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Bull. Tokushima Pref. Mus.
No. 22 : 1-6, 2012

【Article】

First record of the genus Strongyloides (Nematoda : Rhabditoidea)
obtained from a fairy pitta, Pitta brachyura nympha1,**Tomoo Yoshino223, Daisuke Hayakawa , Miku Yoshizawa , Yuichi Osa
1and Mitsuhiko Asakawa

Abstract : Two young individuals of fairy pitta, Pitta brachyura nympha, were rescued
somewhere within Kochi Prefecture, Shikoku, Japan, and housed at the Wanpark Kochi
Animal Land, Kochi city. Each died suddenly, on May 31, 2008 and January 23, 2011,
respectively. In the postmortem and helminthological examinations, four female parasitic
nematode specimens were obtained from the small intestine of one of the birds. They
were identified as Strongyloides sp. based on morphological characters. Several speciesof the genus Strongyloides have been recorded from wild birds and domestic poultry
worldwide, including in Japan, but this is the first record of the nematode genus
Strongyloides from P. b. nympha. We could not definitively identify the present specimens
to species because they had not formed matured eggs.
Key words : new host record, parasitology, passerine birds, Strongyloides sp.

Introduction
The fairy pitta, Pitta brachyura nympha Temminck and Schlegel, 1850 (Passeriformes : Pittidae), is
distributed in warm-temperate broadleaved forests of East Asia. They migrate between southeast Asia,
where they overwinter, to their summer breeding sites in northeast Asia, including the Japanese islandsof Honshu, Shikoku, Kyushu, and Tsushima. They feed on several species of invertebrates, but mainly
on earthworms on the forest floor (Yamaguchi and Kamogawa, 1971, 1972 ; Sawada, 1984 ; Fujita etal ., 1992 ; Minamiya et al ., 2007). Fairy pitta is classified as 1B on the endangered species list (EN :Endangered) in the Japanese Red Data Book. Current estimates suggest a population size of about 150
individuals (Wildlife Division of the Ministry of the Environment, 2002).
In conservation projects in which wild birds are returned to free-living conditions, health risk
assessments are important to avoid detrimental parasitic disease outbreaks, such as fatal helminthiasis(Friend and Franson 1999 ; Asakawa et al ., 2002). However, there is little information regarding thedisease-causing agents, including parasitic helminths, in this species. We therefore investigated theparasites of P. b. nympha.

Received 26 October 2011 ; Accepted 19 January 2012.
1 Department of Pathobiology, School of Veterinary Medicine, Rakuno Gakuen University, Ebetsu-shi, Hokkaido 0698501, Japan.
2 Wanpark Kochi Animal Land, Kochi-shi, Kochi 780-8010, Japan.
3 Institute of Environmental Sciences, Hokkaido Research Organization, Sapporo-shi, Hokkaido 060-0819, Japan.
*Corresponding Author : e-mail, askam@rakuno.ac.jp**Current Affiliation : Kyushu Regional Environment Office, Ministry of the Environment.Kumamoto, Kumamoto 8620913, Japan.

―1―Tomoo Yoshino, Daisuke Hayakawa, Miku Yoshizawa and Yuichi Osa

Materials and Methods
Two young individuals of fairy pitta were rescued in Kochi Prefecture and housed in a captive
facility of the zoo, Wanpark Kochi Animal Land, Kochi, Japan. They died suddenly, one on May 31,
and the other 2008 on January 23, 2011. Postmortem examinations were performed in the zoo. The
digestive tracts of the birds were fixed in 70% ethanol and taken to the Wild Animal Medical Center(WAMC) of Rakuno Gakuen University, Hokkaido, Japan for helminthological examination. A totalof four female parasitic nematode specimens were recovered from the small intestine of one of thepittas. The fixed nematode specimens were cleared in lacto-phenol solution for microscopicobservation. Morphological and biometric data were recorded using a camera lucida (OLYMPUS DP20). The nematode specimens are preserved separately in the WAMC (WAMC-As 11031) and theTokushima Prefectural Museum, Tokushima, Japan (TKPM-IV551).

Results and Discussion
The nematodes isolated from the fairy pitta specimen were identified as Strongyloides sp.
(Strongyloididae) based on morphological characters according to the criteria of Anderson and Bain(1982), Spaere (1989) and Skrjabin (1992). The nematodes had the following characters : bodythreadlike and equipped uninflated cuticle ; buccal cavity reduced and without teeth ; esophagus long,slender and without terminal valved bulb ; vulva in posterior of body. Morphological characters andmeasurements are given in Fig. 1 and Table 1.
Rhabditid nematodes belonging to the genus Strongyloides Grassi, 1879 have been identified so far
from several avian hosts worldwide, mainly Galliformes (including poultry), Anseriformes,Ciconiiformes and Charadriiformes (Barus et al ., 1978 ; Spaere, 1989 ; Skrjabin, 1992). However,few specimens of this genus have been reported from Japan or from Passeriformes. Three species ofFigure 1. Parasitic female of Strongyloides sp. obtained from a fairy pitta. A, anterior extremity ; B, vulva ;C, posterior extremity. Scale bar=50μm―2―

49-55700

3.15

33.9-38.3 (36.3)

Length of Esophagus 410-470 (440.0)

3.7-4.1 (3.90)

900-1130(1020.0)

Body Length/
Body Width

Body Length/
Esophagus Length

Distance of Vuva
from anterior end―3―52-56 x 36-40−Egg size40

40.3-45.7 (43.50)

Body Length/
Tail Length55

35-42 (39.0)

Tail Length

63.7

59.3-63.2 (60.4)

Ratio to Body
Length (%)

1400

40-55

42-50(46.0)

Body Width

2.2

1.5-1.9 (1.69)

39-56 x 24-33

37.9-54.7

39-43

63.7-68.5

1113-1354

2.9-4.5

475-675

35.4-54.7

38-46

1.6-2.1

50 x 28

22.5-35.650−−−

512-550−

37-40

1.1-1.8

S. avium
S. minimum
Sakamoto andTravassos (1930)
Cram (1929)
Sarashina (1968)

Body Length(mm)present specimen

Strongyloides sp．

Table 1. Measurements of the parasitic female of Strongyloides spp. (in mm)

−

−

70-76

−

−

−

540-560−

42-50

2.2-2.4

S. cubaensis
Perez Vigueras(1942)

35-42 x 21-24

−

42-49

−

920-1220

−381-554

−

33-45

−

−

30-50

−

−

−

480-780−

30-40

1.5-2.1

Little (1966)

Kurtieva (1954)
1.7-2.1

S. ardeae

S. turkmenicus

48 x 27

−

48-53

−

1470-1730−

530-660−

32-36

2.4-2.8

Boyd (1966)

S. herodiae

50-54 x 35-40

317-78.9 (56.30)

51-75 (62.0)

59.0-65.3 (61.1)

1690-2500(2090.0)

3.5-5.2 (4.3)

725-915 (800.0)

54-95 (68.2)

43-60 (50)

2.7-4.2 (3.41)

S. pavonis
Sakamoto andYamashita (1970)

Strongyloides sp. from a fairy pitta

Tomoo Yoshino, Daisuke Hayakawa, Miku Yoshizawa and Yuichi Osa

the genus Strongyloides have been recorded from wild and/or captive birds in Japan : S. avium Cram,
1929 from water rail, Rallus aquaticus indicus Blyth, 1849 ; S. pavonis Sakamoto and Yamashita,1970 from green peafowl, Pavo muticus Linnaeus, 1766, Indian peafowl, P. cristatus Linnaeus, 1758,
and domestic chicken, Gallus gallus domesticus Linnaeus, 1758 ; and Strongyloides sp. from theOkinawa rail Gallirallus okinawae (Yamashina and Mano, 1981) (Sakamoto and Sarashina, 1968 ;Sakamoto and Yamashita, 1970 ; Onuma et al ., 2011). Worldwide, several species have been recorded
from wild and captive birds : S. turkumenicus Kurtieva, 1953 from Himantopus himantopus(Linnaeus, 1758) and Larus canus Linnaeus, 1758 ; S. minimum Travassos, 1930 from Anasbahamensis Linnaeus, 1758 ; S. cubaensis Perez Vigueras, 1942 from Butorides virescence(Linnaeus, 1758) ; S. ardeae Little, 1966 from Nyctanassa violacea (Linnaeus, 1758) and B.
virescence ; S. herodiae Boyd, 1966 from Ardea herodias Linnaeus, 1758 ; and Strongyloides sp.
from Agelaius phoeniceus (Linnaeus, 1766) and domestic chicken (Baylis, 1923 ; Cram, 1929 ;Travassos, 1930a, 1930b ; Cram, 1936 ; Pelez Vigueras, 1936 ; Kurtieva, 1954 ; Boyd, 1966 ; Little,1966a, 1966b ; Barus et al ., 1978).
Although the morphological characters of the specimens taken from the fairy pitta seemed to beclosely allied to S. avium, we could not definitively identify them because they had not formed matured
eggs (Cram, 1929 ; Sakamoto and Sarashina, 1968 ; Sato et al ., 2008). More detailed analyses, such asa genetic study or electron microscopy, will be required to identify them (Sato et al ., 2008 ; Hasegawa
et al ., 2009).
Only one nematode species, Aproctella tuberculata Ramnivas, 1979, had previously been reported
from the fairy pitta, but there was no prior record of nematodes belonging to the genus Strongyloides
from this bird (Ramnivas, 1979). This is the first record of Strongyloides from P. b. nympha onworldwide basis.
The postmortem examinations did not determine the causes of death of the two pittas, and there was
no evidence of pathogenicity caused by the nematodes. However, nematodes belonging to the genus
Strongyloides are well-known pathogenic agents that cause thickening of the cecal wall and filling of
the cecal lumen with desquamated debris of degenerated tissue, mucous exudation, and blood (Cram,1929 ; Sakamoto, 1982). Thus, we suggest that this nematode may cause epizootic infections andpathogenicity in these hosts.
The present survey was supported in part by a Grant-in-Aid from the Ministry of Education, Scienceand Culture, Japan, and by the Hokkaido Sougoh Kenkyu Kikoh Juten Kenkyu 2011.

References
Anderson, R. C. and O. Bain. 1982. Keys to the genera of the superfamilies Rhabditoidea, Dictophymatoidea,Trichinelloidea and Muspiceoidea. CIH Keys to the Nematode Parasites of Vertebrates. No. 9, Commonwealth
Agricultural Bureaux, UK, 26p.
Asakawa, M., S. Nakamura and M. A. Brazil. 2002. An overview of infectious and parasitic diseases in relation to theconservation biology of the Japanese avifauna. Journal of the Yamashina Institute for Ornithology, 34 : 200-221.

＾Barus, V., T. P. Sergejeva, M. D. Sonin and K. M. Ryzhikov. 1978. Helminths of fish eating birds of the palaearctic―4―

Strongyloides sp. from a fairy pitta

region. I. Nematoda. Publishing House of the Czechoslovak Academy of Sciences, Prague, 318p.
Baylis, H. A. 1923. Report on a Collection of Parasitic Nematodes, mainly from Egypt. Part III. Camallanidae, etc. witha note on Probstmatria and an appendix on Acanthocephala. Parasitology, 15 : 24-38.
Boyd, E. M. 1966. Observations on nematodes of herons in North America including three new species and new host andstate records. Journal of Parasitology, 52 : 503-511.
Cram, E. B. 1929. A new roundworm parasite, Strongyloides avium of the chicken with observations on its life history
and pathogenicity. North American Veterinarian, 10 : 27-30.
Cram, E. B. 1936. Biological and morphological observations on a species of Strongyloides (Nematoda) of chickens inPuerto Rico. Revista de Parasitologia Clinica y Laboratorio, 2 : 289-304.
Friend, M. and J. C. Franson. 1999. Field Manual of Wildlife Diseases. USGS, Washington, U. S. 426p.
Fujita, G., H. Higuchi and Y. Sawada. 1992. Ecological distribution of fairy pitta Pitta brachyura in Japan. In Tokushu
Chourui Chousa (ed. Wild Bird Society of Japan), p.1-8. Wild Bird Society of Japan, Tokyo (in Japanese withEnglish summary).
Hasegawa, H., S. Hayashida, Y. Ikeda and H. Sato. 2009. Hyper-variable regions in 18S rDNA of Strongyloides spp. asmarkers for species-specific diagnosis. Parasitology Research, 104 : 869-874.
Kurtieva, L. 1954. [Contributions to helminthology published to commemorate the 75th birthday of K. I. Skrjabin, 374p.
Petrov, A. M. (ed.) Akademii Nauk SSSR, Moscow, USSR] (in Russian).
Little, M. D. 1966a. Comparative morphology of six species of Strongyloides (Nematoda) and redefinition of the genus.
Journal of Parasitology, 52 : 69-84.
Little, M. D. 1966b. Seven new species of Strongyloides (Nematoda) from Louisiana. Journal of Parasitology, 52 : 8589.
Minamiya, Y., K. Ishizuka and J. Tsukamoto. 2007. Habitat preference of surface living earthworms as food for fairy
pitta, a forest songbird, in warm-temperate South-western Japan. Edanophologia, 81 : 13-26.
Onuma, M., T. Yoshino, C. Zhao, T. Nagamine and M. Asakawa. 2011. Parasitic helminths obtained from the Okinawa
rails Gallirallus okinawae. Journal of the Yamashina Institute for Ornithology, 43 : 74-81.
Pelez Vigueras, I. 1936. Notas sobre la fauna parasitologica de Cuba, Parte I. Vermes II. Nemathelminthes. Memorias dela Sociedad Cubana de Historia Natura, 10 : 53-86 (in Spanish with English summary).
Ramnivas, D. 1979. On two new species of the family Onchocercidae (Ornithofilariinae) from Indian birds. Journal ofAnimal Morphology and Physiology, 26 : 265-271.
Sakamoto, T. 1982. Studies on strongyloidiasis of the peacock. IV. Observations on pathogenicity of Strongyloides
pavonis Sakamoto et Yamashita, 1970 for various birds. Memories of the Facalty of Agricalture, Kagoshima
University, 18 : 115-125.
Sakamoto, T. and T. Sarashina. 1968. Strongyloides avium Cram, 1929 (Strongyloididae : Nematoda) from Rallus
aquaticus indicus Blyth. Japanese Journal of Veterinary Research, 16 : 44-50.
Sakamoto, T. and J. Yamashita. 1970. Studies on strongyloidiasis of the peacock : II. Strongyloides pavonis n. sp.
(Nematoda : Strongyloididae) from the green peafowl Pavo muticus Linnaeus. Japanese Journal of Veterinary
Research, 18 : 163-171.
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―5―

Tomoo Yoshino, Daisuke Hayakawa, Miku Yoshizawa and Yuichi Osa

Wildlife Division of the Ministry of the Environment. 2002. Red Data Book : Birds. Japan Wildlife Research Center,Tokyo 278p. (in Japanese)
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摘要

ヤイロチョウ Pitta brachyura nympha から得られた Strongyloides 属線虫の初記録
吉野智生

1,**

22・早川大輔 ・吉澤未来 ・長3

雄一 ・浅川満彦

1,*

高知県内某所で保護され，収容先の動物園で死亡したヤイロチョウ 2 個体の消化管を検査したところ，1 個体の腸管から 4 体の線虫が検出された．線虫は形態学的に糞線虫類のStrongyloides 属（Rhabditoidea 上科）に属すると考えられた．日本を含む世界各地の野鳥，飼育鳥類及び家禽からは今までに 7 種ほどの報告があるが，今回の標本は卵形成が十分ではなかったため，種の決定は見送られた．ヤイロチョウからの本属線虫の記録は無く，今回が初報告となった．
（1 酪農学園大学獣医学類感染・病理学分野，〒069-8501 北海道江別市文京台緑町 582・2 わんぱーく高知アニマルランド，〒780-8010 高知県高知市桟橋通 6-9-1・3 北海道総合研究機
構環境科学研究センター，〒060-0819 北海道札幌市中央区北 19 条西 12 丁目）*連絡先著者：浅川満彦（askam@rakuno.ac.jp）**現所属：環境省九州地方環境事務所〒862-0913 熊本県熊本市尾ノ上 1-6-22．

―6―