Nematode Parasites of Lizards (Squamata, Sauria) from the Cerrado Biome in the State of Minas Gerais, Brazil
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Herpetology Notes, volume 12: 855-863 (2019) (published online on 12 August 2019) Nematode parasites of lizards (Squamata, Sauria) from the Cerrado biome in the State of Minas Gerais, Brazil Fabiano M. Vieira1,*, Thais T. Souza2, Iara A. Novelli2, Sueli de Souza Lima3, Luís C. Muniz-Pereira1, and Bernadete M. Sousa2 Abstract. The current study registered the nematode infections in 10 lizard species for a not studied locality in the Cerrado biome in the state of Minas Gerais, Brazil. A total of 101 hosts were analysed, of these 24 were parasitized by at least one species of nematode. We observed a total richness of 10 species of nematodes, and the lizard species with the most records of nematode species were Aspronema dorsivitattum and Ophiodes striatus, with a total of three species each. In addition, seven new host records (NHR) and nine new geographical records (NGR) were recorded in the respective lizard species of the Cerrado biome in state of Minas Gerais, Brazil. Keywords. Squamata, Cerrado, southeastern Brazil, helminth Introduction The aim of this study is to report nematode infections in lizards for a locality in the Cerrado biome in the state Helminthological surveys of lizards from the state of of Minas Gerais, until now not studied, thereby adding Minas Gerais (MG) are fragmented and scarce. Until to our knowledge of the biodiversity of helminth in the current study, 13 helminth species distributed among lizards of Brazil. only six species of lizards were reported in the state of Minas Gerais (Vicente et al., 2000a,b; Fontes et al., Materials and Methods 2003; Sousa et al., 2007; Ávila and Silva, 2010; Pereira et al., 2010, 2011, 2012a,b, 2014; Barreto-Lima et al., We examined 101 specimens from eight lizard species: 2012; Mati et al., 2013; Barreto-Lima and Anjos, 2014). Ameiva ameiva (Linnaeus, 1758) (Teiidae) (n=2); When we consider the helminthological studies with Aspronema dorsivityatum (Cope, 1862) (Mabuyidae) lizards of the Cerrado biome in this State, until current (n=28); Enyalius bilineatus Duméril & Bibron, 1837 study these data are provided by only three publications (Leiosauridae) (n=10); Heterodactylus imbricatus Spix, (Vicente et al., 2000a; Fontes et al., 2003; Sousa et al., 1825 (Gymnophthalmidae) (n=5); Notomabuya frenata 2007). (Cope, 1862) (Mabuyidae) (n=19); Ophiodes striatus (Spix, 1825) (Diploglossidae) (n=13); Tropidurus itambere Rodrigues, 1987 (Tropiduridae) (n=13); and Urostrophus vautieri Duméril & Bibron, 1837 (Leiosauridae) (n=11). Lizards were from municipality of Ingaí (Reserva do Boqueirão) (21° 20’ 47” S e 44° 59’ 1 Laboratório de Helmintos Parasitos de Vertebrados, Instituto Oswaldo Cruz, FIOCRUZ, Av. Brasil 4365, Rio de Janeiro 27” W), state of Minas Gerais. This region is inserted CEP 21040-900, Brazil. in Cerrado biome. All hosts studied were deposited at 2 Laboratório de Herpetologia - Répteis, Departamento de Coleção Herpetológica of the Universidade Federal Zoologia, Universidade Federal de Juiz de Fora – UFJF, de Juiz de Fora - Répteis (CHUFJF - Répteis), in the Rua José Lourenço Kelmer, s/n, Campus Universitário, São municipality of Juiz de Fora, Universidade Federal Pedro. CEP 36036- 900. Juiz de Fora, MG, Brazil. de Juiz de Fora, state of Minas Gerais. Lizards were 3 Laboratório de Taxonomia e Ecologia de Helmintos - Odile identified according to Jackson (1978), Peters et al. Bain, Departamento de Zoologia, Universidade Federal (1986), Rodrigues (1987) e Hedges and Conn (2012). de Juiz de Fora – UFJF, Rua José Lourenço Kelmer, s/n, Campus Universitário, São Pedro. CEP 36036- 900. Juiz de Nematodes collected were fixed in 4% cold Fora, MG, Brazil. formaldehyde solution for two weeks and posteriorly * Corresponding author. E-mail: [email protected] stored in 70°GL ethanol. For identification, the 856 Fabiano M. Vieira et al. nematodes were clarified in Amman’s lactophenol Polychrus marmoratus from the Amazon biome (Ávila and mounted in temporary slides. Parasites were and Silva, 2010); O. spinosa Bain & Sulahian, 1974 was analysed in an Olympus BX41 microscope. All reported in Mabuya mabouya from the Amazon biome nematodes were identified at generic level according (Ávila and Silva, 2010); O. petersi Bain & Sulahian, to Anderson et al. (2009). Species of Skrjabinodon 1974 was reported as parasitizing Tupinambis teguixin Inglis, 1968 (Oxyuroidea, Pharyngodonidae) were (Linnaeus, 1758) (Squamata, Teiidae) and Tropidurus identified according to Vicente et al. (2000, 2002), hispidus (Spix, 1825) of the Amazon and Caatinga and Physaloptera Rudolphi, 1819 (Physalopteroidea, biomes (Ávila and Silva, 2010); and O. belemensis Physalopteridae) according to Pereira et al. (2014). The Bain & Sulahian, 1974 was reported in Dracaena following conventions in relation to the parasite records guianensis from the Amazon biome (Ávila and Silva, are observed: NHR refers to a new host record in 2010). Previous reports of Oswaldofilaria parasitizing Brazil and NGR to a new geographical record. Voucher N. frenata and A. dorsivitattum are nonexistent (Ávila specimens of nematodes are deposited in the Coleção and Silva, 2010); therefore, this is a first report (NRH) Helmintológica do Instituto Oswaldo Cruz (CHIOC), of this nematode genus in both lizard species. Rio de Janeiro, Brazil. Superfamily Oxyuroidea Results Family Pharyngodonidae In the current study, of the total of 101 hosts analysed, 24 were parasitized by at least one species of nematode Parapharyngodon sp. (Table 1). We observed a total richness of 10 species of Hosts: E. bilineatus (NHR), T. itambere (NGR) nematodes. The lizard species with the most records of Infected hosts: E. bilineatus, 2 of 10 hosts (20%); T. nematode species were A. dorsivitattum and O. striatus, itambere 1 of 13 hosts (7.7%) with a total of three species each (Table 1). Site of infection: Intestinal caecum Voucher specimens: CHIOC 38709 Superfamily Filarioidea Remarks. Only female specimens were found; thus, Family Onchocercidae it was not possible to assign it to a species. Currently, the genus Parapharyngodon Chatterji, 1933 comprises Oswaldofilaria sp. 56 nominal species distributed in lizards throughout the Hosts: N. frenata (NHR), A. dorsivitattum (NHR) world (Bursey and Goldberg, 2015). Of the lizards from Infected hosts: N. frenata, 3 of 19 hosts (16%); A. the Neotropics, seven species of this genus are known, of dorsivitattum, 1 of 28 hosts (3.6%) which five occur in lizards from Brazil (Ávila and Silva, Site of infection: Body cavity 2010; Bursey and Goldberg, 2015). Parapharyngodon Voucher specimens: CHIOC 38712 sceleratus Travassos, 1923 was reported in lizards of Remarks. In this study, a more precise identification the genera: Ameiva, Cnemidophorus, Eurolophosaurus, of this nematode was not possible because only female Hemidactylus, Kentropyx, Liolaemus, Mabuya, specimens were found. The genus Oswaldofilaria Phyllopezus, and Tropidurus, which originate from Travassos, 1933 has approximately 15 nominal species several Brazilian biomes (Ávila and Silva, 2010). The that occur in crocodilians from Australia and Africa, and reports of this nematode species in the Cerrado biome in lizards from Australia and South America (Pereira et are restricted to T. itambere from the state of Goiás, al., 2010; Bursey et al., 2014). Of the lizards of South and to Eurolophosaurus nanuzae (Rodrigues, 1981) America, a total of eight species of this genus are (Squamata, Tropiduridae) from the state of Minas reported, of which six occur in hosts from Brazil (Ávila Gerais (Fontes et al., 2003; Ávila and Silva, 2010; Ávila and Silva, 2010; Pereira et al., 2010). Oswaldofilaria et al., 2011). Parapharyngodon alvarengai Freitas, 1957 chabaudi Pereira, Souza Lima & Bain, 2010 was was recorded in Trachylepis atlantica (Schmidt, 1945) described in Tropidurus torquatus of the Atlantic Forest (Squamata, Scincidae) (from the Fernando de Noronha in the municipality of Juiz de Fora, in the state of Minas archipelago, and in A. ameiva from the Atlantic Forest Gerais (Pereira et al., 2010); O. brevicaudata Rodhain in the state of Rio de Janeiro (Ávila and Silva, 2010). & Vuylsteke, 1937 was reported as parasitizing Iguana Parapharyngodon verrucosus Freitas & Dobbin, iguana from the Amazon and Caatinga biomes (Ávila 1959 is a parasite of Diploglossus lessonae (Peracca, and Silva, 2010); O. azevedoi Bain, 1974 is a parasite of 1890) (Squamata, Anguidae) that occurs exclusively Nematode parasites of lizards from the Cerrado biome, Minas Gerais, Brazil 857 in the Caatinga biome from the states of Pernambuco current report is the first occurrence of this nematode and Ceará (Ávila and Silva, 2010). Parapharyngodon in lizards from the Cerrado biome in the state of Minas largitor Alho & Rodrigues, 1963 was reported in A. Gerais (NGR). ameiva, Brasiliscincus agilis (Raddi, 1823) (= Mabuya agilis) (Squamata, Mabuyidae), and Hemidactylus Skrjabinodon sp. mabouia (Moreau de Jonnès, 1818) (Squamata, Host: O. striatus (NHR and NGR) Gekkonidae) of the Atlantic Forest in the states of Infected hosts: 1 of 13 hosts (7.7%) Rio de Janeiro and São Paulo (Ávila and Silva, 2010), Site of infection: Intestinal caecum and in A. dorsivitattum from the Cerrado biome in the Voucher specimens: CHIOC 38707 state of Goiás (Ávila et al., 2011). Parapharyngodon Remarks. Only female specimens were found; thus, bainae Pereira, Sousa & Souza Lima, 2011 is the most it was not possible to assign it to a species. Currently, recent species of this genus described in lizards from the genus Skrjabinodon Inglis,