J. Parasitol., 92(1), 2006, pp. 100–104 q American Society of Parasitologists 2006
A NEW SPECIES OF TRICHURIS (NEMATODA: TRICHURIDAE) FROM PHYLLOTINI RODENTS IN ARGENTINA Marı´a del Rosario Robles, Graciela T. Navone, and Juliana Notarnicola Centro de Estudios Parasitolo´gicos y de Vectores (CEPAVE) (CONICET-UNLP). Calle 2 # 584 (1900) La Plata, Argentina. e-mail:
[email protected] ABSTRACT: A new species of Trichuris is described. Trichuris pardinasi n. sp. was recovered from Phyllotis xanthopygus Waterhouse (Rodentia: Muridae: Phyllotini) in Sierra de la Ventana, Buenos Aires Province, and Pampa de Achala, Co´rdoba Province (Argentina). This is the first record of Trichuris parasitizing Phyllotini rodents. The new species can be differentiated from the other 10 species parasitizing rodents from South America by the absence of the spicular tube, spicular sheath with spines uniformly distributed, the length of spicule, the J-shaped proximal cloacal tube, and the nonprotrusive vulva. Also, a description of the bacillary band is provided. The present and the future findings of shared parasite fauna from both populations of P. xanthopygus in these disjunct areas will support the hypothesis of a continuous distribution of this host species at a past time.
Some specimens were dehydrated in a series of ethanol, dried using the critical point method, examined by SEM (Jeol/SET 100t/Jeol 6360 LV), and photographed. Measurements are presented as follows: holotype, allotype, and paratypes; mean, standard deviations, and ranges enclosed in parentheses. All measurements are given in millimeters. When #3 whipworms are given, the measurements are separated by hyphens. Some authors use different terms when refering to the same structure related to the reproductive system of the male, resulting in a confused terminology. Thus, we summarize below the following terms. Sperm duct: The duct behind the testis, and its end is at the junction with the intestine. The sperm duct is divided in 2 portions, i.e., the anterior portion designated as vas deferens, and the posterior portion designated as ejaculatory duct (Chandler, 1930). The sperm duct has been called vas deferens by other authors (e.g., Suriano and Navone, 1994) or ejaculatory duct (e.g., Spakulova, 1994). Cloacal tube: Begins at the junction of the ejaculatory duct with the intestine. It is a muscular duct divided into 2 portions, the proximal cloacal tube and the distal cloacal tube (Wright, 1978). Proximal cloacal tube is frequently narrow, and ‘‘e’’, ‘‘J’’, ‘‘U’’, or ‘‘8’’ shaped (Babero and Murua, 1990). The distal cloacal tube is wider than the proximal cloacal tube, and the spicule lies into it (Wrigth, 1978). Spicular tube: It is a pouch containing the proximal part of the spicule, and its last portion is included in the distal cloacal tube. It is present in some species, i.e., T. ovis, T. fulvi, T. laevitestis and absent in others, i.e., T. chilensis, T. bradleyi, T. robusti. It is frequently designated as the ‘‘diverticulum’’ (Chandler, 1930), or true spicular tube (Babero and Muru´a, 1990; Suriano and Navone, 1994).
Trichuris Roederer, 1761 (Nematoda: Trichuridae) shows a cosmopolitan distribution, and comprises about 70 species that parasitize a broad spectrum of domestic and wild mammals (rumiants, marsupials, rodents, and primates, including human) (Cafrune et al., 1999). Many species of Trichuris are morphologically well defined; however, others were differentiated only by their host species (Beer, 1976). Therefore, many of these whipworms probably are synonyms. Several authors have attempted to determine what morphological characters are diagnostic at the specific level (Chandler, 1930; Knight, 1984; Tenora et al., 1997). Spakulova (1994) observed a considerable variation in the morphometric intraspecific characters between geographical region and host species. Other authors have used the scanning electron microscope (SEM) as a complement for the diagnosis of the species, detecting cuticular spines at the vulvar region and the spicular sheath (Kikuchi, 1974a, b; Wright, 1978; Gomez et al., 1992; Tenora et al., 1993) or the bacillary bands located in the thin portion (Wright, 1975; Gomez et al., 1992; Lanfredi et al., 1995). Currently, the characters with high discriminatory value for differentiating species of Trichuris include the presence or absence of the spicular tube, length of the spicule and the cloacal tube, shape of the proximal cloacal tube, the testis morphology, the vulvar morphology, the classical metric characteristics, and host species (Babero and Murua, 1990; Suriano and Navone, 1994). In this paper, we describe a new species of Trichuris, recovered from the caecum of Phyllotini rodents, from Buenos Aires and Co´rdoba Provinces, Argentina. Moreover, we summarize some confused terms related to the reproductive system given in the bibliography.
DESCRIPTION Trichuris pardinasi n. sp. (Figs. 1–16) General: Cuticle with fine transversal striation; anterior part of body long, narrow, tapered, and whip-like. Posterior part of body broad and handle-like (Fig. 1). Stichosome with 1 row of stichocytes and 1 pair of conspicuous cells at esophagus-intestinal junction. Female with nonprotusive vulva; vulva at level of esophagus-intestinal junction (Figs. 2, 3); anus subterminal in position at end of body (Fig. 5). Male with proximal cloacal tube J-shaped; spicular tube absent; spicular sheath with spines uniformly distributed from proximal to distal portion (Figs. 6, 7, 11, 12); length of spiny spicular sheath varies according to degree of evagination; 1 pair of paracloacal papillae (Fig. 10). Testis ends near final third of distal cloacal tube, showing different degree of convolutions. The bacillary band 9.70 to 14.55 long, located at the middle region with cuticular inflations and bacillary glands. The bacillary band 0.06–0.09 from anterior extremity of body, and runs at body width region of 0.12–0.17 (Figs. 8, 9). With SEM, cuticular inflations appear bordering bacillary band (Fig. 14). Some elongated, others rounded in shape; another colapsed (Fig. 15). Bacillary glands reduced in number and only visible in anteriad portion (Fig. 16). Cuticle around vulvar aperture shows a transversally striated pattern (Fig. 13). Male holotype (from Sierra de la Ventana): Body length 24.20. Thick portion of body 10.4 long. Anterior body width 0.12; maximun posterior body width 0.56; width at esophagus-intestinal junction 0.22 (Fig. 2).
MATERIAL AND METHODS During a survey of rodents, 6 specimens of Phyllotis xanthopygus Waterhouse, 1837 (Sigmodontinae: Phyllotini) were trapped in Cerro Destierro (38819250S, 628549390W) and Abra de la Ventana (3884930S, 62819170W), over 500 m asl, Sierra de la Ventana (Buenos Aires Province); and another 3 specimens were trapped in Pampa de Achala (318379190S, 648549390W), over 2,000 m asl (Co´rdoba Province), Argentina. The viscera were fixed in 10% formalin, and examined in the laboratory. The nematodes were collected from the host’s caeca and preserved in 70% ethanol. For light microscopy, the worms were cleared in lactophenol. Drawings were made with the aid of a drawing tube. Received 29 December 2004; revised 25 February 2005; accepted 20 May 2005. 100
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FIGURES 1–9. Trichuris pardinasi n. sp. (1) Complete male specimen. (2) Esophagus-intestine junction, and proximal portion of testis. (3) Esophagus-intestine junction, and vulva. (4) Eggs. (5) Female posterior end, lateral view. (6) Detail of the posterior extremity, lateral view. (7) Posterior end, spiny spicular sheath, and spicule, lateral view. (8) Bacillary band, middle region view. (9) Bacillary band, lateral view.
Total length of esophagus 13.77; muscular portion 0.43 long; stichosoma portion 13.35 long (Fig. 1). Length of spicule 4.88 (Fig. 6). Spicular sheath densely spinose, 4.60 long (Fig. 7, 11). Length of evaginated spiny spicular sheath 1.58. Sperm duct 8.84 long; vas deferens 6.37 long; ejaculatory duct 2.47 long. Proximal cloacal tube 3.57 long; distal cloacal tube 4.16 long (Fig. 6). Distance between posterior end of testis and caudal extremity of body 0.28.
Paratypes: Based on 9 specimens. Body length 20.36 6 1.95 (18.81– 22.55). Thick portion of body 11.78 6 1.44 (10.07–12.85) long. Anterior body width 0.14 6 0.016 (0.12–0.16); maximun posterior body width 0.47 6 0,13 (0,35–0,78); width at esophagus-intestinal junction 0.21 6 0.035 (0.15–0.25); esophageal muscular portion 0.40 6 0.05 (0.35–0.45) long; stichosoma 11.17 6 1.67 (9.26–12.41) long. Spicule 4.67 6 0.42 (4.03–5.2) long. Spicular sheath 4.41 6 0.54 (3.45–4.79)
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FIGURES 10–16. Scanning electron micrographs of Trichuris pardinasi n. sp. male. (10) Detail of the proximal portion of spiny spicular sheath, paracloacal papillae, lateral view. (11) Detail of the distal portion of spiny spicular sheath, similar size and morphology of spines, and spicule. (12) Detail of the spines of distal spicular sheath, lateral view. (13) Female, detail of the nonprotusive vulva, ventro-lateral view. (14) Bacillary band, middle region view. (15) Detail of the cuticular inflations bordering the bacillar band. (16) Detail of the cuticular inflation, bacillary glands, and transversal striation.
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long. Sperm duct 7.56 6 1.01 (6.04–8.84); vas deferens 5.77 6 1.34 (4.25–7.21); ejaculatory duct 1.91 6 0.68 (1.23–2.99). Proximal cloacal tube 2.89 6 0.43 (2.14–3.47) long; distal cloacal tube 3.97 6 0.57 (3– 4.81) long. Distance between posterior end of testis and caudal extremity of body 0.675 6 0.39 (0.36–1.5). Male paratypes (from Pampa de Achala): Based on 2 specimens. Thick portion of body 9.52–10.01 long. Anterior body width 0.14–0.13; maximum posterior body width 0.5–0.4; width at esophagus-intestine junction 0.22–0.21. Spicule 3.60–3.70 long; spicular sheath 3.65–3.40 long; vas deferens 5.85 long; ejaculatory duct 1.43 long. Proximal cloacal tube 2.6–2.3 long; distal cloacal tube 3.25–3.20 long. Distance between posterior end of testis and caudal extremity of body 1.17–0.63. Female allotype (from Sierra de la Ventana): Body length 31.69. Thick portion of body 16.99 long. Anterior body width 0.12; maximun posterior body width 0.52; width at esophagus-intestinal junction 0.22 (Fig. 3). Total length of esophagus 15.64; muscular portion 0.58 long; stichosoma portion 15 long. Distance of vulva to anterior extremity 16.07. Paratypes: Based on 4 gravid specimens (2 complete, and 2 incomplete). Body length 37.54–29.03. Thick portion of body 19.93 6 0.65 (19.47–20.93) long. Anterior body width 0.135 6 0.017 (0.12–0.15); maximun posterior body width 0.66 6 0.06 (0.58–0.71); width at esophageal-intestine junction 0.29 6 0.03 (0.22–0.32). Total length of esophagus 16.85; muscular portion 0.41 long; stichosoma 16.05 long. Distance of vulva to anterior extremity 17.04 long. Eggs with oval flat and pugs (n 5 10) 0.03 by 0.06 (Fig. 4). Females paratypes (from Pampa de Achala): Based on 3 gravid specimens. Body length 29.44–42.9. Thick portion of body 15.6–21.97– 20.18 long. Anterior body width 0.13–0.09–0.078, maximum posterior body width 0.4–0.65–0.65; width at esophagus-intestine junction 0.21– 0.19–0.12. Distance of vulva to the anterior extremity 13.19–20.9. Egg oval 0.03 by 0.06 (n 5 6). Taxonomic summary Type host: Phyllotis xanthopygus (Waterhouse, 1837) male, voucher housed at the Mammals Collection from Museo de La Plata, MLP 27.XII.01.12. Other hosts housed at the Mammals Collection from Centro Nacional Patago´nico (Puerto Madryn, Argentina), CNP 810, CNP 811, CNP 814, CNP 815. Type locality: Cerro Destierro (388019250S, 628549390W), Sierra de la Ventana, Buenos Aires Province. Other localities: Abra de la Ventana (388 049030S, 628019170W), Sierra de la Ventana, Buenos Aires, and Pampa de Achala (318379190S, 648549390W), Co´rdoba Province, Argentina. Site of infection: Caecum. Prevalence and mean intensity: Five of 6 hosts examined (83.3%); 21.4 (1–46) parasites (Sierra de la Ventana), and 2 of 3 host examined (66.6%); mean intensity 4 (2–6) (Pampa de Achala). Type specimens: Holotype male, allotype female, and paratypes (n 5 6) deposited at the Helminthological Collection from Museo de La Plata CHMLP, numbers 5455, 5456, and 5457, 5458, respectively. Etymology: Dedicated to Ulyses F. J. Pardin˜as, a recognized paleontologist working on rodents from Argentina. Remarks Ten species of Trichuris are parasites of muridae, octodontid, dasyproctid, and myocastorid rodents in South America. Trichuris pardinasi n. sp. is differentiated from T. fulvi Babero and Murua, 1987 and T. laevitestis Suriano and Navone, 1994 because the spicule lies entirely within the distal cloacal tube (absence of the spicular tube) (Babero and Murua, 1987; Suriano and Navone, 1994). The remaining 8 species without a spicular tube can also be differentiated from the new species by the disposition of the spines from the spicular sheath, the length of spicule, the presence of the accessory caudal structure (pseudobursa or bulb of the spicular sheath), the shape of the proximal cloacal tube, and the vulva. Trichuris pardinasi n. sp. differs from T. bursacaudata Suriano and Navone, 1994 because the males lack a pseudobursa (Suriano and Navone, 1994) and from T. nutriae Schulz and Petrow (in Schulz and Landa, 1934) by the absence of the bulb of the spicular sheath (Vicente et al., 1997). Trichuris pardinasi n. sp. resembles T. robusti Babero and Murua, 1990, T. chilensis Babero, Cattan and Cabello, 1976, and T. bradleyi Babero, Cattan and Cabello, 1975 in the uniform
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distribution of the spines of the spicular sheath, and the nonprotrusive vulva. However, the 2 former species display a shorter spicule (2.30– 3.90 and 2.30–2.50, respectively, versus a mean of 4.67), and the proximal cloacal tube is ‘‘e-’’ and ‘‘U-’’ shaped, respectively, versus ‘‘Jshaped’’. It differs from T. bradleyi because it has a longer spicule (7.13–7.56) (Babero et al., 1975, 1976; Babero and Murua, 1990). Tritchuris pardinasi n. sp. is different from T. travassosi Correa Gomes, Lanfredi, Pinto and Souza, 1992 and from T. pampeana Suriano and Navone, 1994 because these species have the proximal region of the spicular sheath that is densely spinous, and the median and distal regions are more spaced (Correa Gomes et al., 1992; Suriano and Navone, 1994). Finally, T. gracilis (Rudolphi, 1819), described only by a female, is different from the new species because the body is longer and the vulva slightly posterior to the esophagus-intestinal junction (Cameron and Reesal, 1951).
DISCUSSION The bacillary band was only described on 3 of almost 10 species of Trichuris from rodents (Correa Gomes et al., 1992; Lanfredi et al., 1995; Malizia et al., 2005). Using light microscopy, the bacillary band is clearly differentiable from the remaining transversal striated cuticle in the thin portion. The bacillary band is often covered by rest of the intestinal wall tissues of the host. Thus, with SEM the cuticular inflation could not always be observed. Currently, the description of the bacillary band in the Trichuris species is considered as a complementary character (Bird et al., 1991). This is the first record of Trichuris parasitizing Phyllotini rodents. The population of P. xanthopygus from Sierra de la Ventana was originally described as an endemic subspecies, Phyllotis darwini bonariensis Crespo, 1964. Previously, this subspecies was considered a full species P. bonariensis (Crespo, 1964; Reig, 1987; Musser and Carleton, 1993; Galliari et al., 1996). Currently, there is no solid evidence available to justify its specific status; thus, we consider the populations of the hosts examined in this paper as belonging to P. xanthopygus, as stated in Pardin˜as et al. (2004). Phyllotis xanthopygus is frequently found in semi-desert areas on steep rocky slopes with cacti (Polop, 1989; Redford and Eisenberg, 1992). It is distributed from 158 to 518 S in central Peru, Bolivia, and Chile, and along the eastern side of the Andes in Argentina (Kramer et al., 1999). However, there is an isolated population of this rodent species in Sierra de la Ventana, Buenos Aires (Crespo, 1964). Pampa de Achala and Sierra de la Ventana are considered faunistic islands. These localities share a considerable number of species and subspecies, i.e., molluscs, insects, amphibians (Ringuelet, 1961), as well as P. xanthopygus and the present parasite, T. pardinasi n. sp. The present and future findings of shared parasite fauna from both populations of P. xanthopygus in these disjunct areas will support the hypotheses of a continuous distribution of this host species during a past time. ACKNOWLEDGMENTS To Mariano Merino, Agustin Abba, Florencia Cremonte, Ulyses Pardin˜as, Dario Podesta´, and Sebastia´n Cirignoli for collecting hosts from Co Destierro, Abra de la Ventana and Pampa de Achala. To U. Pardin˜as, and Jaime Polop for facilitate bibliography of the hosts. To U. Pardin˜as and Lucy Shirlaw for the critical reading of the ms. To Marı´a Cristina Estivariz, from CEPAVE, Carolina Marengo and Julia Diaz for the drawings; to Rafael Urre´jola and Patricia Sarmiento, from Museo de La Plata for the SEM photographs. This study was fund by Consejo Nacional de Investigaciones Cientı´ficas y Te´cnicas (CONICET).
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