Skip to main content
Log in

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

Parasitology Research Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

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.

References

  • Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 55:539–552

    Article  PubMed  Google Scholar 

  • Atkinson CT, Thomas NJ, Hunter DB (2008) Parasitic diseases of wild birds. Wiley-Blackwell, Ames, Iowa

    Book  Google Scholar 

  • Baruš V, Sergejeva TP (1989a) Capillariids parasitic in birds in the Palaearctic region (1): Genus Capillaria. Acta Sci Natur Brno 23(3):1–50

    Google Scholar 

  • Baruš V, Sergejeva TP (1989b) Capillariids parasitic in birds in the Palaearctic region (2): Genera Eucoleus and Echinocoleus. Acta Sci Natur Brno 23(6):1–47

    Google Scholar 

  • Baruš V, Sergejeva TP (1990) Capillariids parasitic in birds in the Palaearctic region (4): Genera Pterothominx and Aonchotheca. Acta Sci Natur Brno 24(12):1–48

    Google Scholar 

  • Bickford AA, Gaafar SM (1966) Multiple capillariasis in game-farm pheasants. Avian Dis 10:428–437

    Article  CAS  PubMed  Google Scholar 

  • Biswas PG, Ohari Y, Mohanta UK, Itagaki T (2021) Development of a multiplex PCR method for discriminating between Heterakis gallinarum, H. beramporia, and H. indica parasites of poultry. Vet Parasitol 295:109463

    Article  CAS  PubMed  Google Scholar 

  • Bobrek K, Gaweł A, Urbanowicz J (2022) Molecular analysis of the Heterakis dispar population in domestic geese based on the ITS1-5.8rRNA-ITS2 fragment. Animals 12:926. https://doi.org/10.3390/ani12070926

    Article  PubMed  PubMed Central  Google Scholar 

  • Bobrek K, Hildebrand J, Urbanowicz J, Gawei A (2019) Molecular identification and phylogenetic analysis of Heterakis dispar isolated from Geese. Acta Parasitol 64:753–760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borba VH, Martin C, Machado-Silva JR, Xavier SCC, de Mello FL, Iñiguez AM (2021) Machine learning approach to support taxonomic species discrimination based on helminth collections data. Parasit Vectors 14:230. https://doi.org/10.1186/s13071-021-04721-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Callinan RB (1987) Nodular typhilitis in pheasants caused by Heterakis isolonche. Aust Vet J 64:58–59

    Article  CAS  PubMed  Google Scholar 

  • Carvalho EL, Santana RLS, Pinheiro RHS, Giese EG (2019) Eucoleus contortus (Nematoda: Capillariidae), a parasite of Cairina moschata domestica (Anseriformes: Anatidae) on Marajó Island, Pará State, in Brazilian Amazon. Rev Bras Parasitol Vet 28:692–699

    Article  PubMed  Google Scholar 

  • Carvalho EL, Santana RLS, Sindeaux Neto JL, Silva MVO, Giese EG (2023) A new nematode of the family Capillariidae identified in Cairina moschata (Linnaeus) on Marajó Island in the Brazilian Amazon. Braz. J Vet Parasitol 32:e007523. https://doi.org/10.1590/S1984-29612023047

    Article  Google Scholar 

  • Corredor V, Enea V (1994) The small ribosomal subunit RNA isoforms in Plasmodium cynomolgi. Genetics 136:857–865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cram EB (1936) Species of Capillaria parasitic in the upper digestive tract of birds, vol 516. Technical Bulletin of United States Department of Agriculture, Washington, D.C., pp 1–27

    Google Scholar 

  • Cruz CEF, Fredo G, Casagrande R, Oliveira L, Rolim V, Marques S, Pavarini S, Driemeier D (2016) Eucoleus contortus parasitism in captive-bred valley quail Callipepla californica (Shaw, 1798): Disease and control. Zool Gart 85:152–159

    Article  Google Scholar 

  • De Rosa M, Shivapprasad HL (1999) Case report: capillariasis in a vulture guinea fowl. Avian Dis 43:131–135

    Article  PubMed  Google Scholar 

  • Deng Y-P, Suleman ZY, Nie Y, Fu Y-T, Liu G-H (2021) The complete mitochondrial genome of capillariid nematodes (Eucoleus annulatus): A novel gene arrangement and phylogenetic implications. Vet Parasitol 296:109476

    Article  CAS  PubMed  Google Scholar 

  • Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:465–469

    Article  Google Scholar 

  • Doran DJ (1978) The life cycle of Eimeria dispersa Tyzzer 1929 from the turkey in gallinaceous birds. J Parasitol 64:882–885

    Article  CAS  PubMed  Google Scholar 

  • Draycott RAH, Parish DMB, Woodburn MIA, Carroll JP (2000) Spring survey of the parasite Heterakis gallinarum in wild-living pheasants in Britain. Vet Rec 147:245–246

    Article  CAS  PubMed  Google Scholar 

  • Duff AF, Briggs WN, Bielke JC, McGovern KE, Trombetta M, Abdulah H, Bielke LR, Chasser KM (2022) PCR identification and prevalence of Eimeria species in commercial turkey flocks of the Midwestern United States. Poult Sci 101:101995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • El-Sherry S, Ogedengbe ME, Hafeez MA, Barta JR (2013) Divergent nuclear 18S rDNA paralogs in a turkey coccidium, Eimeria meleagrimitis, complicate molecular systematics and identification. Int J Parasitol 43:679–685

    Article  CAS  PubMed  Google Scholar 

  • El-Sherry S, Ogedengbe ME, Hafeez MA, Sayf-Al-Din M, Gad N, Barta JR (2014) Re-description of a genetically typed, single oocyst line of the turkey coccidium, Eimeria adenoeides Moore and Brown, 1951. Parasitol Res 113:3993–4004

    Article  CAS  PubMed  Google Scholar 

  • El-Sherry S, Ogedengbe ME, Hafeez MA, Sayf-Al-Din M, Gad N, Barta JR (2015) Sequence-based genotyping clarifies conflicting historical morphometric and biological data for five Eimeria species infecting turkeys. Poult Sci 94:262–272

    Article  CAS  PubMed  Google Scholar 

  • El-Sherry S, Ogedengbe ME, Hafeez MA, Sayf-Al-Din M, Gad N, Barta JR (2017) Re-description of a genetically typed, single oocyst line of the turkey coccidium, Eimeria dispersa Tyzzer, 1929. Parasitol Res 116:2661–2670

    Article  CAS  PubMed  Google Scholar 

  • Fish FF (1931) Quantitative and statistical analyses of infections with Eimeria tenella in chicken. Am J Epidemiol 14:560–576

    Article  Google Scholar 

  • Fisher JW, Wacha RS (1976) Coccidian parasites from game-farm reared pheasants, Phasianus colchicus, in Iowa. Proc Helminthol Soc Wash 43:226–227

    Google Scholar 

  • Garcia LS (2007) Diagnostic Medical Parasitology, 5th edn. ASM Press, Washington, DC

    Book  Google Scholar 

  • Gassal S, Schmäschke R (2006) Zur Helminthen- und Kokzidienfauna des Jagdfasans (Phasianus colchicus) unter Berücksichtigung der spezifischen Umweltbedingungen in Fasanerien und in freier Wildbahn. Berl Munch Tierarztl Wochenschr 119:295–302

    PubMed  Google Scholar 

  • Gibbons LM (2010) Keys to the nematode parasites of vertebrates. Supplementary volume. CAB International, Oxon, Wallingford, UK, p 416

    Google Scholar 

  • Gjerde B (2013) Characterisation of full-length mitochondrial copies and partial nuclear copies (numts) of the cytochrome b and cytochrome c oxidase subunit I genes of Toxoplasma gondii, Neospora caninum, Hammondia heydorni and Hammondia triffittae (Apicomplexa: Sarcocystidae). Parasitol Res 112:1493–1511

    Article  PubMed  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Haase A (1939) Untersuchungen über die bei deutschen Wildhtihnern vorkommenden Eimeria-Arten. Arch Protistenk 52:329–383

    Google Scholar 

  • Imai RK, Barta JR (2019) Distribution and abundance of Eimeria species in commercial turkey flocks across Canada. Can Vet J 60:153–159

    PubMed  PubMed Central  Google Scholar 

  • Itagaki H, Watanabe T, Kobara J (1974) Studies on Capillaria perforans Kotlán et Orosz, 1931 from the guinea fowl I. Morphology. Bull Azabu Vet Coll 28:77–82 (in Japanese)

    Google Scholar 

  • Joyner LP, Long PL (1974) The specific characters of the Eimeria, with special reference to the Coccidia of the fowl. Avian Pathol 3:145–157

    Article  CAS  PubMed  Google Scholar 

  • Kamimura K, Yonemitsu K, Maeda K, Sakaguchi S, Setsuda A, Varcasia A, Sato H (2018) An unexpected case of a Japanese wild boar (Sus scrofa leucomystax) infected with the giant thorny-headed worm (Macracanthorhynchus hirudinaceus) on the mainland of Japan (Honshu). Parasitol Red 117:2315–2322

    Article  Google Scholar 

  • Kellogg FE, Prestwood AK (1968) Case report and differentiating characteristics of Capillaria phasianina from pen-raised pheasants of Maryland. Avian Dis 12:518–522

    Article  CAS  PubMed  Google Scholar 

  • Kinoshita M, Shibahara T, Sasai K, Matsubayashi M (2021) Morphological characteristics and comparison of Eimeria spp. from phasianid birds. J Jpn Soc Poult Dis 56:174–178 (in Japanese)

    Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Le Blancq SM, Khramtsov NV, Zamani F, Upton SJ, Wu TW (1997) Ribosomal RNA gene organization in Cryptosporidium parvum. Mol Biochem Parasitol 90:463–478

    Article  PubMed  Google Scholar 

  • Long PL, Millard BJ (1979) Studies on Eimeria dispersa Tyzzer 1929 in turkeys. Parasitology 78:41–51

    Article  CAS  PubMed  Google Scholar 

  • Lund EE, Chute AM (1972) The ring-necked pheasant (Phasianus colchicus torquatus) as a host for Heterakis gallinarum and Histomonas meleagridis. Am Midl Nat 87:1–7

    Article  Google Scholar 

  • Madsen H (1951) Note on the species of Capillaria Zeder, 1800 known from gallinaceous birds. J Parasitol 1:257–265

    Article  Google Scholar 

  • Matsubayashi M, Takami K, Kinoshita M, Tsuchida S, Ushida K, Shibahara T, Sasai K (2021) Morphological and molecular identification of Eimeria tetartooimia oocysts from a Japanese green pheasant (Galliformes; Phasianidae; Phasianus versicolor) at a zoo in Japan. Parasitol Res 120:2973–2979

    Article  PubMed  Google Scholar 

  • McCutchan TF, Cruz VF, de la Lal AA, Gunderson JH, Elwood HJ, Sogin ML (1988) Primary sequences of two small subunit ribosomal RNA genes from Plasmodium falciparum. Mol Biochem Parasitol 28:63–68

    Article  CAS  PubMed  Google Scholar 

  • Mendonça JM (1953) Heterakis isolonche Linstow, 1906 e Heterakis gallinae (Gmelin, 1790), agentes causais da Tiflite verrucosa em faisões no Jardim Zoológico do Distrito Federal. Mem Inst Oswaldo Cruz 51:675–687 (in Portuguese)

    Article  PubMed  Google Scholar 

  • Menezes RC, Tortelly R, Gomes DC, Roberto Pinto RM (2003) Nodular typhlitis associated with the nematodes Heterakis gallinarum and Heterakis isolonche in pheasants: Frequency and pathology with evidence of neoplasia. Mem Inst Oswaldo Cruz 98:1011–1016

    Article  PubMed  Google Scholar 

  • Millán J, Gortázar C, Tizzani P, Buenestado FJ (2002) Do helminths increase the vulnerability of released pheasants to fox predation? J Helminthol 76:225–229

    Article  PubMed  Google Scholar 

  • Millán J, Gortázar C, Villafuerte R (2004) A comparison of the helminth faunas of wild and farm-reared red-legged partridge. J Wildl Manage 68:701–707

    Article  Google Scholar 

  • Miska KB, Schwarz RS, Jenkins MC, Rathinam T, Chapman HD (2010) Molecular characterization and phylogenetic analysis of Eimeria from turkeys and gamebirds: implications for evolutionary relationships in galliform birds. J Parasitol 96:982–986

    Article  CAS  PubMed  Google Scholar 

  • Moravec F (1982) Proposal of a new systematic arrangement of nematodes of the family Capillariidae. Folia Parasitol 29:119–132

    CAS  Google Scholar 

  • Moravec F (2001) Trichinelloid Nematodes Parasitic in Cold-blooded Vertebrates. Academia, Prague, Czech Republic

    Google Scholar 

  • Morgan JAT, Godwin RM (2017) Mitochondrial genomes of Australian chicken Eimeria support the presence of ten species with low genetic diversity among strains. Vet Parasitol 30:58–66

    Article  Google Scholar 

  • Norton CC (1967a) Eimeria duodenalis sp. nov. from English covert pheasants (Phasianus sp.). Parasitology 57:31–46

    Article  Google Scholar 

  • Norton CC (1967b) Eimeria colchici sp. nov. (Protozoa: Eimeriidae), the cause of cecal coccidosis in English covert pheasants. J Protozool 14:772–781

    Article  Google Scholar 

  • Norton CC (1976) Coccidia of the pheasant. Folia Vet Lat 6:218–238

    CAS  PubMed  Google Scholar 

  • Ogedengbe JD, Hanner RH, Barta JR (2011) DNA barcoding identifies Eimeria species and contributes to the phylogenetics of coccidian parasites (Eimeriorina, Apicomplexa, Alveolata). Int J Parasitol 41:843–850

    Article  CAS  PubMed  Google Scholar 

  • Ogedengbe ME, El-Sherry S, Whale J, Barta JR (2014) Complete mitochondrial genome sequences from five Eimeria species (Apicomplexa; Coccidia; Eimeriidae) infecting domestic turkeys. Parasites & Vectors 7:335

    Article  Google Scholar 

  • Omoto A, Koresawa M (2015) Syngamus trachea disease in pheasants with coccidiosis and Capillaria spp. infection. J Jpn Soc Poult Dis 51:91–98 (in Japanese with English summary)

    Google Scholar 

  • Ormsbee RA (1939) Field studies on coccidiosis in the ring-neck pheasants of Eastern Washington. Parasitology 31:389–399

    Article  Google Scholar 

  • Phosuk I, Sanpool O, Thanchomnang T, Sadaow L, Rodpai R, Anamnart W, Janwan P, Wijit A, Laymanivong S, Aung WPP, Intapan PM, Maleewong W (2018) Molecular Identification of Trichuris suis and Trichuris trichiura eggs in human populations from Thailand, Lao PDR, and Myanmar. Am J Trop Med Hyg 98:39–44

    Article  PubMed  Google Scholar 

  • Pinto RM, Tortelly R, Menezes RC, Gomes DC (2004) Trichurid nematodes in ring-necked pheasants from backyard flocks of the State of Rio de Janeiro, Brazil: Frequency and Pathology. Mem Inst Oswaldo Cruz 99:721–726

    Article  PubMed  Google Scholar 

  • Poplstein M, Vrba V (2011) Description of the two strains of turkey coccidian Eimeria adenoeides with remarkable morphological variability. Parasitology 138:1211–1216

    Article  CAS  PubMed  Google Scholar 

  • Qari SH, Goldman IF, Pieniazek NJ, Collins WE, Lal AA (1994) Blood and sporozoite stage-specific small subunit ribosomal RNA-encoding genes of the human malaria parasite Plasmodium vivax. Gene 150:43–49

    Article  CAS  PubMed  Google Scholar 

  • Reddy GR, Chakrabarti D, Yowell CA, Dame JB (1991) Sequence microheterogeneity of the three small subunit ribosomal RNA genes of Babesia bigemina: expression in erythrocyte culture. Nucleic Acids Res 19:3641–3645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robertson PA (1997) Pheasants. Voyageur Press, Beverly, Massachusetts, USA

    Google Scholar 

  • Rząd I, Stapf A, Kornaś SA, Dzika E, Sałamatin R, Kaczmarek A, Kowal J, Wajdzik M, Zalewski K (2021) Intestinal helminth communities of grey partridge Perdix perdix and common pheasant Phasianus colchicus in Poland. Animals 2021:3396. https://doi.org/10.3390/ani11123396

    Article  Google Scholar 

  • Saif YM (2008) Diseases of Poultry, 12th edn. Blackwell Publishing Professional, Ames, Iowa, USA

    Google Scholar 

  • Sakaguchi S, Yunus M, Sugi S, Sato H (2020) Integrated taxonomic approaches to seven species of capillariid nematodes (Nematoda: Trichocephalida: Trichinelloidea) in poultry from Japan and Indonesia, with special reference to their 18S rDNA phylogenetic relationships. Parasitol Res 119:957–972

    Article  PubMed  Google Scholar 

  • Schwarz RH, Ryan S, Schwarz RS, Jenkins MC, Klopp S, Miska KB (2009) Genomic analysis of Eimeria spp. populations in relation to performance levels of broiler chicken farms in Arkansas and North Carolina, USA. J Parasitol 95:871–880

    Article  CAS  PubMed  Google Scholar 

  • Sepielak K, Kowal J, Nosal P (2019) Heterakis isolonche Linstow, 1906 – a new nematode species found in ornamental pheasants in Poland. Ann Parasitol 65:167–170

    PubMed  Google Scholar 

  • Tamaru M, Yamaki S, Jimenez LA, Sato H (2015) Morphological and molecular genetic characterization of three Capillaria spp. (Capillaria anatis, Capillaria pudendotecta, and Capillaria madseni) and Baruscapillaria obsignata (Nematoda: Trichuridae: Capillariinae) in avians. Parasitol Res 114:4011–4022

    Article  PubMed  Google Scholar 

  • Tampieri MP, Galuppi R, Rugna G (2005) Survey on helminthofauna in pheasants from eastern Europe. Parasssitologia 47:241–245

    CAS  Google Scholar 

  • Tran BT, Ong AV, Luc PV, Sato H (2016) Morphological and molecular genetic diversity of Strongyluris calotis (Nematoda: Ascaridida: Heterakidae) in South East and East Asian lizards. Acta Parasitol 60:407–416

    Google Scholar 

  • Trigg PI (1967) Eimeria phasiani Tyzzer, 1929 – A coccidium from the pheasant (Phasianus colchicus). I. The life cycle. Parasitology 57:135–145

    Article  Google Scholar 

  • Tyzzer EE (1929) Coccidiosis in gallinaceous birds. Am J Hyg 10:269–383

    Google Scholar 

  • Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3—new capabilities and interfaces. Nucleic Acids Res 40:e115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vrba V, Pakandl M (2014) Coccidia of turkey: from isolation, characterization and comparison to molecular phylogeny and molecular diagnostics. Int J Parasitol 44:985–1000

    Article  CAS  PubMed  Google Scholar 

  • Vrba V, Pakandl M (2015) Host specificity of turkey and chicken Eimeria: controlled cross-transmission studies and a phylogenetic view. Vet Parasitol 208:118–124

    Article  PubMed  Google Scholar 

  • Vrba V, Poplstein M, Pakandl M (2011) The discovery of the two types of small subunit ribosomal RNA gene in Eimeria mitis contests the existence of E. mivati as an independent species. Vet Parasitol 183:47–53

    Article  CAS  PubMed  Google Scholar 

  • Wacha RS (1973) The sporulated oocysts of Eimeria tetartooimia sp. n., and E. duodenalis and E. pacifica (Protozoa: Eimeriidae) redescribed, from the ring-necked pheasant, Phasianus colchicus. Proc Helminth Soc Wash 40:56–58

    Google Scholar 

  • Wakelin D (1964) A survey of the intestinal helminths parasitic in British domestic fowl. J Helminthol 38:191–200

    Article  CAS  PubMed  Google Scholar 

  • Wakelin D (1965) On species of the genus Capillaria Zeder, 1800 (Nematoda) from British domestic fowl. Parasitology 55:285–301

    Article  CAS  PubMed  Google Scholar 

  • Wakelin D (1967) Nematodes of the Genus Capillaria Zeder, 1800, from the Collection of the London School of Hygiene and Tropical Medicine. 1. Capillariids from British birds. J Helminthol 41:401–408

    Article  CAS  PubMed  Google Scholar 

  • Wehr EE (1936) Earthworms as transmitters of Capillaria annulata, the "crop-worm" of chickens. North Am Vet 17:18–20

    Google Scholar 

  • Yakimoff WL, Matschoulsky S-N (1937) Nouvelle coccidie du faisan. Ann Parasitol Hum Comp 15:162–163

    Article  Google Scholar 

  • Yevstafyeva VA, Melnychuk VV, Nikiforova OV, Suprunenko KV, Korchan LN, Lokes-Krupka TP, Nehrebetskyi IS, Korchan NI (2018) Comparative morphology and biology of nematodes of genus Heterakis (Nematoda, Heterakidae), parasites of the domestic goose (Anser anser) in Ukraine. Regul Mech Biosyst 9:229–236

    Article  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

Authors

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.

Ethics declarations

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.

Competing interests

The authors declare no competing interests.

Additional information

Handling Editor: Una Ryan

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

ESM 1

(DOCX 18.3 kb)

ESM 2

(DOCX 107 kb)

ESM 3

(DOCX 96 kb)

ESM 4

(DOCX 132 kb)

ESM 5

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)

ESM 6

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)

ESM 7

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 (ad) are at the same magnification, and the scale bar is shown in (d). Similarly, photographs (fh) 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)

ESM 8

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 (eg), (h and i), and (j and k) are, respectively, at the same magnification, and the scale bar is individually shown. (TIF 34.7 mb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-023-08014-y

Keywords

Navigation