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Detection of Rickettsia spp. in ticks parasitizing toads (Rhinella marina) in the northern Brazilian Amazon

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Abstract

This study evaluated rickettsial infection in ticks collected on toads from the northern Brazilian Amazon (Amapá state), where to our knowledge there are neither records of ticks from amphibians nor rickettsial infections in ticks. During 2016–2017, a total of 22 free-living toads were captured and identified as Rhinella marina. Overall, 12 (54.5%) toads were parasitized by a total of 97 ticks (6 males, 39 females, 31 nymphs, 21 larvae), giving a mean intensity of 8.1 ticks per infested toad. Two tick species were morphologically identified: Amblyomma rotundatum Koch (31 females, 14 nymphs), and Amblyomma dissimile Koch (6 males, 8 females, 17 nymphs). The 21 larvae were morphologically denoted as Amblyomma sp. Five toads were co-infested by A. rotundatum and A. dissimile. Morphological identifications were confirmed by nucleotide sequencing of fragments of the mitochondrial genes 16S rDNA, 12S rDNA and/or COX1. A total of 54 ticks were analyzed for the presence of rickettsial DNA. Eleven (9 females and 2 nymphs) out of 14 A. rotundatum ticks contained Rickettsia bellii. None of the 25 specimens of A. dissimile (6 males, 6 females, 13 nymphs) contained amplifiable rickettsial DNA. From 15 Amblyomma sp. larvae, a pool of 10 individuals contained Rickettsia sp. strain Colombianensi. Sequencing of the 16S rDNA amplicon derived from the positive pool yielded a sequence of A. dissimile. We detected Rickettsia sp. strain Colombianensi for the first time in Brazil. Prior records of this agent were restricted to Colombia and Honduras. In addition, we report the presence of A. rotundatum for the first time in the state of Amapá, where the only other record of A. dissimile was registered over 20 years ago.

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References

  • Almeida AP, Cunha LM, Bello AC, da Cunha AP, Domingues LN, Leite RC, Labruna MB (2011) A novel Rickettsia infecting Amblyomma dubitatum ticks in Brazil. Ticks Tick Borne Dis 2:209–212

    Article  PubMed  Google Scholar 

  • Andoh M, Sakata A, Takano A, Kawabata H, Fujita H, Une Y, Goka K, Kishimoto T, Ando S (2015) Detection of Rickettsia and Ehrlichia spp. in ticks associated with exotic reptiles and amphibians imported into Japan. PLoS ONE 24:10e0133700

    Google Scholar 

  • Aragão H (1936) Ixodidas brasileiros e de alguns paizes limitrophes. Mem Inst Oswaldo Cruz 31:759–843

    Article  Google Scholar 

  • Barros-Battesti DM, Arzua M, Bechara GH (2006) Carrapatos de importância médico veterinária da Região Neotropical: Um guia ilustrado para identificação de espécies, vol 1. Butantan, São Paulo, p 223

    Google Scholar 

  • Barros-Battesti DM, Landulfo GA, Luz HR, Marcili A, Onofrio VC, Famadas KM (2015) Ornithodoros faccini n. sp. (Acari: Ixodida: Argasidae) parasitizing the frog Thoropa miliaris (Amphibia: Anura: Cycloramphidae) in Brazil. Parasites Vectors 8:268

    Article  PubMed  PubMed Central  Google Scholar 

  • Basu A, Charles R (2017) Ticks of Trinidad and Tobago—an overview. Academic Press, London, p 106

    Google Scholar 

  • Beati L, Patel J, Lucas-Williams H, Adakal H, Kanduma EG, Tembo-Mwase E, Krecek R, Mertins JW, Alfred JT, Kelly S, Kelly P (2012) Phylogeography and demographic history of Amblyomma variegatum (Fabricius) (Acari: Ixodidae): the tropical bont tick. Vector Brone Zoonotic Dis 12:514–525

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Clifford CM, Anastos G, Elbl A (1961) The larval ixodid ticks of Eastern United States (Acarina: Ixodidae). Misc Publ Entomol Soc Am 1:213–237

    Google Scholar 

  • Eremeeva ME, Bosserman EA, Demma LJ, Zambrano ML, Blau DM, Dasch GA (2006) Isolation and identification of Rickettsia massiliae from Rhipicephalus sanguineus ticks collected in Arizona. Appl Environ Microbiol 72:5569–5577

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Erster O, Roth A, Avni Z, King R, Shkap V (2015) Molecular detection of Rickettsia bellii in Amblyomma rotundatum from imported red-footed tortoise (Chelonoides carbonaria). Ticks Tick Borne Dis 6:473–477

    Article  PubMed  Google Scholar 

  • Floch H, Fauran P (1958) Ixodidés de la Guyane et des Antilles Françaises. Arch Inst Pasteur Guyane, p 94

  • Guglielmone AA, Nava S (2010) Hosts of Amblyomma dissimile Koch, 1844 and Amblyomma rotundatum Koch, 1844 (Acari: Ixodidae). Zootaxa 2541:27–49

    Google Scholar 

  • Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Peña A, Horak IG (2014) The hard ticks of the world: (Acari: Ixodida: Ixodidae). Springer, New York, p 738

    Book  Google Scholar 

  • Hebert PD, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc Natl Acad Sci USA 101:14812–14817

    Article  PubMed  CAS  Google Scholar 

  • Horta MC, Saraiva DG, Glauber MB, Oliveira GM, Martins TF, Labruna MB (2015) Rickettsia bellii in Amblyomma rotundatum ticks parasitizing Rhinella jimi from northeastern Brazil. Microbes Infect 17:856–858. https://doi.org/10.1016/j.micinf.2015.08.010

    Article  PubMed  Google Scholar 

  • Imaoka K, Kaneko S, Tabara K, Kusatake K, Morita E (2011) The first human case of Rickettsia tamurae infection in Japan. Case Rep Dermatol 3:68–73

    Article  PubMed  PubMed Central  Google Scholar 

  • Jado I, Oteo JA, Aldamiz M, Gil H, Escudero R, Ibarra V, Portu J, Portillo A, Lezaun MJ, Garcia-Amil C, Rodriguez-Moreno I, Anda P (2007) Rickettsia monacensis and human disease, Spain. Emerg Infect Dis 13:1405–1407

    Article  PubMed  PubMed Central  CAS  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. Brigham Young Univ Sci Bull Biol Ser 17:1–40

    Google Scholar 

  • Jongejan F, Uilenberg G (2004) The global importance of ticks. Parasitology 129:3–14. https://doi.org/10.1017/S0031182004005967

    Article  Google Scholar 

  • Karpathy SE, Slater KS, Goldsmith CS, Nicholson WL, Paddock CD (2016) Rickettsia amblyommatis sp. nov., a spotted fever group Rickettsia associated with multiple species of Amblyomma ticks in North, Central and South America. Int J Syst Evol Microbiol 66:5236–5243

    Article  PubMed  PubMed Central  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, Drummond A (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 

  • Krawczak F, Labruna MB, Hecht JA, Paddock CD, Karpathy SE (2018) Genotypic characterization of Rickettsia bellii reveals distinct lineages in the United States and South America. Biomed Res Int. https://doi.org/10.1155/2018/8505483

    Article  PubMed  PubMed Central  Google Scholar 

  • Labruna MB (2009) Ecology of rickettsia in South America. Ann N Y Acad Sci 1166:156–166

    Article  PubMed  Google Scholar 

  • Labruna MB, Whitworth T, Horta MC, Bouyer DH, McBride JW, Pinter A, Popov V, Gennari SM, Walker DH (2004) Rickettsia species infecting Amblyomma cooperi ticks from an area in the state of São Paulo, Brazil, where Brazilian spotted fever is endemic. J Clin Microbiol 42:90–98

    Article  PubMed  PubMed Central  Google Scholar 

  • Labruna MB, Terrassini FA, Camargo LM (2005) First report of the male of Amblyomma rotundatum (Acari: Ixodidae) from a field-collected host. J Med Entomol 42:945–947

    Article  PubMed  Google Scholar 

  • Labruna MB, Pacheco RC, Richtzenhain LJ, Szabo MP (2007) Isolation of Rickettsia rhipicephali and Rickettsia bellii from Haemaphysalis juxtakochi ticks in the state of São Paulo, Brazil. Appl Environ Microbiol 73:869–873

    Article  PubMed  CAS  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. Parasites Vectors 9:511

    Article  PubMed  PubMed Central  Google Scholar 

  • Lampo M, Rangel Y, Mata A (1997) Genetic markers for the identification of two tick species, Amblyomma dissimile and Amblyomma rotundatum. J Parasitol 83:382–386

    Article  PubMed  CAS  Google Scholar 

  • Luz HR, Faccini JLH (2013) Parasitismo por carrapatos em Anuros no Brasil: revisão. Vet Zootec 20:100–111

    Google Scholar 

  • Luz HR, Faccini JLH, McIntosh D (2017) Molecular analyses reveal an abundant diversity of ticks and rickettsial agents associated with wild birds in two regions of primary Brazilian Atlantic Rainforest. Ticks Tick Borne Dis 8:657–665

    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  PubMed  CAS  Google Scholar 

  • Martins TF, Onofrio VC, Barros-Battesti DM, Labruna MB (2010) Nymphs of the genus Amblyomma (Acari Ixodidae) of Brazil: descriptions, redescriptions and identification key. Ticks Tick Borne Dis 1:75–99

    Article  PubMed  Google Scholar 

  • Michel T, Souza U, Dall’Agnol B, Webster A, Peters F, Christoff A, Luza AL, Kasper N, Becker M, Fiorentin G, Klafke G, Venzal J, Martins JR, Jardim MMA, Ott R, Reck J (2017) Ixodes spp. (Acari: Ixodidae) ticks in Rio Grande do Sul state, Brazil. Syst Appl Acarol 22:2057–2067

    Article  Google Scholar 

  • Miranda J, Mattar S (2014) Molecular detection of Rickettsia bellii and Rickettsia sp. strain Colombianensi in ticks from Cordoba, Colombia. Ticks Tick Borne Dis 5:208–212

    Article  PubMed  Google Scholar 

  • Miranda J, Portillo A, Oteo JA, Mattar S (2012) Rickettsia sp. strain Colombianensi (Rickettsiales: Rickettsiaceae): a new proposed rickettsia detected in Amblyomma dissimile (Acari: Ixodidae) from iguanas and free-living larvae ticks from vegetation. J Med Entomol 49:960–965

    Article  PubMed  CAS  Google Scholar 

  • Muñoz-Leal S, Toledo LF, Venzal JM, Marcili A, Martins TF, Acosta IC, 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 AAM, 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. https://doi.org/10.1016/j.ttbdis.2018.03.008

    Article  PubMed  Google Scholar 

  • Nava S, Venzal J, Acuña DG, Martins TF, Guglielmone A (2017) Ticks of the Southern Cone of America: diagnosis, distribution, and hosts with taxonomy, ecology and sanitary importance, 1st edn, p 372

  • Nieri-Bastos FA, Lopes MG, Cançado PHD, Rossa GA, Faccini JL, Gennari SM, Labruna MB (2014) Candidatus Rickettsia andeanae, a spotted fever group agent infecting Amblyomma parvum ticks in two Brazilian biomes. Mem Inst Oswaldo Cruz 109:259–261

    Article  PubMed  PubMed Central  Google Scholar 

  • Nieri-Bastos FA, Marcili A, Sousa R, Paddock CD, Labruna MB (2018) Phylogenetic evidence for the existence of multiple strains of Rickettsia parkeri in the New World. Appl Environ Microbiol. https://doi.org/10.1128/AEM.02872-17

    Article  PubMed  PubMed Central  Google Scholar 

  • Novakova M, Literak I, Chevez L, Martins TF, Ogrzewalska M, Labruna MB (2015) Rickettsial infections in ticks from reptiles, birds and humans in Honduras. Ticks Tick Borne Dis 6:737–742

    Article  PubMed  Google Scholar 

  • Pacheco RC, Moraes-Filho J, Marcili A, Richtzenhain LJ, Szabó MP, Catroxo MH, Bouyer DH, Labruna MB (2011) Rickettsia monteiroi sp. nov., infecting the tick Amblyomma incisum in Brazil. Appl Environ Microbiol 77:5207–5211

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Parola P, Paddock CD, Socolovschi C, Labruna MB, Mediannikov O, Kernif T, Abdad MY, Stenos J, Bitam I, Fournier PE, Raoult D (2013) Update on tick-borne rickettsioses around the world: a geographic approach. Clin Microbiol Rev 26:657–702

    Article  PubMed  PubMed Central  Google Scholar 

  • Regnery RL, Spruill CL, Plikaytis BD (1991) Genotypic identification of Rickettsiae and estimation of intraspecies sequence divergence for portions of two Rickettsial genes. J Bacteriol 173:1576–1589

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sangioni LA, Horta MC, Vianna MCB, Gennari SM, Soares RS, Galvão MAM, Schumaker TTS, 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 

  • Santodomingo A, Cotes-Perdomo A, Foley J, Castro LR (2018) Rickettsial infection in ticks (Acari: Ixodidae) from reptiles in the Colombian Caribbean. Ticks Tick Borne Dis 9:623–628

    Article  PubMed  Google Scholar 

  • Santolin ÍDAC, Famadas KM, Mcintosh D (2013) Detection and identification of Rickettsia agents in ticks collected from wild birds in Brazil by polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) analysis. Rev Bras Med Vet 35:68–73

    Google Scholar 

  • Schumaker TTS, Barros DM (1994) Notes on the biology of Amblyomma dissimile Koch, 1844 (Acari: Ixodida) on Bufo marinus (Linnaeus, 1758) from Brazil. Mem Inst Oswaldo Cruz 89:29–31

    Article  PubMed  CAS  Google Scholar 

  • Szabó MP, Pinter A, Labruna MB (2013) Ecology, biology and distribution of spotted-fever tick vectors in Brazil. Front Cell Infect Microbiol 3:27

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This study received financial support by the São Paulo Research Foundation (FAPESP), National Council for Scientific and Technological Development (CNPq) and Coordination Office for Improvement of Higher-Education Personnel (CAPES).

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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 (USP), Av. Prof. Orlando Marques de Paiva, 87, Cidade Universitária, São Paulo, SP, 05508-000, Brazil

    Hermes Ribeiro Luz, Igor Acosta, Thiago F. Martins, Sebástian Muñoz-Leal & Marcelo B. Labruna

  2. Departamento de Ciências Biológicas e da Saúde, Laboratório de Herpetologia, Universidade Federal do Amapá (UNIFAP), Rodovia Juscelino Kubitschek, Km 02, Jardim Marco Zero, Macapá, Amapá, 69903-419, Brazil

    Ercileide Silva-Santos & Carlos Eduardo Costa-Campos

  3. Departamento de Parasitologia Animal, Instituto de Veterinária, Universidade Federal Rural do Rio de Janeiro (UFRRJ), Seropédica, RJ, 23890-000, Brazil

    Douglas McIntosh & João Luis Horacio Faccini

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  1. Hermes Ribeiro Luz
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  2. Ercileide Silva-Santos
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  3. Carlos Eduardo Costa-Campos
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  4. Igor Acosta
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  5. Thiago F. Martins
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  6. Sebástian Muñoz-Leal
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  7. Douglas McIntosh
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  8. João Luis Horacio Faccini
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  9. Marcelo B. Labruna
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Correspondence to Hermes Ribeiro Luz.

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Luz, H.R., Silva-Santos, E., Costa-Campos, C.E. et al. Detection of Rickettsia spp. in ticks parasitizing toads (Rhinella marina) in the northern Brazilian Amazon. Exp Appl Acarol 75, 309–318 (2018). https://doi.org/10.1007/s10493-018-0270-y

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