Abstract
We conducted a longitudinal survey on 13 alpaca farms in four climatic zones of Australia to understand the epidemiology of gastrointestinal nematodes (GINs) of alpacas. A total of 1688 fresh faecal samples were collected from both sexes of alpacas from May 2015 to April 2016 and processed for faecal egg counts (FEC) and molecular identification of eggs using the multiplexed-tandem PCR assay. Based on egg morphology, the overall prevalence of GINs was 61% while that for strongyles was 53%. The overall mean FEC was 168 eggs per gram (EPG) of faeces, with the highest count of 15,540 EPG. Weaners had the highest prevalence (73%) and mean FEC (295 EPG) of GINs followed by tuis, crias and adults. Alpacas in the winter rainfall zone had the highest prevalence (68%) as well as FEC (266 EPG) followed by Mediterranean-type, non-seasonal and summer rainfall zones. Trichostrongylus spp. (83%, 89/107), Haemonchus spp. (71%, 76/107) and Camelostrongylus mentulatus (63%, 67/107) were the three most common GINs of alpacas across all climatic zones. The mixed-effects zero-inflated negative binomial regression model used in this study showed that it could help to design parasite control interventions targeted at both the herd level and the individual alpaca level. The findings of this study showed that the epidemiology of GINs of alpacas is very similar to those of cattle and sheep, and careful attention should be paid when designing control strategies for domestic ruminants co-grazing with alpacas.
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Abdouslam O, Al-Bassam L, Al-Izzi S, Azwai S (2003) Prevalence of external and internal parasites in llamas (Lama glama) at Surman park in Libya. J Camel Pract Res 10:61–65
Alcaino H, Gorman T, Burgos M (1991) Helmintiasis gastrointestinal en llamas (Lama glama) de la I Región de Chile. Parasitol Día 15:93–96
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
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
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
Ballweber LR (2009) Ecto- and endoparasites of new world camelids. Vet Clin North Am Food Anim Pract 25:295–310
Beltrán-Saavedra LF (2015) Health assessment of free-ranging vicuna of the National Integrated Management Natural Area Apolobamba, Bolivia. J Selva Andina Anim Sci 46:1–17
Beveridge I, Ford GE (1982) The trichostrongyloid parasites of sheep in South Australia and their regional distribution. Aust Vet J 59:177–179
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
Beveridge I, Pullman AL, Henzell R, Martin RR (1987) Helminth parasites of feral goats in South Australia. Aust Vet J 64:111–112
Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Maechler M, Bolker BM (2017) Modeling zero-inflated count data with glmmTMB. bioRxiv 1:132753 https://www.biorxiv.org/content/biorxiv/early/2017/05/01/132753.full.pdf
Carmichael I (1999) Internal parasitism in alpacas in southern Australia. In: Hack W, McGregor B, Ponzoni R, Judson G, Carmichael I, Hubbard D (eds) Australian alpaca fibre improving productivity and marketing. Rural Industries Research and Development Corporation, Australia, pp 92–130
Cebra CK, Stang BV (2008) Comparison of methods to detect gastrointestinal parasites in llamas and alpacas. J Vet Med Assoc 232:733–741
Clarke M (2016) Market assessment—new and emerging animal industries. Tranche 1: Mohair, Alpaca and Camel Milk. NSW, Australia 2016. http://www.agrifutures.com.au/publications/ market-assessment-new-and-emerging-animal-industries-tranche-1-mohair-alpaca-and-camel-milk. Accessed 15 Jan 2018
Copland JW (1965) Ostertagia mentulata recorded in New South Wales. Aust Vet J 41:27–27
Denwood MJ, Stear MJ, Matthews L, Reid SW, Toft N, Innocent GT (2005) The distribution of the pathogenic nematode Nematodirus battus in lambs is zero-inflated. Parasitology 135:1225–1235
Dittmer K, Hinkson J, 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
Dwyer C, et al. (2014) Trichostrongylus askivali—a new record for alpacas in New Zealand. Proceedings of the New Zealand Society for Parasitology: 42nd Conference, Wellington
Edwards EE, Garner BC, Williamson LH, Storey BE, Sakamoto K (2016) Pathology of Haemonchus contortus in New World camelids in the southeastern United States: a retrospective review. J Vet Diagn Investig 28:105–109
Flach E (2008) Alpaca and llama nematodes in Britain. Vet Rec 163:128–128
Franz S, Wittek T, Joachim A, Hinney B, Dadak AM (2015) Llamas and alpacas in Europe: endoparasites of the digestive tract and their pharmacotherapeutic control. Vet J 204:255–262
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
Hill F, Death A, Wyeth T (1993) Nematode burdens of alpacas sharing grazing with sheep in New Zealand. N Z Vet J 41:205–208
Hilton RJ, Barker IK, Rickard MD (1978) Distribution and pathogenicity during development of Camelostrongylus mentulatus in the abomasum of sheep. Vet Parasitol l4:231–242
Hinkson JA (2015) Investigations into common farm management practices and diseases on alpaca farms in New Zealand. Dissertation, Massey University, Palmerston North, New Zealand
Hyuga A, Matsumoto J (2016) A survey of gastrointestinal parasites of alpacas (Vicugna pacos) raised in Japan. J Vet Med Sci 78:719–721
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
Leguía G (1991) The epidemiology and economic impact of llama parasites. Parasitol Today 7:54–56
Margolis L, Esch GW, Holmes JC, Kuris AM, Schad G (1982) The use of ecological terms in parasitology (report of an ad hoc committee of the American Society of Parasitologists). J Parasitol 68:131–133
Masson M, Gutiérrez G, Puicón V, Zárate D (2016) Helmintiasis y eimeriosis gastrointestinal en alpacas criadas al pastoreo en dos granjas comunales de la región Pasco, Perú, y su relación con el peso y condición corporal. Rev. Investig Vet Perú 27:805–812
Mitchell S, Hopkins B, Corfield C (2016) Nematodirus lamae identified in an alpaca in the UK. Vet Rec 178:271–272
Moreno PG, Eberhardt MAT, Lamattina D, Previtali MA, Beldomenico PM (2013) Intra-phylum and inter-phyla associations among gastrointestinal parasites in two wild mammal species. Parasitol Res 112:3295–3304
Nodtvedt A, Dohoo I, Sanchez J, Conboy G, DesCoteaux L, Keefe G, Leslie K, Campbell J (2002) The use of negative binomial modelling in a longitudinal study of gastrointestinal parasite burdens in Canadian dairy cows. Can J Vet Res 66:249–257
Presidente PJA (2007) Alpaca parasites and their control: recent experiences. Australian Alpaca Veterinarians Annual Conference, Australia, pp 1–14
R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Rashid MH, Stevenson MA, Waenga S, Mirams G, Campbell AJ, Vaughan JL, Jabbar A (2018a) Comparison of McMaster and FECPAKG2 methods for counting nematode eggs in the faeces of alpacas. Parasit Vectors 11:278
Rashid MH, Gebrekidan H, Jabbar A (2018b) Multiplexed-tandem PCR (MT–PCR) assay to detect and differentiate gastrointestinal nematodes of alpacas. Parasit Vectors 11:370
Rashid MH, Vaughan JL, Stevenson MA, Saeed MA, Campbell AJD, Beveridge I, Jabbar A (2018c) Anthelmintic resistance in gastrointestinal nematodes of alpacas (Vicugna pacos) in Australia. Parasit Vectors 11:388
Rashid MH, Vaughan JL, Saeed MA, Stevenson MA, Indjein L, Campbell AJD, Beveridge I, (2019a) Epidemiology of gastrointestinal nematodes of alpacas in Australia: I. Cross sectional studies. Parasitol Res. https://doi.org/10.1007/s00436-019-06235-8
Rashid MH, Stevenson MA, Campbell AJD, Vaughan JL, Beveridge I, Jabbar A (2019b) An assessment of worm control practices used by alpaca farmers in Australia. Vet Parasitol 265:91–100
Rashid MH, Vaughan JL, Beveridge I, Jabbar A (2019c) Worm burdens and associated histopathological changes caused by gastrointestinal nematodes in alpacas from Australia. Parasitol Res. https://doi.org/10.1007/s00436-019-06237-6
Rickard LG (1993) Parasitic gastritis in a llama (Lama glama) associated with inhibited larval Teladorsagia spp.(Nematoda: Trichostrongyloidea). Vet Parasitol 45:331–335
Robayo CIS (2015) Prevalencia de parásitos gastrointestinales en alpacas del Inga Alto, Pichincha. Universidad San Francisco de Quito, Ecuador.
Roeber F, Jex AR, Campbell AJ, Campbell BE, Anderson GA, Gasser RB (2011) Evaluation and application of a molecular method to assess the composition of strongylid nematode populations in sheep with naturally acquired infections. Infect Genet Evol 11:849–854
Roeber F, Jex AR, Gasser RB (2013a) Comparative evaluation of two DNA isolation techniques for PCR-based diagnosis of gastrointestinal nematode infections in sheep. Mol Cell Probes 27:153–157
Roeber F, Jex AR, Gasser RB (2013b) Impact of gastrointestinal parasitic nematodes of sheep, and the role of advanced molecular tools for exploring epidemiology and drug resistance—an Australian perspective. Parasit Vectors 6:153
Rogers WP (1939) Nematode parasites of sheep in Western Australia. J Helminthol 17:151–158
Saeed MA, Rashid MH, Vaughan J, Jabbar A (2018) Sarcocystosis in South American camelids: the state of play revisited. Parasit Vectors 11:146
Tait S, Kirwan J, Fair C, Coles G, Stafford K (2002) Parasites and their control in South American camelids in the United Kingdom. Vet Rec 150:637–638
Welchman DB, Parr J, Wood R, Mead A, Starnes A (2008) Alpaca and llama nematodes in Britain. Vet Rec 162:832–832
Windsor RS, Teran M, Windsor RH (1992a) Effects of parasitic infestation on the productivity of alpacas (Lama pacos). Trop Anim Health Prod 24:57–62
Windsor RS, Windsor RH, Teran M (1992b) Economic benefits of controlling internal and external parasites in South American camelids. Ann N Y Acad Sci 653:398–405
Acknowledgments
We are grateful to alpaca farmers across Australia who provided faecal samples for this study.
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.
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The use of alpacas in this study was approved by the Animal Ethics Committee (AEC no. 1413412.1) of the University of Melbourne.
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Rashid, M.H., Stevenson, M.A., Vaughan, J.L. et al. Epidemiology of gastrointestinal nematodes of alpacas in Australia: II. A longitudinal study. Parasitol Res 118, 901–911 (2019). https://doi.org/10.1007/s00436-019-06236-7
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DOI: https://doi.org/10.1007/s00436-019-06236-7