Skip to main content
Springer Nature Link
Log in

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

  • Published:
Experimental and Applied Acarology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • 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 3–4:66–69

    Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • 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 22:443–456

    Article  PubMed  Google Scholar 

  • 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 8:268

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 23:50–57

    Article  Google Scholar 

  • Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583

    Article  CAS  PubMed  Google Scholar 

  • Clifford CM, Kohls GM, Sonenshine DE (1964) The systematics of the subfamily Ornithodorinae (Acarina: Argasidae). I. The genera and subgenera. Ann Entomol Soc Am 57:429–437

    Article  Google Scholar 

  • Cooley RA, Kohls GM (1944) The Argasidae of North America, Central America and Cuba. Midland Natl Monogr No 1. University Press, Notre Dame

    Google Scholar 

  • Dantas-Torres F (2018) Species concepts: what about ticks? Trends Parasitol 34:1017–1026

    Article  PubMed  Google Scholar 

  • Dantas-Torres F, Castilho Onofrio V, Barros-Battesti DM (2009) The ticks (Acari: Ixodida: Argasidae, Ixodidae) of Brazil. Syst Appl Acarol 14:30–46

    Article  Google Scholar 

  • 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 98:36–45

    Article  PubMed  Google Scholar 

  • De La Cruz J (1992) Bioecologia de las grutas de calor. Mundos Subterraneos 3:7–21

    Google Scholar 

  • 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 52:579–586

    Article  Google Scholar 

  • 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), Cochabamba

    Google Scholar 

  • 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 90:490–498

    Article  PubMed  Google Scholar 

  • 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 167–219

    Google Scholar 

  • Gardner AL (2008) Mammals of South America. Volume I. Marsupials, Xenarthrans, Shrews, and Bats. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Guimarães MM, Ferreira RL (2014) Morcegos cavernícolas do Brasil: novos registros e desafios para conservação. Rev Bras Espeleol 2:1–33

    Google Scholar 

  • Hoogstraal H (1985) Argasid and nuttalliellid ticks as parasites and vectors. Adv Parasitol 24:135–238

    Article  CAS  PubMed  Google Scholar 

  • 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 65:730–740

    Article  Google Scholar 

  • 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 17:1–40

    Google Scholar 

  • 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 28:1647–1649

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 58:331–364

    Article  CAS  PubMed  Google Scholar 

  • 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 62:1035–1043

    Article  Google Scholar 

  • Labruna M, Venzal J (2009) Carios fonsecai sp. nov. (Acari, Argasidae), a bat tick from the central-western region of Brazil. Acta Parasitol 54:355–363

    Article  Google Scholar 

  • 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 94:788–792

    Article  PubMed  Google Scholar 

  • 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 97:207–217

    Article  PubMed  Google Scholar 

  • 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 9:511

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 25:484–491

    Article  PubMed  Google Scholar 

  • 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 84:478–484

    Article  CAS  PubMed  Google Scholar 

  • 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 62:121–128

    Article  PubMed  Google Scholar 

  • Matheson R (1935) Three new species of ticks, Ornithodorus (Acarina, Ixodoidea). J Parasitol 21:347–353

    Article  Google Scholar 

  • 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 69:73–85

    Article  PubMed  Google Scholar 

  • 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 8:682–692

    Article  PubMed  Google Scholar 

  • 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 9:864–871

    Article  PubMed  Google Scholar 

  • 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 96:1089–1101

    Article  PubMed  Google Scholar 

  • 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 70:937–945

    Article  PubMed  Google Scholar 

  • 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 11:265–270

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 92:235–253

    Article  Google Scholar 

  • 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 7:449–456

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

  1. Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, São Paulo, Brazil

    S. Muñoz-Leal & M. B. Labruna

  2. Departamento de Zoologia, Centro de Biociências, Universidade Federal de Pernambuco, Recife, Pernambuco, Brazil

    E. Barbier & E. Bernard

  3. Programa de Pós-Graduação em Ecologia, Universidade Federal da Bahia, Salvador, Bahia, Brazil

    F. A. M. Soares

  4. Departamento de Imunologia, Instituto Aggeu Magalhães, Fundação Oswaldo Cruz (Fiocruz), Recife, Pernambuco, Brazil

    F. Dantas-Torres

Authors
  1. S. Muñoz-Leal
    View author publications

    Search author on:PubMed Google Scholar

  2. E. Barbier
    View author publications

    Search author on:PubMed Google Scholar

  3. F. A. M. Soares
    View author publications

    Search author on:PubMed Google Scholar

  4. E. Bernard
    View author publications

    Search author on:PubMed Google Scholar

  5. M. B. Labruna
    View author publications

    Search author on:PubMed Google Scholar

  6. F. Dantas-Torres
    View author publications

    Search author on:PubMed Google Scholar

Corresponding authors

Correspondence to S. Muñoz-Leal or F. Dantas-Torres.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (TIFF 9421 KB)

Supplementary material 2 (TIFF 9408 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Muñoz-Leal, S., Barbier, E., Soares, F.A.M. et al. New records of ticks infesting bats in Brazil, with observations on the first nymphal stage of Ornithodoros hasei. Exp Appl Acarol 76, 537–549 (2018). https://doi.org/10.1007/s10493-018-0330-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10493-018-0330-3

Keywords