Acari of lizards from Atlantic Forest in northeastern Brazil

Although mites are often associated with reptiles, there is little information available about parasites of lizards in Brazil. The aim of this study was to identify the ectoparasites of the lizards Kentropyx calcarata (Squamata: Teiidae), Hemidactylus mabouia (Squamata: Gekkonidae) and Tropidurus hispidus (Squamata: Tropiduridae) from northeastern Brazil. The lizards were captured during the dry season at Mata de Tejipió, a fragment of Atlantic Forest, located in the municipality of Recife, state of Pernambuco, northeastern Brazil. Eutrombicula sp. (Acari: Trombiculidae), Geckobia hemidactyli and Geckobiella harrisi (Acari: Pterygosomatidae) were found associated with adult lizards of K. calcarata, H. mabouia, and T. hispidus, respectively. Mites were found in skin folds of the throat and post femoral regions (Eutrombicula sp.), “mite-pockets” (G. harrisi); and in axillary, dorsal, ventral and pelvic regions (G. hemidactyli). In Brazil, this study widens the known geographical distribution of Geckobiella harrisi on T. hispidus and G. hemidactyli on H. mabouia. In addition, K. calcarata is recorded as a new host of Eutrombicula sp. These findings show the importance of ectoparasites as a tool for ecological and biogeographic studies.

The lizard Kentropyx calcarata Spix 1825 (Squamata, Teiidae) has a wide distribution in forested habitats in the Amazon and the Atlantic Forest (Avila-Pires, 1995), but it can also be associated with forest edge (Morato et al. 2011) and disturbed areas (Prudente et al. 2013).Hemidactylus mabouia (Moreau de Jonnès 1818) (Squamata, Gekkonidae) is an exotic species of lizard from Africa, without micro-environmental specificity that shows a close relationship with anthropic and perianthropic environments and occupies microhabitats, such buildings (Vrcibradic et al. 2011).Tropidurus hispidus (Spix 1825) (Squamata, Tropiduridae) is found in open areas but it can also be associated with forest edge (Morato et al. 2011) or be a generalist regarding to its habitat (Van Sluys et al. 2004;Miranda et al. 2012).This species is in constant contact with human inhabited areas (Vitt et al. 2008).
In the current study, we documented mites infesting free-living lizards K. calcarata, T. hispidus and H. mabouia in a fragment of the Brazilian Atlantic Forest.This study was developed at Mata de Tejipió (08°05'45.59"S;34°57'04.91"W),a fragment of Atlantic Forest located in the municipality of Recife, state of Pernambuco, northeastern Brazil.The area has 172 ha of tropical rain forest in secondary stages of regeneration (Feitosa, 2004), including areas of buildings reserved for military activities.The capture of the lizards occurred during the dry season, with the use of pitfall traps, drift fences and by active search, authorized by Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio N o 31795-1) and approved by Comitê de Ética e Experimentação Animal da Universidade Federal Rural de Pernambuco (CEUA-UFRPE N o 064/2013).
Captured lizards were restrained manually, examined visually, and all detected ectoparasites were collected and preserved in 70% ethanol.The anatomical sites occupied by ectoparasites were recorded.Lizards were released at the same locations of the captures.
Little information is available about the parasites of lizards in Brazil, particularly in the northeast region.The infestation prevalence recorded in this study is lower than reported in other studies with lizards of different habitats from Brazil (Cunha-Barros and Introduction and establishment of exotic vertebrate parasites into any new environment usually leads to increased abundance and diversity of the local parasite fauna, resulting in the introduction of pathogens that could impact the health of local wildlife, domestic animals, and humans (Corn et al. 2011).This is the first record of natural infestation by G. hemidactyli on H. mabouia in northeastern Brazil.According to Martínez-Rivera et al. (2003) these findings serve as evidence for the importance of ectoparasites as a tool for biogeographic and ecological studies.
In the American continent, the genus Geckobiella includes eleven species identified as lizard parasites with main hosts being the families Iguanidae, Phrynosomatidae and Tropiduridae (Paredes-León et al. 2012).In Brazil, the first record of Geckobiella harrisi was made by Davidson (1958) in a tropidurid lizard of the species Plica plica (Linnaeus, 1758) from the state of Pará.Delfino et al. (2011) reported the occurrence of Geckobiella sp. on T. hispidus from Ceará state.Geographic distribution of G. harrisi in Brazil is now extended to Pernambuco state.
In other studies, chiggers were found in axillary, ventral and dorsal regions, tail, and cloaca (Cunha-Barros and Rocha, 2000;Delfino et al. 2011) and the main infestation sites were the mite-pockets and post femoral region in different species of lizards (Carvalho et al. 2006;Rocha et al. 2008;Delfino et al. 2011).Apparently mite-pockets restrict the distribution of chiggers on the lizard's body, reducing damage (Bauer et al. 1990).In the present study, G. harrisi was found in the mitepockets, although pterygosomatids are not usually found in this site (Delfino et al. 2011).According to Fajfer (2012), despite living under the lizard scales, pterygosomatids may also occur in "pocket-like structures" and in completely unprotected sites on the host's body.Imbricate scales and the presence and morphology of mite-pockets influence ectoparasitism in lizards (Cunha-Barros and Rocha, 2000;Bertrand and Modrý, 2004;Carvalho et al. 2006;Menezes et al. 2011).The pattern of scales is very characteristic in K. calcarata and mite-pockets are absent.Mites of lizards can occupy a wide range of parasitic niches and most species are very specific of the location in their host (Fajfer, 2012).In the study made by Delfino et al. (2011), Geckobiella sp.occurred uniformly under the scales throughout the body of T. hispidus, and mite species was found on same host specimen as E. alfreddugesi although they did not occupy the same infestation site.Geckobia hemidactyli was found in specimens of H. mabouia on the ventral surface, axilla, groin and tail (Martínez-Rivera et al. 2003).In adult lizards, mites are particularly abundant on body parts that come in contact during mating (ventral and dorsal surface, axilla, groin and tail) facilitating the transmission (Martínez-Rivera et al. 2003).
According to Martínez-Rivera et al. (2003), sexual contact or other prolonged and direct physical interaction is the most likely way for a host to acquire Geckobia mites.Mites and ticks are vectors of several infectious diseases and may cause direct impact (dermatitis and anemia) on the health of the lizards (Fajfer, 2012).Despite this, parasitized lizards studied here did not present any evidence of skin damage due to external parasites.E. alfreddugesi has previously been found on humans (Clopton and Gold, 1993) and infested lizards may be part of its natural life cycle.Further research of mite infestations in lizards in Brazil is needed to understand the life cycle of these mites and the potential role of lizards as reservoirs of mites infesting humans.The results obtained show the importance of considering the host and parasite relationship as a relevant study tool, since it is possible to evidence patterns of historical biogeography, as well as morphological, physiological and ecological factors determining species distribution.

Figure 1 .
Figure 1.Light microscopy photographs of the mite specimens found infesting lizards in the Atlantic Forest, northeastern Brazil.Geckobia hemidactyli (A and B); Eutrombicula sp.(C and D) and Geckobiella harrisi (E).