Skip to main content
SpringerLink
Log in

Morphology and Molecular Characterization of Parabronema smithii (Cobbold, 1882) (Nematoda: Habronematidae) from Wild Asian Elephant (Elephas maximus maximus) of Sri Lanka

  • Original Paper
  • Published:
Acta Parasitologica Aims and scope Submit manuscript

Abstract

Purpose

The aim of the present study was to carry out a detailed study of morphological features and to determine the phylogenetic position of Parabronema smithii (Cobbold, 1882) found in wild elephants in Sri Lanka.

Methods

Adult worms were collected from stomach ulcers at postmortem examination of wild elephants in the Udawalawe National Park, Sri Lanka. The detailed morphology of P. smithii was studied using light microscopy and, for the first time, scanning electron microscopy. Fifteen morphological characteristics were investigated. The phylogenetic analysis was conducted using the second internal transcribed spacer region (ITS2), and portions of the large subunit ribosomal DNA (28S) and cytochrome c oxidase subunit 1 (cox1). Furthermore, the present study provides a comparison of morphology and morphometrics of Parabronema species that occur in different hosts.

Conclusion

Parabronema smithii isolated from wild elephants exhibited the key morphological features. Phylogenetic analysis of selected genes revealed that P. smithii is closely associated with P. skrjabini and Habronema spp. Findings of the present study enhance our understanding of the biology and taxonomy of P. smithii in wild elephant in Sri Lanka and will contribute to future phylogeographic studies.

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

Access this article

Log in via an institution

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
Fig. 5

Similar content being viewed by others

References

  1. Baylis HA (1939) The Fauna of British India. Nematoda. Vol. II (Filaroidea, Dictophymoidea and Trichinelloidea) Today & Tomorrow´s Printers and Publishers. pp 274

  2. Fitzsimmons WM (1962) Parabronema roundi n.sp. (Spiruridae: Nematoda) from Rhinoceros bicornis in Kenya. J Helminthol 36:39–44

    Article  CAS  Google Scholar 

  3. Seneviratna P, Jayasinghe JB (1968) Some parasites from the Ceylon elephants (Elephas maximus). Ceylon Vet J XV: 28

  4. Al-asadi KBF, Al-emarah GYA (2014) Detection of Nematode Parabronema skrjabini in goats at Basrah Province. J Parasitol Photon 104:94–199

    Google Scholar 

  5. Baylis HA, Daubney R (1926) A synopsis of the families and genera of Nematoda. British Museum (Natural History), London, p 277

    Google Scholar 

  6. Chabaud AG, Mouchet J (1956) A propos d'un spiruride Parabronema africanum Baylis, 1921 présent dans le coeur et le foie d'un éléphant. Remarques sur la filiation des cycles evolutifs entre spirurides et filaires. Bull Soc Path exot 49:388–397

    CAS  PubMed  Google Scholar 

  7. Anderson RC (2000). Nematode Parasites of Vertebrates-Their Development and Transmission (Second Edition). CABI Publishing and The Natural History Museum. pp 650

  8. Fowler ME, Mikota SK (2008) Biology, medicine, and surgery of elephants. Blackwell, London, p 565

    Google Scholar 

  9. Vicente JJ, Muniz-Pereira LC, Noronha D, Pinto RM (2000) Description of males of Parabronema pecariae Ivashkin, 1960 (Nematoda, Habronematoidea) parasitizing peccaries (Mammalia, Tayassuidae) in Brazil. Mem Inst Oswaldo Cruz 95:849–851

    Article  CAS  Google Scholar 

  10. Zhang XD, Yang XY, Yang LR, Li LC, Zuo HT, Na RH, Zhao ZG, Wang JJ (2009) Cloning and sequence analysis of the rDNA-ITS of Parabronema skrjabini. Chin J Ani Vet Sci 5:026

    Google Scholar 

  11. Hasheminasab SS (2015) Molecular characterization of the first internal transcribed spacer of rDNA of Parabronema skrjabini for the first time in sheep. Ann Parasitol 61:241–246

    PubMed  Google Scholar 

  12. Graber M (1975) Parabronema longispiculatum n. sp., parasite stomacal de l´élephant d´Afrique (Loxodonta africana Blumenbach, 1797). Rev Elev Med vét Pays trop 28:473–479

    Article  CAS  Google Scholar 

  13. Kinsella JM, Deem SL, Blake S, Freeman AS (2004) Endoparasites of African forest elephants (Loxodonta africana cyclotis) from the Republic of Congo and Central African Republic. Comp Parasitol 71:104–110

    Article  Google Scholar 

  14. Ajitkumar G, Anil KS, Alex PC (2009) Healthcare management of Captive Asian elephants: feeding and management of Captive Asian Elephants. Director of Extension Kerala Agricultural University Mannuthy, Thrissur 42–65

  15. Fernando CH, Fernando A (1961) Some helminth parasites from elephants in Ceylon. Ceylon Vet J 9:24

    Google Scholar 

  16. Kuruwita VY, Vasanthathilake VWSM (1993) Gastro-intestinal [sic] nematode parasites occurring in free-ranging elephants (Elephas maximus ceylonicus) in Sri Lanka. SL Vet J 40:15–23

    Google Scholar 

  17. Chabaud AG (1975) Keys to general of the order Spirurida. Part 2. Spiruroidea, Habronematoidea and Acuaroidea. In: Anderson RC, Chabaud AG, Willmott S, CIH Keys to the Nematodes Parasites of Vertebrates 6. Commonwealth Agricultural Bureaux, Farnham Royal Bucks. 29–58

  18. Littlewood DT, Johnston DA (1995) Molecular phylogenetics of the four Schistosoma species group determined with partial 28S ribosomal RNA gene sequences. Parasitology 111:167–175

    Article  CAS  Google Scholar 

  19. Bowles J, Blair D, McManus DP (1995) A molecular phylogeny of the human schistosomes. Mol Phylogenet Evol 4:103–109

    Article  CAS  Google Scholar 

  20. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  Google Scholar 

  21. Kumar S, Stecher G, Tamura K (2016) MEGA 7: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 33:1870–1874

    Article  CAS  Google Scholar 

  22. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    CAS  PubMed  Google Scholar 

  23. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  Google Scholar 

  24. Khalil M (1922) A Revision of the nematode parasites of elephants, with a description of four new species. Proc Zool Soc Lond 92:205–279

    Article  Google Scholar 

  25. Aswegen V, Schoeman JH, De Vos V, Noorden V (1994) The oesophagus and stomach of the African elephant: a histological, immunocytochemical and immunofluorescence study. Onderstepoort J Vet Res 61:223–229

    PubMed  Google Scholar 

  26. van der Westhuysen OP (1938) A monograph of the helminth parasites of the elephant. Onderstepoort J Vet Sci Anim Ind 10:49–190

    Google Scholar 

  27. Hasheminasab SS (2016) 5.8S rRNA sequence and secondary structure in Parabronema skrjabini and related Habronematidae species. Iran J Parasitol 11:253–258

    PubMed  PubMed Central  Google Scholar 

  28. Rassowska RJ (1924) Nematodes of cattle in Turkestan. Trud Inst Eksper Vet 2:129–136

    Google Scholar 

  29. Phillips PC (2016) Evolution: five heads are better than one. Curr Biol 26(17):283–285

    Article  Google Scholar 

  30. Haag ES, Fitch DHA, Delattre M (2018) From “the Worm” to “the Worms” and back again: the evolutionary developmental biology of Nematodes. Genetics 210:397–433

    Article  CAS  Google Scholar 

  31. Coomans A (2000) Nematode systematics: past, present and future. Nematology 2(1):3–7

    Article  Google Scholar 

  32. Meldal BHM, Debenham NJ, De Ley P, De Ley IT, Vanfleteren JR, Vierstraete A et al (2007) An improved molecular phylogeny of the Nematoda with special emphasis on marine taxa. Mol Phylogenet Evol 42:622–636

    Article  CAS  Google Scholar 

  33. Holterman M, van der Wurff A, van den Elsen S, van Megen H, Bongers T, Holovachov O et al (2006) Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution towards crown clades. Mol Biol Evol 23:1792–1800

    Article  CAS  Google Scholar 

  34. van Megen H, van den Elsen S, Holterman M, Karssen G, Mooyman P, Bongers T et al (2009) A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology 11:927–950

    Article  Google Scholar 

  35. Abolafia J, Peña-Santiago R (2018) Morphology, taxonomy and phylogeny of the enigmatic genus Aulolaimus de man, 1880 (Nematoda, Aulolaimidae). Zool Anz 277:101–115

    Article  Google Scholar 

  36. Hasheminasab SS, Jalousian F, Meshgi B (2016) Molecular and morphological characterization of Parabronema skrjabini of sheep and goats at three different geographical zones in Iran. Ann Parasitol 62(1):55–61

    PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Mr. Dhammika Perera, Mr. K.P.G Karunaratna and Mr. K.M. Karunajeewa for the technical assistance (University of Peradeniya, Sri Lanka) in this project. The Department of wildlife conservation, Sri Lanka and Udawalawe National Park wildlife officers to assist to collect samples. We wish to express our gratitude to Professor David Blair, School of Marine and Tropical Biology, James Cook University for revision and invaluable comments on an early version of this paper.

Funding

This work was supported by National Research Council of Sri Lanka.

Author information

Authors and Affiliations

  1. Department of Veterinary Pathobiology, Faculty of Veterinary Medicine and Animal Science, University of Peradeniya, Peradeniya, Sri Lanka

    Lasanthika D. Thewarage, Duminda S. B. Dissanayake, Anura T. Bandara & R. P. V. J. Rajapakse

  2. National Institute of Complementary Medicine, School of Science and Health, Western Sydney University, Sydney, Australia

    Udari S. Perera

  3. Department of Wildlife Conservation, Elephant Transit Home, Udawalawe, Sri Lanka

    B. V. P. Perera

  4. Department of Parasitology, Faculty of Medicine, University of Peradeniya, Peradeniya, Sri Lanka

    S. Wickramasinghe

  5. Institute for Applied Ecology, University of Canberra, Canberra, Australia

    Duminda S. B. Dissanayake

Authors
  1. Lasanthika D. Thewarage
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Duminda S. B. Dissanayake
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Udari S. Perera
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anura T. Bandara
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. B. V. P. Perera
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. S. Wickramasinghe
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. R. P. V. J. Rajapakse
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Duminda S. B. Dissanayake.

Ethics declarations

Conflict of interest

The authors have declared that no competing interest exists.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Thewarage, L.D., Dissanayake, D.S.B., Perera, U.S. et al. Morphology and Molecular Characterization of Parabronema smithii (Cobbold, 1882) (Nematoda: Habronematidae) from Wild Asian Elephant (Elephas maximus maximus) of Sri Lanka. Acta Parasit. 65, 504–517 (2020). https://doi.org/10.2478/s11686-020-00193-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2478/s11686-020-00193-3

Keywords

Search

Navigation