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Eimerian and capillariid infection in farmed ring-necked pheasants (Phasianus colchicus karpowi) in Ehime, Japan, with special reference to their phylogenetic relationships with congeners

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Abstract

We performed a parasitological examination of the gastrointestinal tract of farmed ring-necked pheasants (Phasianus colchicus karpowi) on two farms in Ehime, Japan. Fecal examination through flotation and sedimentation methods (43, 103, and 50 samples in three consecutive years from 2020, respectively) detected coccidian oocysts (5–58%), or capillarid (40–56%) and heterakid eggs (45–72%). Following artificial sporology, most sporulated coccidian oocysts were ellipsoidal without micropyle nor residuum, but with 1–3 polar refractile granules, morphologically reminiscent of Eimeria phasiani (Apicomplexa: Eucoccidiorida: Eimeriidae). Intensive sequencing of mitochondrial cytochrome c oxidase subunit I gene (cox-1) using pan-eimerian primers and multiple oocyst samples from different pheasants indicated a single species. We characterized, for the first time, the cox-1 sequence of E. phasiani, known to be prevalent in wild and captive ring-necked pheasants worldwide. Worm recovery under a dissection microscope revealed two capillariid and one heterakid nematode species: Eucoleus perforans (Nematoda: Trichocephalida: Capillariidae) in the esophageal epithelium (prevalence, 8–73%), Capillaria phasianina (Capillariidae) in the cecal mucosa (10–87%), and Heterakis gallinarum (Nematoda: Ascaridida: Heterakidae) in the cecal lumen (69–88%). The small subunit ribosomal RNA gene (SSU rDNA) of E. perforans was perfectly identical to that in a previous isolate from farmed Japanese green pheasants (Phasianus colchicus versicolor) at a distant locality in Japan. The SSU rDNA of C. phasianina was characterized, for the first time, demonstrating a sister relationship with Capillaria anatis, parasites found in the ceca of domestic ducks, geese, and various wild anatid birds.

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Data availability

Coccidian oocyst and nematode specimens collected in this study are deposited in the Meguro Parasitological Museum, Tokyo, Japan, under collection nos. 25017–25024. The nucleotide sequences obtained in this study are available from the DDBJ/EMBL/GenBank databases under accession nos. LC777439–LC777442. The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Acknowledgements

We thank Michika Koresawa (Livestock Pathology Laboratory, Ehime Prefecture) for her arrangement of sample collection as well as laboratory members (Ayaka Kudo, Manami Tokura, Nodoka Shimizu, Misaki Sonoda, Kohtoku Maeda, and Koichi Murata) of Yamaguchi University) for their assistance in fecal examination of pheasants. We also thank the Faculty of Veterinary Medicine, Airlangga University, for supporting this international collaborative study with the Joint Faculty of Veterinary Medicine, Yamaguchi University, including the provision of travelling funds to MY for staying in Yamaguchi. This study was supported in part by Grant-in-Aid for International Collaboration Research in Asia 2023 from the Heiwa Nakajima Foundation (HS).

Funding

We thank the Faculty of Veterinary Medicine, Airlangga University, for supporting this international collaborative study with the Joint Faculty of Veterinary Medicine, Yamaguchi University, including the provision of travel funds to MY for conducting this collaborative study at Yamaguchi University. This study was supported in part by Grant-in-Aid for International Collaboration Research in Asia 2023 from the Heiwa Nakajima Foundation (HS).

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Author notes

  1. Bayanzul Argamjav and Kiyoko Morioka contributed equally to this work.

Authors and Affiliations

  1. Laboratory of Parasitology, Joint Graduate School of Veterinary Medicine, Yamaguchi University, 1677-1 Yoshida, Yamaguchi, 753-8515, Japan

    Bayanzul Argamjav, Imron Rosyadi & Hiroshi Sato

  2. Uwajima Branch, Nanyo Livestock Health Center, Uwajima, Ehime, Japan

    Kiyoko Morioka

  3. Department of Clinical Pathology, Faculty of Veterinary Medicine, Gadjah Mada University, Sleman, Yogyakarta, Indonesia

    Imron Rosyadi

  4. Department of Parasitology, Faculty of Veterinary Medicine, Airlangga University, Campus C, Mulyorejo, Surabaya, Indonesia

    Muchammad Yunus & Hiroshi Sato

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  1. Bayanzul Argamjav
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  2. Kiyoko Morioka
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Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by all authors. The first draft of the manuscript was written by BA, KM and IR, and subsequently revised by MY and HS. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Hiroshi Sato.

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Ethics approval

The ethics of animal processing and sample collection adhered to in this study followed the guidelines outlined in the Veterinary Section of the Ehime Prefecture for the administrative survey of poultry, and those of the Faculty of Joint Faculty of Veterinary Medicine, Yamaguchi University.

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The authors declare no competing interests.

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Supplementary information

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Supplementary Fig. S1 Maximum likelihood phylogenetic tree based on the 420-bp long mitochondrial cox-1 sequences of representative Eimeria spp. from avian hosts. Species names are followed by the GenBank accession number in parentheses for most cases. For several species of particular interest, the species name is followed by the isolate name and/or host name, with the GenBank accession number in parentheses. The newly obtained E. phasiani cox-1 sequence in the present study is marked with a grey background. (TIF 18.9 mb)

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Supplementary Fig. S2 Epithelial sheet of the esophagus showing parasitism of a female Eucoleus phasianina worm in the tissue. A fixed epithelial sheet was immersed in 30% glycerin solution to achieve transparency of the tissue and observed under a dissection microscopy. (TIF 32.7 kb)

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Supplementary Fig. S3 Morphology of Eucoleus perforans collected from farmed ring-necked pheasants. (a) Lateral view of the caudal end of a male worm with two dorsal papilla-like protrusions (arrows). (b) Lateral view of the caudal end of a male worm with two dorsal papilla-like protrusions (arrows). The spiny region of the housed specular sheath is visible between arrowheads. (c) Dorsal view of the caudal end of a male worm with two dorsal papilla-like protrusions (arrows). The spicule (Sp) protrudes through the cloaca. (d) Dorsal view of the caudal end of a male worm with two dorsal papilla-like protrusions (arrows). The spicular sheath (SS) is protruded from the cloaca. (e) Dorsal view of the caudal end of a male worm with two dorsal papilla-like protrusions (arrows). The spicule (Sp) protrudes through the cloaca. Two photographs are combined at the position indicated by a line. (f) Lateral view of a female worm, focusing on the vulva (asterisk). The uterus (two intrauterine eggs are visible) extends to the right side. (g) Ventral view of a female worm, focusing on the vulva (asterisk). The uterus (a single intra-uterine egg is visible) extends to the right side. (h) Intra-uterine egg with two plugs and a thick egg-shell. The surface is not smooth. (i, j) Sagittal and superficial views of an embryonated egg with a reticulated egg-shell surface. This is one of the eggs originating from cecal contents and preserved in a 2.5% potassium bichromate solution for approximately two years. (k) The caudal end of a female worm, showing the terminal anus (arrowhead). Photographs (a – d) are at the same magnification, and the scale bar is shown in (d). Similarly, photographs (f – h) and photographs (i and j), respectively, are at the same magnification, and the scale bar is shown in either photograph of each set (f and j). (TIF 41.9 mb)

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Supplementary Fig. S4. Morphology of Capillaria phasianina collected from farmed ring-necked pheasants. (a) Lateral view of the caudal end of a male worm with two massive ventrolateral lobes (VLL). The spicule (SS), partly covered by the spicular sheath (SS), protrudes from the cloaca. (b) Dorsal view of the caudal end of a male worm with the protruded spicule (Sp). Two massive ventrolateral lobes (VLL), and spicular sheath (SS). (c) Lateral view of the caudal end of a male worm with two massive ventrolateral lobes (VLL). The distal end of the spicule (Sp) and cloaca (Cl) are indicated by arrows. (d) High magnification of the caudal end of a male worm with a protruded spicular sheath (SS) armed by distinct spines. (e) The proximal end of the spicule is in the body of a male worm. (f) The distal end of the spicule protruded from the cloaca of a male worm. (g) Lateral view of a female worm at the mid-body, showing a vulva (Vu) with tubular appendage (asterisk). Esophagus/intestine junction (Es/In). (h) The caudal end of a female worm with a subterminal anus (arrowhead). (i) Intra-uterine eggs with two plugs and a thick egg-shell. The surface is not smooth. (j, k) Sagittal and superficial views of an intrauterine egg with a punctuated egg-shell surface. Photographs (a) to (c) are at the same magnification, and the scale bar is shown in (c). Similarly, different sets of photographs (e–g), (h and i), and (j and k) are, respectively, at the same magnification, and the scale bar is individually shown. (TIF 34.7 mb)

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Argamjav, B., Morioka, K., Rosyadi, I. et al. Eimerian and capillariid infection in farmed ring-necked pheasants (Phasianus colchicus karpowi) in Ehime, Japan, with special reference to their phylogenetic relationships with congeners. Parasitol Res 122, 3189–3203 (2023). https://doi.org/10.1007/s00436-023-08014-y

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