Experimental and Applied Acarology

, Volume 76, Issue 4, pp 537–549 | Cite as

New records of ticks infesting bats in Brazil, with observations on the first nymphal stage of Ornithodoros hasei

  • S. Muñoz-LealEmail author
  • E. Barbier
  • F. A. M. Soares
  • E. Bernard
  • M. B. Labruna
  • F. Dantas-TorresEmail author


In Brazil, at least 14 species of soft ticks (Argasidae) are associated with bats. While Ornithodoros hasei seems to be abundant among foliage-roosting bats, other groups of ticks are found exclusively inside caves. In this paper, noteworthy records of soft ticks infesting bats are documented in new localities from Bahia, Pernambuco, Piauí, and Rondônia states. Out of 201 bats examined, 25 were infested by 152 ticks belonging to seven taxa: Ornithodoros cavernicolous, O. hasei, Ornithodoros marinkellei, Ornithodoros cf. fonsecai, Ornithodoros cf. clarki, Antricola sp., and Nothoaspis amazoniensis. These findings provide new insights into the geographical distribution and host association of soft ticks occurring in the Neotropical region. Remarkably, morphological and biological observations about O. hasei are inferred based on the examination of on-host-collected first stage nymphs.


Ticks Argasidae Hosts Chiroptera Bats Distribution Ecology 



All the staff of the Laboratório de Ciência Aplicada à Conservação da Biodiversidade (Department of Zoology, Universidade Federal de Pernambuco), especially A. Jardelino, É. Figueiredo, F. Hintze, Í. Azevedo, J. Torres, M. Delgado-Jaramillo and M. Barros provided valuable support during the fieldwork at Catimbau National Park. PELD Catimbau team, especially M. Tabarelli and I. Leal provided logistical support. S. Muñoz-Leal was funded by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP; Grant #2018/02521-1), and F.A.M. Soares by Fundação de Amparo à Pesquisa do Estado da Bahia (FAPESB; Grant 8200/2015). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brazil, through Grants awarded to E. Barbier and Grupo Boticário de Proteção à Natureza (Grant #0983-20132) and to M. B. Labruna (Finance Code 001). This project was also supported by CNPq, CECAV, and ICMBio, and we thank all for financial and logistical support. E. Bernard has a fellow Grant from CNPq. Thanks also to L. C. Souza-Paula for preparing the Fig. 1.

Supplementary material

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Supplementary material 1 (TIFF 9421 KB)
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Supplementary material 2 (TIFF 9408 KB)


  1. Acosta ICL, Martins TF, Marcili A, Soares HS, Krawczak FS, Vieira FT, Labruna MB (2016) Ticks (Acari: Ixodidae, Argasidae) from humans, domestic and wild animals in the state of Espírito Santo, Brazil, with notes on rickettsial infection. Vet Parasitol Reg Stud Rep 3–4:66–69Google Scholar
  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefPubMedGoogle Scholar
  3. Barros-Battesti DM, Ramirez DG, Landulfo GA, Faccini JL, Dantas-Torres F, Labruna MB, Venzal JM, Onofrio VC (2013) Immature argasid ticks: diagnosis and keys for Neotropical region. Rev Bras Parasitol Vet 22:443–456CrossRefPubMedGoogle Scholar
  4. Barros-Battesti DM, Landulfo GA, Luz HR, Marcili A, Onofrio VC, Famadas KM (2015) Ornithodoros faccinii n. sp. (Acari: Ixodida: Argasidae) parasitizing the frog Thoropa miliaris (Amphibia: Anura: Cycloramphidae) in Brazil. Parasit Vectors 8:268CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bordignon MO (2006) Padrão de atividade e comportamento de forrageamento do morcego-pescador Noctilio leporinus (Linnaeus) (Chiroptera, Noctilionidae) na Baía de Guaratuba, Paraná, Brasil. Rev Bras Zool 23:50–57CrossRefGoogle Scholar
  6. Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583CrossRefPubMedPubMedCentralGoogle Scholar
  7. Clifford CM, Kohls GM, Sonenshine DE (1964) The systematics of the subfamily Ornithodorinae (Acarina: Argasidae). I. The genera and subgenera. Ann Entomol Soc Am 57:429–437CrossRefGoogle Scholar
  8. Cooley RA, Kohls GM (1944) The Argasidae of North America, Central America and Cuba. Midland Natl Monogr No 1. University Press, Notre DameGoogle Scholar
  9. Dantas-Torres F (2018) Species concepts: what about ticks? Trends Parasitol 34:1017–1026CrossRefPubMedGoogle Scholar
  10. Dantas-Torres F, Castilho Onofrio V, Barros-Battesti DM (2009) The ticks (Acari: Ixodida: Argasidae, Ixodidae) of Brazil. Syst Appl Acarol 14:30–46CrossRefGoogle Scholar
  11. Dantas-Torres F, Venzal JM, Bernardi LFO, Ferreira RL, Onofrio VC, Marcili A, Bermúdez SE, Ribeiro AF, Barros-Battesti DM, Labruna MB (2012) Description of a new species of bat-associated argasid tick (Acari: Argasidae) from Brazil. J Parasitol 98:36–45CrossRefPubMedGoogle Scholar
  12. De La Cruz J (1992) Bioecologia de las grutas de calor. Mundos Subterraneos 3:7–21Google Scholar
  13. Delgado-Jaramillo M, Barbier E, Bernard E (2018) New records, potential distribution, and conservation of the near threatened cave bat Natalus macrourus in Brazil. Oryx 52:579–586CrossRefGoogle Scholar
  14. Díaz M, Aguirre L, Barquez R (2011) Clave de identificación de los murciélagos del cono sur de Sudamérica. Publicación especial PCMA (Programa de Conservación de los Murciélagos de Argentina)-PCMB (Programa para la Conservación. de los Murciélagos de Bolivia), CochabambaGoogle Scholar
  15. Estrada-Peña A, Venzal JM, Barros-Battesti DM, Castilho Onofrio V, Trajano E, Lima Firmino JV (2004) Three new species of Antricola (Acari: Argasidae) from Brazil, with a key to the known species in the genus. J Parasitol 90:490–498CrossRefPubMedGoogle Scholar
  16. Fairchild GB, Kohls GM, Tipton VJ (1966) The ticks of Panama. In: Wenzel RL, Tipton VJ (eds) Ectoparasites of Panama. Field museum of natural history, Chicago, pp 167–219Google Scholar
  17. Gardner AL (2008) Mammals of South America. Volume I. Marsupials, Xenarthrans, Shrews, and Bats. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  18. Guimarães MM, Ferreira RL (2014) Morcegos cavernícolas do Brasil: novos registros e desafios para conservação. Rev Bras Espeleol 2:1–33Google Scholar
  19. Hoogstraal H (1985) Argasid and nuttalliellid ticks as parasites and vectors. Adv Parasitol 24:135–238CrossRefPubMedGoogle Scholar
  20. Jones EK, Clifford CM (1972) The systematics of the subfamily Ornithodorinae (Acarina: Argasidae). V. A revised key to larval Argasidae of the Western Hemisphere and description of seven new species of Ornithodoros. Ann Entomol Soc Am 65:730–740CrossRefGoogle Scholar
  21. 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. Brigh Young Univ Sci Bull Biol Ser 17:1–40Google Scholar
  22. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649CrossRefPubMedPubMedCentralGoogle Scholar
  23. Kohls GM, Sonenshine DE, Clifford CM (1965) The systematics of the subfamily Ornithodorinae (Acarina: Argasidae). II. Identification of the larvae of the Western Hemisphere and descriptions of three new species. Ann Entomol Soc Am 58:331–364CrossRefPubMedGoogle Scholar
  24. Kohls GM, Clifford CM, Jones EK (1969) The systematics of the subfamily Ornithodorinae (Acarina: Argasidae). IV. Eight new species of Ornithodoros from the Western Hemisphere. Ann Entomol Soc Am 62:1035–1043CrossRefGoogle Scholar
  25. Labruna M, Venzal J (2009) Carios fonsecai sp. nov. (Acari, Argasidae), a bat tick from the central-western region of Brazil. Acta Parasitol 54:355–363CrossRefGoogle Scholar
  26. Labruna MB, Terassini FA, Camargo LM, Brandão PE, Ribeiro AF, Estrada-Peña A (2008) New reports of Antricola guglielmonei and Antricola delacruzi in Brazil, and a description of a new argasid species (Acari). J Parasitol 94:788–792CrossRefPubMedGoogle Scholar
  27. Labruna MB, Nava S, Terassini F, Onofrio VC, Barros-Battesti DM, Camargo LM, Venzal JM (2011) Description of adults and nymph, and redescription of the larva, of Ornithodoros marinkellei (Acari: Argasidae), with data on its phylogenetic position. J Parasitol 97:207–217CrossRefPubMedGoogle Scholar
  28. Labruna MB, Nava S, Marcili A, Barbieri AR, Nunes PH, Horta MC, Venzal JM (2016) A new argasid tick species (Acari: Argasidae) associated with the rock cavy, Kerodon rupestris Wied-Neuwied (Rodentia: Caviidae), in a semiarid region of Brazil. Parasit Vectors 9:511CrossRefPubMedPubMedCentralGoogle Scholar
  29. Luz HR, Muñoz-Leal S, de Almeida JC, Faccini JL, Labruna MB (2016) Ticks parasitizing bats (Mammalia: Chiroptera) in the Caatinga Biome, Brazil. Rev Bras Parasitol Vet 25:484–491CrossRefPubMedGoogle Scholar
  30. Mangold AJ, Bargues MD, Mas-Coma S (1998) Mitochondrial 16S rDNA sequences and phylogenetic relationships of species of Rhipicephalus and other tick genera among Metastriata (Acari: Ixodidae). Parasitol Res 84:478–484CrossRefPubMedGoogle Scholar
  31. Martins TF, Venzal JM, Terassini FA, Costa FB, Marcili A, Camargo LM, Barros-Battesti DM, Labruna MB (2014) New tick records from the state of Rondônia, western Amazon, Brazil. Exp Appl Acarol 62:121–128CrossRefPubMedGoogle Scholar
  32. Matheson R (1935) Three new species of ticks, Ornithodorus (Acarina, Ixodoidea). J Parasitol 21:347–353CrossRefGoogle Scholar
  33. Muñoz-Leal S, Eriksson A, Santos CF, Fischer E, de Almeida JC, Luz HR, Labruna MB (2016) Ticks infesting bats (Mammalia: Chiroptera) in the Brazilian Pantanal. Exp Appl Acarol 69:73–85CrossRefPubMedGoogle Scholar
  34. Muñoz-Leal S, Toledo LF, Venzal JM, Marcili A, Martins TF, Acosta ICL, Pinter A, Labruna MB (2017) Description of a new soft tick species (Acari: Argasidae: Ornithodoros) associated with stream-breeding frogs (Anura: Cycloramphidae: Cycloramphus) in Brazil. Ticks Tick Borne Dis 8:682–692CrossRefPubMedGoogle Scholar
  35. Muñoz-Leal S, Faccini-Martínez ÁA, Costa FB, Marcili A, Mesquita ETKC, Marques EP Jr, Labruna MB (2018) Isolation and molecular characterization of a relapsing fever Borrelia recovered from Ornithodoros rudis in Brazil. Ticks Tick Borne Dis 9:864–871CrossRefPubMedGoogle Scholar
  36. Nava S, Venzal JM, Terassini F, Mangold AJ, Camargo LM, Labruna MB (2010) Description of a new argasid tick (Acari: Ixodida) from bat caves in Brazilian Amazon. J Parasitol 96:1089–1101CrossRefPubMedGoogle Scholar
  37. Ortêncio-Filho H, Reis N, Minte-Vera C (2010) Time and seasonal patterns of activity of phyllostomid in fragments of a stational semidecidual forest from the Upper Paraná River, Southern Brazil. Braz J Biol 70:937–945CrossRefPubMedGoogle Scholar
  38. Sangioni LA, Horta MC, Vianna MCB, Gennari SM, Soares RM, Galvão MA, Schumaker TT, Ferreira F, Vidotto O, Labruna MB (2005) Rickettsial infection in animals and Brazilian spotted fever endemicity. Emerg Infect Dis 11:265–270CrossRefPubMedPubMedCentralGoogle Scholar
  39. Sikes RS, Gannon WL, The Animal Care and Use Committee of the American Society of Mammalogists (2011) Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mamm 92:235–253CrossRefGoogle Scholar
  40. Wolf RW, Aragona M, Muñoz-Leal S, Pinto LB, Melo AL, Braga IA, Costa JS, Martins TF, Marcili A, Pacheco RC, Labruna MB, Aguiar DM (2016) Novel Babesia and Hepatozoon agents infecting non-volant small mammals in the Brazilian Pantanal, with the first record of the tick Ornithodoros guaporensis in Brazil. Ticks Tick Borne Dis 7:449–456CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e ZootecniaUniversidade de São PauloSão PauloBrazil
  2. 2.Departamento de Zoologia, Centro de BiociênciasUniversidade Federal de PernambucoRecifeBrazil
  3. 3.Programa de Pós-Graduação em EcologiaUniversidade Federal da BahiaSalvadorBrazil
  4. 4.Departamento de Imunologia, Instituto Aggeu MagalhãesFundação Oswaldo Cruz (Fiocruz)RecifeBrazil

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