Helminth parasites of Phyllodactylidae and Gekkonidae lizards in a Caatinga ecological station , northeastern Brazil

We investigated the parasites of five lizard species belonging to Phyllodactylidae (Phyllopezus pollicaris and Gymnodactylus geckoides) and Gekkonidae (Hemidactylus agrius, Lygodactylus klugei and Hemidactylus brasilianus) families in a semiarid region of Brazil. Six nematode species were identified: Parapharyngodon alvarengai and Spauligodon oxkutzcabiensis (Pharyngodonidae), Physaloptera lutzi (Physalopteridae), Skrjabinelazia intermedia (Seuratidae), Trichospirura sp. (Rhabdochonidae) and Piratuba sp. (Onchocercidae), and a cestode species, Oochoristica sp. (Linstowiidae). The most prevalent species were Spauligodon oxkutzcabiensis, which infected P. pollicaris (75%), and Parapharyngodon alvarengai, which infected G. geckoides (29%). South American lizards were identified as being new hosts for the Trichospirura genus (a usual parasite of mammals), and there were 16 new occurrences of parasite species in the five lizard species studied herein.

Parasites are good indicators of healthy ecosystems, which is essential to studies of conservation and maintenance of host populations (Marcogliese 2004(Marcogliese , 2005)), which may reflect the anthropic influence in the environment in which they reside (Hamman et al. 2006b).Thus, characterization of the parasite population of a certain area of the Caatinga biome is essential, especially for future studies on species conservation.
The current study characterizes the helminth richness of parasitic species and the parameters of parasitic infection (prevalence, mean intensity of infection and range) in lizards of the Phyllodactylidae and Gekkonidae families collected at the Aiuaba Ecological Station, northeastern Brazil.
We conducted manual collections through active searching over four sampling expeditions, two in 2014 (September and November) and two in 2015 (February and April) with authorization provided by the "Sistema de Autorização e Informação em Biodiversidade" (SISBIO order number 43753-1).The lizards were euthanized with a lidocaine lethal dose.Their snout-vent length (SVL) was measured with a digital caliper (± 0.01mm).Thereafter they were labelled, fixed with 10% formaldehyde and preserved in 70% ethyl alcohol.Lizard specimens were deposited in the Herpetological Collection of the Regional University of Cariri, municipality of Crato, state of Ceará, Brazil.The hosts were dissected under a stereomicroscope and their body cavity, lung, stomach, small intestine and large intestine was analyzed in search of helminths.The lizard's gonads were analyzed to determine their gender and sexual maturity.We considered as mature males those with developed testicles and a convoluted epididymis, and as mature females those that had vitellogenic follicles in their oviducts and/ or eggs in their ovaries.
The nematodes were cleared in a Hoyer solution and the cestodes were colored in Carmim and cleared in a Hoyer solution as well for identification (Everhart 1957).The parasites were mounted on temporary slides for identification, and their morphology was compared with specimens present in the parasitological collection of the Universidade Regional do Cariri -URCAP, and bibliographic reference on the description of the parasite species found that did not have specimens in the collection.Subsequently, they were deposited in the Parasitological Collection of the Regional University of Cariri (Appendix 1).The prevalence and the mean intensity of infection for each endoparasite species were calculated for each lizard species according to Bush et al. (1997).

Discussion
Among the parasite species identified, there were 16 new records of hosts distributed among the five lizard species sampled in this study.We found three parasite species in P. pollicaris, four in H. agrius, two in G. geckoides, six in H. brasilianus and one in L. klugei.
The Skrjabinelazia genus was found infecting geckos (Lhermitte et al. 2007;Anjos et al. 2011).Nevertheless, records for S. intermedia were restricted so far to a teid Ameivula nativo (Rocha, Bergallo & Peccinini-Seale, 1997)   Little is known about the biology of the genus Oochoristica.Most studies on the genus were limited to describe new species and record new hosts (Ávila & Silva 2010;Brito et al. 2014b;Sousa et al. 2014).Our study reports three records of hosts (P.pollicaris, H. agrius and H. brasilianus) with two new infection records for the genus Oochoristica.
Currently, there are 23 genera of helminths recognized as parasites of the lizard families Phyllodactylidae and Gekkonidae (Anjos et al. 2005;Ávila & Silva 2010;Ávila et al. 2010;Avila & Silva 2013;Brito et al. 2014a;Sousa et al. 2014;Cazorla & Morales Moreno 2015;Bezerra et al. 2016; this study); for the Caatinga biome, about 10 species of helminths have already been reported with a prevalence above 50% (Anjos et al. 2005;Avila et al. 2012;Brito et al. 2014b;Sousa et al. 2014; this study), and there were four helminth species with prevalences below 60% for deserts and coastal areas in Peru (Goldberg & Bursey 2010); two species had prevalences of 33.3% in the Brazilian Amazon forest (Ávila & Silva 2013); two species had prevalences up to 22.8% in the Atlantic Forest (Ávila et al. 2010;Almeida-Gomes et al. 2012); and three helminth species had prevalences below 15% for the tropical thorny mountain areas of Venezuela (Cazorla & Morales Moreno 2015).Notwithstanding that some genera and species of helminths were previously reported for different biomes as parasites of geckos, as S. oxkutzcabiensis and all species of the genera Oochoristica and Parapharyngodon, almost all prevalences registered for them were below that obtained for the Caatinga biome [e.g., Oochoristica sp. and species of the genus Parapharyngodon presented up to 55% prevalence, while S. oxkutzcabiensis did not exceed 8% in coastal environments of the tropical thorny mountain areas in Peru and Venezuela (Goldberg & Bursey 2010;Cazorla & Morales Moreno 2015)].These results suggest that the different environmental conditions of distinct biomes may favor one parasitic species over another, such as S. oxkutzcabiensis.The presence of Trichospirura in lizards of the genus Sceloporus in Mexico andH. brookii haitianus Meerwarth, 1901 in Hispaniola (Goldberg et al. 2003;Powell et al. 1990), suggests that the new host records documented here may not be species-specific of the studied biome.Therefore, additional studies are necessary in the different biomes to determine the true helminth diversity of these two families of lizards.
The current study increases to 16 the number of new host records in association with the families Phyllodactylidae and Gekkonidae in the Caatinga biome.However, the development of new research on other areas of the biome is essential to enhance our scientific knowledge of the diversity of helminths associated with lizards.

Table 1 .
Helminth parasites collected in lizards belonging to Phyllodactylidae and Gekkonidae families from the Aiuaba Ecological Station, municipality of Aiuaba, state of Ceará, northeastern Brazil.Number of Infected hosts = (NI), Prevalence = P (%), Mean Intensity of Infection = MII and Range (R).(*) New records of hosts.