Helminths and Pentastomida of Two Synanthropic Gecko Lizards, Hemidactylus Mabouia and Phyllopezus Pollicaris, in an Urban Area in Northeastern Brazil

Helminths and pentastomids were examined in exotic Hemidactylus mabouia and native Phyllopezus pollicaris lizards, living synanthropically in an urban area in the municipality of Crato, Ceará state, northeastern Brazil. A total of 194 lizards were collected, being 76 specimens of H. mabouia e 118 specimens of P. pollicaris. Six parasite species were found infecting H. mabouia: the cestode Oochoristica sp., the nematodes Parapharyngodon sceleratus, Physaloptera retusa, Physalopteroides venancioi, and Spauligodon oxkutzcabiensis and the pentastomid Raillietiella mottae; while four parasite species were found associated with P. pollicaris: Oochoristica sp., P. sceleratus, P. retusa, and S. oxkutzcabiensis. Three new host records were reported: P. retusa infecting H. mabouia and P. retusa and Oochoristica sp. infecting P. pollicaris. About 75% of the parasites species found were shared by both lizards. Moreover, H. mabouia showed greater diversity than P. pollicaris (6 versus 4 species), while P. pollicaris had higher intensity of infection than H. mabouia (1536 versus 121 specimens). Helmintos e pentastomídeos de dois lagartos sinantrópicos, Hemidactylus mabouia e Phyllopezus pollicaris, de uma area urbana da região Nordeste do Brasil Resumo Helmintos e pentastomídeos foram analisados em lagartos exóticos Hemidactylus mabouia e nativos Phyllopezus pollicaris, vivendo sinantropicamente em uma área urbana da cidade de Crato, Estado do Ceará, Nordeste do Brasil.

The present study: (i) describes and identifies the macro endoparasitic fauna infecting the exotic lizard species H. mabouia and the native P. pollicaris that inhabit human habitations synanthropically, and (ii) compared the infection rates of host species.

Material and Methods
Lizard specimens were collected between March and November/2011 in human habitations in the municipality of Crato (07°14' S and 39°24' W), Ceará State, semi-arid region of northeastern Brazil.The regional climate is predominantly tropical, hot, and semi-arid (temperatures varying from 20 °C to 34 °C, and average annual varying from 24 °C to 26°C) (IPECE, 2011).
Lizards were collected manually, euthanized with lethal doses of lidocaine 2%, fixed in 10% formaldehyde, and preserved in 70% ethanol.The snout-vent length (SVL) of each lizard was measured using a digital caliper (± 0.01 mm).Lizards were weighed by Pesola® spring scales (precision: 0.1g).Host specimens were deposited in the Coleção Herpetológica of the Universidade Regional do Cariri -URCA.The body cavities of the lizards were exposed by making a longitudinal incision from the neck to the cloaca, and their lungs and digestive tracts were removed and examined for endoparasites using a stereomicroscope.For identification, pentastomids were cleared using Hoyer's solution; nematodes were cleared in lactophenol; and the cestodes were stained with Carmim, dehydrated in an increasing alcohol series and cleared in creosote.The cestodes, nematodes and pentastomids were mounted on temporary slides for identification.Voucher parasite specimens were subsequently deposited in the Coleção parasitological at URCA.
Prevalence (lizards infected/total number of lizards examined x 100), mean intensity of infection (number of parasites/number of infected hosts) were calculated according to Bush et al. (1997).Sorensen's similarity index (range 0 = no similarity, to 1.0 = identical) were calculated for the communities of parasites infecting H. mabouia and P. pollicaris, not considering juvenile parasites.
A Mann Whitney U test was performed to determine differences in the size (SVL) of male and female hosts and check for differences in parasite abundance between the sexes.To check variations in prevalence and intensity of infection between the two species of lizards we used a Z test and a T test, respectively.
Four parasite species were found associated with P. pollicaris: Oochoristica sp., Parapharyngodon sceleratus, Physaloptera retusa, and Spauligodon oxkutzcabiensis (Table 1).Of the 118 specimens of P. pollicaris collected, 58 were infected with one or more parasite (overall prevalence of 49.15%).The prevalence of adult host males was 65.9%, and that of adult females was 70.3%; the prevalence of juveniles was 30%.The overall intensity of infection was 19.25 ± 23.52.
There were no significant differences in the prevalence between H. mabouia and P. pollicaris (Z= 0.63; P = 0.4) and Sorensen index comparing the endoparasite faunas of the two hosts was 0.75 (75%).However, there significant difference in the mean intensity of infection (U=497; Z ajusted =3.82; P< 0.001) between the two lizard species studied.

Discussion
By invading and colonizing new environments, individuals of H. mabouia will encounter new food resources that are intermediate hosts for parasites that differ from those of their African origin.Thus, H. mabouia appeared to be able to rid itself of its original gastrointestinal parasites (escape-from-the-enemy hypothesis, Wolfe 2002) -but the species is then colonized by the autochthonous parasite fauna (the guest-playing-host hypothesis, Criscione and Font, 2001).Hemidactylus mabouia has, however, apparently kept some of its natural parasites (from Africa), such as the acari Geckobia hemidactyli Lawrence, 1936 and the pentastomida Raillietiella frenata (Ali, Riley and Self, 1981) during its colonization of the Caribbean region and South America (Riley et al., 1991;Anjos et al., 2007Anjos et al., , 2008)).Barton (1997) studied the endoparasites associated with a population of the toad Rhinella marina (Linnaeus, 1758) introduced into Australia and discovered that the helminth fauna of this frog had been acquired in its totality from the native fauna.The non-occurrence of exotic parasites in H. mabouia demonstrates that it has acquired endoparasites different from those present in its locality of origin -although Anjos et al. (2007Anjos et al. ( , 2008) ) reported the African pentastomida R. frenata parasitizing H. mabouia in human habitations in Barbalha municipality (about 14 km from the present study site), Ceará state.It has been experimentally demonstrated that cockroaches can serve as intermediate hosts for R. frenata (Ali and Riley, 1983;Jeffery et al., 1985), although cockroaches were not found among the food items taken by the lizards analyzed here (unpublished data).
The genus Oochoristica Lühe 1898 comprises 45 species parasitizing reptiles and mammals, and eight species have been reported parasitizing 13 lizard genera in Brazil (Ávila and Silva, 2010).In the present study, Oochoristica sp. is reported in the two lizard species examined -representing the first record of the genus infecting P. pollicaris.Oochoristica vanzolini Rego & Rodrigues, 1965 has previously been recorded infecting H. mabouia in other regions of Brazil (Ávila and Silva, 2010).Little is known about the biology of this parasite Table 1.Epidemiological data for Hemidactylus mabouia and Phyllopezus pollicaris from an urban area in Crato, Ceará state, Northeastern, Brazil.For each parasite the prevalence (P, in %), intensity of infection (mean ± standard deviation), range and the sites of infection (SI) are given.S, stomach; SI,small intestine; LI, large intestine; LU, lung.& Huey, 1970); Phyllodactylus microphyllus (Cope, 1876); and P. pollicaris (Ávila et al., 2012;Ávila and Silva, 2010).H. mabouia represents a new host of S. oxkutzcabiensis.

H. mabouia
Host biological features, such diet, foraging strategies, physiology, and contact with monoxenous parasites influence the composition, richness, and structure of their helminth communities (Aho, 1990).The cestode, pentastomid, and the two nematodes of the family Physalopteridae found here are heteroxenous and use invertebrates as intermediate hosts (Anderson, 2000).The nematodes P. sceleratus and S. oxkutzcabiensis are monoxenous, and are generally acquired by the ingestion of eggs or through transcutaneous infections by their larval stages (Anderson, 2000).According to Aho (1990), infections are more commonly caused by parasites that complete their lifecycles directly within a single individual.In the present work, a greater diversity of heteroxenous parasites were encountered than monoxenous species (4 versus 2 species), although monoxenous parasites were more abundant (1536 versus 121 parasites).
According to the Sorensen similarity index, 75% of the parasites encountered were associated with both H. mabouia and P. pollicaris.At Valinhos municipality, southeastern Brazil, H. mabouia shared most of its helminth fauna with two other sympatric lizards, Mabuya frenata (Cope, 1862) and Tropidurus itambere Rodrigues, 1987(Anjos et al. 2005).The authors also noted that H. mabouia had colonized the Neotropical region a long time ago and it was not surprising that their parasite communities were exclusively composed of local species, and very similar to those carried by sympatric lizard neighbors.
Largest (and presumably oldest) lizards tend to present higher prevalence and intensity of infection, which probably reflects their greater time of exposure to these parasites (Aho, 1990;Ribas et al., 1995).Adult H. mabouia and P. pollicaris differed significantly in size and weight, with P. pollicaris being significantly larger.Individuals of P. pollicaris had higher abundance of endoparasites (1487 parasites) than H. mabouia (170 parasites).Poulin (1997) noted that larger host species provide parasites with more space and greater niche diversities, and larger hosts also have greater chances of being exposed to parasites as they consume greater numbers of prey.However, of the four parasite species identified in P. pollicaris, two had monoxenous lifecycles and represented 97.4% of the total parasite abundance in these lizards.
The present study increases our knowledge of the parasite fauna and their lizard hosts in Ceará State and northeastern Brazil.Hemidactylus mabouia presented parasite entirely acquired from the native fauna.Hemidactylus mabouia showed greater diversity than P. pollicaris.However, P. pollicaris had higher intensity of infection than H. mabouia, showing a significant difference in the intensity of infection between the two lizards species studied.However, further studies are necessary to better understand their parasite-host interactions and the lack of relationships between the patterns of infection intensity, sex, and host size.