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Parasitology Research

, Volume 113, Issue 3, pp 811–821 | Cite as

Muscular sarcocystosis in two arctic foxes (Vulpes lagopus) due to Sarcocystis arctica n. sp.: sarcocyst morphology, molecular characteristics and phylogeny

  • Bjørn GjerdeEmail author
  • Johan Schulze
Original Paper

Abstract

The arctic fox (Vulpes lagopus) is a critically endangered species in Norway, and therefore, the small population is closely monitored, and most foxes found dead are subjected to necropsy. In two deceased foxes, thin-walled muscular sarcocysts were first detected in histological sections, and numerous sarcocysts were later found in frozen and thawed muscle samples from Fox 1. These sarcocysts measured 1–12 × 0.1–0.25 mm and had closely spaced, short, knob-like protrusions, giving the cysts a serrated outline. Genomic DNA was extracted from eight isolated sarcocysts (Fox 1) and two muscle samples (Fox 2) and subjected to polymerase chain reaction amplification at four loci: the nuclear 18S and 28S ribosomal RNA genes and internal transcribed spacer 1 region and the mitochondrial cytochrome c oxidase subunit 1 gene (cox1). Both foxes were infected by the same Sarcocystis sp., which displayed little or no genetic variation at the three nuclear loci (99.9–100 % identity) and slightly more variation at cox1 (99.4–100 % identity). Sequence comparisons and phylogenetic analyses revealed that this species was distinct from other named Sarcocystis spp. but was closely related to various species using avian intermediate hosts and possibly identical to an unnamed species reported from two American dogs. The species described from the two arctic foxes was named Sarcocystis arctica n. sp.

Keywords

Intermediate Host Definitive Host Cox1 Sequence Sarcocystosis Norwegian Veterinary Institute 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

This study was made possible by the ongoing national monitoring programme for the arctic fox in Norway led by Nina E. Eide, at NINA, Trondheim, and the substantial efforts of Eide and many other persons involved in surveying and collecting material from the Norwegian arctic fox population.

Supplementary material

436_2013_3711_MOESM1_ESM.pdf (141 kb)
ESM 1 (PDF 141 kb)

References

  1. Barta JR, Martin DS, Liberator PA, Dashkevicz M, Anderson JW, Feighner SD, Elbrecht A, Perkins-Barrow A, Jenkins MC, Danforth HD, Ruff MD, Profous-Juchelka H (1997) Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. J Parasitol 83:262–271Google Scholar
  2. Chapman J, Mense M, Dubey JP (2005) Clinical muscular sarcocystosis in a dog. J Parasitol 91:187–190. doi: 10.1645/GE-406R PubMedCrossRefGoogle Scholar
  3. Dahlgren SS, Gjerde B (2007) Genetic characterisation of six Sarcocystis species from reindeer (Rangifer tarandus tarandus) in Norway based on the small subunit rRNA gene. Vet Parasitol 146:204–213. doi: 10.1016/j.vetpar.2007.02.023 PubMedCrossRefGoogle Scholar
  4. Dahlgren SS, Gjerde B (2010) Molecular characterization of five Sarcocystis species in red deer (Cervus elaphus), including Sarcocystis hjorti n. sp., reveals that these species are not intermediate host specific. Parasitology 137:815–840. doi: 10.1017/S0031182009991569 PubMedCrossRefGoogle Scholar
  5. Dubey JP, Chapman JL, Rosenthal BM, Mense M, Schueler RL (2006) Clinical Sarcocystis neurona, Sarcocystis canis, Toxoplasma gondii, and Neospora caninum infections in dogs. Vet Parasitol 137:36–49. doi: 10.1016/j.vetpar.2005.12.017 PubMedCrossRefGoogle Scholar
  6. Dubey JP, Reichard MV, Torretti L, Garvon JM, Sundar N, Grigg ME (2010) Two new species of Sarcocystis (Apicomplexa: Sarcocystidae) infecting the wolverine (Gulo gulo) from Nunavut, Canada. J Parasitol 96:972–976. doi: 10.1645/GE-2412.1 PubMedCrossRefGoogle Scholar
  7. Fenger CK, Granstrom DE, Langemeier JL, Stamper S, Donahue JM, Patterson JS, Gajadhar AA, Marteniuk JV, Xiaomin Z, Dubey JP (1995) Identification of opossums (Didelphis virginiana) as the putative definitive host of Sarcocystis neurona. J Parasitol 81:916–919Google Scholar
  8. Fischer S, Odening K (1998) Characterization of bovine Sarcocystis species by analysis of their 18S ribosomal DNA sequences. J Parasitol 84:50–54PubMedCrossRefGoogle Scholar
  9. Flagstad Ø, Eide NE, Ulvund KR, Tovmo M, Andersen R, Landa A (2011). Arctic fox in Norway 2011. Results from the national monitoring program on arctic fox. [In Norwegian but with English abstract.] NINA Report 767. 53 pp. Norwegian Institute for Nature Research (NINA), Trondheim, Norway. http://www.nina.no/archive/nina/PppBasePdf/rapport/2011/767.pdf
  10. Gerhold RW, Howerth EW, Lindsay DS (2005) Sarcocystis neurona-associated meningoencephalitis and description of intramuscular sarcocysts in a fisher (Martes pennanti). J Wildl Dis 41:224–230. doi: 10.7589/0090-3558-41.1.224 PubMedCrossRefGoogle Scholar
  11. Gillis KD, MacKay RJ, Yowell CA, Levy JK, Greiner EC, Dame JB, Cheadle MA, Hernandez J, Massey ET (2003) Naturally occurring Sarcocystis infection in domestic cats (Felis catus). Int J Parasitol 33:877–883. doi: 10.1016/S0020-7519(03)00090-0 PubMedCrossRefGoogle Scholar
  12. Gjerde B (2013a) Characterisation of full-length mitochondrial copies and partial nuclear copies (numts) of the cytochrome b and cytochrome c oxidase subunit I genes of Toxoplasma gondii, Neospora caninum, Hammondia heydorni and Hammondia triffittae (Apicomplexa: Sarcocystidae). Parasitol Res 112:1493–1511. doi: 10.1007/s00436-013-3296-4 PubMedCrossRefGoogle Scholar
  13. Gjerde B (2013b) Phylogenetic relationships among Sarcocystis species in cervids, cattle and sheep inferred from the mitochondrial cytochrome c oxidase subunit I gene. Int J Parasitol 43:579–591. doi: 10.1016/j.ijpara.2013.02.004 PubMedCrossRefGoogle Scholar
  14. Kubo M, Okano T, Ito K, Tsubota T, Sakai H, Yanai T (2009) Muscular sarcocystosis in wild carnivores in Honshu, Japan. Parasitol Res 106:213–219. doi: 10.1007 /s00436-009-1653-0 PubMedCrossRefGoogle Scholar
  15. Kutkienė L, Prakas P, Sruoga A, Butkauskas D (2012) Description of Sarcocystis anasi sp. nov. and Sarcocystis albifronsi sp. nov. in birds of the order Anseriformes. Parasitol Res 110:1043–1046. doi: 10.1007/s00436-011-2588-9 PubMedCrossRefGoogle Scholar
  16. Landa A, Tovmo M, Meås R, Eide NE, Flagstad Ø, Ulvund K, Andersen R (2011) Arctic fox captive breeding programme. Annual report 2011. NINA Report 796. 51 pp. http://www.nina.no/archive/nina/PppBasePdf/rapport/2012/796.pdf
  17. Larkin JL, Gabriel M, Gerhold RW, Yabsley MJ, Wester JC, Humphreys JG, Beckstead R, Dubey JP (2011) Prevalence to Toxoplasma gondii and Sarcocystis spp. in a reintroduced fisher (Martes pennanti) population in Pennsylvania. J Parasitol 97:425–429. doi: 10.1645/GE-2623.1 PubMedCrossRefGoogle Scholar
  18. Mugridge NB, Morrison DA, Johnson AM, Luton K, Dubey JP, Votýpka J, Tenter AM (1999) Phylogenetic relationships of the genus Frenkelia: a review of its history and new knowledge gained from comparison of large subunit ribosomal ribonucleic acid gene sequences. Int J Parasitol 29:957–972PubMedCrossRefGoogle Scholar
  19. Odening K (1998) The present state of species-systematics in Sarcocystis Lankester, 1882 (Protista, Sporozoa, Coccidia). Syst Parasitol 41:209–233CrossRefGoogle Scholar
  20. Olias P, Gruber AD, Hafez HM, Heydorn AO, Mehlhorn H, Lierz M (2010) Sarcocystis calchasi sp. nov. of the domestic pigeon (Columba livia f. domestica) and the Northern goshawk (Accipiter gentilis): light and electron microscopical characteristics. Parasitol Res 106:577–585. doi: 10.1007/s00436-009-1701-9 PubMedCrossRefGoogle Scholar
  21. Olias P, Olias L, Krücken J, Lierz M, Gruber AD (2011) High prevalence of Sarcocystis calchasi sporocysts in European Accipiter hawks. Vet Parasitol 175:230–236. doi: 10.1016/j.vetpar.2010.10.025 PubMedCrossRefGoogle Scholar
  22. Rosenthal BM, Dunams DB, Pritt B (2008) Restricted genetic diversity in the ubiquitous cattle parasite, Sarcocystis cruzi. Infect Genet Evol 8:588–592. doi: 10.1016/j.meegid.2008.04.004 PubMedCrossRefGoogle Scholar
  23. Sykes JE, Dubey JP, Lindsay LL, Prato P, Lappin MR, Guo LT, Mizisin AP, Shelton GD (2011) Severe myositis associated with Sarcocystis spp. infection in 2 dogs. J Vet Intern Med 25:1277–1283. doi: 10.1111/j.1939-1676.2011.00828.x PubMedCrossRefGoogle Scholar
  24. Tamura K (1992) Estimation of the number of nucleotide substitutions when there are strong transition–transversion and G + C-content biases. Mol Biol Evol 9:678–687PubMedGoogle Scholar
  25. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi: 10.1093/molbev/msr121 PubMedCrossRefGoogle Scholar
  26. Vashisht K, Lichtensteiger CA, Miller LA, Gondim LF, McAllister MM (2005) Naturally occurring Sarcocystis neurona-like infection in a dog with myositis. Vet Parasitol 133:19–25PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of Food Safety and Infection BiologyNorwegian School of Veterinary ScienceOsloNorway
  2. 2.Norwegian Veterinary InstituteTrondheimNorway

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