Introduction
Ecological studies of helminths associated with Brazilian lizards have recently increased (Rocha et al., Reference Rocha, Vrcibradic, Vicente and Cunha-Barros2003; Vrcibradic et al., Reference Vrcibradic, Vicente and Bursey2007), although most available data deal with lizards inhabiting the coastal sand dunes in south-eastern Brazil (Van Sluys et al., Reference Van Sluys, Rocha, Bergallo, Vrcibradic and Ribas1997; Vrcibradic et al., Reference Vrcibradic, Cunha-Barros, Vicente, Galdino, Hatano, Van Sluys and Rocha2000). Studies considering lizards from other biomes or Brazilian regions are even scarcer and restricted to descriptive and/or taxonomic surveys (Vicente et al., Reference Vicente, Van Sluys, Fontes and Kiefer2000; Durette-Desset et al., Reference Durette-Desset, Anjos and Vrcibradic2006).
The small phyllodactylid gecko Bogertia lutzae (Loveridge, 1941) is a bromelicolous species that occurs in coastal sand dunes and Atlantic Forest areas from Pernambuco state to Bahia state in north-eastern Brazil (Carvalho et al., Reference Carvalho, Vilar, Oliveira, Carvalho and Vilar2005). Available information on the ecology of this species is scarce, and no records of endoparasites infecting B. lutzae have been published. In the present study, we survey the helminth fauna associated with a population of B. lutzae from an Atlantic forest site in north-eastern Brazil.
Materials and methods
Fieldwork was conducted in the Mata da Serra da Saudinha (09°22′S, 35°45′W), a 1210 ha Atlantic Forest remnant, near the municipality of Maceió, Alagoas state, north-eastern Brazil. Lizards were collected by hand inside the bromeliads Aechmea Ruiz & Pavón, 1794 and Hohenbergia Schult 1830 (Bromeliaceae: Bromelioideae) for 2–4 days weekly, from July 2004 to December 2005. Bromeliads were located on the ground, in trees and on granitic outcrops, at the edge of and inside the forest. After capture, lizards were euthanized with a lethal injection of lidocaine, fixed with 10% formalin and preserved in 70% ethanol. Voucher specimens were deposited in the Seção Herpetologia do Setor de Zoologia, do Museu de Historia Natural da Universidade Federal de Alagoas, under the acronym MUFAL. In the laboratory, lizards were necropsied and body cavity, lungs and the gastrointestinal tract were surveyed for endoparasites. Helminths found were counted, cleared in phenol, identified and deposited in the Coleção Helmintológica do Instituto de Biociências da Universidade Estadual Paulista Júlio de Mesquita Filho, Instituto de Biociências de Botucatu, São Paulo state, Brazil, under the acronym CHIBB (4756–4768).
Prevalence was calculated as (infected lizards/examined lizards) × 100, mean intensity of infection as arithmetic mean number of worms from infected lizards and mean abundance as total number of a particular parasite divided by total number of hosts (both infected and uninfected hosts), according to Bush et al. (Reference Bush, Lafferty, Lotz and Shostak1997). The discrepancy index (D) was calculated as suggested by Poulin (Reference Poulin1993). The index has a minimum value of zero (D = 0), when all hosts harbour the same number of parasites. When all parasites are found in a single host, aggregation is maximum (D = 1). This index was calculated with the software Quantitative Parasitology 3.0 (Rózsa et al., Reference Rózsa, Reiczigel and Majoros2000).
The effect of host body size (SVL) on the intensity of infection was tested by a Pearson correlation. Differences in prevalence between the sexes were tested by Z-test for proportions. To test for differences in the intensity of infection between males and females, Mann–Whitney U-tests were performed. Throughout the text means are ± 1 standard deviation.
Results
A single species of nematode was associated with B. lutzae: the Pharyngodonidae Spauligodon oxkutzcabiensis (Chitwood, Reference Chitwood1938) Skrjabin, Schikhobalova and Lagodovskaja, 1960, with a total of 34 individuals recovered from the large intestine. Of the 57 lizards examined (38 adult females, 15 adult males and 4 juveniles), 13 were infected with S. oxkutzcabiensis (overall prevalence was 22.8%). The mean intensity of infection was 2.62 ± 1.19. Discrepancy index (D) was 0.813. Lizard SVL (56.4 ± 8.4 mm, range 33.66–68.83 mm) had no effect on the intensity of infection (r = 0.18, P = 0.19, n = 14). The prevalence of S. oxkutzcabiensis between males (26.7%) and females (26.3%) showed no significant difference (Z = 0.03, P = 0.97). There was no significant difference between the mean intensity of infection between males (3 ± 1.4) and females (2.2 ± 1.31) (Mann–Whitney, U = 271.5, P = 0.79).
Discussion
The occurrence of S. oxkutzcabiensis in B. lutzae represents a new host record. Spauligodon oxkutzcabiensis was previously reported from Peru and Paraguay in South America (Bursey & Goldberg, Reference Bursey and Goldberg2004; Bursey et al., Reference Bursey, Goldberg and Parmelee2005). Thus, the present record represents a new country record, extending the actual distribution of S. oxkutzcabiensis to the Atlantic Forest of north-eastern Brazil.
Nine species of lizard are known to harbour S. oxkutzcabiensis: Sceloporus malachiticus (Goldberg & Bursey, Reference Goldberg and Bursey1992), S. formosus, S. grammicus, S. megalepidurus and S. mucronatus (Goldberg et al., Reference Goldberg, Bursey and Camarillo-Rangel2003), Tropidurus guarani (Bursey & Goldberg, Reference Bursey and Goldberg2004), Thecadactylus rapicauda (Chitwood, Reference Chitwood1938), T. solimoensis (Bursey et al., Reference Bursey, Goldberg and Parmelee2005) and Phyllodactylus reissii (Goldberg & Bursey, Reference Goldberg and Bursey2004). The species registered by Bursey et al. (Reference Bursey, Goldberg and Parmelee2005) must actually be the recently described T. solimoensis, the distribution of which encompasses the locality of Cuzco Amazonico, Peru (see Bergmann & Russell, Reference Bergmann and Russell2007). Bogertia lutzae showed a low diversity and isolationist helminth fauna, and this may be the result of a simple enteric system, restricted vagility, ectothermy and a generalist diet (Goater et al., Reference Goater, Esch and Bush1987; Aho, Reference Aho, Esch, Busch and Aho1990). Moreover, the small size of B. lutzae may constrain the establishment of a richer parasite fauna, since many small lizard species have shown a depauperate helminth fauna; for example, Liolaemus lutzae (mean SVL 61.1 mm) and Mabuya dorsivittata (mean SVL 64.9 mm), which had two nematode species each (Rocha, Reference Rocha1995; Rocha et al., Reference Rocha, Vrcibradic, Vicente and Cunha-Barros2003). On the other hand, lizard species that attain higher SVL, such as Anolis punctatus (mean SVL 70.4 mm) (Goldberg et al., Reference Goldberg, Bursey and Vitt2006), harbour more endoparasites than small hosts, by facilitating niche differentiation and habitat segregation by competing species (Kuris et al., Reference Kuris, Blaustein and Alio1980). Host size and sex have a deep impact on diet and habitat preferences of lizards (Fitch, Reference Fitch1981), and this may also influence the patterns of prevalence and intensity of infection (Goater et al., Reference Goater, Esch and Bush1987; Aho, Reference Aho, Esch, Busch and Aho1990). Indeed, these correlations have been observed in a wide variety of Brazilian lizard species (Vrcibradic et al., Reference Vrcibradic, Cunha-Barros, Vicente, Galdino, Hatano, Van Sluys and Rocha2000; Fontes et al., Reference Fontes, Vicente, Kiefer and Van Sluys2003; Anjos et al., Reference Anjos, Rocha, Vrcibradic and Vicente2005; Sousa et al., Reference Sousa, Lima and Oliveira2007). The lack of these correlations in B. lutzae may be due to our small sample size or host ecology, since differences of infection with age and sex are frequently linked with diet and habitat segregation (Van Sluys et al., Reference Van Sluys, Rocha and Ribas1994; Ribas et al., Reference Ribas, Rocha, Teixeira-Filho and Vicente1995, Anjos et al., Reference Anjos, Rocha, Vrcibradic and Vicente2005).
Spauligodon oxkutzcabiensis showed a highly aggregated pattern of distribution in B. lutzae. Poulin (Reference Poulin1993) stated that this pattern is one of the most common features of metazoan parasite infections. In fact, further studies on basic ecological data of B. lutzae, such as diet and habitat use, are necessary to understand the host–parasite relationships, especially the absence of a relationship between patterns of parasitic infection and host size and sex.
Acknowledgements
We thank the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA) for a collection permit (Process 02 010.003061/05-58). This study was partially supported by grants from Fundação de Amparo à Pesquisa de Alagoas (FAPEAL; process 2004 0930160-1) and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP; processes 06/59 692-5 and 08/50 417-7). R.W.A. thanks Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for a grant and E.M.X.F. thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico (Bolsa produtividade Processo no. 304077/2008-9).
