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Spirocerca vulpis sp. nov. (Spiruridae: Spirocercidae): description of a new nematode species of the red fox, Vulpes vulpes (Carnivora: Canidae)

Published online by Cambridge University Press:  21 May 2018

Alicia Rojas ,
Gloria Sanchis-Monsonís ,
Amer Alić ,
Adnan Hodžić ,
Domenico Otranto ,
Daniel Yasur-Landau ,
Carlos Martínez-Carrasco  and
Gad Baneth Open the ORCID record for Gad Baneth [Opens in a new window]
Alicia Rojas
Affiliation:
Koret School of Veterinary Medicine, The Hebrew University of Jerusalem, Rehovot, Israel
Gloria Sanchis-Monsonís
Affiliation:
Department of Animal Health, Regional Campus of International Excellence ‘Campus Mare Nostrum’, University of Murcia, Murcia, Spain
Amer Alić
Affiliation:
Department of Pathology, Veterinary Faculty, University of Sarajevo, Sarajevo, Bosnia and Herzegovina
Adnan Hodžić
Affiliation:
Department of Pathobiology, Institute of Parasitology, University of Veterinary Medicine Vienna, Vienna, Austria
Domenico Otranto
Affiliation:
Department of Veterinary Medicine, University of Bari, Valenzano, Italy
Daniel Yasur-Landau
Affiliation:
Division of Parasitology, Kimron Veterinary Institute, Bet Dagan, Israel
Carlos Martínez-Carrasco
Affiliation:
Department of Animal Health, Regional Campus of International Excellence ‘Campus Mare Nostrum’, University of Murcia, Murcia, Spain
Gad Baneth*
Affiliation:
Koret School of Veterinary Medicine, The Hebrew University of Jerusalem, Rehovot, Israel
*
Author for correspondence: Gad Baneth, E-mail: [email protected]
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Abstract

Previous studies have reported nematodes of the Spirocercidae family in the stomach nodules of red foxes (Vulpes vulpes) described as Spirocerca sp. or Spirocerca lupi (Rudolphi, 1819). We characterized spirurid worms collected from red foxes and compared them to S. lupi from domestic dogs by morphometric and phylogenetic analyses. Nematodes from red foxes differed from S. lupi by the presence of six triangular teeth-like buccal capsule structures, which are absent in the latter. Additionally, in female worms from red foxes, the distance of the vulva opening to the anterior end and the ratio of the glandular-to-muscular oesophagus lengths were larger than those of S. lupi (P < 0.006). In males, the lengths of the whole oesophagus and glandular part, the ratio of the glandular-to-muscular oesophagus and the comparison of the oesophagus to the total body length were smaller in S. lupi (all P < 0.044). Phylogenetic analyses revealed that S. lupi and the red foxes spirurid represent monophyletic sister groups with pairwise nucleotide distances of 9.2 and 0.2% in the cytochrome oxidase 1 and 18S genes, respectively. Based on these comparisons, the nematodes from red foxes were considered to belong to a separate species, for which the name Spirocerca vulpis sp. nov. is proposed.

Keywords

Cytochrome oxidase subunit 1red foxSpirocerca lupiSpirocerca vulpisspirocercosis18S rRNA
Type
Research Article
Information
Parasitology , Volume 145 , Issue 14 , December 2018 , pp. 1917 - 1928
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Copyright
Copyright © Cambridge University Press 2018 

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References

Alexander, AB et al. (2016) Gastrointestinal parasites of captive and free-living lemurs and domestic carnivores in Eastern Madagascar. Journal of Zoo and Wildlife Medicine 47, 141–149.Google Scholar
Al-Sabi, MN et al. (2014) Genetically distinct isolates of Spirocerca sp. from a naturally infected red fox (Vulpes vulpes) from Denmark. Veterinary Parasitology 205, 389–396.Google Scholar
Allen, JE and Maizels, RM (2011) Diversity and dialogue in immunity to helminths. Nature Reviews Immunology 11, 375–388.Google Scholar
Anderson, et al. (2009) Keys to the Nematode Parasites of Vertebrates: Archival Volume. Wallingford: CABI.Google Scholar
Blancou, J and Albignac, R (1976) Infestation of Malagasy lemurs by Spirocerca lupi (Rudolphi, 1809) Revue d'élevage et de médecine vétérinaire des pays tropicaux 29, 127–130.Google Scholar
Blaxter, ML et al. (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392, 71–75.Google Scholar
Blouin, MS (2002) Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. International Journal of Parasitology 32, 527–531.Google Scholar
Blouin, MS et al. (1998) Substitution bias, rapid saturation, and the use of mtDNA for nematode systematics. Molecular Biology and Evolution 15, 1719–1727.Google Scholar
Blume, GR et al. (2014) Spirocerca lupi granulomatous pneumonia in two free-ranging maned wolves (Chrysocyon brachyurus) from central Brazil. Journal of Veterinary Diagnostic Investigation 26, 815–817.Google Scholar
Casiraghi, M et al. (2001) A phylogenetic analysis of filarial nematodes: comparison with the phylogeny of Wolbachia endosymbionts. Parasitology 122, 93–103.Google Scholar
Chabaud, AG (1959) Sur la systematique des nematodes proches de Spirocerca lupi. Parassitologia 1, 129–135.Google Scholar
Clark, WC (1981) Cylicospirura advena n. sp. (Nematoda, Spirocercidae) a stomach parasite from a cat in New Zealand, with observations on related species. Systematic Parasitology 3, 185–191.Google Scholar
Clement, M, Posada, D and Crandall, KA (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.Google Scholar
Dayrat, B (2005) Towards integrative taxonomy. Biological Journal of the Linnean Society 85, 407–415.Google Scholar
Diakou, A et al. (2012) First report of Spirocerca lupi infection in red fox Vulpes vulpes in Greece. Wildlife Biology 18, 333–336.Google Scholar
Dvir, E, Clift, SJ and Williams, MC (2010) Proposed histological progression of the Spirocerca lupi-induced oesophageal lesion in dogs. Veterinary Parasitology 168, 71–77.Google Scholar
Ferrantelli, V et al. (2010) Spirocerca lupi isolated from gastric lesions in foxes (Vulpes vulpes) in Sicily (Italy). Polish Journal of Veterinary Sciences 13, 465–471.Google Scholar
Ferri, E et al. (2009) Integrated taxonomy: traditional approach and DNA barcoding for the identification of filarioid worms and related parasites (Nematoda). Frontiers in Zoology 6, 1.Google Scholar
Floyd, RM et al. (2005) Nematode-specific PCR primers for the 18S small subunit rRNA gene. Molecular Ecology Notes, 5, 611–612.Google Scholar
Goyanes Alvarez, J (1937) Spirocerca sanguinolenta (Rudolphi, 1819) chez les chiens de Madrid (note préliminaire). Annales de Parasitologie Humaine et Comparée 15, 1–8.Google Scholar
Huelsenbeck, JP and Ronquist, F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics (Oxford, England) 17, 754–755.Google Scholar
Huyse, T, Poulin, R and Théron, A (2005) Speciation in parasites: a population genetics approach. Trends in Parasitology 21, 469–475.Google Scholar
Janssen, T et al. (2017) Molecular characterization and species delimiting of plant-parasitic nematodes of the genus Pratylenchus from the penetrans group (Nematoda: Pratylenchidae). Molecular Phylogenetics and Evolution 117, 30–48.Google Scholar
Kearse, M et al. (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics (Oxford, England) 28, 1647–1649.Google Scholar
Kiontke, K et al. (2007) Trends, stasis, and drift in the evolution of nematode vulva development. Current Biology 17, 1925–1937.Google Scholar
Liu, GH et al. (2013) Characterization of the complete mitochondrial genome of Spirocerca lupi: sequence, gene organization and phylogenetic implications. Parasites & Vectors 6, 45.Google Scholar
Magi, M et al. (2015) Extraintestinal nematodes of the red fox Vulpes vulpes in north-west Italy. Journal of Helminthology 89, 506–511.Google Scholar
Mazaki-Tovi, M et al. (2002) Canine spirocercosis: clinical, diagnostic, pathologic, and epidemiologic characteristics. Veterinary Parasitology 107, 235–250.Google Scholar
Meshgi, B et al. (2009) Prevalence of parasitic infections in the red fox (Vulpes vulpes) and golden Jackal (Canis aureus) in Iran. Iranian Journal of Veterinary Research 10, 387–391.Google Scholar
Morandi, F et al. (2014) Fatal spirocercosis in a free-ranging red fox. Veterinary Records 174, 228.Google Scholar
Murray, M (1968) Incidence and pathology of Spirocerca lupi in Kenya. Journal of Comparative Pathology 78, 401–405.Google Scholar
Naem, S (2004) Scanning electron microscopic observations on adult Spirocerca lupi (Nematoda: Spirurida, Thelaziidae). Parasitology Research 92, 265–269.Google Scholar
Palomares-Rius, JE et al. (2017) The utility of mtDNA and rDNA for barcoding and phylogeny of plant-parasitic nematodes from Longidoridae (Nematoda, Enoplea). Scientific Reports 7, 10905.Google Scholar
Pence, DB and Stone, JE (1978) Visceral lesions in wild carnivores naturally infected with Spirocerca lupi. Veterinary Pathology 15, 322–331.Google Scholar
Powers, TO et al. (2010) Morphological and molecular characterization of Discocriconemella inarata, an endemic nematode from North American native tallgrass prairies. Journal of Nematology 42, 35–45.Google Scholar
Pérez-Ponce de León, G and Nadler, SA (2010) What we don't recognize can hurt us: a plea for awareness about cryptic species. Journal of Parasitology 96, 453–464.Google Scholar
Railliet, A and Henry, A (1911) Helminthes du Porc recueillis par M. Bauche en Annam. Bulletin de la Societe de Pathologie Exotique 4, 693–699.Google Scholar
Rinas, MA et al. (2009) Fatal aortic aneurysm and rupture in a neotropical bush dog (Speothos venaticus) caused by Spirocerca lupi. Veterinary Parasitology 164, 347–349.Google Scholar
Rojas, A et al. (2017a) Detection and quantification of Spirocerca lupi by HRM qPCR in fecal samples from dogs with spirocercosis. Parasites & Vectors 10, 435.Google Scholar
Rojas, A et al. (2017b) Influence of physical and chemical factors on the embryonation, hatching and infectivity of Spirocerca lupi. Veterinary Parasitology 242, 71–78.Google Scholar
Rothmann, W and de Waal, PJ (2017) Diversity of Spirocerca lupi in domestic dogs and black-backed jackals (Canis mesomelas) from South Africa. Veterinary Parasitology 244, 59–63.Google Scholar
Rózsa, L, Tryjanowski, P and Vas, Z (2015) Under the changing climate: how shifting geographic distributions and sexual selection shape parasite diversification. In Morand, S, Krasnov, B and Littlewood, DTJ (eds), Parasite Diversity and Diversification: Evolutionary Ecology Meets Phylogenetics. United Kingdom: Cambridge University Press, pp. 58–76.Google Scholar
Rudolphi, C. A. (1819) Entozoorum Synopsis. Berolini: Sumtibus A. Rücker.Google Scholar
Sanchis-Monsonís, G (2015) Parasitofauna del zorro (Vulpes vulpes) en la Comunidad Valenciana. In Facultad de Veterinaria. Murcia, Spain: Universidad de Murcia, p. 269.Google Scholar
Schneider, CA, Rasband, WS and Eliceiri, KW (2012) NIH image to ImageJ: 25 years of image analysis. Nature Methods 9, 671–675.Google Scholar
Segovia, J et al. (2001) Morphological and morphometric study of Spirocerca lupi. Helminthologia 38, 115–121.Google Scholar
Song, H et al. (2008) Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proceedings of the National Academy of Sciences of the USA 105, 13486–13491.Google Scholar
Spindler, LA (1933) Proceedings of the Helminthological Society of Washington one hundred fifty-second meeting. Journal of Parasitology 20, 62–79.Google Scholar
Stewart, TB and Dean, D (1971) Didelphonema longispiculata (Hill, 1939) Wolfgang, 1953 (Nematoda: Spiruroidea) and other helminths from the opossum (Didelphis marsupialis virginiana) in Georgia. Journal of Parasitology 57, 687–688.Google Scholar
Tamura, K et al. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.Google Scholar
van der Merwe, LL et al. (2008) Spirocerca lupi infection in the dog: a review. The Veterinary Journal 176, 294–309.Google Scholar
Weinstein, SB and Lafferty, KD (2015) How do humans affect wildlife nematodes? Trends in Parasitology 31, 222–227.Google Scholar
Wright, I, Stafford, K and Coles, G (2016) The prevalence of intestinal nematodes in cats and dogs from Lancashire, north-west England. Journal of Small Animal Practice 57, 393–395.Google Scholar
Ye, J et al. (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13, 134.Google Scholar
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