Pentastomids infecting an invader lizard , Hemidactylus mabouia ( Gekkonidae ) in northeastern Brazil

From January to April 2006, 37 specimens of Hemidactylus mabouia were collected in houses, in the municipality of Barbalha (7° 20’ S and 39° 18’ W), Ceará State, Northeast Brazil. Among the individuals captured, 17 were infected with pentastomids, totalling a prevalence of 45.9%, which did not differ between sexes. Host size did not influence the infection intensity. Two species of pentastomids were found: Raillietiella frenatus and R. mottae. The prevalence of R. frenatus (43.2%) was higher than R. mottae (2.7%), whereas the infection intensity of R. frenatus was comparatively lower (1.8 1.4) than R. mottae (36 parasites in a single host). Overall mean intensity of infection was 3.8 8.4 pentastomids. We found no pentastomid infecting juvenile geckos. The parameters of infection in this host population are in accordance to the findings of other studies, in which the high parasitism rate was associated to the feeding habits of geckos living in houses and buildings. Hemidactylus mabouia is a new host to R. mottae and the infection by R. frenatus is the first record of the occurrence this pentastomid species in Brazil.


Introduction
Some invader lizards of the genus Hemidactylus (Gekkonidae) have contributed to the decrease and extinction of native lizard fauna in different regions of the planet (Selcer, 1986;Dixon, 1987;Riley et al., 1988;Criscione and Font, 2001).The gecko Hemidactylus mabouia is a broadly distributed species in the tropics which invaded the New World after accidental introductions, becoming a successful colonizer widely represented in southern North America and in Central and South America (Federico and Cacivio, 2000).
Throughout its range, H. mabouia has harboured an extensive parasitic fauna composed of protozoans, platy-helminthes, acanthocephalans, nematodes, pentastomids, and mites (Ali et al., 1985;Simonsen and Sarda, 1985;Lainson and Paperna, 1999;Martínez-Rivera et al., 2003).However, few studies have been performed to evaluate to what extent this parasitic fauna was 'left behind' during the colonization process or if a subset of it was carried with their invader hosts.Recent studies have shown that Hemidactylus turcicus t and H. mabouia have played a minor role in the introduction of their exotic parasites, indeed that exotic hosts have been colonized by native fauna of parasites, as reported by Vicente et al. (1993);Hanley et al. (1995); Criscione and Font (2001); Anjos et al. (2005).However, one parasite mite, Geckobia hemidactyli, seems to have accompanied H. mabouia throughout its dispersion towards the western (Martínez-Rivera et al., 2003).
Pentastomids are common parasites of the respiratory tract of vertebrates, with more than 130 species described (Almeida and Christoffersen, 1999;2002;Rego, 1983;1984).Knowledge on infection by the pentastomid Raillietiella on geckos in the Americas is scarce, although the African pentastomids Raillietiella frenatus and R. teagueselfi were reported in the lungs of the exotic gecko Hemidactylus turcicus in Texas and Florida (USA) (Pence and Selcer, 1988;Riley et al., 1988;1991).In Central America there has been only one report of pentastomid in the lungs of H. mabouia (formerly identified as R. frenatus) in Puerto Rico (Self and Diaz, 1961).In Brazil, few works concerning raillietiellids as lizard parasites have been reported: Raillietiella freitasi in the lungs of Thrachylepis atlanticus (formerly Mabuya punctata), from Fernando de Noronha Island (situated on the northeastern coast) (Motta, 1963;Motta and Gomes, 1968;Rego, 1983;1984); larvae of Raillietiella sp. in skink Mabuya agilis reported by Vrcibradic et al. (2002); Dias et al. (2005)  In this study we evaluate pentastomid infection in a population of the exotic gecko H. mabouia living in an urban area in northeastern Brazil, specifically addressing: i) what is the composition of pentastomid fauna; and ii) to what extent do the host sex and size affect the parameters of infection (prevalence and intensity) by pentastomids.

Material and Methods
We collected 37 specimens of Hemidactylus mabouia from January through April 2006 in human buildings (houses) in the municipality of Barbalha (7°18' S and 39° 18' W, Figure 1), southern Ceará state, in Northeastern Brazil.The climate of the area is predominantly mild hot semi-arid, with a mean annual temperature varying from 24 to 26 °C and an annual rainfall of 1153 mm, with a marked rainy period from January to April and a dry season from May to December.The vegetation in the area is composed of plant species common to Caatinga, Cerrado, wet forest, and transitional zones between these adjacent biomes (IPECE, 2005).
The ecological terms in parasitology used in the present study follow Bush et al. (1997).A t-test was performed to evaluate if there was a significant difference between size (SVL) of hosts and to test for sexual differ- ences in adult lizards in terms of intensity of infection.Sexual differences in overall prevalence were tested using the Z-test for proportions (Zar, 1999).The effect of lizard host size (SVL in mm) on pentastomid lung infection rate was analysed using the Spearman rank correlation (Zar, 1999).For the estimates of the relationship between host size (SVL in mm) and intensity of infection, only the hosts parasitized by R. frenatus were included, because of the greater prevalence of this parasite and also due to the possibility of misunderstanding the interpretation of results due to the occurrence of an 'outlier' (a highly infected female -see below).
We found only two species of Pentastomida infecting H. mabouia: Raillietiella frenatus and R. mottae, which were infecting the lungs of lizards.These are the first records of occurrence of the pentastomids R. frenatus in Brazil, and H. mabouia is a new host to R. mottae.Of the 37 geckos analyzed, 17 individuals were parasitized by at least one species of pentastomid (overall prevalence of 45.9%, Table 1).The overall prevalence in adult females was 54.5% (6/11; Table 1) whereas within adult males, it was 68.8% (11/16; Table 1), but the differences among adults of the sexes was not significant (Z-test: Z c = 0.34; p = 0.730).We found no pentastomid infecting juvenile geckos.
The size of adult host lizards (SVL) did not influence the intensity of infection (r s = 0.489; p = 0.055; n = 16), but this result could be due to the low number of female hosts (r s = 0.229; p = 0.710; n = 5).

Discussion
From a historical perspective, R. frenatus probably followed the colonization movements of Hemidactylus spp.(Self and Diaz, 1961;Riley et al., 1991) whereas R. mottae seems to have been acquired in the New World, from a native lizard species, T. hispidus (Almeida et al., 2008).
Juvenile H. mabouia lizards were not infected by pentastomids.This may result from the fact that larger and probably older geckos tend to present a greater diversity of parasites, prevalence, and mean intensity of infection due to the comparatively longer time of exposition and contact with infection sources (Vogel and Bundy, 1987;Cunha-Barros et al., 2003).The diet composition of hosts also could influence these infection parameters (Rocha, 1989;Vitt, 2000;Anjos et. al., 2005).The diet of host H. mabouia juveniles usually includes only ants and termites; whereas the stomachs of adult individuals contain various types of arthropods, including larger items such as spiders, cockroaches, and moths (Almeida, present data;Rocha and Anjos, 2007).We do not know to what extent such ontogenetic differences in diet composition may favour the absence of pentastomid parasites in juvenile geckos of the population studied here.Raillietiella mottae was found in just one individual lizard host (low prevalence, 2.7%) with high infection intensity (36 pentastomids).The mean intensity of infection by Raillietiella frenatus (1.8 1.4) was similar to other mean intensity values reported for other pentastomids species in Brazil and some other lizard hosts in natural infections: 1.0 0.0 in Mabuya agilis (Vrcibradic et al., 2002); 4.5 0.0 in Cnemidophorus abaetensis (Dias et al., 2005); 1.0 0.0 in C. ocellifer (Dias et al., 2005); and 6.0 1.4 in Tropidurus hispidus (Almeida et al., 2008).However, a single host female parasitized by R. mottae presented a high intensity of infection (36 parasites) as compared with all the abovementioned other host data.We are fully aware that our small sampling does not enable us to make generalizations about the high degree of infection and consequent damage caused by R. mottae in H. mabouia in Brazil.
Although the prevalence between males (68.8%) and females (54.5%) did not differ, the infection intensity was higher in females (2.4 1.9) than in males (1.5 1.0).Since males and females did not differ in size, diet and habitat use, as we observed in situ, this could explain the similar prevalence between males and females.However, the difference in infection rates between males and females could be explained by inherent factors.
In Gekkonidae, particularly in house dweller species, their egg-contaminated faeces and prey items (such as cockroaches) usually result in very high prevalence and intensity of pentastomid infection (Ali and Riley, 1983;Riley et al., 1991).Thus, such trophic relationship of house geckos may explain in part the relative difference between the infection rates of H. mabouia and other sympatric lizards in northeast Brazil and very likely in other regions of this country.
It has been demonstrated experimentally that R. frenatus may utilize cockroaches as intermediate hosts (Ali and Riley, 1983;Jeffery et al., 1985;Bosch, 1986).The success in associating to new intermediate hosts might have been the keystone for R. frenatus to maintain itself in exotic hosts and would be favored due to widely distributed intermediate hosts like cockroaches (Criscione and Font, 2001).
Pentastomids have shown to be regulator parasites of lizard populations (Riley et al., 1991).The way exotic pentastomids act on native lizards and their potential host regulatory capacity upon exotic gecko populations deserves further studies.Our understanding of these questions may contribute to the adaptive success and establishment of this exotic lizard and consequently its regulatory process.

Figure 1 .
Figure 1.Location of the study area in Northeastern Brazil.The municipality of Barbalha (Ceará) is indicated by the black dot.