Abstract
Punjab urial (Ovis vignei punjabiensis) is a wild sheep of Pakistan, considered a vulnerable species by IUCN. Major threats to urial populations include habitat loss and poaching, causing severe declines in its population. Nematode infections may also compromise urial survival, but little is known about Punjab urial gastrointestinal nematodes. In this study, a novel DNA barcoding approach was developed using ITS-I as a target region, with a primer pair designed to amplify frequently reported nematode species for small ruminants. The novel primer pair was validated in silico and in vitro and subsequently used to determine the presence of nematodes in Punjab urial samples from Kala Bagh Game Reserve, District Mianwali (Pakistan). DNA barcoding revealed a higher prevalence of Haemonchus contortus (73.91%), Trichuris ovis (16.30%) and Trichostrongylus axei (3.26%) in Punjab urial. This study demonstrates that the novel DNA barcoding approach is a robust tool to detect nematode parasites from faecal samples of Punjab urial. This method can be used to detect nematode infections in wild and domestic hosts for surveillance and population conservation.
References
Albon S, Stien A, Irvine R, Langvatn R, Ropstad E, Halvorsen O (2002) The role of parasites in the dynamics of a reindeer population. Proc R Soc Lond B Biol Sci 269:1625–1632
Asif M, Azeem S, Asif S, Nazir S (2008) Prevalence of gastrointestinal parasites of sheep and goats in and around Rawalpindi and Islamabad. Pak J Vet Anim Sci 1:14–17
Awan G, Ahmad T, Festa-Bianchet M (2005) Disease spectrum and mortality of Punjab urial (Ovis vignei punjabiensis) in Kalabagh Game Reserve. Pak J Zool 37:175
Awan GA, Festa-Bianchet M, Ahmad T (2006) Poaching, recruitment and conservation of Punjab urial Ovis vignei punjabiensis. Wildl Biol 12:443–449
Bell AS, Ranford-Cartwright LC (2002) Real-time quantitative PCR in parasitology. Trends Parasitol 18:338–342
Bibi R et al (2017) Phenotyping and prevalence of Haemonchus contortus (Nematoda: Trichostongylidae) in ruminants from endemic areas of Pakistan: influence of host species and geographical area on phenotypic traits of worms. Pak Vet J 37
Charlier J, Höglund J, von Samson-Himmelstjerna G, Dorny P, Vercruysse J (2009) Gastrointestinal nematode infections in adult dairy cattle: impact on production diagnosis and control. Vet Parasitol 164:70–79
Dhollander S, Belsham GJ, Lange M, Willgert K, Alexandrov T, Chondrokouki E, Depner K, Khomenko S, Özyörük F, Salman M, Thulke HH, Bøtner A (2016) Assessing the potential spread and maintenance of foot-and-mouth disease virus infection in wild ungulates: general principles and application to a specific scenario in Thrace. Transbound Emerg Dis 63:165–174
Ficetola GF, Coissac E, Zundel S, Riaz T, Shehzad W, Bessière J, Taberlet P, Pompanon F (2010) An in silico approach for the evaluation of DNA barcodes. BMC Genomics 11:434. https://doi.org/10.1186/1471-2164-11-434
Gatongi P, Prichard R, Ranjan S, Gathuma J, Munyua W, Cheruiyot H, Scott M (1998) Hypobiosis of Haemonchus contortus in natural infections of sheep and goats in a semi-arid area of Kenya. Vet Parasitol 77:49–61
Gortazar C, Diez-Delgado I, Barasona JA, Vicente J, De La Fuente J, Boadella M (2015) The wild side of disease control at the wildlife-livestock-human interface: a review. Front Vet Sci 1. https://doi.org/10.3389/fvets.2014.00027
Gross JE, Singer FJ, Moses ME (2000) Effects of disease, dispersal and area on bighorn sheep restoration. Restor Ecol 8:25–37
Hudson PJ (1986) The effect of a parasitic nematode on the breeding production of red grouse. J Anim Ecol 55:85–92
Ito TY, Lhagvasuren B, Tsunekawa A, Shinoda M, Takatsuki S, Buuveibaatar B, Chimeddorj B (2013) Fragmentation of the habitat of wild ungulates by anthropogenic barriers in Mongolia. PLoS One 8:e56995. https://doi.org/10.1371/journal.pone.0056995
Khan W, Ahmed M, Yaqub A, Ali H, Arshad M (2015) Distribution and population status of Punjab Usrial, Ovis vignei punjabiensis (mammalia: Bovidae), in soan valley, salt range, Punjab. Pak J Anim Plant Sci 25:851–859
McCallum H, Dobson A (1995) Detecting disease and parasite threats to endangered species and ecosystems. Trends Ecol Evol 10:190–194. https://doi.org/10.1016/S0169-5347(00)89050-3
Önder Z, Yildirim A, Incİ A, Düzlü Ö, Çİloğlu A (2016) Molecular prevalence, phylogenetic characterization and benzimidazole resistance of Haemonchus contortus from sheep. Kafkas Univ Vet Fak Derg 22:93–99
Pandey V, Ndao M, Kumar V (1994) Seasonal prevalence of gastrointestinal nematodes in communal land goats from the highveld of Zimbabwe. Vet Parasitol 51:241–248
Pinol J, Senar MA, Symondson WOC (2018) The choice of universal primers and the characteristics of the species mixture determine when DNA metabarcoding can be quantitative. Mol Ecol 28:407–419. https://doi.org/10.1111/mec.14776
Qasim HM, Avais M, Durrani AZ, Khan MA, Shahzad AH (2016) Dynamic dispersal of Haemonchosis, its treatment and effect on blood profile of small ruminants of Lodhran District, Punjab, Pakistan. Pak J Zool 48:755–761
Raza MA, Younas M, Schlecht E (2014) Prevalence of gastrointestinal helminths in pastoral sheep and goat flocks in the cholistan desert of Pakistan. J Anim Plant Sci 24:127–134
Rizwan HM, Sajid MS, Iqbal Z, Saqib M (2017) Point prevalence of gastrointestinal parasites of domestic sheep (Ovis aries) in district Sialkot, Punjab, Pakistan. J Anim Plant Sci 27:803–808
Shahzad S et al (2015) Comparative hemato-biochemical study on theileriosis in naturally infected Punjab urial (Ovis vignei punjabiensis) and domestic sheep (Ovis aries) in Pakistan. J Anim Plant Sci 25:472–476
Sim KA, Hoar B, Kutz SJ, Chilton NB (2010) Amplification of the second internal transcribed spacer ribosomal DNA of individual trichostrongylid nematode larvae by nested polymerase chain reaction. J Vet Diagn Investig 22:433–437
Tan TK, Panchadcharam C, Low VL, Lee SC, Ngui R, Sharma RS, Lim YA (2014) Co-infection of Haemonchus contortus and Trichostrongylus spp. among livestock in Malaysia as revealed by amplification and sequencing of the internal transcribed spacer II DNA region. BMC Vet Res 10:38
Valdez R (2008) Ovis orientalis. The IUCN Red List of Threatened Species 2008:e.T15739A5076068. https://doi.org/10.2305/IUCN.UK.2008.RLTS.T15739A5076068.en
von Samson-Himmelstjerna G, Harder A, Schnieder T (2002) Quantitative analysis of ITS2 sequences in trichostrongyle parasites. Int J Parasitol 32:1529–1535
Walker JG, Morgan ER (2014) Generalists at the interface: nematode transmission between wild and domestic ungulates. Int J Parasitol Parasites Wildl 3:242–250. https://doi.org/10.1016/j.ijppaw.2014.08.001
Zapata Salas R, Velásquez Vélez R, Herrera Ospina LV, Ríos Osorio L, Polanco Echeverry DN (2016) Prevalence of gastrointestinal nematodes in sheep and goat production systems under confinement, semi-confinement and grazing in municipalities of Antioquia, Colombia. Revista de Investigaciones Veterinarias del Perú (RIVEP) 27:344–354. https://doi.org/10.15381/rivep.v27i2.11647
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Bajwa, A.A., Cuff, J.P., Imran, M. et al. Assessment of nematodes in Punjab Urial (Ovis vignei punjabiensis) population in Kalabagh Game Reserve: development of a DNA barcode approach. Eur J Wildl Res 65, 63 (2019). https://doi.org/10.1007/s10344-019-1298-y
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DOI: https://doi.org/10.1007/s10344-019-1298-y