Skip to main content
SpringerLink
Log in

Worm burdens and associated histopathological changes caused by gastrointestinal nematodes in alpacas from Australia

  • Helminthology - Short Communication
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

In this study, 100 gastrointestinal tracts of Australian alpacas were examined to assess the worm burden and to identify the species of nematode present. Faecal samples were collected from 97 alpacas and processed for faecal egg counts (FECs). For identification of the species, both molecular (multiplexed-tandem polymerase chain reaction [MT-PCR]) and morphological techniques were used. Total worm counts (TWCs) revealed a mean burden of 1300 worms, with the highest burden of 29,000 worms. The average egg count was 501 eggs per gram of faeces (EPG), with the highest count of 3500 EPG. Nineteen different species of gastrointestinal nematodes (GINs) were identified, and Graphinema auchenia, Camelostrongylus mentulatus and Trichuris tenuis were recovered from Australian alpacas for the first time. Haemonchus contortus was the most prevalent nematode (81%) followed by C. mentulatus (60%). The majority of the nematodes found are shared with sheep, goats and cattle. Findings of this study provide useful insights into the spectrum of GINs and their burden in Australian alpacas.

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

References

  • Altman DG (1991) Practical statistics for medical research. Chapman and Hall, London

    Google Scholar 

  • Anderson N (1972) Trichostrongylid infections of sheep in a winter rainfall region. 1. Epizootiological studies in the Western District of Victoria, 1966–67. Aust J Agric Res 23:1113–1129

    Article  Google Scholar 

  • Anderson N (1973) Trichostrongylid infections of sheep in a winter rainfall region. 2. Epizootiological studies in the Western District of Victoria, 1967–68. Aust J Agric Res 24:599–611

    Article  Google Scholar 

  • Averbeck GA, Scholtthauer JC, Hinueber JG (1981) Camelostrongylus mentulatus infection in a camel (Camelus dromedarius): a case report. J Zoo Anim Med 12:24–26

    Article  Google Scholar 

  • Ballweber LR (2009) Ecto- and endoparasites of new world camelids. Vet Clin North Am Food Anim Prac 25:295–310

    Article  Google Scholar 

  • Barger IA (1993) Control of gastrointestinal nematodes in Australia in the 21st century. Vet Parasitol 46:23–32

    Article  PubMed  CAS  Google Scholar 

  • Becklund WW, Walker ML (1967) Nematodirus of domestic sheep, Ovis aries, in the United States with a key to the species. J Parasitol 53:777–781

    Article  PubMed  CAS  Google Scholar 

  • Beldomenico PM, Uhart M, Bono MF, Marull C, Baldi R, Peralta JL (2003) Internal parasites of free-ranging guanacos from Patagonia. Vet Parasitol 118:71–77

    Article  PubMed  CAS  Google Scholar 

  • Beveridge I, Ford GE (1982) The trichostrongyloid parasites of sheep in South Australia and their regional distribution. Aust Vet J 59:177–179

    Article  PubMed  CAS  Google Scholar 

  • Beveridge I, Barker I, Rickard M, Burton J (1974) Experimental infection of sheep with Camelostrongylus mentulatus and associated gastritis. Aust Vet J 50:36–37

    Article  PubMed  CAS  Google Scholar 

  • Beveridge I, Pullman AL, Henzell R, Martin RR (1987) Helminth parasites of feral goats in South Australia. Aust Vet J 64:111–112

    Article  PubMed  CAS  Google Scholar 

  • Beveridge I, Pullman AL, Phillips PH, Martin RR, Barelds A, Grimson R (1989) Comparison of the effects of infection with Trichostrongylus colubriformis, T. vitrinus and T. rugatus in merino lambs. Vet Parasitol 32:229–245

    Article  PubMed  CAS  Google Scholar 

  • Brunsdon RV (1971) Trichostronglye worm infection in cattle: further studies on problems of diagnosis and on seasonal patterns of occurrence. N Z Vet J 19:203–212

    Article  PubMed  CAS  Google Scholar 

  • Bryan R, Kerr J (1989) The relation between the natural worm burden of steers and the faecal egg count differentiated to species. Vet Parasitol 30:327–334

    Article  PubMed  CAS  Google Scholar 

  • Cafrune MM, Aguirre DH, Rickard LG (1999) Recovery of Trichuris tenuis Chandler, 1930, from camelids (Lama glama and Vicugna vicugna) in Argentina. J Parasitol 85:961–962

    Article  PubMed  CAS  Google Scholar 

  • Carmichael IH (1999) Internal parasitism in alpacas in southern Australia. In: Australian Alpaca Fibre – Improving Productivity and Marketing. Rural Industries Research and Development Corporation, Canberra, pp. 92–130

  • Chandler AC (1930) Specific characters in the genus Trichuris, with a description of a new species, Trichuris tenuis, from a camel. J Parasitol 16:198–206

  • Contreras S, Chávez V, Pinedo V, Leyva V, Suárez A (2014) Helminthiasis in alpacas (Vicugna pacos) of two peasant communities in Macusani, Puno during the dry season. Rev Investig Vet Perú 25:268–275

    Article  Google Scholar 

  • Copland JW (1965) Ostertagia mentulata recorded in New South Wales. Aust Vet J 41:27–27

    Article  Google Scholar 

  • Dittmer KE, Hinkson JA, Dwyer C, Adlington B, van Andel M (2018) Prevalence of Candidatus Mycoplasma haemolamae, bovine viral diarrhoea virus, and gastrointestinal parasitism in a sample of adult New Zealand alpaca (Vicugna pacos). N Z Vet J 66:9–15

    Article  PubMed  CAS  Google Scholar 

  • Gibbons LM, Khalil LF (1982) A key for the identification of genera of the nematode family Trichostrongylidae Leiper, 1912. J Helminthol 56:185–233

  • Gordon HM, Whitlock H (1939) A new technique for counting nematode eggs in sheep faeces. J CSIR 12:50–52

    Google Scholar 

  • Hertzberg H, Kohler L (2006) Prevalence and significance of gastrointestinal helminths and protozoa in south American camelids in Switzerland. Berl Munch Tierarztl Wochenschr 119:291–294

    PubMed  Google Scholar 

  • Hill F, Death A, Wyeth T (1993) Nematode burdens of alpacas sharing grazing with sheep in New Zealand. NZ Vet J 41:205–208

    Article  CAS  Google Scholar 

  • Hilton RJ, Barker IK, Rickard MD (1978) Distribution and pathogenicity during development of Camelostrongylus mentulatus in the abomasum of sheep. Vet Parasitol 4:231–242

    Article  Google Scholar 

  • Hutchinson G (2009) Nematode parasites of small ruminants, camelids and cattle: diagnosis with emphasis on anthelmintic efficacy and resistance testing. Aquatic and Terrestrial Australian and New Zealand Standard Diagnostic Procedures (ANZSDPs) http://www.agriculture.gov.au/animal/health/laboratories/procedures/anzsdp

  • Hyuga A, Matsumoto J (2016) A survey of gastrointestinal parasites of alpacas (Vicugna pacos) raised in Japan. J Vet Med Sci 78:719–721

    Article  PubMed  Google Scholar 

  • Jabbar A, Campbell AJD, Charles JA, Gasser RB (2013) First report of anthelmintic resistance in Haemonchus contortus in alpacas in Australia. Parasit Vectors 6:243

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • McKenna PB (1981) The diagnostic value and interpretation of faecal egg counts in sheep. N Z Vet J 29(8):129–132

    Article  PubMed  CAS  Google Scholar 

  • Michel JF (1969a) Observations on the faecal egg count of calves naturally infected with Ostertagia ostertagi. Parasitology 59:829–835

    Article  Google Scholar 

  • Michel JF (1969b) The regulation of egg output by Ostertagia ostertagi in calves infected once only. Parasitology 59:767–774

    Article  Google Scholar 

  • Presidente PJA (2007) Alpaca parasites & their control: recent experiences. Australian Alpaca Veterinarians Annual Conference, Australia, pp 1–14

    Google Scholar 

  • R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria https://www.R-project.org/

    Google Scholar 

  • Rashid MH, Gebrekidan H, Jabbar A (2018a) Multiplexed-tandem PCR (MT-PCR) assay to detect and differentiate gastrointestinal nematodes of alpacas. Parasit Vectors 11:370

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rashid MH, Stevenson MA, Waenga S, Mirams G, Campbell AJD, Vaughan JL, Jabbar A (2018b) Comparison of McMaster and FECPAKG2 methods for counting nematode eggs in the faeces of alpacas. Parasit Vectors 11:278

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rashid MH, Vaughan JL, Stevenson MA, Campbell AJD, Saeed MA, Indjein L, Beveridge I, Jabbar A (2019a) Epidemiology of gastrointestinal nematodes of alpacas in Australia: I. a cross-sectional study. Parasitol Res. https://doi.org/10.1007/s00436-019-06235-8

  • Rashid MH, Vaughan JL, Stevenson MA, Saeed MA, Campbell AJD, Beveridge I, Jabbar A (2019b) Epidemiology of gastrointestinal nematodes of alpacas in Australia: II. A longitudinal study. In: Parasitol res. https://doi.org/10.1007/s00436-019-06236-7

  • Rickard LG (1993) Parasitic gastritis in a llama (Lama glama) associated with inhibited larval Teladorsagia spp. (Nematoda: Trichostrongyloidea). Vet Parasitol 45:331–335

    Article  PubMed  CAS  Google Scholar 

  • Rickard LG, Bishop JK (1991) Redescription of Trichuris tenuis Chandler, 1930, from llamas (Lama glama) in Oregon with a key to the species of Trichuris present in north American ruminants. J Parasitol 77:70–75

    Article  PubMed  CAS  Google Scholar 

  • Roberts F (1957) Reactions of calves to infestation with the stomach worm, Haemonchus placei (place, 1893) ransom, 1911. Aust J Agric Res 8:740–767

    Article  Google Scholar 

  • Roeber F, Jex AR, Gasser RB (2013) Comparative evaluation of two DNA isolation techniques for PCR-based diagnosis of gastrointestinal nematode infections in sheep. Mol Cell Probes 27:153–157

    Article  PubMed  CAS  Google Scholar 

  • Rogers WP (1939) Nematode parasites of sheep in Western Australia. J Helminthol 17:151–158

    Article  Google Scholar 

  • Rose JH, Small AJ (1980) Transmission of Oesophagostomum spp. among sows at pasture. Vet Rec 107:223–225

    Article  PubMed  CAS  Google Scholar 

  • Rubin R (1967) Some observations on the interpretation of fecal egg counts. Amer J Vet Clin Path 1:145–148

    Google Scholar 

  • Schmäschke R (2015) Endo-and ectoparasites of south American camelids and their control. Tierarztl Prax Ausg G Grosstiere Nutztiere 43:169–179

    Article  PubMed  Google Scholar 

  • Stevenson M, Nunes T, Heuer C, Marshall J, Sanchez J, Thornton R, Reiczigel J, Robison-Cox J, Sebastiani P, Solymos P, Yoshida K, Jones G, Pirikahu S, Firestone S, Kyle R, Popp J, Mathew J (2018) epiR: tools for the analysis of epidemiological data. Faculty of Veterinary and Agricultural Sciences, the. University of Melbourne, Melbourne

    Google Scholar 

  • Tait SA, Kirwan JA, Fair CJ, Coles GC, Stafford KA (2002) Parasites and their control in south American camelids in the United Kingdom. Vet Rec 150:637–638

    Article  PubMed  CAS  Google Scholar 

  • Thomas RJ, Boag B (1973) Epidemiological studies on gastro-intestinal nematode parasites of sheep. The control of infection in lambs on contaminated pasture. Res Vet Sci 14:11–20

    Article  PubMed  Google Scholar 

  • Welchman DB, Parr J, Wood R, Mead A, Starnes A (2008) Alpaca and llama nematodes in Britain. Vet Rec 162:832–832

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to alpaca farmers who provided the gastrointestinal and faecal samples for this study. We are thankful to Ms. Christine Andersen and Doctor of Veterinary Medicine Students for their technical assistance.

Funding

The financial assistance for this project was provided by the AgriFutures Australia and the Australian Alpaca Association. M.H.R. is a grateful recipient of the Australian Postgraduate Award through the University of Melbourne and the PhD top-up scholarship from the AgriFutures Australia.

Author information

Authors and Affiliations

  1. Department of Veterinary Biosciences, Melbourne School of Veterinary Science, The University of Melbourne, Werribee, Victoria 3030, Australia

    Mohammed H. Rashid, Ian Beveridge & Abdul Jabbar

  2. Cria Genesis, PO Box 406, Ocean Grove, Victoria, 3226, Australia

    Jane L. Vaughan

Authors
  1. Mohammed H. Rashid
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ian Beveridge
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jane L. Vaughan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Abdul Jabbar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Abdul Jabbar.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests.

Additional information

Section Editor: Dante Zarlenga

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

Rashid, M.H., Beveridge, I., Vaughan, J.L. et al. Worm burdens and associated histopathological changes caused by gastrointestinal nematodes in alpacas from Australia. Parasitol Res 118, 1031–1038 (2019). https://doi.org/10.1007/s00436-019-06237-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-019-06237-6

Keywords

Search

Navigation