Zootaxa 4012 (2): 386 390 www.mapress.com/zootaxa/ Copyright 2015 Magnolia Press Correspondence http://dx.doi.org/10.11646/zootaxa.4012.2.10 http://zoobank.org/urn:lsid:zoobank.org:pub:118849d4-9d42-4e26-be84-7297b2bdea3f A new species of Parapharyngodon (Nematoda: Pharyngodonidae) infecting Dermatonotus muelleri (Anura: Microhylidae) from Caatinga, Northeastern Brazil ISSN 1175-5326 (print edition) ZOOTAXA ISSN 1175-5334 (online edition) JOÃO A. DE ARAUJO FILHO 1,5, SAMUEL V. BRITO 2, WALTÉCIO DE O. ALMEIDA 2, DRAUSIO H. MORAIS 4 & ROBSON W. ÁVILA 3 ¹Programa de Pós-graduação em Bioprospecção Molecular, Universidade Regional do Cariri URCA, R. Cel Antônio Luis, 1161, Pimenta, CEP 63100-000, Crato, CE, Brazil ²Departamento de Química Biológica, Universidade Regional do Cariri URCA, R. Cel. Antônio Luiz, 1161, Pimenta, CEP 63105-000, Crato, CE, Brazil ³Departamento de Ciências Biológicas, Universidade Regional do Cariri URCA, R. Cel. Antônio Luiz, 1161, Pimenta, CEP 63105-000, Crato, CE, Brazil 4 UNESP Univ Estadual Paulista, Campus de Botucatu, Instituto de Biociencias, Departamento de Parasitologia Av. Bento Lopes s/ n. Distrito de Rubião Junior, CEP 18618-970 Botucatu, SP, Brasil 5 Corresponding author: E-mail: araujofilhoaj@gmail.com Abstract. Parapharyngodon silvoi n. sp. (Nematoda: Pharyngodonidae) is described from the large and small intestine of the Muller s termite frog Dermatonotus muelleri (Boettger, 1885) from the biome Caatinga, Exu municipality, Pernambuco State, Brazil, Dermatonotus muelleri is a fossorial species with a specialized termite diet, and feeding and reproductive behavior occurring only during the wet season. The new species is distinguished from other species of the genus Parapharyngodon by showing ovary not coiled around the esophagus, morphology of anterior cloacal lip, spicule size and number of caudal papillae. Key words: Nematoda, Parapharyngodon, new species, Amphibian parasites Introduction The nematode genus Parapharyngodon (Chatterji, 1933), (Cosmocercoidea: Pharyngodonidae) is currently composed of 57 species (Bursey & Goldberg., 2015). They are globally distributed parasites, found in Australian (Johnston & Mawson, 1941), Ethiopian (Malan, 1939; Hering-Hagenbeck et al., 2002), Palearctic (Castaño-Fernandez et al., 1987; Roca et al., 1986), and Oriental (Chatterji, 1933) and Neotropical regions (Freitas, 1957a; Ramallo et al., 2002; Bursey & Brooks, 2004; Pereira et al., 2011; Velarde-Aguilar et al., 2015; Bursey & Goldberg., 2015). Parapharyngodon is a typical lizard parasite (Ramallo et al., 2002), however eight species are known to parasitize anurans: Parapharyngodon alvarengai (Freitas, 1957a) in the toad Rhinella icterica (Spix, 1824), (Luque et al., 2005); P. garciae (Schmidt & Whittaker, 1975) in the frogs Eleutherodactylus coqui (Thomas, 1966) and Eleutherodactylus spp. (Schimidt & Whittaker, 1975; Dyer et al., 1995); P. osteopili (Adamson, 1981) in the treefrog Osteopilus septentrionalis (Duméril & Bibron, 1841), (Adamson, 1981); P. duniae (Bursey & Brooks, 2004) in the treefrog Trachycephalus typhonius (Linnaeus, 1758); P. verrucosus (Freitas, 1957b) in the frog Dermatonotus muelleri (Boettger, 1885), (McAllister et al., 2010); and P. grenadaensis in the toad Rhinella marina (Linnaeus, 1758) (Bursey et al., 2013); P. chamelensis and P. hylidae in the treefrogs Diaglena spatulata, Tripion petasatus, and Trachycephalus typhonius (Velarde-Aguilar et al., 2015). During a survey of helminth parasites of frogs from Caatinga biome, Northeastern Brazil, the microhylid frog D. muelleri (Boettger, 1885) was found to harbor nematodes of a new species of Parapharyngodon, described herein. 386 Accepted by R. Carreno: 13 Aug. 2015; published: 3 Sept. 2015
Material and methods Forty-eight specimens of D. muelleri (Anura: Microhylidae) were collected by hand in temporary ponds in the rainy season (February to April 2012), during a herpetofaunal inventory at Sítio Colônia, Exu municipality, Pernambuco State, Northeastern Brazil. The host frogs were fixed in 10% formalin, preserved in 70% alcohol and deposited in the Coleção Herpetológica da Universidade Regional do Cariri (URCA H 1450, 1451,1574-88; 2201-15; 2699-2711; 3223-25), Crato municipality, Ceará State, Brazil. Necropsy revealed 142 nematodes (only 16 specimens were used in the species description) in the small and large intestine. The helminths were fixed in formalin, cleared using lactophenol, mounted on temporary slides, and analyzed under a light microscope. The holotype, allotype and paratypes were deposited in the Coleção Parasitológica da Universidade Regional do Cariri (URCA P 370; 386 388), Crato municipality, Ceará State, Brazil. Morphological data are generally presented as mean ± 1 standard deviation (minimum and maximum) values. Measurements in µm, unless otherwise noted. Parapharyngodon silvoi n. sp. (Figs. 1) Male (Fig. 1) based in four adult specimens (URCA-P 386): Length 1.1± 0.8mm (1.0 1.1 mm); width at midbody 219.2 ± 19.8 (205 233). Triangular oral opening surrounded by 3 lips, esophagus 130.43 ± 12.32 (116 140) long: bulb length 71.1 ± 3.16 (67.7 73.9); bulb width 73.4 ± 3.89 (69.8 77.5); nerve ring 76.1 ± 10.65 (63.8 83.3); excretory pore 150.8 ± 12.76 (138.3 150.4) from anterior end. Tail 76.2 ± 6.72 (71.4 80.9) long; spicules equal, 63.3 ± 7.10 (56.6 70.8) long. Lateral alae 690.4 ± 251.8, beginning at 620.9 ± 186.17 from anterior end and ending at 55.7 ± 17.24 from posterior end; anterior cloacal lip smooth; caudal alae absent; caudal papillae in four pairs plus one unpaired papilla: 1 median precloacal pair, 1 sublateral pair in cloacal opening line, 1 median postcloacal pair, 1 pair in proximal region of caudal appendix; single median and postcloacal papilla. Female (Figs, 1), based on 12 adult specimens URCA-P, 387 388: Length 2.2 ± 0.19 mm (1.4 2.6 mm); width at midbody 384 ± 46 (345.3 436.9). Triangular oral opening surrounded by 3 lips, esophagus 241 ± 38 (141 277.6) long; bulb length 106.8 ± 19.8 (54.4 125.1); bulb width 124.6 ± 26 (57.1 149.7); nerve ring 122.1 ± 19.5 (92.9 146.2), from anterior end. Excretory pore prebulbar, 248.2 ± 48.5 (142.9 323.9), from anterior end; median vulvar opening, without prominent lips, 1.2 ± 0.2 mm (0.7 1.4), from anterior end; ovaries prebulbar, with convoluted uterus full of eggs; eggs oval, with thick and punctuated shell with subpolar operculum, 114.94 ± 11.7 (71.8 151.6) long, 51.48 ± 6.4 (33.8 66.8) wide (Figs. 01); tail 303.16 ± 34.9 (230.4 339.3) long. Taxonomic summary. Type host: Dermatonotus muelleri (Muller s termite frog; sapo boi); Coleção Herpetológica da Universidade Regional do Cariri (URCA H 1450, 1451,1574-88; 2201-15; 2699-2711; 3223-25); collection date (February to April of 2012). Type locality: Sítio colônia municipality of Exu, Pernambuco State, Brazil, 39º45'W; 07º34'S. Site of infection: Small and large intestine. Prevalence 14.58%, mean intensity of infection 20.28 ± 13.29. Specimens deposited: Coleção Parasitológica da Universidade Regional do Cariri, CE, Brazil; Holotype No. URCA- P 386; Allotype No. URCA-P 387; Paratypes, 3 adult females, URCA-P 370. Etymology: this species is named after Reinaldo José da Silva (Laboratório de Parasitologia de Animais Silvestres, Universidade Estadual Paulista) who made pioneer contributions to the taxonomy and biology of Neotropical parasite nematodes. Remarks. Parapharyngodon silvoi n. sp. is promptly distinguished from other species of Parapharyngodon by the female ovary that does not reach the esophageal bulb and prebulbar excretory pore. From the 57 described species, only P. senisfaciecaudus (Freitas, 1957b), P. riojensis (Ramallo et al., 2002), and P. duniae (Bursey & Brooks, 2004) have an ovary not coiled around the esophagus. The new species can be differentiated from these by an anterior cloacal lip smooth (echinate in P. duniae, P. riojensis P. senisfaciecaudus; Pereira et al., 2011) and smaller females, with length 1.4 2.6 mm and width 349 436 (P. senisfaciecaudus 9.9 10.7 mm and 900 1040; P. riojensis 4.2 5.4 mm and 840 1040; P. duniae 3.8. 4.5 mm and 318 434). Moreover, males of P. silvoi n. sp. have four pairs of cloacal papillae plus one unpaired papillae, while P. senisfaciecaudus, P. riojensis, and P. duniae have three pairs of caudal papillae and one unpaired papilla. Furthermore, P. riojensis and P. senisfaciecaudus have spicules larger than the new species (90 110; 88 100, respectively) and P. duniae have spicules smaller than P. silvoi n. sp. (40 49). The only species which have four NEW SPECIES PARAPHARYNGODON Zootaxa 4012 (2) 2015 Magnolia Press 387
pairs plus one unpaired papillae is Parapharyngodon sceleratus (Travassos, 1923), and the new species can be differentiated, besides female morphology, by possessing only one pair of precloacal and two pairs of postcloacal papillae, whereas P. scleratus have two precloacal pairs and one postcloacal pair of papillae (Freitas, 1957a). FIGURE 1. Parapharyngodon silvoi n. sp. (A) male, entire and ventral view. (B) female, entire ventral view. (C) male, posterior end, ventral view. (D) excretory pore. (E) female, anterior end, en face view. (F) copulatory spicule. (G) female egg. Discussion Parapharyngodon spp. are primarily parasites of reptiles (Garcia-Calvante, 1948; Freitas, 1957b; Castaño-Fernandes et al., 1987; Vicente et al., 1993; Ramallo et al., 2002; Bursey & Brooks, 2004; Gupta et al., 2009; Pereira et al., 2011; 388 Zootaxa 4012 (2) 2015 Magnolia Press FILHO ET AL.
Ávila et al., 2012; Bursey & Goldberg, 2015), with currently only eight species parasitizing anuran (Adamson, 1981; Bursey & Brooks, 2004; Luque et al, 2005; McAllister et al., 2010; Bursey et al., 2013; Velarde-Aguilar et al., 2015) and one found in a Caudata (Bursey & Goldberg, 1999). Thus, P. silvoi n. sp. is the ninth species of Parapharyngodon found in an anuran, and the third described from Brazil. In the biome Caatinga, the species Parapharyngodon alvarengai and P. sceleratus are found parasitizing insectivorous lizards (Anjos et al., 2012; Ávila et al., 2012; Brito et al., 2014), but these species present postbulbar ovary, contrasting with the prebulbar ovary found in P. silvoi n. sp. Parapharyngodon silvoi n. sp. probably presents a monoxenous life cycle, as reported for pharyngodonids (Anderson, 2000). The infection commonly occurs by ingestion of infective larvae, as well by coprophagy (Anderson, 2000). Dermatonotus muelleri is a fossorial species with a specialized termite diet (Nomura & Rossa-Feres, 2011). The feeding and reproductive behavior occurs only during the wet season, when the species emerges at night by a tunnel dug from a subterranean chamber under the ground (Nomura & Rossa-Feres, 2011). There are only a few records of parasitism in D. muelleri, with reports for the nematodes Aplectana sp., Cosmocercidae gen. sp in Brazil, Aplectana hylambatis (Baylis, 1927) in Peru (Campião et al. 2014) and P. verrucosus in Paraguay (Baker & Vaucher, 1986, McAllister et al., 2010) for the cestode Ophiotaenia cohospes (Cordero, 1946) in Paraguay (Campião et al. 2014) and spargana infection, order Pseudophyllidea in northeastern Brazil (Bezerra et al., 2012). The description of this new species increases the knowledge on amphibian parasites in the Caatinga biome. Moreover, new research on the anuran communities of this region is extremely needed and can reveal unexpected parasite diversity. Acknowledgments We are grateful to Conselho Nacional de Desenvolvimento Científico e Tecnológico CNPq for the research grant awarded to W. O. Almeida (PQ-311713/2012-2); to Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico FFUNCAP for the research grant awarded to João. A. Araujo Filho; R. W. Ávila and postdoctoral fellowship to Samuel V. Brito (BPI-0067-00006.01.00/12); to Fundação de Amparo a Pesquisa do Estado de São Paulo FAPESP for the research grant awarded to Drausio H. Morais (Process 2012/24945-1). To Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis IBAMA for the collecting permissions. We are grateful to Igor Joventino Roberto and Herivelto F. Oliveira for helping with the amphibian samplings. We also thank the Dr. Ramon A. Carreno and to two anonymous reviewers for their valuable suggestions and comments on the manuscript. Finally, we thank Paulo Emilio Santos Costa for the final artwork. References Adamson, M.L. (1981) Parapharyngodon osteopili n. sp. (Pharyngodonidae: Oxyuroidea) and a revision of Parapharyngodon and Thelandros. Systematic Parasitology, 10, 105 117. Anderson, R.C. (2000) Nematode parasites of vertebrates. Their development and transmission. 2 nd Edition. CABI Publishing, Wallingford, 650 pp. Anjos, L.A., Ávila, R.W., Ribeiro, S.C., Almeida, W.O. & da Silva, R.J. (2012) Gastrointestinal nematodes of the lizard Tropidurus hispidus (Squamata: Tropiduridae) from a semi-arid region of Northeastern Brazil. Journal of Helmintology, 87 (4), 443 449. Ávila, R.W., Anjos, L.A., Ribeiro, S.C., Morais, D.H., Silva, R.J. & Almeida, W.O. (2012) Nematodes of Lizards (Reptilia: Squamata) from Caatinga Biome, Northeastern Brazil. Comparative Parasitology, 79, 56 63. Baker, M.R. & Vaucher, C. (1986) Parasitic helminths from Paraguay. XII. Aplectana railliet and Henry, 1916 (Nematoda: Cosmocercoidea) from frogs. Revista Suisse du Zoologie, 93, 607 616. Baylis, H.A. (1936) Nematoda. I. Ascaridoidea and Strongyloidea. The fauna of British India. Taylor and Francis, London, 408 pp. Bezerra, C.H., Braga, R.R., Borges-Nojosa., D.M. & Silva, G.A. (2012) Occurence of spargana infection in Dermatonotus muelleri (Boettger 1885) (Anura, Microhylidae) from a coastal complex in northeastern Brazil. Herpetology Notes, 5, 69 71. Brito, S.V., Ferreira, F.S., Ribeiro, S.C., Anjos, L.A., Almeida, W.O., Mesquita, D.O. & Vasconcellos, A. (2014) Spatialtemporal variation of parasites in Cnemidophorus ocellifer (Teiidae) and Tropidurus hispidus and Tropidurus semitaeniatus (Tropiduridae) from Caatinga áreas in northeastern Brazil. Parasitology Research, 113, 1163 1169. http://dx.doi.org/10.1007/s00436-014-3754-7 NEW SPECIES PARAPHARYNGODON Zootaxa 4012 (2) 2015 Magnolia Press 389
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