A NEW SPECIES OF SPAULIGODON (NEMATODA: PHARYNGODONIDAE) PARASITE OF CNEMIDOPHORUS SPP. (LACERTILIA: TEIIDAE) FROM SOUTHERN MEXICO

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1 J. Parasitol., 89(2), 2003, pp American Society of Parasitologists 2003 A NEW SPECIES OF SPAULIGODON (NEMATODA: PHARYNGODONIDAE) PARASITE OF CNEMIDOPHORUS SPP. (LACERTILIA: TEIIDAE) FROM SOUTHERN MEXICO F. Agustín Jiménez-Ruiz, Virginia León-Règagnon*, and Jonathan A. Campbell The Harold W. Manter Laboratory of Parasitology, W529 Nebraska Hall, University of Nebraska, Lincoln, Nebraska fruiz@unlserve.unl.edu ABSTRACT: A new species of Spauligodon collected from Cnemidophorus mexicanus and C. deppii is described in this study. The species is placed in Spauligodon because the caudal alae start at the level of the precloacal papillae and embed the adcloacal papillae. The new species is most similar to S. goldbergi, but diagnostic traits of the former are the presence of 2 ridges in lateral alae, flaplike expansions in the caudal end of lateral alae, and a smooth tail for males. This species is the eighth recorded in the neotropics. Spauligodon Skrjabin, Schikhobalova and Lagodovskaja, 1960, is a cosmopolitan genus of pharyngodonid nematodes that comprises 36 species (see Bursey and Goldberg, 1999; Ramallo et al., 2002); 4 of them occur in the Nearctic region and 7 in the neotropics, and 1 was known in Mexico (Goldberg et al., 1996), occurring in the transition zone. As part of a recent inventory of parasites of amphibians and reptiles in Oaxaca, Mexico, an undescribed species of Spauligodon was found in specimens of Cnemidophorus deppii Wiegmann, 1834 and C. mexicanus Peters, Cnemidophorus (Wright, 1993) contains around 50 species occurring in the New World; whiptails and racerunners are common in southwestern United States and Mexico (Reeder et al., 2002). The black-bellied racerunner, C. deppii, occurs in middle America, it ranges from the coastal lands of Michoacán and Veracruz to Costa Rica. It is found in open sunny areas in the lowlands (up to 1,500 m) and forages on a variety of insects (Duellman and Wellman, 1960). The Mexican whiptail, C. mexicanus, is a species restricted to the highlands of central Oaxaca (Wright, 1993). Although whiptails and racerunners are common members of the Mexican herpetofauna, only C. tigris Baird and Girard, 1852 has been surveyed for parasites in Mexico (Goldberg et al., 1998). MATERIALS AND METHODS In September 2001, specimens of C. mexicanus (2 individuals), C. deppei (3), and C. guttatus (3) were collected by hand in Oaxaca, Mexico. Whiptails were killed within 12 hr after capture with an overdose of sodium pentobarbital; carcasses were processed for preservation and deposition in museums according to techniques described by Simmons (1987). Voucher specimens are deposited in the Museo de Zoología, Facultad de Ciencias (MZFC), Universidad Nacional Autónoma de México (UNAM), and in the Herpetological Collection, University of Texas at Arlington (UTA). Both viscera and body cavity were examined for parasites in the field laboratory. Nematodes were killed in glacial acetic acid and stored in 70% ethanol. Nematodes were cleared in lactophenol fluid and identified following Petter and Quentin (1976) and Ramallo et al. (2002). Specimens described were compared with type and voucher specimens of S. goldbergi Bursey and McCallister, 1996 (accession numbers: 84520, of the United States National Parasite Collection, USNPC), type specimens of Pharyngodon kirbii Specian and Ubelaker, 1974 (USNPC 72618), vouchers of P. warneri Har- Received 10 August 2002; revised 4 November 2002; accepted 4 November * Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Apartado Postal , México, Distrito Federal, 04510, Mexico. Department of Biology, UTA Box 19498, University of Texas at Arlington, Arlington, Texas wood, 1932 (accession number: of the Harold W. Manter Laboratory of Parasitology [HWML] of the University of Nebraska Lincoln), and vouchers of P. giganticus (Read and Amrein, 1953) (HWML 22989). Drawings were made with a drawing tube attached to a Wild microscope. Measurements were made using a Zeiss Ultraphot microscope and digital measuring software (SigmaPro, San Rafael, California; Albinger et al., 1995). All measurements are provided in micrometers ( m); range, average, and coefficient of variation (Sokal and Rohlf, 1981) are provided. DESCRIPTION Spauligodon garciaprietoi n. sp. (Figs. 1 13) General: Small nematodes, white color in vivo. Both ends tapering gradually (Figs. 1, 2). Lateral alae with 2 ridges (Figs. 3, 4), extending from level of nerve ring to anal or cloacal level (Figs. 1, 2). Cuticle with fine transverse striations (Fig. 5). Stoma with 3 lips (Figs. 6, 7), esophagus divided into corpus and esophageal bulb (Figs. 8, 9). Excretory pore with conspicuous cuticularized walls (Figs. 5, 9, 10), surrounded by a rough cuticular area (Fig. 5). Male: Measurements based on 13 specimens, unless stated otherwise. Nematodes , 1891 (6.8) long; , 148 (10.3) wide at midbody level. Lateral alae , 1642 (7.6) long, starting slightly anterior to nerve ring (Fig. 8) and extending up to cloacal level (Figs. 11, 12); expanding in their posteriormost part forming flaplike expansions, , 145 (24) long and 12 47, 27 (25) wide. Esophagus , 286 (5.2) long; stoma 5 11, 8 (22) deep; corpus , 217 (5.8) long and 22 36, 29 (15.4) wide; bulb 62 77, 69 (5.9) long and 63 96, 78 (9.4) wide. Nerve ring and excretory pore at , 104 (13.7, n 9) and , 469 (7.6) from anterior end, respectively. Three pairs of mamiliform genital papillae present. Precloacal pair of papillae on swollen last portion of body; adcloacal pair completely embedded on caudal alae; postcloacal papillae mamiliform. Caudal alae embed precloacal and adcloacal papillae (Figs. 11, 12). Prominent, heavily cuticularized genital cone in midventral line (Figs. 11, 12). Spicule weakly cuticularized, 53 82, 69 (14.1) long. Tail acute, smooth; , 127 (19) long (Figs. 1, 11, 12). Female: Measurements based on 10 gravid specimens. Length , 4413 (6.3) by , 295 (12) width at midbody. Lateral alae uniform along their extension, from nerve ring to anal level. Stoma 7 10, 8 (14.1) deep; esophagus , 434 (7.5) in total length, corpus , 345 (8.8) long by 36 41, 38 (4) wide, bulb 77 95, 87 (5.9) long by , 99 (6.1) wide. Nerve ring, excretory pore, and vulva at , 131 (21.9), , 493 (7.3), and , 549 (7.7) from anterior end, respectively (Fig. 9). Ovijector , 698 (13.8) long, continued by vagina of variable length (Fig. 10). Two uteri present. Tail conical, smooth, , 960 (7.4) long (Fig. 2). Eggs barrel shaped, with polar plugs on each pole, , 148 (6.7) long by 31 52, 43 (11) wide (Fig. 13). Taxonomic summary Type specimens: Holotype Male Colección Nacional de Helmintos del Instituto de Biología, Universidad Nacional Autónoma de México, CNHE 4563; allotype CNHE 4564; paratypes CNHE 4565, CNHE 4566, and HWML Voucher USNPC

2 352 THE JOURNAL OF PARASITOLOGY, VOL. 89, NO. 2, APRIL 2003 FIGURES 1 7. Spauligodon garciaprietoi n. sp. 1. Ventral view of male; reference bar 150 m. 2. Lateral view of female; reference bar 300 m. 3. Cross section of male; reference bar 50 m. 4. Cross section of female; reference bar 50 m. 5. Ventral view of excretory pore of male; reference bar 30 m. 6. Face view of male; reference bar 10 m. 7. Face view of female; reference bar 15 m. Symbiotype: Cnemidophorus mexicanus Peters, 1869, UTA R51915, collected 22 September Type locality: Mitla, Oaxaca; N, W; 1,790 m. Other hosts: Cnemidophorus deppii Wiegmann, 1834, MZFC 14257; Elgaria kingii Gray, 1838, University of Arizona Herptile Collection UAZ 40032, Other localities: Cnemidophorus deppi from NW Totolapan, Oaxaca; N, W; 1,100 m. Elgaria kingii from Arizona. Site of infection: Rectum. Etymology: The species is named in honor of Luis García-Prieto, professor of parasitology at UNAM, collection manager of the CNHE, and a friend of ours. Diagnosis Species of Spauligodon differ from species of Skrjabinodon Inglis, 1968 because males of species of Skrjabinodon do not have caudal ala; they also differ from species included in Pharyngodon Diesing, 1861 because males of species in the latter have a caudal ala that includes the third pair of caudal papillae. Spauligodon garciaprietoi n. sp. was placed in the genus Spauligodon because the caudal alae of males of this species are supported by pairs 1 and 2 of caudal papillae. The new species is diagnosed by the presence of 2 ridges in the lateral alae (Figs. 3, 4), the position of the vulva in the anterior half of the body (Figs. 2, 9), the conical and smooth tail

3 JIMÉNEZ-RUIZ ET AL. A NEW SPECIES OF PINWORM IN WHIPTAILS 353 FIGURES Spauligodon garciaprietoi n. sp. 8. Anterior end of male in ventral view; reference bar 50 m. 9. Anterior end of female in lateral view; reference bar 100 m. 10. Ovijector and vagina; reference bar 50 m. 11. Ventral view of caudal end of male; reference bar 30 m. 12. Lateral view of caudal end of male; reference bar 50 m. 13. Eggs; reference bar 50 m.

4 354 THE JOURNAL OF PARASITOLOGY, VOL. 89, NO. 2, APRIL 2003 FIGURE 14. Cross section of Spauligodon goldbergi, male, note outline of lateral alae; reference bar 30 m. of females (Fig. 2), the formation of flaplike expansions in the caudal end of lateral alae (Fig. 11), and the acute and smooth tail of males (Figs. 11, 12). Spauligodon garciaprietoi n. sp. is most similar to S. goldbergi in that females of both species show a tail tapering to a point. Nevertheless, S. garciaprietoi n. sp. is unique in that the tails of the males show a smooth surface and in that lateral alae have 2 ridges, whereas S. goldbergi has 3 7 spines on the tail of males, and the lateral alae has a simple ridge, as observed on paratypes USNPC (Fig. 14) (Bursey and McCallister, 1996). DISCUSSION Spauligodon garciaprietoi n. sp. is the eighth species recorded in the neotropics, and it may be added to the list provided by Bursey and Goldberg (1999), with the following features: spicule present, tail of male smooth, tail of female tapering to a point, and barrel-shaped eggs. In addition, it may be differentiated from all the neotropical species in that males have 3 pairs of papillae and females have no filamentous tail. It is worth noting that S. garciaprietoi n. sp. is also similar to some species in the genus Pharyngodon that occur in the Nearctic. Shape of eggs and the overall structure of the tail in both males and females are some of the traits shared among these species. The species of Pharyngodon and Spauligodon that are included in this grouping also infect lizards of the family Teiidae or semifossorial reptiles (i.e., Sonora semmianulata) in both the Neotropic and Nearctic regions. These species are in group 1 of Table I. In contrast, the rest of the species in both Pharyngodon and Spauligodon that do not fit into the aforementioned group infect terrestrial or climbing reptiles (mainly Coleonyx, Tarentola, and Sceloporus). The common trait among these species of nematodes is the filiform tail of females, whereas the shape of the eggs seems to be variable. The species in which females have filiform tails are listed under group 2 of Table I. This entangled grouping of organisms belonging to 2 different genera seems to be a consequence of the heterogeneous perception that taxonomists have of the caudal papillae and their relationship to the caudal alae (see Read and Amrein, TABLE I. Groups of species of Spauligodon and Pharyngodon from the Nearctic and Neotropical realms (as presented by Golberg and Bursey, 1996, 1999) that occur in semifossorial host species (group 1) and in terrestrial or climbing species (group 2).* Group 2 species infecting terrestrial and climbing lizards Group 1 species infecting semifossorial lizards Species of nematode Host Species of nematode Host Coleonyx brevis Coleonyx elegans Anolis spp. Coleonyx variegatus Tarentola americana Sceloporus spp. Liolaemus spp. Streptosaurus mearnsi Thecadactylus rapicaudus P. mudgi Specian and Ubelaker, 1974 P. yucatanensis Chitwood, 1938 S. anolis (Chitwood, 1938) S. californiensis (Read and Amrein, 1953) S. cubensis (Read and Amrein, 1953) S. giganticus (Read and Amrein, 1953) S. loboi Ramallo et al., 2002 S. mearnsi (Edgerly, 1952) S. oxkutzcabiensis (Chitwood, 1938) Cnemidophorus lemniscatus Cnemidophorus resselatus Cnemidophorus scalaris Cnemidophorus sp. Ameiva sp. Cnemidophorus sexlineatus Sonora semiannulata Cnemidophorus spp. P. cesarpintoi Pereira, 1935 P. cnemidophori Read and Amrein, 1953 P. kirbii Specian and Ubelaker, 1974 P. papillocauda Hannum, 1942 P. travassosi Pereira, 1935 P. warneri Harwood, 1932 S. goldbergi Bursey and McAllister, 1996 S. garciaprietoi n. sp. * Both S. antillarum, S. maytacapaci, and S. viracochai were excluded because species of host is not stated. Description of P. micrurus was unavailable. Neotropic region. Nearctic region.

5 JIMÉNEZ-RUIZ ET AL. A NEW SPECIES OF PINWORM IN WHIPTAILS ; Specian and Ubelaker, 1974). A revision of both genera is needed. The coevolutionary or colonization patterns (or both) among species of pharyngodonid nematodes and lizards must be tested, and only the continuation of the systematic survey of parasites of lizards in this and other areas in both the Neotropic and Nearctic regions and the study of their phylogenetic relationships will allow scientists to test these hypotheses within a phylogenetic framework. The key that we provide below include the species of Spauligodon of the New World. KEY FOR SPECIES OF SPAULIGODON IN THE NEW WORLD 1a. Tail of females tapering to a point b. Tail of female filiform or spikelike a. Tail of male with 3 7 spines S. goldbergi Bursey and McCallister, b. Tail of male smooth...s. garciaprietoi n. sp. 3a. Tail of female spikelike with 2 terminal papillae, eggs knobbed...s. maytacapaci (Vicente and Ibañez, 1968) 3b. Tail of females filiform a. Spicule present, eggs barrel shaped, spiny tail of females S. mearnsi (Edgerly, 1952) 4b. Spicules absent a. Tail of males spined b. Tail of males smooth a. Tail of females smooth, eggs knobbed......s. loboi Ramallo et al., b. Tail of females spined a. Ten to eleven spines on female tail, eggs knobbed......s. giganticus (Read and Amrein, 1953) 7b. Eight to fifteen spines on female tail, eggs barrellike S. antillarum Barûs and Coy Otero, c. Eight to eleven spines on female tail, eggs oval S. anolis (Chitwood, 1938) 8a. Tail of female smooth...s. cubensis (Read and Amrein, 1953) 8b. Tail of female spined a. Tail of females with 2 spines on tip, eggs spindle shaped......s. viracochai (Freitas, Vicente and Ibañez, 1968) 9b. Tail of females with more than 9 spines on surface, eggs knobbed or barrellike a. Eggs knobbed, spines on tail of females......s. oxkutzcabiensis (Chitwood, 1938) 10b. Eggs truncated, 9 12 spines on tail of females......s. californiensis (Read and Amrein, 1953) ACKNOWLEDGMENTS We thank Ma. Antonieta Arizmendi, Luis Canseco, Sergio Guillén, Valerie Mackenzie, Adrián Nieto, Alejandro Oceguera, Laura Paredes, Edmundo Pérez, and Erik Smith for their help in the collection of specimens. We thank the following individuals for the loan of specimens: Eric Hoberg and Pat Pilitt from the USNPC and Scott Gardner and Mauritz Sterner from HWML. We also thank Scott Gardner for critical review of the manuscript. This study was funded by National Science Foundation grant DEB to J.A.C., CONACYT projecto J27985-N to V.L.-R., and CONACYT in the form of a graduate scholarship to F.A.J.-R. LITERATURE CITED ALBINGER, G. A. F., JR., K. KERLE, N. LINK, A. MACY, AND S. SIMON SigmaScan Pro. Jandel Scientific Software, San Rafael, California. BURSEY, C. R., AND S. R. GOLDBERG Pharyngodon lepidodactylus sp. n. 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