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First Record of Amblyomma Dissimile (Acari: Ixodidae) Infesting the Granular Toad Rhinella Major (Anura: Bufonidae) in the Eastern Amazon Region

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First Record of Amblyomma Dissimile (Acari: Ixodidae) Infesting the Granular Toad Rhinella Major (Anura: Bufonidae) in the Eastern Amazon Region Herpetology Notes, volume 13: 385-387 (2020) (published online on 26 May 2020) First record of Amblyomma dissimile (Acari: Ixodidae) infesting the Granular Toad Rhinella major (Anura: Bufonidae) in the Eastern Amazon region Fillipe Pedroso-Santos1, Ercileide da Silva Santos1, Patrick Ribeiro Sanches1, Carlos Eduardo Costa-Campos1,*, Hermes Ribeiro Luz2, and João Luiz Horacio Faccini3 Occurrence of ectoparasites as ticks have been also reports for R. schneideri and R. bergi for the state registered for different species of anurans of the of Mato Grosso, Brazil (Witter et al., 2016), the latter Bufonidae Gray, 1825 family in Brazil, such as Rhinella belonging to the Rhinella granulosa species group. schneideri (Luz et al., 2015; Benício and Silva, 2017), Rhinella major (Muller & Helmich, 1936) is a Rhinella icterica, Rhinella bergi (Woehl, 2002), terrestrial species of moderate size (Snout-Vent Length Rhinella marina (Ahid et al., 2009; Oda et al., 2018), [SVL] 35.8–72.8 mm in adult males and 33.9–81.1 mm Rhinella jimi (Horta et al., 2015), Rhinella crucifer, in adult females), belonging to the R. granulosa group. Rhinella arenarum (Luz and Faccini, 2013), Rhinella �he species occurs in the Chaco region, Argentina, margaritifera, Rhinella granulosa, Rhinella pygmaea, Paraguay, and Bolivia, and in open formations along Rhaebo guttatus (Kelehear et al., 2017; Oda et al., the rivers Beni, Madeira, Amazonas, �apajos, and 2018) and Rhinella ornata (Luz et al., 2018). �he tick Xingu, and in the Amapa state, Brazil. Rhinella major Amblyomma dissimile Kock, 1844 is an ectoparasite is characterized by having a small parotoid gland, warty commonly found on cold-blooded animals (amphibians skin, and well-developed and keratinized cranial crests and reptiles), with wide distribution in the neotropics, (Narvaes and Rodrigues, 2009). In the literature, there including Brazil. �here are also reports in the Nearctic are no reports of ticks parasitizing this species. region (Guglielmone and Nava, 2010; Guglielmone et In this note, we provide the first report of parasitism al., 2014; Kelehear et al., 2017). on R. major by ticks of the species A. dissimile. We In Brazil, in addition to its association with different collected the toads through the method of active visual species of reptiles, A. dissimile is commonly reported in and auditory search (Crump and Scott Jr., 1994; Heyer anurans of the genus Rhinella Fitzinger, 1826, especially et al., 1994) during an amphibian survey in an urban R. marina in the Amazonia and Pantanal biomes (Lampo area in the municipality of Macapá, Amapá (0.0083ºS, and Bayliss, 1996; Guglielmone and Nava, 2010; Luz 51.0953ºW; Datum: WGS84; 7 m a.s.l), located in the and Faccini, 2013; Guglielmone et al., 2014). �here are extreme north of Brazil. Our registers occurred on 5 and 9 July 2017, at around 20:30 h, when we observed two female ticks of the species A. dissimile attached to the dorsal surface of two males R. major (SVL = 34 mm and 49 mm; 6 1 Departamento de Ciências Biológicas e da Saúde, g and 10 g) (Fig. 1, 2). �he ticks were collected, sent Universidade Federal do Amapá, Campus Marco Zero do to the Laboratory of Acarology of the Federal Rural Equador, 68.903-419, Macapá, Amapá, Brazil. University of Rio de Janeiro, where they were identified 2 Departamento de Medicina Veterinária Preventiva e Saúde morphologically with aid of a stereoscope and of the Animal, Faculdade de Medicina Veterinária e Zootecnia, key to adult ticks of the Amblyomma genus (Onofrio Universidade de São Paulo, São Paulo, Brazil. et al., 2006). �he anurans were fixed in formaldehyde 3 Departamento de Parasitologia Animal, Universidade Federal Rural do Rio de Janeiro, 23.890-000, Seropédica, Rio de 10%, preserved in alcohol 70% and deposited in the Janeiro, Brazil. Herpetological Collection of Universidade Federal * Corresponding author. E-mail: [email protected] do Amapá (CECCAMPOS 01254; CECCAMPOS 386 Fillipe Pedroso-Santos et al. Figure 1. Parasitism on a male Rhinella major by Amblyomma Figure 2. Parasitism on a male Rhinella major by Amblyomma dissimile in an urban area in the municipality of Macapá, dissimile in an urban area in the municipality of Macapá, Amapa State, Brazil. Amapa State, Brazil. 01255). Collected ticks were deposited in the tick References collection “Coleção Nacional de Carrapatos (CNC)” of Ahid, S.M.M., Fonseca, Z.A.A.S., Ferreira, C.G.�., Martins, �.F., the University of São Paulo under accession numbers Oliveira, M.F. (2009): Parasitismo de Amblyomma rotundatum CNC-3875. (Koch) (Acari: Ixodidae) em Bufo marinus (Linnaeus) (Anura: In Brazil, there are only six species of hard ticks Bufonidae), em Mossoró, Rio Grande do Norte, Brasil. Revista in association with anurans of the genus Rhinella: Brasileira de Zoociências 11: 153–156. Amblyomma fuscum, Amblyomma goeldii, Amblyomma Barros-Batestti, D.M., Arzua, M., Bechara, G.H. (2006): Carrapatos de Importância Médico-Veterinária da Região Neotropical: um humerale, Amblyomma cajennense s.l., A. dissimile and guia ilustrado para identificação de espécies. Vox/ICTTD-3/ Amblyomma rotundatum, of which the last two species Butantan, São Paulo. 223p. the most common, while the others are considered Benício, R.A., Silva, F.R. (2017): Natural History Notes: Rhinella unusual or concern identification errors (Wells et al., schneideri (Cururu �oad). Ectoparasitism. Herpetological 1981; Petit et al., 1990; Brum and Costa, 2003; Barros- Review 48: 170–171. Battesti et al., 2006; Szabó et al., 2007; Guglielmone Brum, J.G.W., Costa, P.R.P. (2003): Confirmação da ocorrência da and Nava, 2010; Luz and Faccini, 2013; Guglielmone et Amblyomma rotundatum Koch, 1844 (Acari: Ixodidae) no Rio Grande do Sul. Arquivos do Instituto Biológico 70: 105–106. al., 2014; Luz et al., 2015; Oda et al., 2018). Crump, M.A., Scott Jr., N.J. (1994): Visual Encounter Surveys. �he tick fauna of Brazil is currently composed by In: Measuring and Monitoring Biological Diversity: Standard 72 species, 47 in the Ixodidae family, and 25 in the Methods for Amphibians, pp. 84–92. Heyer, W.R., Donnelly, Argasidae family (Labruna et al., 2016; Dall’Agnol et M.A., Mcdiarmid, R.W., Hayek, L.C., Foster, M.S., Eds., al., 2017; Muñoz-Leal et al., 2017). In Amapá state, Washington, USA, Smithsonian Institution Press. the record of A. dissimile it occurred in a study done by Dall’Agnol, B., Michel, �., Weck, B., Souza, U.A., Webster, A., Schumaker and Barros (1994), which the authors used Leal, B.F., Klafke, G.M., Martins, J.R., Ott, R., Venzal, J.M., Ferreira, C.A.S., Reck, J. (2017): Borrelia burgdorferi sensu R. marina as hosts for observations on the life cycle of lato in Ixodes longiscutatus ticks from Brazilian Pampa. �icks tick in laboratory. and �ick-borne Diseases 8: 928–932. Hence, the present study records the first occurrence Guglielmone, A.A., Nava, S. (2010): Hosts of Amblyomma of parasitism on R. major by ticks, specifically by A. dissimile Koch, 1844 and Amblyomma rotundatum Koch, 1844 dissimile, and reports again the presence of this tick in (Acari: Ixodidae). Zootaxa 2541: 27–49. the state of Amapá 24 years later. Guglielmone, A.A., Robbins, R.G., Apanaskevich, D.A., Petney, �.N., Estrada-Peña, A., Horak, I.G. (2014): �he hard ticks of the Acknowledgments. We are also grateful to Gabriel Landulfo world: (Acari: Ixodida: Ixodidae). London, Springer. 738 p. and Diego Ramirez for the comments and suggestions on the Heyer, W.R., Donnelly, M.A., McDiarmid, R.W., Hayek, L.C., manuscript. We also would like to acknowledge the Instituto Foster, M.S. (1994): Measuring and monitoring biological Chico Mendes de Conservação da Biodiversidade (ICMBio) for diversity. Standard methods for Amphibians. Washington, the collecting license (SISBIO �48102-248102-2).). Smithsonian Institution Press. Horta, M.C., Saraiva, D.G., Oliveira, G.M.B., Martins, �.F., Labruna, M.B. (2015): Rickettsia bellii in Amblyomma First record of Amblyomma dissimile infesting Rhinella major 387 rotundatum ticks parasitizing Rhinella jimi from northeastern Onofrio, V.C., Labruna, M.B., Pinter, A., Giacomin, F.G., Barros- Brazil. Microbates and Infection 17: 856–858. Battesti, D.M. (2006): Família Comentários e chaves para as Kelehear, C., Keightley, S.J., Ritzi, C.M. (2017): First Record of espécies do gênero Amblyomma., p. 56–113. In: Barros-Batestti, Amblyomma dissimile Infesting the South American Common D.M., Arzua, M., Bechara, G.H., Eds, Carrapatos de Importância �oad (Rhinella margaritifera) in French Guiana. Comparative Médico-Veterinária da Região Neotropical: um guia ilustrado Parasitology 84: 163–164. para identificação de espécies. Vox/ICTTD-3/Butantan, São Labruna, M.B., Nava, S., Marcili, A., Barbieri, A.R., Nunes, P.H., Paulo. 223p. Horta, M.C., Venzal, J.M. 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