Parasitology Research

, Volume 111, Issue 5, pp 1907–1912 | Cite as

Tunga penetrans and further parasites in the giant anteater (Myrmecophaga tridactyla) from Minas Gerais, Brazil

  • Raphael Frank
  • Christian Melaun
  • Maria Marlene Martins
  • André Luiz Quagliatto Santos
  • Jörg Heukelbach
  • Sven Klimpel
Original Paper

Abstract

The Brazilian savannah-like area, the Cerrado region, covers large areas of the country and provides a habitat for a multitude of different animal species. The giant anteater (Myrmecophaga tridactyla) is geographically widespread and one of the typical inhabitants of the Cerrado. They are listed as vulnerable by the International Union for Conservation of Nature and Natural Resources. A population loss of at least 30 % over the past 10 years has been estimated based on local extinctions, habitat loss and deaths caused by fires, roadkills and hunting. Little is known about ecological and in particular parasitic conditions of this highly specialised insectivore species. During September and November 2010 we examined three roadkilled giant anteater for the presence of metazoan ecto- and endoparasites. Besides the cestode species Oochoristica tetragonocephala and the tick species Amblyomma nodosum, we found for the first time the flea Tunga penetrans. Beside morphological flea species identification, we compared a fragment of the 16S rRNA gene of eggs, a molecular method utilised for the first time in this combination. The identification of T. penetrans in M. tridactyla represents a new host record and expands the host and distribution range of the zoonotic flea species.

References

  1. Bechara GH, Szabo MPJ, Duarte JMB, Matushima ER, Pereira MC, Rechav Y, Keirans JE, Fielden LJ (2000) Ticks associated with wild animals in the Nhecolândia Pantanal. Ann N Y Acad Sci 916:289–297. doi:10.1603/0022-2585-37.6.979 PubMedCrossRefGoogle Scholar
  2. Bechara GH, Szabo MPJ, Almeida Filho WV, Bechara JN, Pereira RJG, Garcia JE, Pereira MC (2002) Ticks associated with armadillo (Euphractus sexcinctus) and anteater (Myrmecophaga tridactyla) of Emas National Park, State of Goias, Brazil. Ann N Y Acad Sci 969:290–293. doi:10.1111/j.1749-6632.2002.tb04394.x PubMedCrossRefGoogle Scholar
  3. Briceno AM, Chiachio N, Lugo G, Rodríguez C, García F, Mayoral CT, Valenti MR (2009) Miositis parasitaria asociada a la infestación por Trichinella en Myrmecophaga Trydactila: registro de un caso en Venezuela. Neotrop Helminthol 3:111–114Google Scholar
  4. Coke RL, Carpenter JW, Aboellail T, Armbrust L, Isaza R (2002) Dilated cardiomyopathy and amebic gastritis in a Giant Anteater (Myrmecophaga tridactyla). J Zoo Wildl Med 33:272–279PubMedGoogle Scholar
  5. Costa LP, Leite YLR, Mendes SL, Ditchfield AD (2005) Mammal conservation in Brazil. Conserv Biol 19:672–679. doi:10.1111/j.1523-1739.2005.00666.x CrossRefGoogle Scholar
  6. da Fonseca F (1954) Notas de Acarologia XXXVI Aquisicoes novas para a fauna brasileira de Acaros hematophagos (Acari, Macronyssidae). Rev Brasil Ent 1:79–92Google Scholar
  7. Da Silva JMC, Bates JM (2002) Biogeographic patterns and conservation in the South American Cerrado: a tropical Savanna hotspot. Bioscience 52:225–234. doi:10.1641/0006-3568(2002)052[0225:BPACIT]2.0.CO;2 CrossRefGoogle Scholar
  8. De Avelar DM, Linhares AX, Linardi PM (2012) A new species of Tunga (Siphonaptera: Tungidae) from Brazil with a key to the adult species and neosomes. J Med Entomol 49:23–28. doi:10.1603/ME11111 PubMedCrossRefGoogle Scholar
  9. Diniz LSM, Costa EO, Oliveira PMA (1995) Clinical disorders observed in anteaters (Myrmecophagidae, Edentata) in captivity. Vet Res Commun 19:409–415. doi:10.1007/BF01839320 PubMedCrossRefGoogle Scholar
  10. Gordon RM (1941) The jigger flea. Lancet 2:47–49CrossRefGoogle Scholar
  11. Hall (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp 41:95–98Google Scholar
  12. Hesse P (1899) Die Ausbreitung des Sandflohs in Afrika. Geogr Z 5:522–530Google Scholar
  13. Heukelbach J (2005) Tungiasis. Rev Inst Med Trop S Paulo 47:307–313. doi:10.1590/S0036-46652005000600001 PubMedCrossRefGoogle Scholar
  14. Heukelbach J, Wilcke T, Harms G, Feldmeier H (2005) Seasonal variation of tungiasis in an endemic community. Am J Trop Med Hyg 72:145–149PubMedGoogle Scholar
  15. Hinz E (1996) Zur Verbreitung und Ausbreitung der Gattung Tunga (Siphonaptera: Pulicidae) unter besonderer Berücksichtigung von T. penetrans. Mitt Österr Ges Tropenmed Parasitol 18:173–182Google Scholar
  16. Hughes RC (1940) The genus Oochoristica Luhe 1898. Am Midl Nat 23:368–381CrossRefGoogle Scholar
  17. Jones EK, Clifford CM, Keirans JE, Kohls GM (1972) The ticks of Venezuela (Acarina: Ixodoidea) with a key to the species of Amblyomma in the Western hemisphere. Brigham Young Univ Sci Bull XVII:1–40Google Scholar
  18. Khalil LF, Jones A, Bray RA (1994) Keys to the Cestode parasites of vertebrates. CAB International, WallingfordGoogle Scholar
  19. Klimpel S, Mehlhorn H, Heukelbach J, Feldmeier H, Mencke N (2005) Field trial of the efficacy of a combination of imidacloprid and permethrin against Tunga penetrans (sand flea, jigger fela) in dogs in Brazil. Parasitol Res 97:S113–S120. doi:10.1007/s00436-005-1454-z PubMedCrossRefGoogle Scholar
  20. Klimpel S, Heukelbach J, Pothmann D, Rückert S (2010) Gastrointestinal and ectoparasites from urban stray dogs in Fortaleza (Brazil): high infection risk for humans? Parasitol Res 107:713–719. doi:10.1007/s00436-010-1926-7 PubMedCrossRefGoogle Scholar
  21. Klink CA, Machado RB (2005) Conservation of the Brazilian Cerrado. Conserv Biol 19:707–713. doi:10.1111/j.1523-1739.2005.00702.x CrossRefGoogle Scholar
  22. Labruna MB, Sanfilippo LF, Demetrio C, Menezes AC, Pinter A, Guglielmone AA, Silveira LF (2007) Ticks collected on birds in the state of São Paulo, Brazil. Exp Appl Acarol 43:147–160. doi:10.1007/s10493-007-9106-x PubMedCrossRefGoogle Scholar
  23. Linardi PM, Guimaraes LR (2000) Sifonapteros do Brasil. FAPESP, Sao PauloGoogle Scholar
  24. Luchetti A, Mantovani B, Trentini M (2005a) Rapid identification of non-neosomic Tunga penetrans and Tunga trimamillata (Insecta Siphonaptera) specimens through PCR-RFLP method. B Insectol 58:15–18Google Scholar
  25. Luchetti A, Mantovani B, Pampiglione S, Trentini M (2005b) Molecular characterisation of Tunga trimamillata and T. penetrans (Insecta, Siphonaptera, Tungidae): taxonomy and genetic variability. Parasite 12:123–129PubMedGoogle Scholar
  26. Meggitt FJ (1934) On some tapeworms from the bullsnake (Pityopis sayi), with remarks on the species of the genus Oochoristica (Cestoda). J Parasitol 20:181–189CrossRefGoogle Scholar
  27. Mehlhorn H, Piekarski G (2002) Grundriß der Parasitologie. Spektrum, HeidelbergGoogle Scholar
  28. Mittermeier RA, Myers N, Mittermeier CG (2000) Hotspots: earth’s biologically richest and most endangered terrestrial ecoregions. Conservation International, WashingtonGoogle Scholar
  29. Möcklinghoff L (2011) Der Große Ameisenbär. Dissertation, Zoologische Forschungsmuseum A. Koenig, University BonnGoogle Scholar
  30. Mutlow AG, Dryden MW, Payne PA (2006) Flea (Pulex simulans) infestation in captive Giant Anteaters (Myrmecophaga tridactyla). J Zoo Wildl Med 37:427–429PubMedCrossRefGoogle Scholar
  31. Nagy N, Abari E, D’Haese J, Calheiros CM, Heukelbach J, Mencke N, Feldmeier H, Mehlhorn H (2007) Investigations on the life cycle and morphology of Tunga penetrans in Brazil. Parasitol Res 101:233–242. doi:10.1007/s00436-007-0683-8 CrossRefGoogle Scholar
  32. Nofs S, Abd-Eldaim M, Thomas KV, Toplon D, Rouse D, Kennedy M (2009) Influenza virus A (H1N1) in Giant Anteaters (Myrmecophaga tridactyla). Emerg Infect Dis 15:1081–1083. doi:10.3201/eid1507.081574 PubMedCrossRefGoogle Scholar
  33. Oliver JH (1989) Biology and systematics of ticks (Acari: Ixodida). Annu Rev Ecol Syst 20:397–430CrossRefGoogle Scholar
  34. Pampiglione S, Trentini M, Fioravanti ML, Onore G, Rivasi F (2002) A new species of Tunga (Insecta, Siphonaptera) from Ecuador. Parassitologia 44:127Google Scholar
  35. Pampiglione S, Fioravanti ML, Gustinelli A, Onore G, Rivasi F, Trentini M (2005) Anatomy of Tunga trimamillata Pampiglione et al., 2002 (Insecta, Siphonaptera, Tungidae) and developmental phases of the gravid female. Parasite 12:241–250PubMedGoogle Scholar
  36. Pampiglione S, Fioravanti ML, Gustinelli A, Onore G, Mantovani B, Luchetti AR, Trentini M (2009) Sand flea (Tunga spp.) infections in humans and domestic animals: state of the arts. Med Vet Entomol 23:172–186. doi:10.1111/j.1365-2915.2009.00807.x PubMedCrossRefGoogle Scholar
  37. Pereira M, Szabo MPJ, Bechara GH, Matushima ER, Duarte JMB, Rechav Y, Fielden L, Keirans JE (2000) Ticks (Acari: Ixodidae) associated with wild animals in the Pantanal region of Brazil. J Med Entomol 37:979–983. doi:10.1603/0022-2585-37.6.979 CrossRefGoogle Scholar
  38. Pinto C, Dreyfus A (1927) Tunga travassosi n. sp. parasita de Tatusia novemcinctus do Brasil. Bol Biol 9:174–178Google Scholar
  39. Redford KH (1985) Feeding and food preference in captive and wild Giant anteaters (Myrmecophaga tridactyla). J Zool 205:559–572. doi:10.1111/j.1469-7998.1985.tb03544.x CrossRefGoogle Scholar
  40. Resh VH, Carde RT (2009) Encyclopedia of insects. Academic, BurlingtonGoogle Scholar
  41. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  42. Shaw JH, Machado-Neto J, Carter TS (1987) Behavior of free-living anteaters (Myrmecophaga tridactyla). Biotropica 19:255–259CrossRefGoogle Scholar
  43. Szabo MPJ, Olegario MMM, Santos ALQ (2007) Tick fauna from two locations in the Brazilian savannah. Exp Appl Acarol 43(1):73–84. doi:10.1007/s10493-007-9096-8 PubMedCrossRefGoogle Scholar
  44. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599. doi:10.1093/molbev/msm092 PubMedCrossRefGoogle Scholar
  45. Wagner J (1932) Tunga bondari, eine neue Art der Sandflöhe. Novit Zool 38:248–249Google Scholar
  46. Widmer C, Azevedo CC (2011) Tungiasis in a free-ranging jaguar (Panthera onca) population in Brazil. Parasitol Res 110:1311–1314. doi:10.1007/s00436-011-2625-8 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Raphael Frank
    • 1
    • 2
    • 3
  • Christian Melaun
    • 1
    • 2
    • 3
  • Maria Marlene Martins
    • 4
  • André Luiz Quagliatto Santos
    • 4
  • Jörg Heukelbach
    • 5
  • Sven Klimpel
    • 1
    • 2
    • 3
  1. 1.Medical Biodiversity and ParasitologyBiodiversity and Climate Research Centre (BiK-F)Frankfurt am MainGermany
  2. 2.Senckenberg Gesellschaft für Naturforschung (SGN)Frankfurt am MainGermany
  3. 3.Institute for Ecology, Evolution and DiversityGoethe University (GO)Frankfurt am MainGermany
  4. 4.Faculdade de Medicina VeterináriaUniversidade Federal de UberlândiaUberlândiaBrazil
  5. 5.Departamento de Saúde Comunitária, Faculdade de MedicinaUniversidade Federal do CearáFortalezaBrazil

Personalised recommendations