Herpetology Notes, volume 8: 413-416 (published online on 12 August 2015)

Low prevalence of hemoparasites in a lizard assemblage from a coastal environment of southeastern Brazil

Leandro Talione Sabagh1,*, Vitor Nelson Teixeira Borges Júnior1, Gisele R. Winck1, Lúcio André Viana2 and Carlos Frederico Duarte Rocha1

Blood parasites of encompass haemogregarins, (Schall, 1992). However, the real virulence effects trypanosomes, microfilaria, piroplasmids, and of heamogregarines on their lizards hosts are poorly (Arikan and Çiçek, 2014). Among these, understood (Amo et al., 2005). In this study we provide the haemogregarines () are the most a first approach on the prevalence of haemogregarines common blood parasite in reptiles (Telford, 2009). in an assemblage of lizards from southeastern Brazil. Haemogregarines are often recorded in snakes (e.g. We examined lizard hosts and also potential mosquitoes O’Dwyer et al., 2003), crocodiles (e.g. Viana et al., (Culicidae) vectors. 2010b), lizards (e.g. Damas-Moreira et al., 2014) The study was conducted in December 2010 and and turtles (e.g. Soares et al., 2014). Hematophagous February 2011 at Grussaí (-21.732943°, -41.031830°), invertebrates are the main vectors of hemoparasites a coastal sand dune environment (called “restinga”), responsible for transmission between hosts (Jacobson, in the municipality of São João da Barra, state of Rio 2007), although some items composing diet may also de Janeiro, Brazil. Restingas are habitats of dunes be an important route of infection (Viana et al., 2012a). and sandy plains covered with xerophytic herbaceous Among hematophagous, the mosquitos of the family vegetation and shrubs that occur along the coast of Culicidae (Diptera) are the main potential vectors of Brazil (Eiten, 1992). The climate in Grussaí is tropical hemoparasites in snakes (e.g. Sloboda et al., 2007), subhumid and semi-arid, with mean annual rainfall crocodiles (e.g. Viana et al., 2010a), lizards (e.g. Lainson ranging from 800 up to 1,200 mm and higher rainfall et al., 2003) and turtles (e.g. Crans and Rockel, 1968). incidence during the summer (RADAMBRASIL, Parasites are known for their influence on 1983). Lizards were collected by compressed air rifles communities’ structure, both directly on the hosts and immediately dissected in the field. Samples were behaviour and/or density, and indirectly when the obtained from blood of peritoneal cavity. We made effect on hosts reflects on other interaction as two blood smears for each lizard. Thin blood smears competition and predation (Minchella and Scott, 1991; were air-dried, fixed in absolute methanol, and then Goater et al., 2013). High rates of parasite infection in stained with Giemsa. We searched for hemoparasites by lizards may influence the competitive ability of species scanning each blood smear for up to 15 min under a Carl and ultimately the composition of a lizard assemblage Zeiss binocular microscope (x400). Mosquitoes were collected with one CDC light traps during one night, one meter above ground for 12 h (18h00 pm to 6h00 am). The specimens were returned to the laboratory for dissection and identification using dichotomous keys 1 Laboratório de Ecologia de Vertebrados, Departamento de of Pecor et al. (1992), and Consoli and Lourenço-de- Ecologia, Pavilhão Haroldo Lisboa da Cunha, Universidade Oliveira (1994) for mosquitoes and Telford (2009) for do Estado do Rio de Janeiro, Rua São Francisco Xavier 524, hemoparasites. After dissections, searching for parasite Maracanã, CEP 20550-013, Rio de Janeiro, Brazil. forms was performed with microscope (x400) following 2 Laboratório de Parasitologia Veterinária, Centro de Ciências Biológicas e da Saúde, Universidade Federal do Mato Grosso Lainson et al. (2003). do Sul, Campo Grande, Mato Grosso do Sul, Brazil. We sampled a total of 128 specimens from six lizard * Corresponding author e-mail: [email protected] species: Brasiliscincus agilis (Raddi, 1823), Psychosaura 414 Leandro Talione Sabagh et al. ͳ Table 1. Lizard hosts, sample size and prevalence of hemoparasites from Restinga of Grussaí, Table 1. Lizard hosts,Rio sample de Janeiro, size andBrazil. prevalence N = sample of hemoparasitessize. * = hemococcidian from Restinga parasites of ofGrussaí, the family Rio de Janeiro, Brazil. N = sample size. * = hemococcidianͳ Lankestereliidae. parasites of **the = family Lankestereliidae. ameivae. ** = Hepatozoon ameivae. ʹ ͵ N N Prevalence Ͷ Host Total Infected (%) Gekkonidae Hemidactylus mabouia (Moreau de Jonnès, 1818) 25 0 0 Scincidae Brasiliscincus agilis (Raddi, 1823) 30 1* 3.3 Psychosaura macrorhyncha Hoge, 1946 7 0 0 Teiidae Ameiva ameiva (Linnaeus, 1758) 10 1** 10.0 Cnemidophorus littoralis Rocha et al., 2000 5 0 0 Tropiduridae Tropidurus torquatus (Wied-Neuwied, 1820) 51 3* 5.9 TOTAL 128 5 3.9

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͸ macrorhyncha Hoge, 1946, Ameiva ameiva (Linnaeus, at São Paulo State inland (Rocha-e-Silva and Rodrigues, 1758), Tropidurus torquatus (Wied-Neuwied, 1820), 1974). A study carried out in Brazilian Amazonian also Cnemidophorus littoralis Rocha et al., 2000, and the found low prevalence (5%) of Plasmodium carmelinoi exotic invasive Hemidactylus mabouia (Moreau de Lainson, Franco & da Matta, 2010 infecting Ameiva Jonnès, 1818). We found only five out of the 128 lizards ameiva (Lainson et al., 2010). However, it is possible infected with hemoparasites, representing 3.9% of to find much higher prevalence, such as Plasmodium prevalence (Table 1). We identified Hepatozoon ameivae kentropyxi Lainson, Landau & Paperna, 2001 infecting (Hepatozoidae) infecting A. ameiva. Its morphology is from 61.4% up to 79.5% individuals from populations in accordance to the original description by Carini and of Kentropyx calcarata in Pará state, northern Brazil Rudolph (1912), with intraerythrocytic gametocytes (Lainson et al., 2001). In this case, however, host lizards overlapped on the nucleus of the host cell. Hepatozoon had no apparent ill effects (Lainson et al., 2001). ameivae was described from Ameiva surinamensis (= A. Among mosquitoes, samples contained 18 specimens, ameiva) in the state of Minas Gerais, Brazil. However, all from the same morphotype of Culex (Melanoconion). due to the lack of information on its life cycle, the We did not find any parasite infecting the mosquitoes. natural history of the parasite remains unclear. A second However, we found the tick Amblyomma rotundatum parasite was an unidentified Lankesterellidae (Figure Koch, 1844 attached to individuals of A. ameiva 1) whose forms were found in Brasiliscincus agilis and T. torquatus in a previous study in the same area and Tropidurus torquatus. The lizards B. agilis and T. (Viana et al., 2012b). Ticks of the Amblyomma torquatus are here first recorded being parasitized by a spp. are known as vectors of hemoparasites to lizards Lankesterellidae, given that in Brazil the records were (Smallridge and Paperna, 1997; Lainson et al., 2003) restricted to the lizards A. ameiva (Lainson et al., 2003) and A. rotundatum has been previously recorded as and Tupinambis nigropunctatus (Landau et al., 1974). vector of hemoparasites of toads Rhinella marina The low prevalence of hemoparasites recorded in this (Linnaeus, 1758) and lizards A. ameiva (i.e. Lainson study is suggestive that hemoparasitism, even though et al., 2007). This suggests that A. rotundatum may present, may not constitute a major role affecting constitute a potential vector of hemoparasites for lizards relations among sympatric lizard species at Grussaí. at Grussaí restinga. In conclusion, the low prevalence of It has been shown that prevalence of hemoparasites hemoparasites found in lizards of Grussaí is suggestive in lizard species is somewhat variable. Some studies that this interaction does not impose a negative effect showed low prevalence, such as Plasmodium tropiduri in the individual species or in the structure of the local Aragão & Neiva, 1909 infecting Tropidurus torquatus lizard community. Furthermore, our results suggest the Low prevalence of hemoparasites in a lizard assemblage from southeastern Brazil 415

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Accepted by Vinicius Caldart