Lung Infection Rates in Two Sympatric Tropiduridae Lizard Species by Pentastomids and Nematodes in Northeastern Brazil

We present data on pulmonary infection rates by parasites in the lizards Tropidurus hispidus Spix, 1825 and T. semitaeniatus (Spix, 1825) living sympatrically in the Chapada do Araripe mountain Range, northeastern Brazil. We found no parasite pulmonary infection in T. semitaeniatus. However, two pulmonary parasite species were found in the T. hispidus hosts, the pentastomid Raillietiella mottae Almeida, Freire and Lopes, 2008 and the nematode Rhabdias sp. Overall prevalence was 5%. Prevalence of R. mottae was 2.5% and corresponded to only one parasite on each infected host. Prevalence of Rhabdias sp. was 2.5% and the range of infection was 1-2 parasites per host. This represents the first record of Rhabdias infecting lizards of the family Tropiduridae in the Neotropical region. Furthermore, we present a comparison of parameters of infection by pulmonary parasites including some recent studies in Brazil. Taxas de infecção pulmonar em duas espécies simpátricas de lagartos Tropiduridae por pentastomídeos e nematódeos na região Nordeste do Brasil Resumo Apresentamos dados sobre taxas de infecção pulmonar por parasitas nos lagartos Tropidurus hispidus e T. semitaeniatus que vivem simpatricamente na encosta da Chapada do Araripe, situada na região Nordeste do Brasil. Não encontramos infecção parasitária nos pulmões dos espécimes de T. semitaeniatus. Entretanto, foram encontradas duas espécies de parasitas nos hospedeiros T. hispidus, os pentastomídeos Raillietiella mottae e os nematódeos Rhabdias sp. A preva-lência geral de infecção foi de 5%. A prevalência de infecção de R. mottae foi de 2,5% correspondendo a apenas um parasita por hospedeiro. A prevalência de infecção de Rhabdias sp. foi de 2,5% e a amplitude de infecção de 1-2 para-sitas por hospedeiros. Esses resultados compreendem o primeiro registro de Rhabdias infectando lagartos da família Tropiduridae em toda a região Neotropical. Apresentamos também uma comparação com os parâmetros de infecção pulmonar por parasitas incluindo os estudos mais recentes no Brasil.

Pentastomids and the nematode Rhabdias Stiles and Hassall, 1905 are common parasites of the respiratory tracts of vertebrates (Riley, 1986;Almeida and Christoffersen, 2002;Bursey et al., 2003).Pentastomids have been relatively poorly studied in the Neotropical region, despite its importance as a parasite of vertebrate (Almeida and Christoffersen, 2002).However, the recent reports of parasite occurrence, the new species descriptions, and the information concerning new host records have added knowledge on pentastomid-lizard interactions (Vrcibradic et al., 2002a;Dias et al., 2005;Anjos et al., 2007;2008;Almeida et al., 2008a;2008b;2009).On the other hand, reports concerning lung infections by Rhabdias have been relatively less frequent -and only an infection in the lizard Enyalius bilineatus (Duméril and Bibron, 1837) (Leiosaurinae) from an area of Atlantic Rainforest in Espírito Santo state, southeastern Brazil (Vrcibradic et al., 2007) and an infection of Norops fuscoauratus (d'Orbingy, 1837) (Polychrotidae) in northern Brazil (Goldberg et al., 2006) have been previously reported.
In the present study we provide data on pulmonary infections caused by pentastomids and nematodes species associated with two sympatric species of lizard hosts, Tropidurus hispidus Spix, 1825 and T. semitaeniatus (Spix, 1825), from northeastern Brazil.Further, our data were contrasted with the recent literature on pulmonary infection of lizards.

Materials and Methods
Field work was carried out on the lower slopes of the Chapada do Araripe Mountains (07° 16' S and 39° 26' W) within the limits of the environmental protection area (EPA) of Chapada do Araripe in the municipality of Crato, Ceará state, Brazil.The vegetation of the region comprises a mosaic of palm tree, montane forest, and secondary forests.The area has been subjected to anthropogenic alteration due to land occupation for agricultural purposes, the harvesting of natural products, and the speculation in property.The regional climate is warm, semi-arid tropical, with the mean annual temperatures ranging between 24 and 26 °C.The rainy season extends from January to May and the annual mean rainfall is 1,100 mm (IPECE, 2005).
Lizards were captured using rubber slings, nooses, or by hand.Immediately after capture each lizard was transferred to a plastic sack containing cotton embedded in ether, in order to anaesthetize and euthanize them.The snout-vent length (SVL) of the lizards was measured with a caliper (to the nearest 0.05 mm).Lizards were fixed in 10% formalin and storage in 70% alcohol.
The lungs of the lizards were removed and checked under a stereo-microscope for the presence of parasites.The parasites found were removed and preserved in 70% alcohol.For species identification, the pentastomid specimens were mounted on permanent slides in Hoyer medium, and the nematodes were fixed in situ, cleared in glycerol on a glass slide, and subsequently examined under a light microscope.

Results
A total of 99 lizards were captured.The 80 specimens of T. hispidus ranged in SVL from 41.0 to 113.0 mm (mean = 80.8 ± 18.5 mm) and the 19 specimens of T. semitaeniatus ranged from 31.0 to 77.0 mm (mean = 55.9 ± 15.7 mm).
Analysis of T. hispidus revealed that four individuals were infected by pulmonary parasites (overall prevalence was 5%).Two adult males (SVL = 95 mm and 110 mm) were infected by the pentastomid Raillietiella mottae Almeida, Freire and Lopes, 2008 (pentastomid prevalence was 2.5%; intensity of infection was one parasite in each lizard infected) while two other specimens (an adult male, SVL = 78 mm, and an adult female, SVL = 85 mm) were infected by an unidentified species of nematode Rhabdias sp.(nematode prevalence was 2.5%, range of infection was 1-2).No juvenile host was infected.Due to the low overall prevalence, ontogenetic and sexual differences could not be estimated.
There were no pulmonary parasites in the specimens of T. semitaeniatus analyzed.

Discussion
Interactions between the parasite Raillietiella mottae and the lizard host T. semitaeniatus have been studied in the Caatinga region, northeastern Brazil (Almeida et al., 2008).The absence of these parasites in the lungs of T. semitaeniatus in the present study may simply be related to the low numbers of that host sampled.These two lizard species share similar feeding resources and microhabitats (Vanzolini et al., 1980;Vitt, 1995), which would otherwise favor the acquisition of a similar parasite fauna (see Almeida et al., 2008b).
Nematode parasites of the genus Rhabdias have been little studied in Brazil and could not be identified to the species level in this study.Rhabdias has been reported in the Neotropical region in host species of the genera Anolis (Polychrotidae) (Bundy et al., 1987;Dobson et al., 1992;Bursey et al.;2003;2004), Enyalius (Leisosauridae) (Vrcibradic et al., 2007) and in Tropidurus (Tropiduridade) in the present study.Rhabdias is a parasite less frequently found in the lungs of lizards (Bursey et al., 2003).However, it is important to stress that due to the low numbers of studies on endoparasites of lizards in South America (Vrcibradic, 2007), many groups of lizard from so many distinct environments still need to be more fully investigated.The current knowledge of infections by Rhabdias in lizards in Brazil is based on two studies that reported the presence of parasites in the lizards Norops fuscoauratus (Goldberg et al., 2006) and in Enyalius bilineatus (Vrcibradic et al., 2007).The former species presented prevalence values of 1.8% and mean intensity of infection of 2.0 ± 0.0 (Goldberg et al., 2006), values somewhat similar to those found to T. hispidus (2.5%; range of infection was 1-2), in the present study.According to Vrcibradic et al. (2007), E. bilineatus showed the greatest prevalence (33.3%) and mean intensity of infection (2.0 ± 1.1).
In the present study, T. hispidus constitutes a new host for Rhabdias sp., being also the first record of this parasite species in a Tropiduridae lizard species in the Neotropical region.
The presence of the pentastomid R. mottae and the nematode Rhabdias sp. both infecting the lungs of the same host species, and with similar infection rates, suggests that these parasites can share simultaneously the same microhabitat in the host body.The low prevalence of R. mottae and Rhabdias sp. in the host species analyzed suggests that these two parasites do not represent core species in that area, and that their occurrence may be an occasional or accidental occurrence.With the development of further studies involving new hosts, we can understand the patterns of infection and the aspects of relationship between the parasites and lizards in the region of Cariri, northeastern Brazil.