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Redescription of the larva, and description of the nymphal and adult stages of Ornithodoros peruvianus Kohls, Clifford & Jones, 1969 (Acari: Argasidae)

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Abstract

The soft tick Ornithodoros peruvianus Kohls, Clifford & Jones, 1969 was described as a parasite of bats in Peru upon the examination of engorged larvae only. Recently, larvae of this tick species were reported on bats from northern Chile. However, the adult and nymphal stages of O. peruvianus have remained undescribed. This study aimed to redescribe the larva of O. peruvianus based on unfed specimens, and to describe nymphs, the male and the female of this species. Ticks were collected on the walls inside three caves in northern Chile. Two females laid eggs in the laboratory. Part of the unfed larvae was separated for morphological and morphometrical analyses, and the remaining specimens were fed upon laboratory mice in order to obtain subsequent nymphal and adult stages. The first nymphal stage (N1) moulted either to male or to a second nymphal stage (N2) without feeding. Obtained N2 moulted either to male or female after one meal. PCR amplification of tick mitochondrial 16S rRNA of specimens from the three caves revealed almost identical sequences. The unfed larva of O. peruvianus has an elongated idiosoma, and fringed setae cover the ventral surfaces of coxae, palps and tarsi. Nymph 1 has a thin integument covered by incipient mammillae and barely noticeable dorsal disks; it lacks cheeks and possesses few short setae on the basis capitulum. Nymph 2 has a pair of small cheeks and resembles adult stages in its tegumentary traits and capitulum. Adult stages exhibit developed cheeks (larger in females) without the capacity to completely cover the capitulum. Very small and low mammillae cover the surface of the dorsal idiosoma in adults. As this feature also occurs in other bat-associated soft ticks, regardless of their phylogenetic relatedness, small mammillae in bat soft ticks are suggestive of convergent evolution.

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References

  • Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology,215, 403–410.

    Article  CAS  Google Scholar 

  • Bakkes, D. K., De Klerk, D., Latif, A. A., & Mans, B. J. (2018). Integrative taxonomy of Afrotropical Ornithodoros (Ornithodoros) (Acari: Ixodida: Argasidae). Ticks and Tick-borne Diseases,9, 1006–1037.

    Article  Google Scholar 

  • Balashov, Y. S. (1972). Bloodsucking ticks (Ixodidae)—Vectors of diseases of man and animals. Miscelaneous Publications of the Entomological Society of America,8, 160–376.

    Google Scholar 

  • Barros-Battesti, D. M., Landulfo, G. A., Luz, H. R., Marcili, A., Onofrio, V. C., & Famadas, K. M. (2015). Ornithodoros faccinii n. sp. (Acari: Ixodida: Argasidae) parasitizing the frog Thoropa miliaris (Amphibia: Anura: Cycloramphidae) in Brazil. Parasites & Vectors, 8, 268.

    Article  Google Scholar 

  • Beati, L., & Klompen, H. (2019). Phylogeography of ticks (Acari: Ixodida). Annual Review of Entomology,64, 379–397.

    Article  CAS  Google Scholar 

  • Cooley, R. A., & Kohls, G. M. (1941). Three new species of Ornithodoros (Acarina: Ixodoidea). Public Health Reports (1896–1970),56, 587.

    Article  Google Scholar 

  • Cooley, R. A., & Kohls, G. M. (1944). The Argasidae of North America, Central America and Cuba. The American Midland Naturalist. Monograph No. 1. Notre Dame: The University Press.

    Google Scholar 

  • Dantas-Torres, F., Venzal, J. M., Bernardi, L. F. O., Ferreira, R. L., Onofrio, V. C., Marcili, A., et al. (2012). Description of a new species of bat-associated argasid tick (Acari: Argasidae) from Brazil. Journal of Parasitology,98, 36–45.

    Article  Google Scholar 

  • González-Moraga, M., Esquivel, C., Moreno-Salas, L., Troncoso, I., Torres-Fuentes, L., Ardiles, K., et al. (2018). Development cycle of Ornithodoros peruvianus Kohls, Clifford & Jones (Ixodoidea: Argasidae) under laboratory conditions. Acarologia,58, 186–191.

    Google Scholar 

  • Guzmán-Cornejo, C., García-Prieto, L., Rebollo-Hernández, A., Venzal, J. M., Nava, S., & Sánchez-Montes, S. (2017). Molecular evidence and additional morphological characters to distinguish Ornithodoros brodyi and Ornithodoros yumatensis (Ixodida: Argasidae) in their different developmental stages. Acta Parasitologica,62, 432–448.

    Article  Google Scholar 

  • Hoogstraal, H., Wassef, H. Y., Hays, C., & Keirans, J. E. (1985). Ornithodoros (Alectorobius) spheniscus n. sp. [Acarina: Ixodoidea: Argasidae: Ornithodoros (Alectorobius) capensis group], a tick parasite of the Humboldt penguin in Peru. Journal of Parasitology,71, 635–644.

    Article  CAS  Google Scholar 

  • Jones, E. K., & Clifford, C. M. (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. Annals of the Entomological Society of America,65, 730–740.

    Article  Google Scholar 

  • Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., et al. (2012). Geneious basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics,28, 1647–1649.

    Article  Google Scholar 

  • Klompen, J. S., Black, W. C., Keirans, J. E., & Oliver, J. H. (1996). Evolution of ticks. Annual Review of Entomology,41, 141–161.

    Article  CAS  Google Scholar 

  • Klompen, J. S. H. (1992). Comparative morphology of argasid larvae (Acari: Ixodida: Argasidae), with notes on phylogenetic relationships. Annals of the Entomological Society of America,85, 541–560.

    Article  Google Scholar 

  • Klompen, J. S. H., & Oliver, J. H. (1993). Systematic relationships in the soft ticks (Acari: Ixodida: Argasidae). Systematic Entomology,18, 313–331.

    Article  Google Scholar 

  • Kohls, G. M., Clifford, C. M., & Jones, E. K. (1969). The systematics of the subfamily Ornithodorinae (Acarina: Argasidae). IV. Eight new species of Ornithodoros from the Western Hemisphere. Annals of the Entomological Society of America,62, 1035–1043.

    Article  Google Scholar 

  • Kohls, G. M., Sonenshine, D. E., & Clifford, C. M. (1965). The systematics of the subfamily Ornithodorinae (Acarina: Argasidae). II. Identification of the larvae of the Western Hemisphere and descriptions of three new species. Annals of the Entomological Society of America,58, 331–364.

    Article  CAS  Google Scholar 

  • Labruna, M. B., Marcili, A., Ogrzewalska, M., Barros-Battesti, D. M., Dantas-Torres, F., Fernandes, A. A., et al. (2014). New records and human parasitism by Ornithodoros mimon (Acari: Argasidae) in Brazil. Journal of Medical Entomology,51, 283–287.

    Article  Google Scholar 

  • Labruna, M. B., Nava, S., Terassini, F. a, Onofrio, V. C., Barros-Battesti, D. M., Camargo, L. M. A., & Venzal, J. M. (2011). Description of adults and nymph, and redescription of the larva, of Ornithodoros marinkellei (Acari: Argasidae), with data on its phylogenetic position. Journal of Parasitology, 97, 207–217.

    Article  Google Scholar 

  • Labruna, M. B., Terassini, F. A., Camargo, L. M. A., Brandão, P. E., Ribeiro, A. F., & Estrada-Peña, A. (2008). New reports of Antricola guglielmonei and Antricola delacruzi in Brazil, and a description of a new argasid species (Acari). Journal of Parasitology,94, 788–792.

    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 Parasitologica,54, 355–363.

    Article  Google Scholar 

  • Landulfo, G. A., Pevidor, L. V., Luz, H. R., Faccini, J. L. H., Nunes, P. H., & Barros-Battesti, D. M. (2013). Description of nymphal instars of Ornithodoros mimon Kohls, Clifford & Jones, 1969 (Acari: Argasidae). Zootaxa,3710, 179.

    Article  Google Scholar 

  • Mangold, A. J., Bargues, M. D., & Mas-Coma, S. (1998). Mitochondrial 16S rDNA sequences and phylogenetic relationships of species of Rhipicephalus and other tick genera among Metastriata (Acari: Ixodidae). Parasitology Research,84, 478–484.

    Article  CAS  Google Scholar 

  • Matheson, R. (1935). Three new species of ticks, Ornithodorus (Acarina, Ixodoidea). Journal of Parasitology,21, 347.

    Article  Google Scholar 

  • Muñoz-Leal, S., Terassini, F. A., Luz, H. R., Fontana, I., Camargo, L. M. A., & Labruna, M. B. (2018). First report of Ornithodoros peropteryx in Brazil, and the occurrence of Ornithodoros cavernicolous in the western Brazilian Amazon. Systematic and Applied Acarology,23, 2113.

    Article  Google Scholar 

  • Muñoz-Leal, S., Toledo, L. F., Venzal, J. M., Marcili, A., Martins, T. F., Acosta, I. C. L., et al. (2017). Description of a new soft tick species (Acari: Argasidae: Ornithodoros) associated with stream-breeding frogs (Anura: Cycloramphidae: Cycloramphus) in Brazil. Ticks and Tick Borne Diseases,8, 682–692.

    Article  Google Scholar 

  • Muñoz-Leal, S., Venzal, J. M., González-Acuña, D., Nava, S., Lopes, M. G., Martins, T. F., et al. (2016). A new species of Ornithodoros (Acari: Argasidae) from desert areas of northern Chile. Ticks and Tick Borne Diseases,7, 901–910.

    Article  Google Scholar 

  • Nava, S., Venzal, J. M., Terassini, F. A., Mangold, A. J., Camargo, L. M. A., Casás, G., et al. (2013). Ornithodoros guaporensis (Acari, Ixodida: Argasidae), a new tick species from the Guaporé River Basin in the Bolivian Amazon. Zootaxa,3666, 579.

    Article  Google Scholar 

  • Sonenshine, D. E. (1962). External anatomy of the bat tick Ornithodoros kelleyi Cooley and Kohls (Acarina: Argasidae). Journal of Parasitology,48, 470–485.

    Article  CAS  Google Scholar 

  • Venzal, J., González-Acuña, D., Mangold, A., & Guglielmone, A. (2012). Ornithodoros peruvianus Kohls, Clifford & Jones (Ixodoidea: Argasidae) in Chile: a tentative diagnosis. Neotropical Entomology,41, 74–78.

    Article  CAS  Google Scholar 

  • Venzal, J. M., Estrada-Peña, A., Mangold, A. J., González-Acuña, D., & Guglielmone, A. A. (2008). The Ornithodoros (Alectorobius) talaje species group (Acari: Ixodida: Argasidae): description of Ornithodoros (Alectorobius) rioplatensis n. sp. from southern South America. Journal of Medical Entomology,45, 832–840.

    CAS  PubMed  Google Scholar 

  • Venzal, J. M., Nava, S., González-Acuña, D., Mangold, A. J., Muñoz-Leal, S., Lado, P., et al. (2013a). A new species of Ornithodoros (Acari: Argasidae), parasite of Microlophus spp. (Reptilia: Tropiduridae) from northern Chile. Ticks and Tick Borne Diseases,4, 128–132.

    Article  Google Scholar 

  • Venzal, J. M., Nava, S., Terassini, F. A., Ogrzewalska, M., Camargo, L. M. A., & Labruna, M. B. (2013b). Ornithodoros peropteryx (Acari: Argasidae) in Bolivia: an argasid tick with a single nymphal stage. Experimental and Applied Acarology,61, 231–241.

    Article  Google Scholar 

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Acknowledgements

We thank Alejandro Márquez and Ana Laura Reyes from the Unidad de Microscopía Electrónica, Facultad de Ciencias-UdelaR, Montevideo (Uruguay) for their assistance in obtaining scanning electron micrographs.

Funding

SML and fieldwork was funded by the “Programa de Formación de Capital Humano Avanzado” (CONICYT, Chile), Grant # 72140079. Laboratory work was supported by the “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior” (CAPES, Brazil), finance Code 001. The collection of samples was funded in part by Fondecyt Projects Nos. 1100695, 1130948 and 1170972.

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Authors and Affiliations

  1. Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, Av. Prof. Orlando Marques de Paiva, 87, Cidade Universitária, São Paulo, SP, 05508-270, Brazil

    Sebastián Muñoz-Leal & Marcelo B. Labruna

  2. Laboratorio de Parásitos y Enfermedades de Fauna Silvestre, Departamento de Ciencia Animal, Facultad de Ciencias Veterinarias, Universidad de Concepción, Av. Vicente Méndez 595, CP 3780000, Chillán (Ñuble), Chile

    Daniel González-Acuña

  3. Laboratorio de Vectores y Enfermedades Transmitidas, Facultad de Veterinaria, CENUR Litoral Norte, Salto, Universidad de la República, Rivera 1350, CP 50000, Salto, Uruguay

    José M. Venzal

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  1. Sebastián Muñoz-Leal
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Correspondence to Sebastián Muñoz-Leal.

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The authors declare that they have no conflict of interest.

Ethical approval

The collection of ticks was approved by the “Servicio Agrícola y Ganadero” of the Chilean government, and the “Corporación Nacional Forestal” with the licenses 033/2014, 074/2015 and 001/2016. Mice used to feed ticks in the laboratory belong to an animal room in the “Departamento de Medicina Veterinária e Saúde Animal” at the São Paulo University, São Paulo, Brazil. The use of laboratory animals was approved by the Ethics Committee of the Veterinary Faculty from the São Paulo University (CEUA 4425171018). All applicable international, national, and institutional guidelines for the care and use of animals were followed.

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Muñoz-Leal, S., González-Acuña, D., Labruna, M.B. et al. Redescription of the larva, and description of the nymphal and adult stages of Ornithodoros peruvianus Kohls, Clifford & Jones, 1969 (Acari: Argasidae). Syst Parasitol 97, 201–215 (2020). https://doi.org/10.1007/s11230-020-09908-6

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