Herpetology Notes, volume 12: 981-985 (2019) (published online on 10 October 2019)

Parasitism by Amblyomma rotundatum (Acari: Ixodidae) on diptycha (Anura: Bufonidae) in the Atlantic Forest: geographic expansion of species interactions

Daniela Neris Nossa1,2, Leticia Coutinho Sangy Dias2, Igor Cunha Lima Acosta3,4, Thiago Fernandes Martins3, and Ana Carolina Srbek-Araujo1,2,5,6,*

Host-parasite interactions between ticks and wild humans (Nava et al., 2017; Guglielmone and Robbins, species are fundamentally important for examining 2018). Unlike the other ticks in the family Ixodidae, A. the ecology and distribution of ticks, as well as the rotundatum reproduces by parthenogenesis and, despite consequences of those interactions for the hosts and Labruna et al. (2005) reported the presence of a male diseases (Horta et al., 2011). Ticks are also very individual, the significance of males in the life cycle of important in veterinary and human medicine as vectors this species remains unknown. of several microorganisms and pathogens, such as Amblyomma rotundatum commonly infests cold- viruses, bacteria and protozoa, that may be transmitted blooded vertebrates (Rodrigues et al., 2010; Guglielmone to humans and other , often causing serious et al., 2014) and parasitism by A. rotundatum has been diseases (Massard and Fonseca, 2004). reported in several representatives of the neotropical Amblyomma rotundatum (Koch 1844) is a tick of the herpetofauna, such as , lizards, turtles and family Ixodidae, which is a family composed of obligate crocodilian species (Table 1). hematophagous ectoparasites that feed on a wide variety Here we report on parasitism by A. rotundatum of wild animals and rarely on domestic animals and on the Cururu (Cope, 1862; previously Rhinella schneideri and Bufo paracnemis - Lavilla and Brusquetti, 2018; Figure 1) in the Reserva Natural Vale (RNV - Vale Natural Reserve; -19.0211ºS, -40.0717ºW, and -19.2536ºS, -39.8686ºW), located in the municipality of Linhares, in the northern portion 1 Programa de Pós-graduação em Ciência , Universidade of the state of Espírito Santo, southeastern Brazil. Two Vila Velha (UVV), Rua Comissário José Dantas de Melo, n° 21, Bairro Boa Vista, CEP 29.102-920, Vila Velha, Espírito free-living adult R. diptycha were captured by hand in Santo, Brazil. the RNV (27 January 2016 and 20 October 2016). Upon 2 Laboratório de Ecologia e Conservação de Biodiversidade, inspection of the specimens, one engorged female of Universidade Vila Velha (UVV), Vila Velha, Espírito Santo, hard tick was found parasitizing each of the hosts. Ticks Brazil. were collected (collection authorization SISBIO 21990- 3 Departamento de Medicina Veterinária Preventiva e Saúde 11) and immediately stored in 70% alcohol (ethanol) Animal, Faculdade de Medicina Veterinária e Zootecnia, for later identification. Identification was done under Universidade de São Paulo (USP), CEP 05.508-270, São Paulo, São Paulo, Brazil. a stereomicroscope, using morphological characters 4 Programa de Monitoramento da Biodiversidade Aquática following the literature (e.g. Barros-Battesti et al., na Área Ambiental I, Universidade Federal do Rio Grande 2006; Luz et al., 2018). One tick was deposited in the (FURG), Av. Itália, km 8 S/N, Campus Carreiros, CEP tick collection Coleção Nacional de Carrapatos Danilo 96.203-900, Rio Grande, Rio Grande do Sul, Brazil. Gonçalves Saraiva (CNC) at the Faculty of Veterinary 5 Programa de Pós-graduação em Ecologia de Ecossistemas, Medicine of the University of São Paulo, with voucher Universidade Vila Velha (UVV), Vila Velha, Espírito Santo, number CNC-3825. Brazil. 6 Instituto SerraDiCal de Pesquisa e Conservação, Belo The genus Amblyomma was previously found in the Horizonte, Minas Gerais, Brazil. RNV, where it is represented by the species A. naponense * Corresponding author. E-mail: [email protected] (Packard, 1869), A. oblongoguttatum Koch, 1844, A. 982 Daniela Neris Nossa et al.

Table 1. Reports of and reptiles parasitized by Amblyomma rotundatum including the location found (state or province, country)Table 1. and Reports the source of amphibians (reference). and reptiles parasitized by Amblyomma rotundatum including the location found (state or province, country) and the source (reference).

Host Location Reference Order Anura Leptodactylus pentadactylus (Laurenti, 1768) Mato Grosso, Brazil Oda et al. (2018) Rhaebo guttatus (Schneider, 1799) Mato Grosso, Brazil Oda et al. (2018) Rhinella gildae Vaz-Silva, Maciel, Bastos & Pombal, 2015 Maranhão, Brazil Alcantra et al. (2018) (Spix, 1824) Formosa, Argentina Smith et al. (2008) (Spix, 1824) Santa Catarina, Brazil Woehl Jr. (2002) São Paulo, Brazil Antonucci et al. (2012) (Stevaux, 2002) Pernambuco, Brazil Dantas-Torres et al. (2010a) Ceará, Brazil Alcantra et al. (2018) Rhinella marina (Linnaeus, 1758) Assunción, Paraguai Nava et al. (2007) Rio Grande do Norte, Brazil Ahid et al. (2009) Maranhão, Brazil Alcantra et al. (2018) Mato Grosso, Brazil Oda et al. (2018) Rhinella diptycha (Cope, 1862) Pernambuco, Brazil Santos et al. (2002) Goiás, Brazil Szabó et al. (2007) Corrientes, Argentina Smith et al. (2008) Formosa, Argentina Smith et al. (2008) Paraná, Brazil Antonucci et al. (2011) Minas Gerais, Brazil Luz et al. (2015) Order Squamata - Suborder Serpentes Boa constrictor Linnaeus, 1758 Rio Grande do Norte, Brazil Labruna et al. (2007) Pernambuco, Brazil Dantas-Torres et al. (2010a) Pernambuco, Brazil Dantas-Torres et al. (2010b) Roraima, Brazil Martins et al. (2010) Pernambuco, Brazil Horta et al. (2011) Mato Grosso, Brazil Oda et al. (2018) Bothropoides neuwiedi (Wagler, 1824) Minas Gerais, Brazil Rodrigues et al. (2010) Bothrops erythromelas Amaral, 1923 Ceará, Brazil Alcantra et al. (2018) ChironiusBothrops leucurus flavolineatus Wagler, (Boettger, 1824 1885) Ceará, Brazil Alcantra et al. (2018) Drymarchon corais (Boie, 1827) Ceará, Brazil Alcantra et al. (2018) Lygophis dilepis Cope, 1862 Ceará, Brazil Alcantra et al. (2018) Micrurus ibiboboca (Merrem, 1820) Pernambuco, Brazil Dantas-Torres et al. (2010b) Ceará, Brazil Alcantra et al. (2018) Oxyrhopus trigeminus Duméril, Bibron & Duméril, 1854 Ceará, Brazil Alcantra et al. (2018) Philodryas nattereri Steindachner, 1870 Ceará, Brazil Alcantra et al. (2018) Philodryas olfersii (Lichtenstein, 1823) Rio de Janeiro, Brazil Viana et al. (2012) Ceará, Brazil Alcantra et al. (2018) Rhinocerophis alternatus (Duméril, Bibron & Duméril, 1854) Rio Grande do Sul, Brazil Brum and Costa (2003) Xenopholis scalaris (Wucherer, 1861) Pernambuco, Brazil Alcantra et al. (2018) Order Squamata - Suborder Sauria Ameiva ameiva (Linnaeus, 1758) Rio de Janeiro, Brazil Viana et al. (2012) Iguana iguana (Linnaeus, 1758) Paraíba, Brazil Dantas-Torres et al. (2010b) Tropidurus torquatus (Wied-Neuwied, 1820) Rio de Janeiro, Brazil Viana et al. (2012) Order Testudinata Chelonoidis carbonarius (Spix, 1824) Pernambuco, Brazil Dantas-Torres et al. (2010a) Chelonoidis denticulatus (Linnaeus, 1766) Pernambuco, Brazil Dantas-Torres et al. (2010b) Rondônia, Brazil Labruna et al. (2010) Kinosternon scorpioides (Linnaeus, 1766) Pernambuco, Brazil Dantas-Torres et al. (2010a) Order Crocodylia Caiman latirostris (Daudin, 1802) Espírito Santo, Brazil Acosta et al. (2019) Paleosuchus palpebrosus (Cuvier, 1807) Mato Grosso do Sul, Brazil Morais et al. (2010)

Parasitism by Amblyomma rotundatum on Rhinella diptycha in the Atlantic Forest 983

Figure 1. Rhinella diptycha parasitized by Amblyomma rotundatum (A) in the Reserva Natural Vale, northern portion of the state of Espírito Santo, south-eastern Brazil, and detail of the parasite before (B) and after preservation in 70% alcohol (C).

brasiliense Aragão, 1908 and A. humerale Koch, 1844 Acknowledgements. We thank Vale S.A./Instituto Ambiental (Ogrzewalska et al., 2007). With our report, both A. Vale for the support in field activities. D.N. Nossa thanks the rotundatum in the RNV and parasitizing R. diptycha Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) for the postgraduate scholarship (Finance are first records in the reserve and regionally. Previous Code 001). A.C. Srbek-Araujo thanks the Fundação de Amparo records of A. rotundatum parasitizing R. diptycha are à Pesquisa e Inovação do Espírito Santo (FAPES 0607/2015) from northern Argentina (provinces of Corrientes and which sponsored the research of the Laboratório de Ecologia Formosa; Smith et al., 2008), and in the Brazilian e Conservação de Biodiversidade (LECBio - UVV). James J. states of Paraná (Terra Rica; Antonucci et al., 2011), Roper reviewed the English. Minas Gerais (Três Marias; Luz et al., 2015), Goiás (Araguapaz; Szabó et al., 2007) and Pernambuco (São References Lourenço da Mata; Santos et al., 2002). These Brazilian Acosta, I.C.L., Martins, T.F., Nóbrega, Y.C., Mantovani, T.C., records are in the south, south-eastern, central-western Silva-Soares, T., Santos, M.R.D., Tadokoro, C.E., Labruna, M.B. and north-eastern regions, respectively. Thus, with our (2019): First record of Amblyomma rotundatum Koch, 1844 (Acari: Ixodidae) parasitizing wild Caiman latirostris (Reptilia: findings, we provide the first records of A. rotundatum Crocodylidae) in the Atlantic rainforest biome, Southeastern on R. diptycha in the eastern Brazilian state of Espírito Brazil. Herpetology Notes 12: 9–11. Santo, and thereby increase the geographic range of Ahid; S.M.M., Fonseca, Z.A.A.S., Ferreira, C.G.T., Martins, T.F., tick-host interactions involving the genus Amblyomma. Oliveira, M.F. (2009): Parasitismo de Amblyomma rotundatum 984 Daniela Neris Nossa et al.

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Accepted by Christoph Liedtke