Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-18T17:46:05.857Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular identification of parasitic nematodes (Nematoda: Strongylida) in feces of wild ruminants from Tunisia

Published online by Cambridge University Press:  08 November 2017

Yousra Said Open the ORCID record for Yousra Said [Opens in a new window] ,
Mohamed Gharbi ,
Moez Mhadhbi ,
Moktar Dhibi  and
Samia Lahmar
Yousra Said*
Affiliation:
Faculty of Science of Bizerte, University of Carthage, Jarzouna, Bizerte 7021, Tunisia Parasitology Laboratory, National School of Veterinary Medicine, University of Manouba, Sidi Thabet 2020, Tunisia
Mohamed Gharbi
Affiliation:
Parasitology Laboratory, National School of Veterinary Medicine, University of Manouba, Sidi Thabet 2020, Tunisia
Moez Mhadhbi
Affiliation:
Parasitology Laboratory, National School of Veterinary Medicine, University of Manouba, Sidi Thabet 2020, Tunisia
Moktar Dhibi
Affiliation:
Parasitology Laboratory, National School of Veterinary Medicine, University of Manouba, Sidi Thabet 2020, Tunisia
Samia Lahmar
Affiliation:
Parasitology Laboratory, National School of Veterinary Medicine, University of Manouba, Sidi Thabet 2020, Tunisia
*
Author for correspondence: Yousra Said, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

In Tunisia and other North African countries, there is a lack of knowledge about parasite biodiversity within threatened wild ruminants and there are not any studies on their gastrointestinal nematodes. Thus the aim of this study was to identify gastrointestinal fauna in the faecal samples of Tunisian wild ruminants. A total of 262 faecal samples were collected from domestic sheep and goat, and wild ruminants (Addax, Barbary sheep, Barbary red deer, Dorcas gazelle, Slender-horned gazelle and Scimitar-horned Oryx) living in protected areas. Samples were examined with floatation (saturated sodium chloride solution), polymerase chain reaction and sequencing of the second internal transcribed spacer region of the rDNA. Microscopic analysis allowed the identification of only Nematodirus genus or molecular tools allowed a first identification of five gastrointestinal nematode species in North African wild ruminants: Chabertia ovina (1.6%), Camelostrongylus mentulatus (1.6%), Marshallagia marshalli (4.7%), Nematodirus helvetianus (62.5%) and Nematodirus spathiger (29.7%). This study reported the first records of C. mentulatus and M. marshalli in Addax and of M. marshalli in Dorcas gazelle and it was the first reported record of N. helvetianus and M. marshalli in Tunisia.

Keywords

Biodiversitygastrointestinal nematodesCamelostrongylus mentulatusMarshallagia marshalliNematodirus helvetianuswild ruminantsthreatened speciesTunisiaNorth Africa
Type
Research Article
Information
Parasitology , Volume 145 , Issue 7 , June 2018 , pp. 901 - 911
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albon, SD, Stien, A, Irvine, RJ, Langvatn, R, Ropstad, E and Halvorsen, O (2002) The role of parasites in the dynamics of a reindeer population. Proceedings of the Royal Society of London. Series B, Biological Sciences 269, 1625–1632.CrossRefGoogle ScholarPubMed
Anderson, RC (2000) Nematode Parasites of Vertebrates: Their Development and Transmission. UK: Commonwealth Agricultural Bureau International (CABI Publishing).CrossRefGoogle Scholar
Anonymous (2013) Forêt Tunisienne Habitat pour la Faune et la Flore sauvage. Tunisia: Direction Générale des forêts, Ministère de l'Agriculture.Google Scholar
Arneberg, P, Folstad, I and Karter, AJ (1996) Gastrointestinal nematodes depress food intake in naturally infected reindeer. Parasitology 112(Pt 2), 213–219.CrossRefGoogle ScholarPubMed
Audebert, F, Durette-Desset, MC and Chilton, NB (2000) Internal transcribed spacer rDNA can be used to infer the phylogenetic relationships of species within the genus Nematodirus (Nematoda: molineoidea). International Journal for Parasitology 30, 187–191.CrossRefGoogle ScholarPubMed
Azizi, A (1985) Les strongles gastro-intestinaux de la chèvre : identification et étude épidemiologique dans la region de Ain Draham. DVM thesis, National School of Medecine Veterinary of Sidi Thabet, Tunisia.Google Scholar
Bott, NJ, Campbell, BE, Beveridge, I, Chilton, NB, Rees, D, Hunt, PW and Gasser, RB (2009) A combined microscopic-molecular method for the diagnosis of strongylid infections in sheep. International Journal for Parasitology 39, 1277–1287.CrossRefGoogle ScholarPubMed
Brooker, S (2010) Estimating the global distribution and disease burden of intestinal nematode infections: adding up the numbers – a review. International Journal for Parasitology 40, 1137–1144.CrossRefGoogle ScholarPubMed
Dobson, AP and Hudson, PJ (1986) Parasites, disease and the structure of ecological communities. Trends in Ecology and Evolution 1, 11–15.CrossRefGoogle ScholarPubMed
Dunn, AM (1969) The wild ruminant as reservoir host of helminth infection. Symposia of the Zoological Society of London 24, 221–248.Google Scholar
Flach, EJ and Sewell, MMH (1987) Gastrointestinal nematodiasis in Blackbuck (Antilope cervicapra) at Edinburgh Zoo. Journal of Zoo and Wildlife Medicine 18, 56–61.CrossRefGoogle Scholar
Fukumoto, S, Uchida, T, Ohbayashi, M, Ikebe, Y and Sasano, S (1996) A new host record of Camelostrongylus mentulatus (Nematoda; Trichostrongyloidea) from abomasum of a giraffe at a zoo in Japan. Journal of Veterinary Medical Science 58, 1223–1225.CrossRefGoogle Scholar
Gasser, R, Nansen, P and Guldberg, P (1996) Fingerprinting sequence variation in ribosomal DNA of parasites by DGGE. Molecular and Cellular Probes 10, 99–105.CrossRefGoogle ScholarPubMed
Gharaibeh, BM (1997) Systematics, distribution, and zoogeography of mammals of Tunisia. PhD theses, Faculty of Texas Tech University, Lubbock, Texas, USA.Google Scholar
Gilbert, T and Woodfine, T (2008) The Reintroduction of Scimitar-Horned Oryx Oryx Dammah to Dghoumes National Park, Tunisia, Report to Members of the European Endangered Species Programme for Scimitar-Horned Oryx. Winchester: Marwell Preservation Trust.Google Scholar
Goossens, E, Dorny, P, Boomker, J, Vercammen, F and Vercruysse, J (2005) A 12-month survey of the gastro-intestinal helminthes of antelopes, gazelles, and giraffids kept at two zoos in Belgium. Veterinary Parasitology 127, 303–312.CrossRefGoogle ScholarPubMed
Hajji, GM, Zachos, FE, Charfi-Cheikrouha, F and Hartl, GB (2007) Conservation genetics of the imperilled Barbary red deer in Tunisia. Animal Conservation 10, 229–235.CrossRefGoogle Scholar
Heise, M, Epe, C and Schnieder, T (1999) Differences in the second internal transcribed spacer (ITS-2) of eight species of gastrointestinal nematodes of ruminants. Journal of Parasitology 85, 431–435.CrossRefGoogle ScholarPubMed
Hmidi, A (1982) Contribution a l'etude des strongyloses digestives du moutons: caracteres epidemiologiques dans la region de Sousse. DVM thesis, National School of Medecine Veterinary of Sidi Thabet, Tunisia.Google Scholar
Hoberg, EP, Monsen, KJ, Kutz, S and Blouin, MS (1999) Structure, biodiversity, and historical biogeography of nematode faunas in holarctic ruminants: morphological and molecular diagnoses for Teladorsagia boreoarcticus n. sp. (Nematoda: Ostertagiinae), a dimorphic cryptic species in muskoxen (Ovibos moschatu) Journal of Parasitology 85, 910–934.CrossRefGoogle Scholar
Hughes, J, Albon, SD, Irvine, RJ and Woodin, S (2009) Is there a cost of parasites to caribou? Parasitology 136, 253–265.CrossRefGoogle Scholar
Kimura, M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.CrossRefGoogle ScholarPubMed
Lichtenfels, JR and Hoberg, EP (1993) The systematics of nematodes that cause ostertagiasis in domestic and wild ruminants in North America: an update and a key to species. Veterinary Parasitology 46, 33–53.CrossRefGoogle Scholar
Lovari, S, Lorenzini, R, Masseti, M, Pereladova, O, Carden, RF and Brook, SM (2016) Cervus elaphus. The IUCN Red List of Threatened Species 2016: e.T55997072A22155320. http://dx.doi.org/10.2305/IUCN.UK.2016-2.RLTS.T55997072A22155320.en.CrossRefGoogle Scholar
Lyles, AM and Dobson, AP (1993) Infectious disease and intensive management: population dynamics, threatened hosts, and their parasites. Journal of Zoo and Wildlife Medicine 24, 315–326.Google Scholar
Mabrouk, T (1988) Contribution à l’étude des helminthes gastro-intestinaux du dromadaire en Tunisie. DVM thesis, National School of Medecine Veterinary of Sidi Thabet, Tunisia.Google Scholar
Meradi, S, Bentounsi, B, Zouyed, I and Cabaret, J (2011) The steppe species of gastrointestinal nematodes of small ruminants, with a focus on Marshallagia: climate as a key determinant. Parasite: Journal de la Société Française de Parasitologie 18, 261–269.CrossRefGoogle ScholarPubMed
Mohammed, OB, Omer, SA and Sandouka, MA (2007) The efficacy of ivermectin and levamisole against natural Nematodirus spathiger infection in the Arabian sand gazelle (Gazella subgutturosa marica) and the Arabian mountain gazelle (Gazella gazella) in Saudi Arabia. Veterinary Parasitology 150, 170–173.CrossRefGoogle ScholarPubMed
Morgan, ER, Clare, EL, Jefferies, R and Stevens, JR (2012) Parasite epidemiology in a changing world: can molecular phylogeography help us tell the wood from the trees? Parasitology 139, 1924–1938.CrossRefGoogle Scholar
Nadler, SA, Hoberg, EP, Hudspeth, DS and Rickard, LG (2000) Relationships of Nematodirus species and Nematodirus battus isolates (Nematoda: Trichostrongyloidea) based on nuclear ribosomal DNA sequences. Journal of Parasitology 86, 588–601.CrossRefGoogle ScholarPubMed
Ortiz, J, Ruiz de Ybáñez, R, Abaigar, T, Goyena, M, Garijo, M, Espeso, G and Cano, M (2006) Output of gastrointestinal nematode eggs in the feces of captive gazelles (Gazella dama mhorr, Gazella cuvieri and Gazella dorcas neglecta) in a semiarid region of southeastern Spain. Journal of Zoo and Wildlife Medicine 37, 249–254.CrossRefGoogle Scholar
Pauling, CD, Oller, AR and Jackson, V (2016) Fecal parasite identification by microscopy and PCR in scimitar-horned oryx, Oryx dammah, managed at two sites. International Journal for Parasitology: Parasites and Wildlife 5, 312–320.Google ScholarPubMed
Perry, BD and Randolph, TF (1999) Improving the assessment of the economic impact of parasitic diseases and of their control in production animals. Veterinary Parasitology 84, 145–168.CrossRefGoogle ScholarPubMed
Ruiz de Ybáñez, MR, Garijo, MM, Carpintero, M, Martínez-Carrasco, C and Ortiz, JM (2003) Camelostrongylus mentulatus in domestic goats from the Iberian Peninsula. Journal of Helminthology 77, 371–372.CrossRefGoogle ScholarPubMed
Saitou, N and Nei, M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.Google Scholar
Sharhuu, G and Sharkhuu, T (2004) The helminth fauna of wild and domestic ruminants in Mongolia – a review. European Journal of Wildlife Research 50, 150–156.Google Scholar
Sim, KA, Hoar, B, Kutz, SJ and Chilton, NB (2010) Amplification of the second internal transcribed spacer ribosomal DNA of individual trichostrongylid nematode larvae by nested polymerase chain reaction. Journal of Veterinary Diagnostic Investigation 22, 433–437.CrossRefGoogle ScholarPubMed
Steele, J, Orsel, K, Cuyler, C, Hoberg, EP, Schmidt, NM and Kutz, SJ (2013) Divergent parasite faunas in adjacent populations of west Greenland caribou: natural and anthropogenic influences on diversity. International Journal for Parasitology: Parasites and Wildlife 2, 197–202.Google ScholarPubMed
Stien, A, Irvine, RJ, Ropstad, E, Halvorsen, O, Langvatn, R and Albon, SD (2002) The impact of gastrointestinal nematodes on wild reindeer: experimental and cross-sectional studies. Journal of Animal Ecology 71, 937–945.CrossRefGoogle Scholar
Tamura, K, Stecher, G, Peterson, D, Filipski, A and Kumar, S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.CrossRefGoogle ScholarPubMed
Thienpont, D, Rochette, F and Vanparijs, OF (1979) Diagnosing Helminthiasis Through Coprological Examination, 18th edn. Beerse, Belgium: Janssen Research Foundation.Google Scholar
Thornton, JE, Galvin, TJ, Bell, RR and Ramsey, CW (1973a) Parasites of the blackbuck antelope (Antilope cervicapra) in Texas. Journal of Wildlife Diseases 9, 160–162.CrossRefGoogle ScholarPubMed
Thornton, JE, Galvin, TJ, Bell, RR and Ramsey, CW (1973b) Transmissibility of gastrointestinal nematodes from blackbuck antelope to cattle, sheep, and goats. Journal of the American Veterinary Medical Association 163, 554–555.Google ScholarPubMed
Thumbi, SM, Bronsvoort, BMDC, Poole, EJ, Kiara, H, Toye, P, Ndila, M, Conradie, I, Jennings, A, Handel, IG, Coetzer, J A W, Hanotte, O and Woolhouse, MEJ (2013) Parasite co-infections show synergistic and antagonistic interactions on growth performance of East African zebu cattle under one year. Parasitology 140, 1789–1798.CrossRefGoogle ScholarPubMed
Walker, JG and Morgan, ER (2014) Generalists at the interface: nematode transmission between wild and domestic ungulates. International Journal for Parasitology: Parasites and Wildlife 3, 242–250.Google ScholarPubMed
Woodfine, T, Chetoui, A, Zahzah, K and Gilbert, T (2011) Re-introduction of scimitar-horned oryx to Dghoumes National Park, Tunisia. In Soorae, PS (ed.). Global Re-Introduction Perspectives: 2011, More Case Studies from Around the Globe. IUCN Publication, pp. 190–193.Google Scholar
Supplementary material: File

Said et al supplementary material 1

Supplementary Figure

Download Said et al supplementary material 1(File)
File 111.6 KB