty of Medi good condition to observe. cine, Tokyo Medical and Dental University, Yu- shima, Bunkyo-ku, Tokyo 113, Japan. Description •f Department of Parasitology, National Institute of Health, Kamiosaki, Shinagawa-ku, Tokyo 141, Female and male permanently joined in Japan.

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Table 1 Measurements in mm (means)

Female Male

1. Body length 13.7-25.9 (19.4) 3.9-6.7 (5.5) 2. Body width 0.72-1.19 (1 .08) 0.25-0.45 (0.36) 3. Distance from head end to 5.6-9.6 (7.3 ) vulva (female) 3'. Ratio to body length 31.7-45.2% (38.2%) 4. Width of buccal capsule 0.242-0.455 (0. 360) 0.144-0.202 (0.176) 5. Depth of buccal capsule 0.212-0.303 (0.259) 0.152-0.228 (0.189) 6. Diameter of mouth opening 0.172-0.394 (0. 266) 0.073-0.114 (0.090) 7. Diameter of head 0.394-0.636 (0. 539) 0.192-0.323 (0.257) 8. Distance from head end to 0.657-0.828 (0. 762) 0.404-0. 606a(0.484) nerve ring 9. Distance from head end to 0. 838-1. 295b (1.041) 0.545-0. 778C(0. 670)

excretory pore 10. Distance from head end to 0.929-1. 4l7d (1.216) 0.657-0.889*(0. 777) cervical papillae 11. Length of esophagus 0.970-1.265 (1.083) 0.444-0.717 (0.627) 11'. Ratio to body length 4.0-7.8% (5 •9%) 9.9-13.1% (11.4%) 12. Minimal width of esophagus 0.086-0.111 (0. 099) 0.035-0.076 (0.062) 13. Maximal width of esophagus 0.192-0.404 (0. 257) 0.086-0.201 (0.134) 14. Tail length (female) 0.263-0.414f (0. 324) 15. Length of spicules (male) right 0.035-0.0463(0.041) left 0. 038-0.048s(0. 042) 16. Egg 0. 078-0. 096X0. 046-0.058* (0. 089x0. 051)

* Number of specimen in measurement is as follows: a, 12; b, 4; c, 11; d, 5; e, 8; r f, 10; ff, 13; h, 33; other data of female, 11; male , 15. copula and showing Y-shaped appearance extending to a short rib. Many small (Fig. 1; Photo. 1). Bright red in color granulations on the inner surface. Through while alive and becoming white or brown head-on view dorsal and ventral sector of after fixed. Body transparent and internal capsular rims broader than other four organs seen while alive. Cuticles very lateral ones (Fig. 4). Esophagus relatively finely striated transversely. Table 1 shows short and posterior half is about twice as the measurements of the worms. wide as anterior half. Nerve ring situated Female: Body uniformly cylindrical and at the middle portion of esophagus. A tapering gradually from vulvar region to pair of non-protuberant cervical papillae either extremity. Posterior end narrowing at the lateral sides of body about the level suddenly and sharply pointed. A pair of of posterior end of esophagus. Excretory phasmids at the caudal end (Fig. 5). Dis pore at the ventral side of body and slight tance of vulva from anterior end of body ly anterior to cervical papillae. is 31.7-43.5% of total body length. Ovar Egg resembling that of , but ian tubules and uteri reaching near the a little larger than the latter (Fig. 11; level of anus. Mouth widely open at the Photo. 4). Egg shell thick without opercula anterior extremity. Buccal capsule broader and numerous indentation on its surface. than long and cupule-like form (Fig. 3). Egg usually found to be eight-cell stage in At its base eight stoutly-built teeth each the feces of infected cats.

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Male: Body entirely cylindrical. Buccal Table 2 List of genus Mammomonogamus capsule is as broad as deep (Fig. 2). Other Ryzhikov, 1948 basic characters of the anterior part similar Genotype to those of female. Copulatory spicules 1. M. laryngeus (Railliet, 1899) small and fine (Fig. 10). Right spicule and Host: cattle, buffalo, sheep, goat, deer, man. left one similar and subequal. They could Habitat: trachea, larynx, nasal cavity. be observed only after separation and Geographical distribution: Asia (India, Ma clarification with lactophenol, although in laya), Africa (Cameroon), Central and South some specimens they could not be found. America. Gubernaculum absent. Copulatory bursa supported by blunt rays (Figs. 6, 7). Ven Other species tral rays short and thick, with two branches 2. M. auris (Faust et Tang, 1934) subequal and close together. Lateral rays Host: domestic cat. Habitat: middle ear. having common stem and branching into Geographical distribution: China. three, medio-lateral considerably shorter 3. M. dispar (Diesing, 1851) than the other two. Externo-dorsal ray Host: puma. isolated and relatively long. Dorsal ray Habitat: trachea. bifurcating at the middle part of the ray. Geographical distribution: Brazil.

In some specimens it bifurcating at the 4. M. felis (Cameron, 1931) base. Its tip often digitating or having Host: tiger. some appendices, but many variations Habitat: bronchi. about the shape of dorsal ray (Figs. 8, 9). Geographical distribution: Malaya. 5. M. hippopotami (Gedoelst, 1924) Host: hippopotamus. Discussion Habitat: nasal sinuses. Geographical distribution: Zaire. Genus Mammomonogamus was estab 6. M. ierei (Buckley, 1934) lished in 1948 by Ryzhikov, separating Host: domestic cat. from genus Syngamus Siebold, 1836. Ryzhi Habitat: nasal cavity. kov (1949) listed eight species of Mammo Geographical distribution: West Indies.

monogamus in his monograph of Syngami- 7. M. indicus (Monnig, 1932) dae, and Skrjabin (1952) added M. auris Host: Indian elephant. and listed nine species. Lengy (1969) pro Habitat: pharynx. posed that family Syngamidae comprised Geographical distribution: India. one genus Syngamus which contained 8. M. loxodontis (Vuylsteke, 1935) Mammomonogamus as subgenus. Barus Host: African elephant. Habitat: trachea. and Tenora reviewed taxonomic problems Geographical distribution: Zaire. of Syngamidae (1972, a), and listed ten 9. M. mcgaughei (Seneviratne, 1954) species of this genus (1972, b) (Table 2). Host: domestic cat. Five species have been recorded from Habitat: frontal sinus, nasal cavity, pharynx. family Felidae, and three have been from Geographical distribution: Sri Lanka.

the domestic cat, Fells catus Linnaeus. 10. M. okapiae (Berghe, 1937) Three species from the domestic cat are as Host: okapi. follows. Habitat: trachea, bronchi. Geographical distribution: Zaire.

1. M. auris (Faust et Tang, 1934) * M. nasicola (Linstow, 1899) and M. kingi (Leiper, Habitat: middle ear. 1913) are generally regarded as synonyms of M. Geographical distribution: China. laryngeus.

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2. M. ierei (Buckley, 1934) covered. Our specimen is morphologically Habitat: nasal cavity. similar to M. ierei. The shape of male Geographical distribution: West Indies. dorsal ray and the length of spicules ac 3. M. mcgaughei (Seneviratne, 1954) cord with those of M. ierei described by Habitat: frontal sinus, nasal cavity, Buckley (1934). However our specimen pharynx. differs from M. ierei in providing ribs in Geographical distribution: Sri Lanka. the buccal capsule. Seneviratne's description (1954) of M. Our specimen under discussion coincides mcgaughei was so insufficient that we could with M. auris on the point that both of not compare our specimen with M. mc them live in the middle ear of the domestic gaughei. It is interesting that he reported cat. Morphologically our specimen has M. auris was also found from the middle some differences from Faust and Tang's ear of cats in his survey. description (1934). They described that The of genus Mammomono- male dorsal ray of M. auris was practically gamus is in the state of disorder. For ex vestigial and consisted of a single bulb-like ample, M. nasicola is generally regarded as thickening with a pair of minute bifurca a synonym of M. laryngeus (Vaz, 1935; tions. The dorsal ray of our specimen Ryzhikov, 1949; Lengy, 1969; etc.), but basically has Y-shaped appearance (Fig. 6), Buckley (1934), Graber et al. (1972) and although its shape has many variations Mejia-Garcia et al (1979) asserted the (Figs. 8, 9). Their measurement of buccal identity of M. nasicola. Macko et al. (1981) capsule and copulatory spicules are slight made deliberations on this problem but ly larger than our measurement, but the they did not give a clear answer. Lengy discrepancy can be explained by such (1969) claimed that M. laryngeus, M. felis things that the method of fixation is dif and M. ierei were so similar that there was ferent and they used only type specimen no possibility to differentiate among them in measurement of buccal capsule and or establish their identity without addi spicules. They also described that there tional knowledge. Presently available keys was a suggestion of a pair of papillae in of the genus are quite insufficient. In the female caudal extremity, but there are Ryzhikov's key (1949) mammomonogamids no papillae but a pair of phasmids in that are divided into two groups on the stand of our specimen. We think they must mis point that family Felidae is the host or not. take phasmids as papillae. Though there As the key is premised on the host specifi are some differences between Faust and city, it is inappropriate to use. In Lengy's Tang's description and our specimen, par key (1969) he regarded Mammomonogamus ticularly in the size of spicules and in the as subgenus and listed 14 species. He used shape of dorsal ray, the present specimens the shape of the male dorsal ray as a key, are identified as M. auris until more de for example, dorsal ray not splitting, or tailed observation on the variations could splitting at some distance from its base become available. into two branches, or splitting at its base M. ierei was found from nasal cavity or into two separate branches. But the shape nasopharynx of the domestic cat (Buckley, of dorsal ray has many individual varia 1934; Cuadrado et aL, 1980), but our speci tions and such forms can be observed all men was obtained only from the middle in our specimens. So it may be inappro ear. We examined nasal cavity, pharynx, priate to use the shape of male dorsal ray larynx, trachea and alimentary tract of in as a key. He also used the presence of fected cats but the worm was not dis small papillae at the female tail, but such

(128) 475 papillae must be same as phasmids judg References ing from descriptions in original papers, 1) Barns, V. and Tenora, F. (1972, a): Notes on so it cannot be used in the key. the systematics and taxonomy of the nematodes Causes of such perplexity are as follows: belonging to the family Syngamidae Leiper, 1. As life-cycle has been still unknown, ex 1912. Acta Univ. Agric, (Brno), Fac. Agron., perimental study has not been succeeded. 20, 275-286. 2. Individual variability is very large and 2) Barus, V. and Tenora, F. (1972, b): Notes on the evolution of the nematodes belonging to moreover some descriptions of Mammo the family Syngamidae Leiper, 1912. Acta monogamus spp. were made from observa Univ. Agric, (Brno), Fac. Agron., 20, 287-295. tion of only small number of specimens. 3) Buckley, J. J. C. (1934): On Syngamus nasicola So there is a possibility that the individual Linstow, 1899, from sheep and cattle in the variations might lead to diagnose the same West Indies. J. Helminth., 12, 47-62. 4) Buckley, J. J. C. (1934): On Syngamus ierei species as different one. sp. nov. from domestic cats, with some ob To establish appropriate taxonomy of servations on its life-cycle. J. Helminth., 12, genus Mammomonogamus, it is indispens 89-98. able to disclose the life-cycle and to revise 5) Cuadrado, R., Maldonaldo-Moll, J. F. and species so far reported. We hope these Segarra, J. (1980): infection of do problems will be solved in the near future. mestic cats in Puerto Rico. JAVMA, 176, 996- 997. 6) Faust, E. C. and Tang, C. C. (1934): A new Summary species of Syngamus (S. auris) from the middle ear of the cat in Foochow, China. Parasitology, Nematodes belonging to genus Mammo 26, 455-459. monogamus were obtained from the mid 7) Graber, M., Euzeby, J., Gevrey, J. and Troncy, dle ear of domestic cats in Saitama Pref., P.-M. (1972): Mammomonogamus des rumi nants domestiques et sauvages. Annls. Parasit. Japan. They were identified as M. auris Hum. Comp., 47, 225-241. (Faust et Tang, 1934), and their morpho 8) Lengy, J. (1969): Notes on the classification of logical features are described. This is the Syngamidae (Nematoda) with new data on some first record of the genus from animals liv of the species. Israel J. Zool., 18, 9-23. 9) Macko, J. K., Birova, V. and Flores, R. (1981): ing in Japan. Deliberations on the problems of Mammomo Nematodes belonging to the genus have nogamus species (Nematoda, Syngamidae) in many individual variations. The taxonomy ruminants. Folia Parasit., 28, 43-49. of the genus is in the state of disorder. To 10) Mejia-Garcia, A., Graber, M., Gevrey, J. and establish appropriate taxonomy it is in Euzeby, J. (1979): La mammomonogamose des dispensable to disclose the life-cycle and bovins an Mexique. Bull. Acad. Vet. Fr., 52, 367-374. to revise species so far reported. 11) Ryzhikov, K. M. (1948): Filogeneticheskijc vzaimosvjazi nematod sem. Syngamidae i opyt perestrojki ikh sistematiki. Dokl. Akad. Nauk Acknowledgement SSSR, 62, 733-736. (in Russian) We are greatly indebted to Dr. S. I to, Tokyo 12) Ryzhikov, K. M. (1949): Osnovy nematodologii Medical and Dental University, who found the t. I., Singamidy domashnikh i dikikh zhivot- worm first and offered it to us. We are much nykh. Izdat. Akad. Nauk SSSR, Moskva Lenin grateful to each department of Tokyo Medical and grad, 1-164. (in Russian) Dental University mentioned later, for their kind 13) Sakamoto, T., Kaneda, H. and Nakagawa, S. offer of domestic cats after their use. They are (1971): Ten species of parasites from leopard Dept. Physiology I in Faculty of Medicine, Dept. Panthera pardus (Linnaeus). Jap. J. Parasit., Oral Physiology in Faculty of Dentistry, Dept. 20, 59. (Suppl.), (in Japanese) Neurophysiology and Dept. Pathology in Medical 14) Seneviratne, P. (1954): Syngamus macgaughei Research Center, Institute of Stomatognathic Science sp. nov. in domestic cats in Ceylon. Ceylon and Research Center. Vet. J., 2, 55-60.

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15) Skrjabin, K. I. (1952): Key to parasitic nema- 16) Vaz, Z. (1935): Sobre a pretensa validez de todes, vol. III. Strongylata. (English transla "Syngamus nasicola" presenca do "Syngamus tion, 1961), Israel Program for Scientific Trans laryngeus" nas fossas de carneiros do Brasil. lation, Jerusalem, 177-193. Arch. Inst. Biol., S. Paulo, 6, 35-39.

Mammomonogamus auris

»# m-

(5.6%) (D%M(D *^KJ: P !+46*fcO^* Mammo- monogamus auris (Faust et Tang, 1934) £; %fz.

Explanation of Figures

Fig. 1 Coupled female and male.

Fig. 2 Anterior part of male, ventral view.

Fig. 3 Anterior part of female, lateral view.

Fig. 4 Head-on view of female. V: ventral. D: dorsal.

Fig. 5 Tail of female, ventral view.

Fig. 6 Male copulatory bursa, dorsal view.

Fig. 7 Male copulatory bursa, lateral view, one side only.

Figs. 8, 9 Variation of the shape of dorsal ray.

Fig. 10 Male copulatory spicules.

Fig. 11 Egg.

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m®m

Explanation of Photographs

Photo. 1 The whole body of Mammomonogamus auris. Large one is female and small one is

male. The bar indicates 0.2 mm.

Photo. 2 Mammomonogamus auris in the middle ear of a domestic cat.

Photo. 3 Male copulatory spicules (arrow). The bar indicates 0.1 mm.

Photo. 4 Egg (eight-cell stage). The bar indicates 0.05 mm.

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