Acta Herpetologica 13(1): 95-100, 2018 ISSN 1827-9635 (print) © Firenze University Press ISSN 1827-9643 (online) www.fupress.com/ah DOI: 10.13128/Acta_Herpetol-21100 Helminths of the lizard Colobosauroides cearensis (Squamata, Gymnophthalmidae) in an area of Caatinga, Northeastern Brazil Aldenir F. da Silva Neta*, Robson W. Ávila Programa de Pós-graduação em Bioprospecção Molecular, Departamento de Química Biológica, Universidade Regional do Cariri – URCA, Rua Coronel Antônio Luis, 1161, Pimenta, CEP 63100-000, Crato, CE, Brazil.*Corresponding author. E-mail: aldenirferreira_@ hotmail.com Submitted on: 2017, 4th August; revised on: 2017, 25th September; accepted on: 2018, 25th January Editor: Dario Ottonello Abstract. Lizards are hosts to a variety of parasites, but in South America only 15% of lizard species have been stud- ied for helminths. In the present study, the component community of helminths associated with the gymnophthalmid Colobosauroides cearensis in an area of Caatinga (7°22’46.08” S, 38°38’47.87”W) is reported. We examined 91 speci- mens from the Brazilian state of Ceará, and five taxa of helminths were recovered: four Nematoda (Parapharyngodon largitor, Spauligodon sp., Physaloptera sp. and Oswaldocruzia sp.) and one Cestoda (Oochoristica sp.). Parapharyngodon largitor was the most prevalent species (61%), and presented the highest mean abundance of infection (1.60 ± 0.18). Lizard body size influenced the richness and abundance of helminths, while infection parameters were not related to lizard sex. Keywords. Parasites, nematodes, cestodes, neotropical. Parasitological studies are necessary to understand host–parasite interactions and the role of parasite spe- cies within ecosystems (Bittencourt and Rocha, 2003; Hudson, 2005). Although the richness of parasites is greater than that of hosts, they are much less studied, which means a considerable portion of the biodiversity is unknown (Poulin and Morand, 2000; Rocha et al., 2016). Lizards are host to a variety of parasites, including helminths (Anderson, 2000; Ávila and Silva, 2010; Ávila et al., 2011; 2012). Despite the recent increase in parasi- tological studies in lizards (Anjos et al., 2005; Ávila and Silva, 2010; Brito et al., 2014a; Bezerra et al., 2015), the knowledge of helminths remains scarce. For example, South America harbors more than 1120 lizard species (Uetz and Hosek, 2016), but only 15% of these species have had their associated helminths studied (Ávila and Silva, 2010). The new world lizard family Gymnophthalmidae includes 235 species (Uetz and Hosek, 2016), and less than 10% of these species have been studied regard- ing their parasitological aspects (Ávila and Silva, 2010). Information about parasitism in Gymnophthalmidae is punctual and usually appears in descriptions or records of new occurrences of parasites (Bursey et al., 2005; Ávila et al., 2011; Albuquerque et al., 2012). In Brazil, data on the parasitic fauna of gymnophthalmids is concentrated in studies of the Amazon (Baker and Bain, 1981; Bur- sey et al., 2005; Albuquerque et al., 2012; Ávila and Silva, 2013), Cerrado (Ávila et al., 2011) and Restinga (Almei- da et al., 2009). In the Caatinga domain, the knowledge related to helminth communities associated with gym- nophthalmids remains little explored (Brito et al., 2014a). Colobosauroides cearensis is a semifossorial and diur- nal lizard with relictual distribution in the Caatinga. To the best of our knowledge, there are no records of hel- minths being associated with this lizard, mainly due to its fossorial habits (Cunha et al., 1991). Herein, we pre- sent data on the helminth community composition of the 96 Aldenir F. da Silva Neta, Robson W. Ávila lizard Colobosauroides cearensis in an area of Caatinga in the Northeast Region of Brazil. We conducted this study in the municipality of Mau- riti (7°22’46.08”S, 38°38’47.87”W), state of Ceará, North- eastern Brazil (Fig. 1). The vegetation is characterized mainly by deciduous forest and hypoxerophytic Caatinga. The local climate is hot and semiarid, with the rainy peri- od occurring from October to April, and the mean annu- al precipitation ranging from 500 to 800 mm (IPECE, 2015). We captured 91 Colobosauroides cearensis (39 ± 7 mm SVL) by hand during three to five-day fieldtrips from December 2015 to December 2016; this comprised 47 adult females (39.9 ± 7.5 mm SVL), 36 adult males (42.8 ± 5.5 mm SVL) and 8 juveniles (22.0 ± 0.9 mm SVL). We euthanized the lizards with a lethal injection of sodium thiopental (CFMV, 2013); these were then fixed in 10% formalin, preserved in 70% alcohol and deposited in the Herpetological Collection of the Regional Univer- sity of Cariri (8451, 8452, 8453, 11453–11490; 11663– 11687; 12399–12423). For each specimen, we measured the snout–vent length (SVL) with a digital caliper (± 0.01 mm) and mass to the nearest gram with a Pesola® spring scale (± 0.1 g). We removed all organs of the respiratory and gastro- intestinal tracts and examined them individually under a stereoscope for helminths. We transferred the collected helminths to 70% ethanol. We stained the cestodes with alcoholic hydrochloric acid-carmine, which were sub- sequently cleared in creosote, while nematodes were diaphanized in lactophenol. For each helminth species, the prevalence, mean abundance, and mean intensity of infection (following Bush et al., 1997) were estimated, where parasite mean abundance is defined as the arith- Fig. 1. Collecting site in State of Ceará (A) in Northeast Brazil; Mauriti municipality (B); Study area (C): São Miguel district. 97Helminths of the lizard Colobosauroides cearensis metic mean of the number of individuals of a particu- lar parasite species per host examined; mean intensity of infection is the total number of parasites found in a sample, divided by the number of hosts infected with that parasite; and prevalence (P%) is the number of hosts infected with one or more individuals of a particular par- asite species divided by the total host number. Through- out the text, results are reported as means ± SE. We used a generalized linear model with Poisson dis- tribution (GLM) to analyze the relationship between abun- dance and helminth species richness with host body size and sex. We used a t-test to infer intersexual differences between SVL and mean helminth richness. All analyses were performed using the package Rcmdr in the R plat- form, version 2.15.0 (R Development Core Team, 2013). We recovered 165 helminths with an overall preva- lence of 69.2%. Mean overall abundance was 1.8 ± 0.2 and mean intensity of infection was 2.6 ± 1.6. The com- ponent community of helminths associated with Colo- bosauroides cearensis comprised five taxa (Table 1): one cestode, Oochoristica sp., and four nematodes, Paraphar- yngodon largitor, Spauligodon sp., Physaloptera sp. and Oswaldocruzia sp. Fifty-six individuals of C. cearensis (32 females and 24 males) were parasitized with Parapharyngodon largitor (61% prevalence), with this nematode also presenting the highest mean abundance (1.60 ± 0.18). Oswaldocruzia sp. were the least prevalent (1.1%) and the least abundant (0.02 ± 0.02). The relationship between lizard SVL and the mean abundance of helminths was significant (Z = 2.604; P = 0.009). Although males (42.8 ± 5.5) were larger than females (39.9 ± 7.4; t = 2.212; P = 0.029), sex did not influence mean abundance (Z = 0.935; P = 0.30). The mean richness of helminths was low (0.736 ± 0.050), with no influence of host sex (Z = -0.068; P = 0.60), but the SVL influenced helminth mean richness (Z = 2.282; P = 0.02). Intersexual differences in mean richness were not found, even when the effect of SVL was removed (t = 0.267; df = 80.91; P = 0.70). Moreover, no juvenile lizards were parasitized. Our study provides the first parasitological record to the host Colobosauroides cearensis. Most taxa reported here were not identified to species level due to juvenile condition (Physaloptera sp.), bad conditions of preserva- tion (Oochoristica sp. and Oswaldocruzia sp.) or because the present species probably represented an undescribed species (Spauligodon sp.). Parapharyngodon largitor is a generalist species, since it has been reported in several lizard species (Rodrigues, 1970; Vicente et al., 1993; Vrci- bradic et al., 2002; Bittencourt and Rocha, 2003; Anjos et al., 2005; Ávila and Silva, 2010; Ávila et al., 2011). Despite the higher prevalence, P. largitor presented low intensity of infection (2.6 ± 1.6), which is also noted for the genus Parapharyngodon in other lizard species: Hemidactylus mabouia (Squamata: Gekkonidae), Phyl- lopezus pollicaris (Squamata: Phyllodactylidae), Tropidurus itambere, T. torquatus, T. hispidus (Squamata: Tropiduri- dae) (Rodrigues, 1987; Anjos et al., 2005; Pereira et al., 2011; Sousa et al., 2014; Araújo-Filho et al., 2016). Higher prevalence (61%) of P. largitor indicates success in coloni- zation within host populations, which suggests that this species may be important in parasite community structure (Bush and Holmes, 1986; Holmes, 1987). Specimens of genus Oswaldocruzia sp. are frequently found infecting the intestines of amphibians and reptiles (Santos et al., 2008). Oswaldocruzia sp. has direct life cycle, transmission can occur through ingestion or larvae penetration in the skin (Anderson, 2000). Oswaldocruzia sp. was observed para- sitizing several lizards from Brazil (Ávila and Silva, 2010), including Tropidurus semitaeniatus, Brasiliscincus heathi and Anotosaura vanzolinia in a Caatinga area (Brito et al., 2014a; Oliveira et al., 2017). The low prevalence and inten- sity of infection found here suggests accidental ingestion of eggs, which could occur through tongue-flicking behavior in substrate (Menezes et al., 2004). Table 1. Mean abundance (MA), mean intensity of infection (MII) with range, prevalence (P) and site of infection of helminth commu- nity associated with the lizard Colobosauroides cearensis in the Caatinga, Northeastern Brazil. Values are mean ± SE. SI: small intestine; ST: stomach; LI: large intestine. Helminth MA MII P Site of infection Cestoda Oochoristica sp. 0.05 ± 0.03 1.6 ± 0.7 (1-2) 3.3% SI Nematoda Physaloptera sp. 0.09 ± 0.07 4.5 ± 3.5 (2-7) 2.2% ST Parapharyngodon largitor 1.60 ± 0.18 2.6 ± 1.6 (1-10) 61.0% SI, LI, ST Oswaldocruzia sp. 0.02 ± 0.02 2.0 ± 2.0 (-) 1.1% SI Spauligodon sp. 0.06 ± 0.04 2.0 ± 1.0 (1-3) 4.4% SI, LI 98 Aldenir F. da Silva Neta, Robson W. Ávila The other helminth taxa found in the present study have been recorded in lizards from South America (Ávi- la et al., 2010), which have also been reported in oth- er gymnophthalmids: Oochoristica sp. (Apoglossus sp., Micrablepharus maximiliani), Physaloptera sp. (Cerco- saura argulus, Bachia scolecoides), Spauligodon sp. (Micra- blepharus maximiliani) (Ávila et al., 2011; Brito et al., 2014a). The infection of other gymnophthalmids by the same taxa of parasites reported here may suggest phylo- genetic relationships, since phylogenetically close taxa may present similarity in the use of a niche, body shape and behavior (Wiens and Graham, 2005; Lima et al., 2012; Brito et al., 2014a). Host body size influences the establishment of pop- ulations and communities of parasites (Poulin, 2004; Kamiya et al., 2014a; 2014b). The individual’s parasitic load (Poulin and George-Nascimento, 2007) is due in part to a larger ‘area’ of exploration and colonization pro- vided by larger-sized specimens (MacArthur and Wilson, 1967; Aho, 1990). In addition, another relevant factor is that larger individuals are older and have therefore suf- fered longer exposure to parasitic agents (Aho, 1990). Studies of lizard populations have found a positive rela- tionship between host body size and helminth infection rates (Barreto-Lima et al., 2011; Ávila and Silva, 2013; Araújo-Filho et al., 2014; Brito et al., 2014b). There was no variation of richness and abundance between the sexes in C. cearensis, contrary to findings for other gymnophthalmids (Brito et al., 2014a). Intersexual variation in parasite loads may be related to hormonal, physiological and behavioral features; for example, larger males exhibit territorial behavior and frequently engaged in combat with other individuals, which may increase stress levels while decrease their immune response, thus becoming more susceptible to parasitic agents. In addi- tion, testosterone production could be a powerful sup- pressor of immune system (Zuk and McKean, 1996). However, data regarding physiological and behavioral variation are lacking for C. cearensis. Moreover, other studies found no relationship between the parasitic rates and the sex of the lizards (Anjos et al., 2011; Bezerra et al., 2015). Gymnophthalmids present low helminth rich- ness, when compared to other lizards of the superfam- ily Teiioidea (Goldberg et al., 2013; Teixeira et al., 2016). Small body sizes in lizards of this family could restrict available niches to colonization and habitat segregation for endoparasites. Poor helminth richness compared to other lizard species in the same family was also reported in Cercosaura argulus (4 spp), Cercosaura ocellata (1 spp), Leposoma osvaldoi (1 spp), Micrablepharus maximiliani (3 spp) e Anotosaura vanzolinia (1 spp) (Ávila and Silva, 2010; Brito et al., 2014a; Oliveira et al., 2017). In the pre- sent study, we found the highest helminth richness within the lizard family Gymnophthalmidae, also providing new locality and host records. 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