Herpetology Notes, volume 11: 565-572 (2018) (published online on 29 July 2018) Helminth communities of Pithecopus nordestinus (Anura: Phyllomedusidae) in forest remnants, Brazil Priscila Almeida de Sena1,4, Breno Moura Conceição2, Paula Fonseca Silva2, Winny Gomes O Silva1, Wagner Berenguel Ferreira2, Valdemiro Amaro da Silva Júnior3, Geraldo Jorge Barbosa de Moura2,4,5 and Jaqueline Bianque de Oliveira1,4,5,* Abstract. The helminth parasite communities of anurans are determined by environmental and host factors. For to describe the parasites and to investigate the host and environmental factors that can influence the composition and structure of the helminth fauna were studied 72 specimens of Pithecopus nordestinus (Caramaschi 2006) collected in two different areas in northeastern region of Brazil: Estação Ecológica do Tapacurá (EET), a remnant of Atlantic Rainforest in Pernambuco state (n=39), and Floresta Nacional do Araripe (FLONA), a remnant of Altitudinal Forest in Ceará state (n=33). Helminths of six taxa (five nematodes and one acanthocephalan) were identified, being the nematodes the most prevalent helminths (Cosmocercidae gen. sp., Cosmocerca parva, Cosmocercella phyllomedusae, Oxyascaris caudacutus and Rhabdias sp.), followed by acanthocephalans (Centrorhynchus sp.). The prevalence and the mean intensity of infection were higher in the animals from FLONA. Body size and sex of hosts did not influence the abundance of helminths, but the parasites abundance was different between the two study sites, being higher in FLONA than in EET. The two studied populations of P. nordestinus presented a higher parasite richness when compared to other studies with species from the Phyllomedusidae family, and the abundance of helminths was different between the two study areas, demonstrating that local characteristics as well as the host ecology and diet are crucial in host-parasite relationship in forested environments. The knowledge about the composition and structure of helminth fauna is important for the conservation of anurans and ecosystems where they live. Keywords: anurans, parasites, Nematoda, Acanthocephala, Atlantic Rainforest, Altitudinal Forest, conservation Introduction Amphibians are excellent models for the parasite-host relationships studies, since they occupy a variety of 1 Laboratório de Parasitologia, Universidade Federal Rural de habitats, have different patterns of life cycle, different Pernambuco, Rua Dom Manoel de Medeiros SN, CEP 52171- reproductive strategies and occupy various positions in 900, Recife, Pernambuco, Brazil food webs (Koprivnikar et al., 2012). Although Brazil 2 Laboratório de Estudos Herpetológicos e Paleoherpetológicos, has the most diverse anurofauna (Segalla et al., 2014), Universidade Federal Rural de Pernambuco, Rua Dom Manoel studies on the helminth fauna associated with these de Medeiros SN, CEP 52171-900, Recife, Pernambuco, hosts are still scarce (Santos and Amato 2010a) and, Brazil 3 Laboratório de Patologia, Universidade Federal Rural de most of them, restricted to taxonomic descriptions and/ Pernambuco, Rua Dom Manoel de Medeiros SN, CEP 52171- or records of occurrence (Pinhão et al., 2009). 900, Recife, Pernambuco, Brazil The parasites may act as opportunistic or as primary 4 Programa de Pós-Graduação em Ciência Animal Tropical, agents of diseases in anurans (Koprivnikar et al., 2012), Universidade Federal Rural de Pernambuco, Rua Dom Manoel influencing growth and reproduction rates (Campião de Medeiros SN, CEP 52171-900, Recife, Pernambuco, et al., 2009). Furthermore, they are considered as Brazil 5 bioindicators of environmental change, providing Programa de Pós-Graduação em Ecologia, Universidade Federal Rural de Pernambuco, Rua Dom Manoel de Medeiros information on the ecosystems health and structure of SN, CEP 52171-900, Recife, Pernambuco, Brazil the food web (Campião et al., 2009; Koprivnikar et al., 6 Programa de Educação Tutorial (PET-Biologia), Universidade 2012). The body size, age, sex, diet and host behavior are Federal Rural de Pernambuco, Rua Dom Manoel de Medeiros important variables in the composition and structure of SN, CEP 52171-900, Recife, Pernambuco, Brazil parasite communities of anurans (Hamann et al., 2009; * Corresponding author. E-email: [email protected] 566 Priscila Almeida de Sena et al. Santos and Amato 2010a; Toledo et al., 2013, 2015; specimens of P. nordestinus that were evaluated, Campião et al., 2014a, 2016), which act as definitive, which were deposited in the Coleção Herpetológica e intermediate and paratenic hosts of a wide variety of Paleoherpetológica of the Universidade Federal Rural helminths (Santos and Amato 2010a; Toledo et al., de Pernambuco: 39 were collected in September 2014 2013, 2015; Campião et al., 2009, 2014a, 2014b). Body in the Estação Ecológica do Tapacurá - EET, in the size is a determining factor for the composition of the municipality of São Lourenço da Mata, Pernambuco anuran parasite community, due to the greater amount of state, and 33 were collected in July 2012 in the Floresta food eaten and added extra and intracorporeal surface, Nacional do Araripe - FLONA, in the municipality of increasing the possibilities of oral and skin infection Jardim, state of Ceará. (Hamann et al., 2009; Santos and Amato 2010a; The EET (08°03’S/ 35°10’W) is a remnant of the Campião et al., 2016). On the other hand, environmental Atlantic Rainforest, consisting of a stationary forest characteristics can influence the helminth community of semi-deciduous evergreen type (Andrade-Lima 1957), anurans (Campião et al., 2012). with a total area of approximately 800 ha, of which Pithecopus nordestinus (Caramaschi 2006) (Anura: about 400 ha are made up of forested areas, surrounded Phyllomedusidae) was described in 2006 from a by sugarcane monoculture (Azevedo-Júnior 1990). It taxonomic revision of Phitecopus hyponcondrialis has an As’ climate type with average annual rainfall of (Daudin, 1800) by Caramaschi (2006). At this time, both 1300 mm per year and six months with less than 100 species were inserted in the genus Phyllomedusa, but mm. recent phylogenetic analysis placed all the Phyllomedusa The FLONA (7°22’5.12’’S/39°20’18.83’’O), a from the hypocondrialis group in a resurrected genus remnant of Altitudinal Forest, covers an area of around named Pithecopus (Duellman et al., 2016). 38,262 ha and 720 m altitude, between the municipalities of Barbalha, Crato, Jardim and Santana do Cariri, in the This anuran is widely distributed in Atlantic Forest state of Ceará (Muniz et al.,, 2015). Located at the top of morphoclimatic areas, including Caatinga enclaves the Chapada do Araripe, with a predominantly rainforest moist forests and Caatinga shrubland (Moura et al., vegetation, but with lots of babaçu palms (Orbignya 2015). It is arboreal, “sit-and-wait” predator and phalerata Mart) which features a secondary forest. It preferably occupying the herbaceous layer, where it lays has a tropical rainy climate, with annual rainfall around its eggs in leaves located on the water depth (Moura et 1000 mm with less than 30 mm of rainfall in the driest al., 2015). As regards the conservation status, this species months. is classified as DD (data deficient) by the International Union for Conservation of Nature (IUCN 2017) and as Collection and processing of parasites.—The snout- LC (Least Concern) in the Brazilian list of endangered vent length (SVL) of each animal was recorded (average species by the Ministério de Meio Ambiente e Recursos of 3 cm SVL) and sex determination (45 males and 27 Naturais Renováveis (Portaria MMA 444/14) and in females) was performed from the view of the gonads. the state list of endangered species of the Secretaria The animals had their stomachs, intestines, liver, gall Estadual de Meio Ambiente de Pernambuco (SEMA bladders, lungs, kidneys, bladders and body cavities Resolução 01-08/01/2015). systematically examined for the presence of parasites. The only record of parasites of this species is the The acanthocephalans were stained and cleared with description of the nematode Raillietnema minor carmine and eugenol, respectively, and nematodes were Freitas and Dobbin Jr, 1961 (Vicente et al., 1991) cleared with lactophenol. Identified parasites were when this species was still considered as Phyllomedusa deposited in the Parasite Collection of the Laboratório de hypocondrialis (Campião et al., 2014b). So this is the Parasitologia (CPLAPAR) of the Universidade Federal first effort to identify the parasite fauna of P. nordestinus. Rural de Pernambuco, state of Pernambuco, Brazil. Besides this, we hypothesized that helminth communities Samples of parasitized organs and/or tissues were fixed present differences between the two study environments in buffered 10% formalin and processed by standard (Atlantic Rainforest and Altitudinal Forest) and that histological techniques. host characteristics (size and sex) play an important role Data analysis.—The prevalence, mean intensity of in structuring parasitic communities. infection and the mean abundance were calculated as proposed by Bush et al., (1997). Materials and Methods Parasites abundance data were tested for normality by Origin of animals and study sites.—Seventy-two the Kolmogorov-Smirnov test. As the data did not show Helminth communities of Pithecopus nordestinus in forest remnants, Brazil 567 Table 1. Prevalence (%), mean intensity (MI ± SD), mean abundance (MA ± SD), richness and mean richness of the helminth parasites of Pithecopus nordestinus (Caramaschi, 2006) in