SPAULIGODON LOBOI N. SP. (NEMATODA: PHARYNGODONIDAE) PARASITE OF LIOLAEMUS SPP. (IGUANIA: LIOLAEMIDAE) FROM NORTHWESTERN ARGENTINA Author(s): Geraldine Ramallo , Charles R. Bursey , Stephen R. Goldberg Source: Journal of Parasitology, 88(2):370-374. 2002. Published By: American Society of Parasitologists DOI: http://dx.doi.org/10.1645/0022-3395(2002)088[0370:SLNSNP]2.0.CO;2 URL: http://www.bioone.org/doi/full/10.1645/0022-3395%282002%29088%5B0370%3ASLNSNP %5D2.0.CO%3B2
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J. Parasitol., 88(2), 2002, pp. 370–374 q American Society of Parasitologists 2002
SPAULIGODON LOBOI N. SP. (NEMATODA: PHARYNGODONIDAE) PARASITE OF LIOLAEMUS SPP. (IGUANIA: LIOLAEMIDAE) FROM NORTHWESTERN ARGENTINA Geraldine Ramallo, Charles R. Bursey*, and Stephen R. Goldberg† Instituto de Invertebrados, Fundacio´n Miguel Lillo, Miguel Lillo 251, (4000) San Miguel de Tucuma´n, Argentina. e-mail:
[email protected] ABSTRACT: Three-hundred and forty-nine specimens of Spauligodon loboi n. sp. (Nematoda, Pharyngodonidae) were found in the large intestines of 55 of 225 adult specimens representing 5 species of Liolaemus collected in 11 localities of northwestern Argentina. Prevalence of infection was 24% (mean intensity 5 6.3 6 3.4, range 5 2–28). Spauligodon loboi n. sp. differs from other neotropical species in that the filamentous portion of the tail of males is spiny, whereas that of females is smooth. A key to the species of Spauligodon in the Neotropical Realm is provided.
tonio de los Cobres, Cachi, and La Poma, Province of Salta; and Tilcara and Humahuaca, Province of Jujuy, Argentina, at 3,800 to 4,500-m elevation. The stomach, intestines, cloaca, liver, lungs, gonads, and peritoneum of each specimen were searched for helminths using a stereomicroscope. Nematodes were placed in lactophenol, allowed to clear, and examined under a light microscope. Nematodes were deposited in the Coleccio´n Helmintolo´gica Fundacio´n Miguel Lillo (CH-FML). Drawings were made using a camera lucida. Prevalence and mean intensity were calculated based on the definitions of Bush et al. (1997). Measurements are in millimeters, unless otherwise indicated, and are presented as mean 6 SD followed by range in parentheses.
Liolaemus Wiegman, 1834, (Iguania: Liolaemidae) is a large genus (approximately 150 species) of small- to moderate-sized lizards that are mostly terrestrial and restricted to austral South America, where they occupy a variety of habitats from sea level to 5,000 m in elevation (Etheridge, 2000). They are typically omnivorous, although a few vegetarian species exist (Cei, 1986). Sister genera include Tropidurus Wied-Neuwied, 1825, Phymaturus Gravenhorst, 1838, and Sternocercus Dume´ril and Bibron, 1837 (see Cei, 1993). There are only a few reports of parasitism in species of Liolaemus (Rodrigues, 1992; Rocha, 1995; Ramallo and Diaz, 1998; Goldberg et al., 2001). Pharyngodonidae Travassos, 1919 (Nematoda: Oxyuroidea) contains 21 genera (Petter and Quentin, 1976). Of these, 3 genera, Pharyngodon Diesing, 1861, Spauligodon Skrjabin, Schikhobalova, Lagodovskaja, 1960, and Skrjabinodon Inglis, 1968, found primarily in reptiles, exhibit a vulvar opening in the anterior part of the body just behind the postbulbar excretory pore. These genera are separated by the relationship of the caudal alae to the genital papillae (Bursey and Goldberg, 1995). There are currently 35 nominal species of Spauligodon that occur in lizards of the Agamidae, Chamaleonidae, Gekkonidae, Lacertidae, Opluridae, Phrynosomatidae, Polychrotidae, Scincidae, Teiidae, and Tropiduridae. Of these, 18 are found in the Palearctic Realm, 6 in the Neotropical Realm, 4 in the Nearctic Realm, 4 in the Ethiopian Realm, 2 in Oceania, and 1 in the Australian Realm (Bursey and Goldberg, 1999, table I). This paper describes the seventh species of Spauligodon from the Neotropical Realm. A key for the identification of the members of Spauligodon, parasitic in lizards of the Neotropical Realm, is provided.
DESCRIPTION
Spauligodon loboi n. sp. (Figs. 1–3)
MATERIALS AND METHODS Thirteen Liolaemus capillitas Hulse, 1979 (10 females and 3 males), 51 Liolaemus huacahuasicus Laurent, 1985 (29 females, 22 males), 53 Liolaemus ornatus Koslowsky, 1898 (34 females, 19 males), 53 Liolaemus quilmes Etheridge, 1993 (32 females, 21 males), and 55 Liolaemus ramirezae Lobo and Espinoza, 1999 (31 females, 24 males) were dissected. Lizards were collected (1974–1991) in the localities of Tafı´ del Valle and Amaicha del Valle, Province of Tucuma´n; El Cerrillo, Andalgala´, Bele´n, and Santa Marı´a, Province of Catamarca; San An-
Received 17 May 2001; revised 23 August 2001; accepted 23 August 2001. * Department of Biology, Pennsylvania State University, Shenango Campus, Sharon, Pennsylvania 16146. † Department of Biology, Whittier College, Whittier, California 90608. 370
General: Nematodes of small size, with cylindrical body tapering both anteriorly and posteriorly. Cuticule transversely striated. Lateral alae present only in males. Mouth opening triangular, bounded by 3 bilobed lips, each with 1 small papilla (Fig. 1a). Esophageal bulb valvulate, subspherical, separated from esophageal corpus by slight constriction. Excretory pore behind esophageal bulb. Male (based on 23 adult specimens): Small, white, fusiform. Length (to second postanal pair of caudal papillae) 2.20 6 0.57 (1.02–3.36), maximum width 0.52 6 0.14 (0.25–0.76). Lateral alae 0.022 6 0.003 (0.017–0.033) wide. Cuticule with striations at approximately 2.9mm interval width. Esophagus (including bulb) 0.36 6 0.04 (0.28– 0.43) long; bulb 0.10 6 0.01 (0.06–0.11) long; 0.10 6 0.01 (0.07– 0.12) wide. Nerve ring 0.14 6 0.02 (0.10–0.17), excretory pore 0.74 6 0.15 (0.44–1.03) from anterior end (Fig. 1b). Caudal alae present, 0.28 6 0.07 (0.16–0.43) wide by 0.27 6 0.06 (0.17–0.36) long. Three pairs of caudal papillae present: preanal pair situated on slightly inflated ventral surface, first postanal pair posteriolaterally directed, second postanal pair not enclosed by caudal alae. Spicule absent. Prominent genital cone in midventral line consisting of small, pointed anterior anal lip and larger posterior anal lip. Anus 0.10 6 0.02 (0.06–0.12) from second postanal caudal papillae. Filiform tail extending 0.49 6 0.06 (0.34–0.60) beyond second postanal papillae, with 5 (3–7) cuticular spines (Fig. 1c). Female (based on 24 gravid specimens): Medium, yellowish, fusiform. Length (to tail spike) 6.60 6 1.82 (3.80–10.07); maximum width 0.91 6 0.21 (0.56–1.29). Cuticule with striations at approximately 4.1mm interval width. Esophagus (including bulb) 0.71 6 0.04 (0.63–0.80) long; bulb 0.14 6 0.01 (0.12–0.16) long, bulb 0.17 6 0.01 (0.15–0.19) wide. Nerve ring 0.16 6 0.01 (0.15–0.19), excretory pore 0.91 6 0.11 (0.72–1.13), vulva 1.01 6 0.13 (0.80–1.21) from anterior end (Fig. 2a). Ovary and uterus not extending anteriorly beyond esophageal bulb. Eggs fusiform 0.11 6 0.01 (0.10–0.13) 3 0.040 6 0.004 (0.040–0.050), slightly flattened on 1 side, no polar adornment (Fig. 2b). Anus 0.77 6 0.23 (0.48–1.24) from posterior end of body. Stiff tail spike 0.18 6 0.02 (0.13–0.20) long, terminating in smooth filamentous extension 0.34 6 0.01 (0.32–0.36) in length (Fig. 2c). Sometimes filamentous extension not observed, probably because it is somewhat fragile and breaks away during collection and processing (Fig. 3).
RAMALLO ET AL.—SPAULIGODON LOBOI N. SP.
FIGURE 1.
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Spauligodon loboi n. sp. a. Female, en face view. b. Male, anterior end, lateral view. c. Male, posterior end, ventral view.
Taxonomic summary Type specimen: Holotype: female CH-FML # 03911; allotype: male # 03916; paratypes (2 females, 2 males) # 03970. Type host: Liolaemus capillitas Hulse, 1979 (Iguania, Liolaemidae), Herpetology Collection FML # 2029-3, collected 2 November 1987. Additional hosts: Liolaemus huacahuasicus, L. quilmes, L. ornatus, L. ramirezae. Type locality: Morro El Arenal (3,800 m.a.s.l), Andalgala´, Province of Catamarca, Argentina, 278369S, 668199W. Additional localities: km 98, Route 307, Amaicha del Valle, Tafı´ del Valle, Tucuma´n and Huacahuasicus lagoons (4,250 m.a.s.l.) E Isabel hill, W El Negrito hill, Tafı´ del Valle, Province of Tucuma´n, Argentina. Site of infection: Large intestine.
Prevalence: Six of thirteen (46%) L. capillitas harbored 45 S. loboi n. sp. Mean intensity: 7.5 nematodes for each lizard. Etymology: The specific epithet is given in honor of Dr. Fernando Lobo, Professor of Comparative Anatomy, Faculty of Natural Sciences, National University of Salta, Province of Salta, Argentina.
REMARKS The present species is assigned to Spauligodon because only the 2 anterior pairs of caudal papillae are enclosed within the caudal alae. Species of Spauligodon are distinguished on the basis of the presence or the absence of a spicule and cuticular
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FIGURE 2.
Spauligodon loboi n. sp. a. Female, anterior end, lateral view. b. Eggs. c. Female, posterior end, lateral view.
spines on the tail filaments of adult specimens, the shape of the egg, and the geographical distribution (Bursey and Goldberg, 1999, table I). Only 1 species has been reported to have tail filaments, without spines in females and with spines in males, i.e., Spauligodon tectipenis Gedoelst, 1919 (Skrjabin et al., 1960). This Palaearctic species is geographically isolated from S. loboi n. sp. Chabaud and Brygoo (1962) suggested that geographical distribution is the most important factor in the speciation of reptilian oxyurids. Six previously described species have been found in the Neotropical Realm, i.e., S. oxkutzcabiensis Chitwood, 1938, S. cubensis Read and Amrein, 1953, S. maytacapaci (Vicente and Iba´n˜ez, 1968), S. antillarum Barusˇ and Coy Otero, 1974, S. viracochai Freitas, Vicente, and Iba´n˜ez, 1968, and S. anolis Chitwood,
1934 (syn. S. caymanensis [Bursey and Goldberg, 1995]). Spauligodon loboi n. sp. is most similar to S. maytacapaci (compare Fig. 3 with Fig. 4), especially when the filamentous extension has broken away; however, the adorned tail spike (2 terminal sessile papillae) of S. maytacapaci easily distinguishes it from S. loboi which lacks such an adornment (Vicente and Iba´n˜ez, 1968). Spauligodon loboi also differs from other Neotropical species in which females have a filamentous and flexible tail. Liolaemus capillitas had the highest prevalence (46%), whereas L. ornatus had the lowest prevalence (15%). Liolaemus huacahuasicus had the greatest mean intensity (11.1), whereas the lowest mean intensity (2) was recorded in L. ornatus and L. ramirezae. Ecological parameters for the infected species of Liolaemus are given in Table I.
RAMALLO ET AL.—SPAULIGODON LOBOI N. SP.
FIGURE 3. mm. FIGURE 4.
Photomicrograph of the tail spike of female Spauligodon loboi n. sp., in which the filamentous portion has broken away. Bar 5 36 Photomicrograph of the tail spike of female S. maytacapaci. Note the 2 terminal sessile papillae. Scale 5 35.4 m.
KEY TO THE NEOTROPICAL SPECIES OF THE GENUS SPAULIGODON SKRJABIN, SCHIKHOBALOVA, LAGODOVSKAJA, 1960 1a. Male with more than 4 pairs of caudal papillae; female without filamentous tail but with 2 sessile papillae at the caudal end . . . . . . . . . . . . . . . . S. maytacapaci Vicente and Iba´n˜ez, 1968 1b. Male with 3 or 4 pairs of caudal papillae; female with filamentous tail . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 2a. Eggs oval shaped; filamentous tail of both male and female with cuticular spines . . . . . . . . . . . . . . . S. anolis Chitwood, 1938 2b. Eggs not oval shaped . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 3a. Male or female (or both) with smooth filamentous tail . . . . . . . . . . . . . . . . . . . . . . . . . . S. cubensis Read and Amrein, 1953 3b. Male and female with no smooth filamentous tail . . . . . . . . . 4 4a. Male and female with spiny filamentous tail . . . . . . . . . . . . . . . . . . . . . . . . . . . S. antillarum Barusˇ and Coy-Otero, 1974 4b. Male or female spiny filamentous tail, but not in both . . . . . . 5 5a. Male with spiny filamentous tail; females with smooth filamentous tail . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .S. loboi n. sp. 5b. Male with smooth filamentous tail; females with spiny filamentous tail . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
TABLE 1. Ecological parameters (as defined by Bush et al., 1997) for the nematode Spauligodon loboi n. sp. in Liolaemus spp. from northwestern Argentina.
L. L. L. L. L.
373
Host species
n
A*
B†
C‡
capillitas huacahuasicus ornatus quilmes ramirezae
13 51 53 53 55
6 20 8 9 12
46 39 15 17 22
7.5 11.1 2 5 2
n 5 number of examined lizards; A* 5 number of infected lizards; B† 5 prevalence; C‡ 5 mean intensity.
6a. Filamentous tail with 2 spines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . S. viracochai Freitas, Vicente, and Iba´n˜ez, 1968 6b. Filamentous tail with more than 2 spines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . S. oxkutzcabiensis Chitwood, 1938
ACKNOWLEDGMENT We thank Fundacio´n Miguel Lillo (FML) for permission to examine Liolaemus spp. from the Herpetology Collection for helminths.
LITERATURE CITED BURSEY, C. R., AND S. R. GOLDBERG. 1995. Spauligodon caymanensis sp n. (Nematoda: Pharyngodonidae) from Anolis conspersus (Sauria: Polychridae) from Grand Cayman Island, British West Indies. Journal of the Helminthological Society of Washington 62: 183– 187. ———, AND ———. 1999. Spauligodon ovifilus n. sp. (Nematoda: Pharyngodonidae) and other helminths from Diplodactylus stenodactylus (Reptilia: Gekkonidae) from Australia. Journal of Parasitology 85: 898–902. BUSH, A. O., K. D. LAFFERTY, J. M. LOTZ, AND A. W. SHOSTAK. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83: 575–583. CEI, J. M. 1986. Reptiles del centro, centro-oeste y sur de la Argentina. Herpetofauna de las zonas a´ridas y semia´ridas. Museo Regionale di Scienze Naturali Torino, Monografı´a IV, Torino, Italia, 527 p. ———. 1993. Reptiles del noroeste, nordeste y este de la Argentina. Herpetofauna de las selvas subtropicales, puna y pampas. Museo Regionale di Scienze Naturali Torino, Monografı´a XIV, Torino, Italia, 949 p. CHABAUD, A. G., AND E. R. BRYGOO. 1962. Ne´matodes parasites de Came´leons malgaches. Deuxieme note. Annales de Parasitologie Humaine et Compare´e 37: 569–602. ETHERIDGE, R. 2000. A review of lizards of the Liolaemus wiegmannii group (Squamata, Iguania, Tropiduridae), and a history of morphological change in the sand-dwelling species. Herpetological Monographs 14: 293–352. GOLDBERG, S. R., G. MUN˜OZ, F. GARCIAS, AND C. R. BURSEY. 2001.
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RODRIGUES, H. DE O. 1992. Pseudocapillaria (Ichthyocapillaria) maricaensis n. sp. (Nematoda, Capillariidae) and remarks on the helminthological fauna of Liolaemus lutzae Mertens, 1938 (Lacertilia, Iguanidae). Memorias do Instituto Oswaldo Cruz 87: 297–300. SKRJABIN, K. I., N. P. SCHIKHOBALOVA, AND E. A. LAGODOVSKAJA. 1960. Oxyurata of animals and man. Part one. Oxyuroidea. Izdatel’stvo Akademii Nauk SSSR, Moskva. Israel Program for Scientific Translation, Jerusalem, 526 p. [Translated from Russian.] VICENTE, J. J., AND N. H. IBA´N˜EZ. 1968. Nova espeˆcie do geˆnero Parathelandros Baylis, 1930 (Nematoda, Oxyuroidea). Atas Sociedade de Biologia de Rio de Janeiro 11: 185–187.
