A New Species of Cosmocercoides (Nematoda: Cosmocercidae) From a Gymnophthalmid Lizard of Western Brazil

J. Parasitol., 96(3), 2010, pp. 558–560 F American Society of Parasitologists 2010

A NEW SPECIES OF COSMOCERCOIDES (NEMATODA: COSMOCERCIDAE) FROM A GYMNOPHTHALMID LIZARD OF WESTERN BRAZIL ´ vila, Christine Stru¨ssmann*, and Reinaldo J. da Silva Robson W. A Departamento de Parasitologia, Instituto de Biocieˆncias, UNESP, Distrito de Rubia˜o Jr., CEP 18618-000, Botucatu, SP, Brazil. e-mail: robsonavila@ gmail.com ABSTRACT: Cosmocercoides sauria n. sp., an intestinal parasite of the gymnophthalmid lizard Iphisa elegans from western Brazil, is described. Of the 18 species previously described, C. sauria represents the 19th species, and is the third to be reported in the Neotropical region. Moreover, C. sauria is the second species reported from a reptilian host and is distinguished by a smaller number of rosette papillae (4 pairs). Additionally, the new species can be distinguished from the other Neotropical species (Cosmocercoides lilloi Ramallo, Bursey and Goldberg, 2007 and C. variabilis (Harwood, 1930)) by possessing smaller spicule size and presence of both gubernaculum and lateral alae in Cosmocercoides lilloi.

the Depart, amento de Parasitologia, Instituto de Biocieˆncias (CHIBB 3123, 3125, and 3089), Universidade Estadual Paulista – UNESP, Botucatu municipality, Sa˜o Paulo State, Brazil. Illustrations were made with the aid of a drawing tube. The host lizards were fixed in 10% formalin, preserved in 70% alcohol, and deposited in the Colec¸a˜o Zoolo´gica da Universidade Federal de Mato Grosso, Cuiaba´ municipality, Mato Grosso State, Brazil (UFMT 866, 5291, 5383, and 5328). Morphological data are generally presented as mean ± 1 SD (minimum and maximum) values. Measurements are in mm unless otherwise noted.

Although surveys on helminth parasites of South American lizards have recently increased (Goldberg et al., 2006; Sousa et al., 2007; Vrcibradic et al., 2008), reports on associated parasites of the diverse Gymnophthalmidae (40 genera presently known; see Uetz and Hallermann, 2008) are still scarce and are restricted to a few genera, i.e., Cercosaura Wagler, 1830, Neusticurus Dume´ril and Bribon, 1839, Potamites Doan and Castoe, 2005, and Alopoglossus Boulenger, 1885, (Bursey and Goldberg, 2004; Bursey et al., 2005; Goldberg and Bursey, 2007; Goldberg et al., 2007). Available data on major families of nematodes infecting Gymnophthalmidae lizards refer mainly to Cosmocercidae and, to a lesser extent, to Kathlanidae, Molineidae, and Physalopteridae. Species of Cosmocercinae (Cosmocercidae) belong to genera commonly reported as parasites of amphibians and reptiles, i.e., Aplectana Railliet and Henry, 1916, Cosmocerca Diesing, 1861, Cosmocercella Steiner, 1924, and Cosmocercoides Wilkie, 1930 (Travassos, 1931). There are currently 18 species of Cosmocercoides, with a worldwide distribution (Rizvi, 2009). In the Neotropical region, only Cosmocercoides lilloi Ramallo, Bursey and Goldberg, 2007 and C. variabilis (Harwood, 1930) have been reported in the bufonid toad Rhinella arenarum (Hensel, 1867) (Ramallo et al., 2007). During a helminthological survey of helminth parasites of lizards from a locality in western Brazil, the gymnophtalmid lizard Iphisa elegans Gray, 1851, was found to harbor nematodes of an undescribed species of Cosmocercoides, which are herein described as new.

RESULTS Necropsy revealed 9 nematodes in the small and large intestine of 4 lizards. Two adult females of I. elegans harbored only 1 nematode, and 2 other adult female lizards had 3 and 4 nematodes each. The nematodes were found in the small and large intestine of 4 of the 11 examined lizards, a prevalence of 36%. After careful examination and comparison with available descriptions of congenerics, it became clear that the nematodes found in I. elegans belonged to a previously undescribed species. DESCRIPTION Cosmocercoides sauria n. sp. (Figs. 1A–G) Male (Figs. 1A–D) based on 1 adult specimen (CHIOC 35654a): Length 1.3 mm; width at midbody 156.2. Esophagus 288 long: pharyngeal portion 22.3 long, corpus 237.4 long, bulb length 51.5; bulb width 62.1. Nerve ring 92.0; excretory pore 134.9 from anterior end. Tail 54.3 long, tappering. Spicules equal, 103.7 long, width at distal portion 9.6. Gubernaculum 96.5 long, width at distal portion 27.8. Lateral alae 871.2, beginning at 335.7 from anterior end and ending at 93.3 from posterior end. Twenty-two pairs of caudal papillae, plus 3 unpaired papillae (Figs. 1A, C); 4 precloacal pairs in rosette (Fig. 1D) with the last pair 69.6 from anal aperture; 5 pairs of simple papillae; 1 adanal pair of simple papillae and 12 pair of postanal simple papillae, with 1 pair dorsal plus 3 unpaired postanal papillae. Female (Fig. 1E–G), based on 4 adult specimens CHIOC 35654b, CHIBB 3125, and 3089): Length 5.2 ± 0.6 mm (4.7–6); width at midbody 329 ± 118.4 (262.5–505). Esophagus 467 ± 22.2 (444.2–493.5) long; pharyngeal portion 35.6 ± 3.4 (31.8–39.7) long, corpus 379.4 ± 18.3 (365.9–405.7) long, bulb length 99.7 ± 8.9 (88.8–110.4), bulb width 104 ± 6.4 (95.3–110.8). Nerve ring 194.2 ± 13.3 (180.3–209.1) from anterior end. Excretory pore 321.2 ± 63.0 (255.4–395.9) from anterior end. Vulva 2.2 ± 0.2 mm (2.1–2.2) from anterior end. Eggs (n 5 15) oval, thin-shelled with embryos, 57.1 ± 4.4 (48.9–65.1) long, 38.8 ± 2.7 (34.4–37.1) wide (Fig. 1G). Tail 244.8 ± 35.4 (196.7–280.9) long.

MATERIALS AND METHODS Eleven adult specimens of I. elegans (mean snout vent length 5 47.07 mm, SD 6.68 mm) were analyzed. All the lizards were collected by hand, from May–October 2002, during a faunal rescue program at the site of construction of the reservoir of the Guapore´ hydroelectric power plant, Vale de Sa˜o Domingos municipality, Mato Grosso State, Brazil. Helminths found in the small and large intestine of the lizards were fixed in a solution of alcohol–formalin–acetic acid, cleared in lactophenol, and examined using a light microscope. The holotype and allotypes of the new nematode species described herein were deposited in the Colec¸a˜o Helmintolo´gica of the Instituto Oswaldo Cruz (CHIOC 35654a and 35654b, respectively), Rio de Janeiro State, Brazil. Paratypes were deposited in the Colec¸a˜o Helmintolo´gica of Received 16 September 2009; revised 9 December 2009; accepted 10 December 2009. * Departamento de Cieˆncias Ba´sicas e Produc¸a˜o Animal, Faculdade de Agronomia e Medicina Veterina´ria, UFMT, Av. Fernando Correˆa da Costa, CEP 78060-900, Cuiaba´, MT, Brazil. DOI: 10.1645/GE-2336.1

Taxonomic summary Type host: Iphisa elegans (glossy shade lizard); Universidade Federal de Mato Grosso (UFMT 5291); collection date 3 October 2002. 558

A´VILA ET AL.—COSMOCERCOIDES SAURIA N. SP.

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FIGURE 1. Cosmocercoides sauria n. sp. (A) Male holotype. Bar 5 200 mm. (B) Anterior end of male. Bar 5 200 mm. (C) Posterior end of male, lateral view. Bar 5 50 mm. (D) Caudal rosette papilla. Bar 5 10 mm. (E) Anterior end of female. Bar 5 200 mm. (F) Posterior end of female, lateral view. Bar 5 500 mm. (G) Egg. Bar 5 30 mm. Arrows indicate the unpaired papillae.

Type locality: Vale de Sa˜o Domingos municipality, Mato Grosso state, Brazil, 15u079S, 58u589W. Site of infection: Small and large intestine. Specimens deposited: Instituto Oswaldo Cruz, Rio de Janeiro, RJ, Brazil; Holotype No. CHIOC 35654a, adult male; Allotype No. CHIOC

35654b, adult female; Colec¸a˜o Helmintolo´gica do Instituto de Biocieˆncias, Botucatu, SP, Brazil; Paratypes, 3 adult females, CHIBB 3125 and 3089, and 1 juvenile female, CHIBB 3123. Etymology: The new species is named in reference to the order Sauria, to which the host belongs.

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Remarks

LITERATURE CITED

By possessing only 4 pairs of rosette papillae, the new species is promptly distinguished from the 18 previously described species of Cosmocercoides. The number of rosette papillae is the lowest recorded for the genus, followed by 5 pairs in C. lanceolatus Rao, 1979 and C. barodensis Rao, 1979, and by 8 pairs in C. oligodentis Wang, Sun, Zhao, and Zhang, 1981. The new species is also distinguished from C. lilloi Ramallo, Bursey, and Goldberg, 2007 and C. microhylae (Wang, Zhao, and Chen, 1978) by gubernaculum present (gubernaculum absent in C. lilloi and C. microhylae; see Ramallo et al., 2007). It differs from C. fotedari Arya, 1991 and C. kumaoni Arya, 1991, by the presence of lateral alae and equal spicules (see Rizvi, 2009); from C. nainitalensis Arya, 1979 by its small body size (1.3 mm vs. 4.9–5.5 mm) and equal spicules (Arya, 1979); and from C. lilloi, C. karnatakaensis, C. pulcher Wilkie, 1930, and C. tibetanum (Baylis, 1927) by the presence of lateral alae and smaller spicule size (103 vs. 160–210, 245–265, 247, and 580, respectively). Smaller spicule size also distinguishes the new species from C. dukae (Holl, 1928) (290), C. variabilis (Harwood, 1930) (250–420), C. barodensis (230–240), C. bufonis Karve, 1944 (190–260), C. lanceolatus (210), C. multipapillata Khera, 1958 (200–240), C. rickae Ogden, 1966 (168), C. ranae Wang, Sun, Zhao, and Zhang, 1981 (192), and C. tridens Wilkie, 1930 (270–530).

DISCUSSION Cosmocercoides sauria n. sp. is the 19th species assigned to the genus and the Cosmocercoides third species recorded for the Neotropical region (Bursey and Goldberg, 2006; Ramallo et al., 2007; Rizvi, 2009). All species of Cosmocercoides have been reported from amphibian hosts, except for C. variabilis (which has amphibian hosts, too) and Cosmocercoides sauria n. sp., which have reptilian hosts (Bursey et al., 2007; present work). The life cycle of the new species is unknown, but studies with C. variabilis in anurans showed that eggs laid by female worms develop into first stage larvae in the external environment, and molt twice to the infective third stage larvae, before they infect the host via skin penetration (Anderson, 2000). ACKNOWLEDGMENTS We are grateful to Marcos Andre´ de Carvalho, who provided access to lizards for dissection. This study had financial support by FAPESP (process 06/59692-5). R.W.A. thanks CAPES for a grant.

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