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Home , Imantodes, Imantodes cenchoa

Herpetology Notes, volume 14: 331-333 (2021) (published online on 14 February 2021)

First record of cenchoa (Linnaeus, 1758) (Reptilia: Dipsadidae) as hosts of Amblyomma dissimile (Acari: Ixodidae) in the Eastern Amazon,

Vinícius A. M. B. de Figueiredo1,*, Ercileide Silva-Santos1, Rodrigo Tavares-Pinheiro1, Hermes R. Luz2, and Carlos Eduardo Costa-Campos1

Ticks are among the most important ectoparasites of Torres et al., 2008; Lopes et al., 2010), crocodilians wildlife and can transmit a huge variety of pathogens for (Serra-Freire and Peralta, 1993; Guglielmone and their hosts (Shearer, 2010). Ticks are widely distributed Nava, 2010), turtles (Teixeira et al., 2003) and around the world and parasitize all vertebrate classes, (Aragão, 1936; Brum and Rickes, 2003; Fischer et al., from small amphibians and (Nava et al., 2007) 2009; Guglielmone and Nava, 2010; Teixeira et al., to large mammals (Jongejan and Uilenberg, 2004; 2013; Verbel-Vergara et al., 2015; Ogrzewalska et al., Dantas-Torres and Figueredo, 2006) and birds (Luz 2019). In addition, studies have reported the infection et al., 2017). The tick fauna of Brazil is currently of Rickettsia strain Colombianensi in A. dissimile in composed by 75 , 51 in the Ixodidae family, the Amazonian biome, an agent with zoonotic potential and 24 in the Argasidae family (Labruna et al., 2016; (Luz et al., 2018; Ogrzewalska et al., 2019). Dall’Agnol et al., 2017; Muñoz-Leal et al., 2017; 2018; (Linnaeus, 1758) is an arboreal Dantas-Torres et al., 2019) of these, most belong to the and elongate widely distributed throughout Amblyomma (Evans et al., 2000; Teixeira et al., , from the tropical region of the island 2003; Onofrio et al., 2006). of Trinidad through , , , The genus Amblyomma contains 136 recognised , Guyana, Suriname, and species, 57 of these are endemic to the Neotropics and to Brazil (Cunha and Nascimento, 1978). 33 to Brazil (Guglielmone and Nava, 2010; Krawczak This species is oviparous and feeds on small frogs et al., 2015; Martins et al., 2019). Although most species and lizards during the night on bromeliads, shrubs or of ticks of this genus have a preference for birds and in the underbrush (Robinson, 1977; Zug et al., 1979). mammals as hosts, two species are exclusive to reptiles During the day, it may be found hidden in bromeliads and amphibians (Voltzit, 2007; Guglielmone and Nava, 2010). Amblyomma dissimile is a common tick parasitizing reptiles and amphibians throughout all its distribution range (Freitas et al., 2004; Guglielmone and Nava, 2010). This species has been well reported to parasitize amphibians (Schumaker and Barros, 1994; Kelehear et al., 2007; Guglielmone and Nava, 2010; Luz et al., 2018), lizards (Freitas et al., 2004; Dantas-

1 Universidade Federal do Amapá, Departamento de Ciências Biológicas e da Saúde, Laboratório de Herpetologia, Campus Marco Zero do Equador, 68.903-419, Macapá, AP, Brazil. 2 Programa de Pós Graduação em Biotecnologia do RENORBIO, Ponto Focal Maranhão, Universidade Federal do Maranhão. * Corresponding author. E-mail: [email protected] Figure 1. I. cenchoa collected with the A. dissimile attached to © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. its dorsum. Photo: Rodrigo Tavares. 332 Vinícius A. M. B. de Figueiredo et al.

(Henderson and Nickerson, 1976), where it may feed on guia ilustrado para identificação de espécies. São Paulo, Instituto sleeping lizards and lizard eggs (Landry et al., 1966). Butantan 1: 53. Based on literature records, Imantodes cenchoa has Cunha, O.R., Nascimento, F.P. (1978): Ofídios da Amazônia X - As cobras da região leste do Pará. Publicações Avulsas do Museu never been reported as a host of A. dissimile; thus, Paraense Emilio Goeldi 32: 1–218. we here present the first record of this tick species Dall’Agnol, B., Michel, T., Weck, B., Souza, U.A., Webster, A., parasitizing on the Blunthead Tree Snake I. cenchoa in Leal, B.F., Klafke, G.M., Martins, J.R., Ott, R., Venzal, J.M., the Eastern Amazon, Amapá state. Ferreira, C.A.S., Reck, J. (2017): Borrelia burgdorferi sensu During field work performed on the 2nd January 2019 lato in Ixodes longiscutatus ticks from Brazilian Pampa. Ticks at 20:15 h, in the municipality of Macapá (0.0315ºN, and Tick-Borne Diseases 8: 928–932. Dantas-Torres, F., Figueredo, L.A. (2006): Canine babesiosis: A 51.1025ºW; Datum: WGS 84), Amapá, Brazil, we Brazilian perspective. Veterinary Parasitology 141: 197–203. found a specimen of I. cenchoa perched on a branch 1 Dantas-Torres, F., Oliveira-Filho, E.F., Soares, F.A.M., Souza, m above the ground. The snake was visually examined B.O.F., Valença, R.B.P., Sá, F.B. (2008): Ticks infesting for the presence of ectoparasites and an adult tick amphibians and reptiles in Pernambuco, Northeastern was found attached to its dorsal region (Figure 1). Brazil. Revista Brasileira de Parasitologia Veterinária 17: 218– 221. We removed the tick with the aid of a clip and then Dantas-Torres, F., Martins, T.F., Muñoz-Leal, S., Onofrio, V.C., released the snake. The engorged tick was collected, Barros-Battesti, D.M. (2019): Ticks (Ixodida: Argasidae, preserved in 70% ethanol and sent to the laboratory of Ixodidae) of Brazil: Update species checklist and taxonomic Acarology of the Federal University of Maranhão for keys. Ticks and Tick Borne Diseases 10: 101252. subsequent identification by Dr. Hermes R. Luz. We Evans, D.E., Martins, J.R., Guglielmone, A.A. (2000): A review of identified the tick as a female of A. dissimile following the ticks (Acari, Ixodida) of Brazil, their hosts and geographic distribution - 1. The state of Rio Grande do Sul, southern Brazil. morphological characteristics of Barros-Battesti et al. Memórias do Instituto Oswaldo Cruz 95: 453–470. (2006) and Luz et al. (2018). According to Guglielmone Fischer, C.D.B., Mottin, V.D., Heerdt, M., et al (2009): Amblyomma and Nava (2010), A. dissimile has been reported to be dissimile (Acari: Ixodidae) em Hydrodynastes gigas (: a parasite of 101 vertebrate species. Among these, the ) no estado Mato Grosso do Sul, Brasil-Nota Prévia. 69 reptiles known as hosts of this tick do not include Brazilian Journal of Veterinary Research and Science I. cenchoa or other dipsadidae snakes. However, Torres 46: 400–403. Freitas, L.H.T., Faccini, J.L.H., Daemon, E., Prata, M.C.A., et al. (2018) reported some snakes which include Barros-Battesti, D.M. (2004): Experimental infestation with dipsadidae individuals. I. cenchoa is abundant in natural the immatures of Amblyomma dissimile Koch, 1844 (Acari: and anthropogenic areas, representing a potential host Ixodidae) on Tropidurus torquatus (Lacertilia: Iguanidae) for ticks of the genus Amblyomma. Ogrzewalska et al. and Oryctolagus cuniculus. Arquivos Brasileiros de Medicina (2019) analysed a total of 17 snake specimens obtained Veterinária e Zootecnia 56: 126–129. from four Brazilian states and A. dissimile (four larvae, Guglielmone, A.A., Nava, S. (2010): Hosts of Amblyomma dissimile Koch, 1844 and Amblyomma rotundatum Koch, 1844 16 nymphs, 40 adults) were collected only in Boa (Acari: Ixodidae). Zootaxa 2541: 27–49. constrictor and Bothrops atrox, both in the Amazonia Henderson, R.W., Nickerson, M.A. (1976): Observations on the biome. behavioral ecology of three species of Imantodes (Reptilia, Serpentes, Colubridae). Journal of Herpetology 10: 205–210. Acknowledgments. We would like to thank Dr. Diego Garcia Jongejan, F., Uilenberg, G. (2004): The global importance of ticks. Ramirez for providing the pre-peer review of this manuscript Parasitology 129: 3–14. and helpful comments. We thank the Instituto Chico Mendes Krawczak, F.S., Martins, T.F., Oliveira, C.S., Binder, L.C., de Conservação da Biodiversidade (ICMBio) for providing Costa, F.B., Nunes, P.H., Gregori, F., Labruna, M.B. collection permits (SISBIO/48102-2) (2015): Amblyomma yucumense n. sp. (Acari: Ixodidae), a Parasite of Wild Mammals in Southern Brazil. Journal of References Medical Entomology 52: 28–37. Kelehear, C., Keightley, S.J., Ritzi, C.M. (2017): First Record of Aragão, H.B. (1936): Ixodidas brasileiros e de alguns paizes Amblyomma dissimile Infesting the South American Common limitrophes. Memórias do Instituto Oswaldo Cruz 31: 759–843. Toad (Rhinella margaritifera) in French Guiana. Comparative Brum, J.G.W, Rickes, E.M. (2003): Amblyomma dissimile koch, Parasitology 84: 163–164. 1844 (Acari: Ixodidae) em serpente Sucuri (Eunectes murinus) Labruna, M.B., Nava, S., Marcili, A., Barbieri, A.R., Nunes, P.H., (Reptilia: Boidae) no Parque Zoológico do Rio Grande do Sul. Horta, M.C., Venzal, J.M. (2016): A new argasid tick species Arquivos do Instituto Biológico 70: 215–216. (Acari: Argasidae) associated with the rock cavy, Kerodon Barros-Battesti, D.M., Arzua, M., Bechara, G.H. (2006): Carrapatos rupestris Wied-Neuwied (Rodentia: Caviidae), in a semiarid de importância médico-veterinária da Região Neotropical: um region of Brazil. Parasites and Vectors 9: 511. First record of Imantodes cenchoa as hosts of Amblyomma dissimile, Brazil 333

Landry, M.J., Langebartel, D.A., Moll, E.O., Smith, H.M. (1966): Onofrio, V.C. (2007). Revisão do gênero Amblyomma Koch, 1844 A collection of snakes from Volcan Tacana, Chiapas, Mexico. (Acari: Ixodidae) no Brasil. 80 p. Journal of the Ohio Herpetological Society 5: 93–101. Onofrio, V.C., Labruna, M.B., Pinter, A., Giacomin, F.G., Barros- Lopes, S.G., Andrade, G.V., Costa-Júnior, L.M. (2010): A first Battesti, D. (2006): Comentários E Chaves Para As Espécies Do record of Amblyomma dissimile (Acari: Ixodidae) parasitizing Gênero Amblyomma. In: Vox, p. 53–113. the lizard Ameiva ameiva (Teiidae) in Brazil. Revista Brasileira Robinson, D.C. (1977): Herpetofauna bromelícola costarricense de Parasitologia Veterinária 19: 262–264. y renacuajos de Hyla picadoi Dunn, Historia Natural de Costa Luz, H.R., Silva Santos, E., Costa-Campos, S.E., Acosta, I., Rica. Museo Nacional de 1: 31–43. Martins, T.F., Muñoz-Leal, S., McIntosh, D., Faccini, J.L.H., Schumaker, Teresinha Tizu Sato; Barros, Darci Moraes. Notes on Labruna, M.B. (2018): Detection of Rickettsia spp. in ticks the biology of Amblyomma dissimile Kock, 1844 (Acari: Ixodida) parasitizing toads (Rhinella marina) in the northern Brazilian on Bufo marinus (Linnaeus, 1758) from Brazil. Memórias do Amazon. Experimental and Applied Acarology 75: 309–318. Instituto Oswaldo Cruz 89: 29–31. Luz, H.R., Faccini, J.L.H., McIntosh, D. (2017): Molecular Serra-freire, N.M., Peralta, A.S.L (1993): Primeiro registro do analyses reveal an abundant diversity of ticks and rickettsial parasitismo de Caiman crocodilus crocodilus por Amblyomma agents associated with wild birds in two regions of primary dissimile no Brasil. Revista Brasileira de Parasitologia Brazilian Atlantic Rainforest. Ticks and Tick-Borne Diseases 8: Veterinária 7: 105–108. 657–665. Shearer, P. (2010): Tick literature review. Bark. Available at: http:// Martins, T.F., Luz, H.R., Muñoz-Leal, S., Ramirez, D.G., Milanelo, www.banfield.com/veterinary-professionals/resources/research/ L., Marques, S. et al. (2019): A new species of Amblyomma white-pape. Accessed on 8 May 2019. (Acari: Ixodidae) associated with monkeys and passerines of the Teixeira, R., Amorim, M., Gazeta, G., Serra-Freire, N. (2003): Atlantic rainforest Biome, southeastern Brazil. Ticks and Tick- Ixodofauna de répteis cativos no Zoológico de Sorocaba, São borne Diseases 10: 1–10. Paulo, Brasil. Entomologia y Vectores 10: 319–329. Muñoz-Leal, S., Toledo, L.F., Venzal, J.M., Marcili, A., Martins, Verbel-Vergara, D.E., Bejarano, E.E., Paternina, L.E. (2015): First T.F., Acosta, I.C., Pinter, A., Labruna, M.B. (2017): Description report of Amblyomma dissimile (Acari: Ixodidae) on Spilotes of a new soft tick species (Acari: Argasidae: Ornithodoros) pullatus (Squamata: Colubridae) from Colombia. Revista de associated with stream-breeding frogs (Anura: Cycloramphidae: Investigaciones en Medicina Tropical 1: 23–25. Cycloramphus) in Brazil. Ticks and Tick-Borne Diseases 8: Voltzit, O.V. (2007): A review of Neotropical Amblyomma species 682–692. (Acari: Ixodidae). Acarina 15: 3–134. Muñoz-Leal, S., Faccini, A.A.M., Costa, F.B., Marcili, A., Zug, G.R., Hedges, S.B., Sukel, S. (1979): Variation in reproductive Mesquita, E.T.K.C., Marques, E.P.J, Labruna, M.B. (2018): parameters of three Neotropical snakes, Coniophanes fissidens, Isolation and molecular characterization of a relapsing Dipsas catesbyi, and Imantodes cenchoa. Smithsonian fever Borrelia recovered from Ornithodoros rudis in Brazil. Contribution Zoology 300: 1–20. Ticks and Tick-Borne Diseases 9: 864–871. Nava, S., Lareschi, M., Rebollo, C., Benítez Usher, C., Beati, L., Robbins, R.G., Durden, L.A., Mangold, A.J., Guglielmone, A.A. (2007): The ticks (Acari: Ixodida: Argasidae, Ixodidae) of . Annals of the Tropical Medicine and Parasitology 101: 255–270. Ogrzewalska, M., Machado, M.C., Rozental, T., Forneas, D., Cunha, L.E., de Lemos, E.R.S (2019): Microorganisms in ticks Amblyomma dissimile Koch 1844 and Amblyomma rotundatum Koch 1844 (Acari: Ixodidae) collected on snakes (Reptilia: Squamata: Serpentes) in Brazil. Medical and Veterinary Entomology 33: 154–161.

Accepted by Michael Jowers