Acta Herpetologica 13(2): 171-175, 2018 ISSN 1827-9635 (print) © Firenze University Press ISSN 1827-9643 (online) www.fupress.com/ah DOI: 10.13128/Acta_Herpetol-23366 Helminths infecting the black false boa Pseudoboa nigra (Squamata: Dipsadidae) in northeastern Brazil Cicera Silvilene L. Matias1,*, Cristiana Ferreira-Silva2, José Guilherme G. Sousa3, Robson W. Ávila1,3 1 Laboratório de Herpetologia, Departamento de Química Biológica, Universidade Regional do Cariri, Campus do Pimenta, CEP 63105000, Crato, CE, Brazil. *Corresponding author. E-mail: silvilenematias@gmail.com 2 Programa de Pós-Graduação em Ciências Biológicas (Zoologia), Departamento de Parasitologia, Instituto de Biociências, Universidade Estadual Paulista, CEP 18080-970, Botucatu, SP, Brazil 3 Programa de Pós-Graduação em Ecologia e Recursos Naturais, Departamento de Ciências Biológicas, Universidade Federal do Ceará, Campus Universitário do Pici, CEP 60021970 Fortaleza, CE, Brazil Submitted on: 2018, 8th June; revised on: 2018, 28th August; accepted on: 2018, 13th September Editor: Daniele Pellitteri-Rosa Abstract. Knowledge about endoparasites of snakes is essential to understand the ecology of both parasites and hosts. Herein, we present information on helminths parasitizing the black false boa Pseudoboa nigra in northeastern Bra- zil. We examined 32 specimens from five Brazilian states (Ceará, Piauí, Pernambuco, Maranhão and Rio Grande do Norte). We found six helminths taxa: two acanthocephalans (Acanthocephalus sp. and Oligacanthorhychus sp.), three nematodes (Hexametra boddaertii, Physaloptera sp. and Physalopteroides venancioi), and one cestode (Ophiotaenia sp.). All parasites are reported for the first time infecting P. nigra, providing relevant information on infection patterns in this snake. Keywords. Acanthocephala, Cestoda, Nematoda, Reptilia, snake. Surveys of endoparasites associated with wild ani- mals are key features to understand ecology, natural his- tory, life cycles and evolution of parasites and their hosts (Silva, 2008). Parasites can influence their hosts in dif- ferent ways, affecting their physiological and behavioural patterns (Levri, 1999), which can cause changes in color- ation, and decrease in reproductive capacity, resulting in reduced reproductive success (Schall and Dearing, 1987; Dunlap and Schall, 1995). Studies focusing on endoparasites in reptiles has grown in the past few years, and the diversity of para- sites tends to increase as new hosts are studied (Ávila and Silva, 2010). In Brazilian snakes there is also an increase, especially in parasite species descriptions and new records of hosts (Bursey and Brooks, 2011; Norval et al., 2012; Pinto et al., 2012; Araújo-Filho et al., 2013; Ávila et al., 2013; Kuzmin et al., 2014, 2016; Mati et al., 2015). However, little is known about infection patterns in snakes from Brazil (Almeida et al., 2008). The black false boa Pseudoboa nigra (Duméril, Bibron and Duméril, 1854) is widely distributed in Bra- zil, Bolivia, Paraguay and Argentina (Etchepare et al., 2015). Several aspects of its biology are known, such as diet and reproduction (Orofino et al., 2010; Gaiarsa et al., 2013; Mesquita et al., 2013). However, data on parasitism in this snake is restricted to the description of Protozoa Trypanosoma serpentis (Viola et al., 2009) and a report of the pentastomid Raillietiella furcocerca (Alcantara et al., 2014). Herein, we describe both the helminths rich- ness and infection patterns (prevalence and intensity) in P. nigra from northeastern Brazil. We examined 32 specimens of P. nigra from five Bra- zilian states in the northeastern region: Ceará (N = 20), Maranhão (N = 1), Piauí (N = 4), Pernambuco (N = 5) 172 Cicera Silvilene L. Matias et alii and Rio Grande do Norte (N = 2). We used specimens deposited at Coleção Herpetológica da Universidade Regional do Cariri (URCA-H 379, 507, 916, 2222, 2381, 3377, 3432, 3742, 3982, 4510, 4755, 4916, 5104, 5632, 5694, 5885, 5886, 7090, 8507, 9400, 9482, 9536, 10043, 10594, 10629, 11031, 11348, 11075, 11899, 11900, 12108, 12266), collected from 2011 to 2016. We checked carefully for helminths, under a stereom- icroscope, the gastrointestinal tract (esophagus, stomach, small and large intestines), liver, kidneys, lungs, gallblad- der and coelomic cavity. For helminths identification, we stained acanthocephalans and cestodes with alcoholic hydrochloric acid-carmine and cleared in eugenol, while nematodes were diaphanized in lactic acid (Amato and Amato, 2010). After identification, all helminths species were deposited at Coleção Parasitológica da Universidade Regional do Cariri (URCA-P 476–521). We calculated parasitological parameters (prevalence, mean abundance and mean intensity of infection) according to Bush et al. (1997). Of the black false boas analyzed, 23 specimens con- tained parasites, represented by six helminths species: two acanthocephalans (prevalence 59.3%) (Acantho- cephalus sp., and Oligacanthorhychus sp.), three nema- todes (43.75%) (Hexametra boddaertii, Physaloptera sp. and Physalopteroides venancioi), and one cestode (3.1%) (Ophiotaenia sp.). The overall prevalence was 71.9%, mean abundance 230.5 ± 126.5, mean intensity of infec- tion 320.7 ± 173.4 (range: 1-3648) and richness 1.12 ± 0.15 in P. nigra (n = 32; SVL 579.8 ± 166.2) (Table 1). P. nigra presented high helminth overall prevalence (71.9%), similarly to other snakes, such as in Bothrops moojeni (68%; Barrella and Silva, 2003), Crotalus durissus terrificus (66%; Dias et al., 2004), Erythrolamprus miliaris (44.4 %, 72.7%; Roldan and Fiorillo, 2016 and Mati et al., 2015, respectively). The richness and abundance of para- sitic groups that contribute to high prevalence in these snake species vary according to the habits of their hosts. For example, Nematoda richness tends to be higher in terrestrial snakes, such as P. nigra (3 spp.; present study), C. d. terrificus (7 spp.; Dias et al., 2004) and Crotalus mitchelli (5 spp.; Goldberg et al., 2013), while Trematoda richness is higher in aquatic species, such as E. miliaris (17 spp.; Mati et al., 2015) and N. natrix (5 spp.; Yildi- rimhan, 2007). Thus, the richness, abundance and high prevalence of nematodes may be directly related to the host habitat (Brouat et al., 2007). Acanthocephalans present indirect life cycle and use snakes as paratenic host (e.g., Travassos, 1917; Pizzatto and Madi, 2002; Pizzatto and Marques, 2006; Smales, 2007). Oligacanthorhynchus is represented actually by 34 species (Amin, 2013), two of these known to infect South American snakes: Oligacanthorhynchus spira infecting Boa constrictor, Boiga dendrophila, Bothrops jararacussu, Bothrops neuwiedi, Clelia clelia, Erythrolamprus aesculapii, Erythrolamprus miliaris, Erythrolamprus poecilogyrus, Mastigodryas bifossatus, Micrurus corallinus, Philodryas olfersii, Xenodon merremii and Xenodon histricus (Travas- sos, 1917; Pizzatto and Madi, 2002; Pizzatto and Marques, 2006); and Oligacanthorhynchus taenioides infecting B. constrictor, B. dendrophila, B. jararacussu, B. neuwiedi, C. clelia, E. aesculapii, M. bifossatus, P. olfersii, X. merremii and X. histricus (Travassos, 1917). Cystacanths of Oliga- canthorhynchus sp. have also been reported in Philodryas patagoniensis (Smales, 2007). Another acantocephalan found in the present study belongs to the genus Acanthocephalus. From the 54 known species (Amin, 2013; Amin et al., 2014), only Acanthocephalus lutzi has been reported infecting Brazil- ian snakes (X. merremii and X. neuwiedii; Smales, 2007). Table 1. Helminths parasites associated with Pseudoboa nigra in five states from Northeastern Brazil. CE = Ceará; PE = Pernambuco; PI = Piauí; RN = Rio Grande do Norte, P = Prevalence; MA = Mean Abundance (± standard error); MII = Mean Intensity of Infection (± stand- ard error); SI= Site of Infection; (Cc = Coelomic cavity, S = Stomach, Li = Large intestine, Si = Small intestine). Helminths States P % MA ± SE MII ± SE SI Acanthocephala 62.5 377.74 ± 207.94 Acanthocephalus sp. CE, PE 6.25 2.5 ± 1.74 40.0 ± 3.0 S Oligacanthorhychus sp. CE, PE, PI 56.25 225.75 ± 126.5 401.33 ± 218.52 Cc, Si, Li Nematoda 43.75 14.43 ± 9.51 Hexametra boddaerti CE, PE, PI 15.62 1.28 ± 0.69 8.20 ± 3.07 Cc, S, Si Physaloptera sp. CE, PE, RN, 31.25 4.83 ± 4.55 49.66 ± 47.02 Cc, S, Li Physalopteroides venancioi CE 3.13 0.03 ± 0.03 1.0 Si Cestoda 3.13 4.0 Ophiotaenia sp. CE 3.13 0.12 ± 0.12 4.0 Si 173Helminths infecting Pseudoboa nigra from Brazil In the present study, only cystacanths were found, sug- gesting that P. nigra acts as paratenic host for Acantho- cephalus, with insects being the intermediate and birds the definitive hosts (Travassos, 1917; Schmidt and Rob- erts, 1996), thus suggesting that Acanthocephalus spp. may use P. nigra to reach its definitive hosts. Identification of Acanthocephalus sp. and Oligacan- thorhynchus sp. found in this study was not possible due to immature condition of specimens (cystacanths), mak- ing it difficult to analyze the proboscis hook formulas. Nematodes were represented by Hexametra boddaerti, Physaloptera sp. and Physalopteroides venancioi. H. bod- daerti is commonly found in lizards (Ávila and Silva, 2010) and snakes (Bursey and Brooks, 2011). The genus Hexam- etra contains 7 species (Baker, 1987), of which H. boddaerti is known to infect the following snakes in South Ameri- can: Bothrops sp., Crotalus durissus, Oxyrhopus trigeminus, Philodryas baroni, and Philodryas patagoniensis (Skrjabin, 1916; Sprent, 1978; Hartdegen and Gamble, 2002; Pinto et al., 2010). Among the 105 Physaloptera species known (Pereira et al., 2014; Luiz et al., 2015) P. monodens infects Boa constrictor, P. obitusissima infects Bothrops jararaca (Skrjabin and Sobolev, 1964) and Physaloptera sp. infects Micrurus surinamensis (Ávila et al., 2013). Physalopteroides venancioi is the only species with occurrence in the South America and is a generalist par- asite of lizards (Ávila and Silva, 2010) and amphibians (Campião et al., 2014). However, this is the first record of P. venancioi infecting snakes. We suggest that infection of P. nigra by P. venancioi is accidental, being the parasite acquired from the feeding of the snake, since its diet con- sists mainly of lizards (Orofino et al., 2010). In Brazil, there are five Ophioteania species infect- ing snakes: Ophiotaenia calmetti, O. elongata, O. flava, O. hyalina, and O. macrobothria. Only a few Brazilian snakes have been reported as host for Ophiotaenia species, among them, Bothrops jararaca, Bothrops atrox, Corallus caninus and Micrurus corallinus (Silva et al., 2006). In conclusion, we found a high prevalence (71.9%) of helminths in the black false boa, reporting it as a new host for all helminth species here recorded, contributing to the increase of diversity and knowledge on parasites. ACKNOWLEDGEMENTS We thank the Conselho Nacional de Desenvolvi- mento Científico e Tecnológico (CNPq) for providing a research fellowship to RWA (# 303622/2015-6), sci- entific initiation fellowship to CSLM (121944/2017-4) and fellowship to CFS (140871/2017-9). JGGS thanks to Coordenação de Aperfeiçoamento de Pessoal de Nív- el Superior – CAPES for the fellowship. We are grate- ful to the CNPq/FUNCAP/CAPES for  financial support (PROTAX – Processes 440511/2015-1; 5574685/2017; 88882.156872/2016-01). Thanks to Instituto Chico Mendes de Conservação da Biodiversidade ICMBio for collecting permit (26913-1). This study was authorized by ethics committee of the Universidade Regional do Cariri (CEUA/URCA, process No. 00260/2016.1). REFERENCES Alcantara, E.P., Ferreira-Silva, C., Ávila, R.W., Oliveira, W.A. (2014): Pseudoboa nigra (Black False Boa) Endo- parasites. Herpetol. Rev. 45: 343. Almeida, W.O., Guedes, T.B., Freire, E.M.X., Vasconcel- los, A. 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