Skip to main content
Log in

Morphological and molecular identification of Habronema spp. (Nematoda: Habronematidae) from donkeys in Xinjiang, China, and notes on the taxonomical status of Habronema majus (Creplin, 1849) and H. microstoma (Schneider, 1866)

  • Published:
Systematic Parasitology Aims and scope Submit manuscript

Abstract

Habronematid nematodes were collected from the stomachs of donkeys, Equus asinus L., in the Tarim Basin, Xinjiang, China. After examination by light and scanning electron microscopy, Habronema muscae (Carter, 1861) and H. majus (Creplin, 1849) were identified. The morphology of our specimens representing H. muscae (Carter, 1861) agreed well with previous redescriptions in the shape of the lateral lips, origin of the lateral alae, ratio of left and right spicules, and number and arrangement of caudal papillae. However, H. majus (Creplin, 1849) differs from H. microstoma (Schneider, 1866) in the arrangement of the caudal papillae in the male. Moreover, molecular analysis also showed interspecific differences of 26.2–28.2% in ITS2 and 8.6–8.9% in cox1 between H. majus and H. microstoma, a divergence much higher than the known intraspecific variation of Habronema spp. (6.6–8.7% in ITS2; 0.2–2.2% in cox1). The results indicate that both H. microstoma (Schneider, 1866) and H. majus (Creplin, 1849) are valid species.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Anderson, R. C. (2000). Nematode parasites of vertebrates, their development and transmission. Wallingford, UK: CABI.

    Book  Google Scholar 

  • Casiraghi, M., Anderson, T. J. C., Bandi, C., Bazzocchi, C., & Genchi, C. (2001). A phylogenetic analysis of filarial nematodes: comparison with the phylogeny of Wolbachia endosymbionts. Parasitology, 122, 93–103.

    Article  CAS  PubMed  Google Scholar 

  • Euzeby, J. (1961). Les Maladies Vermineuses des Animaux Domestiques et leurs Incidences sur la Pathologie Humaine. Maladies dues aux Nemathelminthes. Fascicule Premier.. Paris: Vigot Frères, pp. 252–292.

    Google Scholar 

  • Iorio, R., Slapeta, J., Otranto, D., Paoletti, B., Giangaspero, A., & Traversa, D. (2009). Phylogenetic relationships of Habronema microstoma and Habronema muscae (Spirurida: Habronematidae) within the order Spirurida inferred using mitochondrial cytochrome c oxidase subunit 1 (cox1) gene analysis. Parasitology Research, 104, 979–984.

    Article  PubMed  Google Scholar 

  • Lichtenfels, J. R. (1975). Helminths of domestic equids: illustrated keys to genera and species with emphasis on North American forms. Proceedings of the Helminthological Society of Washington, 42, 1–92.

    Google Scholar 

  • Marcato, P. S. (2002). [Sistema gastroenterico e peritoneo. Lesioni Parassitarie.] In: Patologia Sistematica Veterinaria, Edizioni Agricole - Il Sole 24 Ore, Bologna, Italy, pp. 670–672.

  • Murray, D. R., Ladds, P. W., & Campbell, R. S. F. (1978). Granulomatous and neoplastic diseases of the skin of horses. Australian Veterinary Journal, 54, 338–341.

    Article  CAS  PubMed  Google Scholar 

  • Naem, S. (2007a). First description of the horse stomach worm, Habronema muscae (Spirurida: Habronematidae) by scanning electron microscopy. Parasitology Research, 101, 427–432.

    Article  PubMed  Google Scholar 

  • Naem, S. (2007b). First SEM observations on adult Habronema microstoma (Spirurida: Habronematidae), a parasite of the horse. Parasitology Research, 101, 743–749.

    Article  PubMed  Google Scholar 

  • Posada, D., & Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics, 14, 817–818.

    Article  CAS  PubMed  Google Scholar 

  • Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., et al. (2012). MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.

    Article  PubMed  PubMed Central  Google Scholar 

  • Scott, D. W., & Miller, W. H. (2003). Parasitic diseases. Equine dermatology. St. Louis, MO, USA: Saunders, pp. 357–360.

    Google Scholar 

  • Skrjabin, K. I., & Sobolev, A. A. (1963). [Principles of Nematology 11. Spirurata of animals and man and the diseases caused by them. Part 1. Spiruroidea.] Moscow: Izdatel’stvo Nauka, 333 pp (in Russian).

  • Subbotin, S. A., Vierstraete, A., De Ley, P., Rowe, J., Waeyenberge, L., Moens, M., et al. (2001). Phylogenetic relationships within the cyst-forming nematodes (Nematoda, Heteroderidae) based on analysis of sequences from the ITS regions of ribosomal DNA. Molecular Phylogenetics and Evolution, 21, 1–16.

    Article  CAS  PubMed  Google Scholar 

  • Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., & Higgins, D. G. (1997). The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25, 4876–4882.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Traversa, D., Giangaspero, A., Galli, P., Paoletti, B., Otranto, D., & Gasser, R. B. (2004). Specific identification of Habronema microstoma and Habronema muscae (Spirurida, Habronematidae) by PCR using markers in ribosomal DNA. Molecular and Cellular Probes, 18, 215–221.

    Article  CAS  PubMed  Google Scholar 

  • Yamaguti, S. (1943). Studies on the helminth fauna of Japan. Part 43. Mammalian nematodes IV. Japanese Journal of Zoology, 10, 427–454.

    Google Scholar 

  • Yamaguti, S. (1961). Systema Helminthum. Vol. III. The nematodes of vertebrates, part I and II. New York: Interscience.

    Google Scholar 

  • Zhang, L.-P., & K’ung, F.-Y. (2002). Parasitic Nematodes from Equus spp. Beijing: China Agricultural Publication, pp. 145–151.

    Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This study was supported by the National Natural Science Foundation of China (Grant No. 31260604).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lu-Ping Zhang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable institutional, national and international guidelines for the care and use of animals were followed.

Additional information

This article was registered in the Official Register of Zoological Nomenclature (ZooBank) as 2E50EB7C-C10B-4EAA-82BA-71017E1863C3. This article was published as an Online First article on the online publication date shown on this page. The article should be cited by using the doi number. This is the Version of Record.

This article is part of the Topical Collection Nematoda.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jian, R., Wang, SW., Zhang, WX. et al. Morphological and molecular identification of Habronema spp. (Nematoda: Habronematidae) from donkeys in Xinjiang, China, and notes on the taxonomical status of Habronema majus (Creplin, 1849) and H. microstoma (Schneider, 1866). Syst Parasitol 94, 511–525 (2017). https://doi.org/10.1007/s11230-017-9714-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11230-017-9714-8

Keywords

Navigation