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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

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Abstract

Morphological and genetic analyses were performed on seven species of the family Capillariidae (Nematoda: Trichocephalida: Trichinelloidea), viz. Eucoleus perforans, Eucoleus contortus, Aonchotheca bursata, Baruscapillaria obsignata, Capillaria anatis, Capillaria phasianina, and Capillaria spinulosa, detected in poultry from Japan and Indonesia. Two Eucoleus spp., perforating the esophageal mucosa of the Japanese green pheasant farmed in Japan (E. perforans) and domestic goose in Indonesia (E. contortus), were morphologically characterized. Furthermore, we observed substantial nucleotide differences between their 18S ribosomal RNA gene (rDNA), revealing maximum identity (97.27%) over the 1797-bp length. Similarly, B. obsignata in the small intestine of Japanese green pheasants in Japan, a chicken, geese, domestic pigeons, and a turkey in Indonesia, and C. anatis in the ceca of chickens in Indonesia were morphologically and molecular-genetically compared with previously reported isolates of these species in Japan. Aonchotheca bursata collected from the small intestine of the Japanese green pheasant was also molecular-genetically characterized for the first time; however, sequencing of the 18S rDNA of C. phasianina from the cecum of the same bird was unsuccessful. Capillaria worms in the ceca of a domestic duck and geese in Indonesia were identified as C. spinulosa, which had only previously been recorded in wild birds of the Anseriformes in the Palaearctic region. Morphologically, this species was closest to Capillaria pudendotecta recorded from the ceca of wild and captive swans, except for the lack of vaginal appendages in female worms and shorter esophagi relative to the body length in both male and female worms. Phylogenetically, these two species were closely related, although substantial nucleotide changes were noted. The 18S rDNA nucleotide sequences of the species isolated here were consistent with the recent taxonomic system established for Capillariidae based primarily on the morphology of male caudal ends.

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References

  • Anderson RC (1992) Nematode parasites of vertebrates: their development and transmission. CAB International, Oxon, p 578

    Google Scholar 

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

    Article  Google Scholar 

  • Baruš V, Sergejeva TP (1989a) Capillariids parasitic in birds in the Palaearctic region (1): Genus Capillaria. Acta Sci Nat 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 Nat Brno 23(6):1–47

    Google Scholar 

  • Baruš V, Sergejeva TP (1990a) Capillariids parasitic in birds in the Palaearctic region (3): Genus Baruscapillaria. Acta Sci Nat Brno 24(10):1–53

    Google Scholar 

  • Baruš V, Sergejeva TP (1990b) Capillariids parasitic in birds in the Palaearctic region (4): Genera Pterothominx and Aonchotheca. Acta Sci Nat 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  Google Scholar 

  • Cram EB (1936) Species of Capillaria in the upper digestive tract of birds. Tech Bull U S Dept Agric 516:1–27

    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  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 

  • Di Cesare A, Otranto D, Latrofa MS, Veronesi F, Perrucci S, Lalosevic D, Gherman CM, Traversa D (2014) Genetic variability of Eucoleus aerophilus from domestic and wild hosts. Res Vet Sci 96:512–515

    Article  Google Scholar 

  • Di Cesare A, Veronesi F, di Regalbono AF, De Liberato C, Perrucci S, Iorio R, Morganti G, Marangi M, Simonato G, Traversa D (2015) PCR-based assay for the mitochondrial cox1 specific amplification of Eucoleus böhmi. Vet Parasitol 211:67–70

    Article  Google Scholar 

  • Fantozzi MC, Robles MR, Peña FE, Antoniazzi LR, Beldomenico PM, Monje LD (2018) Calodium hepaticum (Nematoda: Capillariidae) in wild rodent populations from Argentina. Parasitol Res 117:2921–2926

    Article  Google Scholar 

  • Feldman SH, Ramirez M (2014) Molecular phylogeny of Pseudocapillaroides xenopi (Moravec et Cosgrov 1982) and development of a quantitative PCR assay for its detection in aquarium sediment. J Am Assoc Lab Anim Sci 53:668–674

    PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Graybill HW (1924) Capillaria columbae (Rud.) from the chicken and turkey. J Parasitol 10:205–207

    Article  Google Scholar 

  • Guardone L, Deplazes P, Macchioni F, Magi M, Mathis A (2013) Ribosomal and mitochondrial DNA analysis of Trichuridae nematodes of carnivores and small mammals. Vet Parasitol 197:364–369

    Article  CAS  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  Google Scholar 

  • Hodda M (2011) Phylum Nematoda Cobb 1932. In: Zhang ZQ (ed) Animal biodiversity: an outline of higher-level classification and survey of taxonomic richness, pp 63–95. Zootaxa 3148 (Monograph)

  • Honisch M, Krone O (2008) Phylogenetic relationships of Spiruromorpha from birds of prey based on 18S rDNA. J Helminthol 82:129–133

    Article  CAS  Google Scholar 

  • Itagaki H (1966) Studies on Capillaria sp. from the upper digestive tract of the guinea fowl. I. Morphology and development. Jpne Jf Parasitol 15:368–370 (in Japanese)

    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 

  • 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  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 

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

    CAS  PubMed  Google Scholar 

  • Moravec F (2001) Trichinelloid nematodes parasitic in cold-blooded vertebrates. Academia, Prague, p 430

    Google Scholar 

  • Saif YM (2008) Diseases of poultry, 12th edn. Blackwell Publishing Professional, Ames, p 1324

    Google Scholar 

  • Skrjabin KI, Shikhobalova NP, Orlov IV (1957) Essentials of nematology. Trichocephalidae and Capillariidae of animals and man and diseases caused by them. vol. VI. Academy of Sciences of the USSR (Jerusalem, Israel Program for Scientific Translations, 1970), p 599

  • 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  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  Google Scholar 

  • Tran BT, Sato H, Luc PV (2015) A new Cosmocercoides species (Nematoda: Cosmocercidae), C. tonkinensis n. sp., in the scale-bellied tree lizard (Acanthosaura lepidogaster) from Vietnam. Acta Parasitol 60:407–416

    Article  Google Scholar 

  • Varcasia A, Briant E, Tamponi C, Pipia AP, Cabras PA, Mereu M, Dantas-Torres F, Scala A, Otranto D (2015) Simultaneous infection by four feline lungworm species and implications for the diagnosis. Parasitol Res 114:317–321

    Article  CAS  Google Scholar 

  • Wakelin D (1963) Capillaria obsignata Madsen, 1945 (Nematoda) from the black swan. J Helminthol 37:381–386

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Zhu X, Spratt DM, Beveridge I, Haycock P, Gasser RB (2000) Mithochondrial DNA polymorphism within and among species of Capillaria sensu lato from Australian marsupials and rodents. Int J Parasitol 30:933–938

    Article  CAS  Google Scholar 

  • Zucchero PJ (1942) Notes on the life cycle of Capillaria annulata. Proc West Va Acad Sci 15:96–106

    Google Scholar 

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Acknowledgment

We thank Professor Emeritus Shuhei Tanaka (Faculty of Agriculture, Yamaguchi University) for assistance with the SEM analysis.

Funding

We also thank the Faculty of Veterinary Medicine, Airlangga University, for supporting the international collaborative study with the Joint Faculty of Veterinary Medicine, Yamaguchi University.

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Author notes

  1. Seiho Sakaguchi and Muchammad Yunus contributed equally to this work.

Authors and Affiliations

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

    Seiho Sakaguchi & Hiroshi Sato

  2. Department of Parasitology, Faculty of Veterinary Medicine, Airlangga University, Campus C, Mulyorejo, Surabaya, 60115, Indonesia

    Muchammad Yunus & Hiroshi Sato

  3. United Graduate School of Veterinary Science, Yamaguchi University, 1677-1 Yoshida, Yamaguchi, 753-8515, Japan

    Shinji Sugi & Hiroshi Sato

Authors
  1. Seiho Sakaguchi
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  2. Muchammad Yunus
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  3. Shinji Sugi
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  4. Hiroshi Sato
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Corresponding author

Correspondence to Hiroshi Sato.

Ethics declarations

The ethics of animal processing and sample collection adhered to in this study followed the guidelines outlined in the veterinary section of the Kumamoto Prefecture for Municipal Routine Survey and Faculty of Veterinary Medicine, Airlangga University for Veterinary Professional Education and Research (Ethical Clearance No. 1.KE.047.04.2019).

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The authors declare that they have no conflicts of interest.

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Sakaguchi, S., Yunus, M., Sugi, S. et al. 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 (2020). https://doi.org/10.1007/s00436-019-06544-y

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