New species of Aspiculuris (Nematoda: Heteroxynematidae), parasite of Mus musculus (Rodentia: Muridae), from Hidalgo, Mexico

Una nueva especie de Aspiculuris (Nematoda: Heteroxynematidae), parásito de Mus musculus (Rodentia: Muridae), de Hidalgo, México

Jorge Falcón–Ordaz, Griselda Pulido–Flores and Scott Monks*

Universidad Autónoma del Estado de Hidalgo, Centro de Investigaciones Biológicas, Apartado postal 1–69, 42001 Pachuca, Hidalgo, México. *Correspondent: smonks@uaeh.edu.mx

Recibido: 28 enero 2009
Aceptado: 28 enero 2010

Abstract

Aspiculuris huascaensis n. sp. was found in the intestine of Mus musculus collected from 2 localities in Hidalgo, Mexico, and is described herein. The new species possesses cervical alae abruptly interrupted at mid–length of esophageal bulb form an acute angle, distinguishing it from 5 of the 17 species in the genus. The new species is differentiated from 11 of the remaining species by having cervical alae that form an acute angle and end at mid–length of the esophageal bulb. Aspiculuris huascaensis n. sp. most closely resembles A. tetraptera in the position of the terminal end of the cervical alae. However, the new species can be distinguished from that species by the number of caudal papillae (12 vs. 14), the presence of a sessile precloacal papilla between 2 cuticular folds, and by having a single pedunculate papilla located slightly posterior to the cloaca.

Key words: Aspiculuris huascaensis n. sp., Mus musculus, Mexico, Hidalgo.

Resumen

Se describe una especie nueva, Aspiculuris huascaensis n. sp., proveniente del intestino de Mus musculus de 2 localidades de Hidalgo, México. Esta especie cuenta con 1 ala cervical interrumpida abruptamente formando un ángulo agudo; con base en este carácter, la especie nueva se distingue de 5 de las 17 especies que contiene el género. De 11 especies más, A. huascaensis n. sp. se diferencia por el ángulo agudo que forma el ala cervical y porque ésta finaliza a la mitad de la longitud del bulbo esofágico. Aspiculuris huascaensis n. sp. se asemeja a A. tetraptera por la terminación del ala cervical. Sin embargo, puede distinguirse de dicha especie por el número de papilas caudales (12 vs. 14), por la presencia de una papila precloacal sésil entre 2 pliegues cuticulares y por una papilla sencilla detrás de la cloaca.

Introduction

The diversity of helminths parasitizing rodents of Hidalgo, Mexico, is relatively unknown. To date, 27 helminth species parasitizing 8 hosts species have been recorded (Carmona, 1994; Falcón–Ordaz and Sanabria–Espinoza, 1995, 1996, 1999; Pulido–Flores et al., 2005; García–Prieto et al., 2008) (see Table 1), but specimens of Mus musculus Linnaeus, 1758, collected recently from the region of Huasca de Ocampo, Hidalgo, were found to harbor a previously unknown species of Aspiculuris Schultz, 1924. That species is described herein.

Materials and methods

Eighteen individuals of Mus musculus, 3 of Rattus rattus (Linnaeus, 1758), 3 of R. norvegicus (Berkenhout, 1769), 1 of Reithrodontomys fulvescens Allen, 1894, and 1 of Peromyscus sp. were collected from Cerro del Tezontle and 11 individuals of M. musculus were collected from San Juan Hueyapan, Huasca de Ocampo, Estado de Hidalgo, México, in July 2003 using small Sherman traps with various types of bait. Animals were transported alive to the laboratory in the traps and killed by an overdose of ether. The digestive tract (from lower esophagus to anus) was removed and examined for helminths. Three individuals of M. musculus from Cerro del Tezontle and 1 from San Juan Hueyapan were infected with an undescribed species of Aspiculuris. Worms were fixed according to standard practices (Pritchard and Kruse, 1982): nematodes were killed in Berland's solution, preserved in 70% alcohol, and cleared with glycerol for study in temporary mounts. En face preparations and cross sections of the anterior, middle, and posterior regions were made and mounted for examination. For scanning electron microscopy (SEM), nematodes were dehydrated in a graduated series of alcohol, critical–point–dried, coated with a gold–palladium mixture and examined in a Hitachi S–2460N scanning electron microscope at 15 kV. Type and voucher specimens were deposited in the Colección Nacional de Helmintos (CNHE), Universidad Nacional Autónoma de México, Mexico City, the Harold W. Manter Laboratory of Parasitology (HWML), University of Nebraska–Lincoln, Nebraska, and the Colección de Helmintos, Universidad Autónoma del Estado de Hidalgo (CHE). Drawings and measurements were made using a Zeiss microscope equipped with a drawing tube. Measurements are given in micrometers (μm) unless otherwise indicated; range is followed by the mean, standard deviation, and sample size (n) in parentheses. Measurements of holotype and allotype are in brackets.

Description

Aspiculuris huascaensis n. sp. (Figs. 1A–D, 2A–H, 3A–D)

Male: Based on 13 mature specimens. Length 2.16–2.69 mm (2.48±0.172 mm; n = 11) [2.45 mm]; width 78–114 (96±10; n = 12) [78] at midbody. Cephalic inflation 39–69 long (58±10; n = 11) [60] by 54 –75 wide (65±8; n = 11) [60]. Esophagus with bulb 291–294 (272±13; n = 12) [270] long; esophageal bulb 90–110 (97±6; n = 12) [96] long, 40–63 (51±6; n = 12) [48] wide. Distance from anterior end to nerve ring 72–93 (80±8; n = 9) [66]; to excretory pore 495–579 (545±35; n = 4) [492]. Cervical alae begin 12–24 (18±5; n = 14) [21] from anterior end, 180–246 (208±20; n = 10) [189] long. Cloaca to tip of tail 75–114 (102±13; n = 10) [99]. Length to pre–cloacal alae 105–156 (131±20; n = 8) [150]; to post–cloacal alae 48–96 (67±20; n = 5) [60]; to caudal alae 42–45(45±10; n = 6) [36]. The 12 caudal papillae are arranged as follows: single sessile precloacal papillae between 2 cuticular folds (not observed easily using light microscopy), 1 pair precloacal close to margin of cloaca, 1 pair of adcloacal papilliform formations, 2 pairs pedunculate and postcloacal, a single pedunculate papillae follows immediately, 1 subventral pair midway between cloaca and end of tail (Fig. 1B, 3C, 3D).

Female: Based on 15 mature specimens. Length 3.024–3.528 mm (3.219±0.150 mm; n = 14) [3.332 mm]; width 99–153 (120±16; n = 14) [126] at midbody. Cephalic inflation 60–90 long (74±7; n = 14) [72] by 69–84 wide (76±3; n = 14) [75]. Esophagus length 312–351 (322±12; n = 14) [324]; esophageal bulb 90–111 (103±5; n = 14) [108] long, 54–87 (63±8; n = 14) [60] wide. Distance from anterior end to nerve ring 81–105 (93±7 n = 11) [105], to excretory pore 555–675 (590±38; n = 10) [624]. Cervical alae begin 12–30 (18±5; n = 10) [18] from anterior end; with a length of 213–255 (235±10; n = 14) [249]. Vulva pre–equatorial, opening 1.204–1.428 mm (1.269±0.066; n = 14) [1.302 mm] from anterior end. Ovejector 144–195 (170±15; n = 12) [159] long. Distance from caudal extremity to anus 330–372 (358±16; n = 14) [372]. Eggs 54–69 (61±3; n = 50) long by 18–30 (22±3; n = 50) wide; eggs of allotype 60–69 (64±2; n = 6) long by 18–21 (20±2; n = 6) wide.

Taxonomic summary

Type material: holotype CNHE 6935 (male), Allotype CNHE–6936 (female), Paratypes CNHE–6937 and HWML–64565.

Type–host: Mus musculus Linnaeus, 1758.

Site: ceacum.

Prevalence and intensity: 3 of 18 (17%) individuals of M. musculus from the type locality (Cerro del Tezontle), infected with 84 nematodes, and 1 of 11 (9%) from San Juan Hueyapan infected with 2 nematodes.

Type–locality: Cerro del Tezontle (20Ëš15'47.40"N; 98Ëš30'59.71"W; elevation= 2 072m), Huasca de Ocampo, Hidalgo.

Etymology: the name of new species is in reference to the municipality of the type locality.

Remarks

The genus Aspiculuris, characterized by possessing 3 pairs of alae in the tail of male specimens, currently encompasses 17 species (Hugot, 1980; Inglis et al., 1990). Quentin (1975) separated the members of the genus into 2 groups based on the outline shape of the cervical alae. Members of the first group are characterized by having cervical alae that are abruptly interrupted with the posterior ends pointed and forming an acute angle toward the anterior [A. tetraptera (Nitzsch, 1821); A. dinnicki Schulz; 1927, A. schulzi Popov and Nasarova, 1930; A. kazakstanica Nasarova and Sweschikova, 1930; A. americana Erickson, 1938; A. lahorica Akhtar, 1955; A. pakistanica Akhtar, 1955; A. tschertkowi Tarzhimanova, 1969; A. azerbaidjanica Tarzhimanova, 1969 A. arianica Kotrla and Daniel, 1970; A. rysavyi Kotrla and Daniel, 1970; A. versterae Hugot, 1980]. In the second group, the posterior end of the cervical alae is rounded at the level of the esophageal bulb and not pointed, but gradually tapering posteriorly without forming an acute angle; in accordance with Quentin (1975), this group is constituted by A. ackerti Kruideiner and Mehra, 1959, A. asiatica Schulz, 1927, A. africana Quentin, 1966, A. ratti Johnston, 1970, A. witenbergi Quentin, 1975, and A. shikoloveta Inglis, Harris and Lewis, 1990. However, A. ackerti [considered species dubium by Hugot (1980) and Inglis et al., (1990)] recently was transferred to the new genus Lamotheoxyuris by Falcón–Ordaz et al. (2010).

The new species most closely resembles to the species included in the first group by having cervical alae abruptly interrupted. However, it differs from A. americana, A. lahorica, A. pakistanica, A. tschertkowi, A. rysavyi, and A. versterae because the posterior end of the cervical alae of those species do not form an acute angle (present in the new species); in addition, with exception of A. tschertkowi that have 16 caudal papillae, the remaining 5 species have a smaller number of papillae than A. huascaensis, varying from 7 to 10 vs. 12 papillae (Erickson, 1938; Akhtar, 1955; Yamaguti, 1961; Erhadová–Kotrlá and Daniel, 1970; Hugot, 1980; Miller and Schmidt, 1982). Aspiculuris huascaensis n. sp. can be distinguished from A. azerbaidjanica, A. dinnicki, and A. kazakstanica because the cervical alae in these species extend to the esophagus–intestine junction, while in the new species cervical alae are abruptly interrupted at mid–length of esophageal bulb level; likewise, the number of caudal papillae of A. kazakstanica and A. dinnicki is smaller than in A. huascaensis (7,10, and 12 papillae, respectively). Males of A. azerbaidjanica are unknown. Finally, A. schulzi and A. arianica can be distinguished of the new species by the extent of the cervical alae (ending anterior to the esophageal bulb in those species vs. reaching the middle of the esophageal bulb level in the Mexican specimens) and by having a smaller number of caudal papillae (7, 10 and 12, respectively) (Erhadová–Kotrlá and Daniel, 1970; Skjabin et al. 1960; Miller and Schmidt, 1982).

Aspiculuris huascaensis n. sp. most closely resembles A. tetraptera by having cervical alae ending at mid–length of the esophageal bulb. However, the new species can be distinguished from A. tetraptera by the number of caudal papillae (12 vs. 14, respectively). In addition, Aspiculuris huascaensis n. sp. have a single sessile precloacal papilla located between 2 cuticular folds and slightly anterior to the cloaca, whereas A. tetraptera lack both the sessile precloacal papilla and the 2 cuticular folds. In addition, males of the new species lack a medial papilla (double) associated with the cloaca and those of A. tetraptera have a double pedunculate papilla immediately posterior to the cloaca. Finally, in the new species, the anteriormost papilla located between the caudal folds of the tail is simple and that of males of A. tetraptera is double (Fig. 1B, 1E, 3C, 3D) (Skjabin et al. 1960; Hugot, 1980).

Discussion

The state of Hidalgo, Mexico, is located at the intersection of the ''Eje Neovolcánico'' and the ''Sierra Madre Oriental'', a region characterized by extreme variation in local ecological systems and a high diversity of flora and fauna that was produced by geographic isolation of local populations. No rigorous biogeographic study has been performed with the helminths of rodents, but several authors have suggested that helminths of rodents could be relatively diverse and contain Neotropic, Nearctic, and Mexican transition zone components (Falcón–Ordaz and Sanabria–Espinoza, 1995, 1996, 1999; Pulido–Flores et al., 2005). The knowledge of helminths of rodents of Hidalgo is still far from complete, but previous studies have failed to report A. huascaensis n. sp. from the few other regions of the state that have been studied (Falcón–Ordaz and Sanabria–Espinoza, 1995, 1996, 1999; Pulido–Flores et al., 2005). However, the finding of this new species only in animals collected from a restricted locality lends support to that hypothesis since it appears to be a geographically isolated local population.

Acknowledgments

The authors thank Berenit Mendoza–Garfias (Scanning Electron Microscopy, Instituto de Biología, UNAM) for assisting in processing samples for SEM. Alejandro Oceguera–Figueroa (Division of Invertebrate Zoology, American Museum of Natural History) and Luis García–Prieto, Collection Manager of the Colección Nacional de Helmintos, Instituto de Biología, UNAM, provided bibliographic references. The Programa de Mejoramiento del Profesorado (PROMEP), Fondos Mixtos (FOMIX CONACYT–Hidalgo, project 8695, to GP–F), and the Programa Anual de Investigación "Dra. Honoris Causa Elisa Vargas–Lugo Rangel" (projects 19B and 20B of SM and GP–F, respectively) provided funding for the collection of material for this project. During the writing of this paper, J.F.O. was a Postdoctoral Fellow in the Laboratorio de Morfología Animal, Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Hidalgo, supported by a fellowship grant "Estancias Posdoctorales y Sabáticas Vinculadas al Fortalecimiento de la Calidad del Posgrado Nacional, 2008" (CONACyT).

Literature cited

Akhtar, S. A. 1955. On nematode parasites of rats and mice of Lahore, with some remarks on the genus Aspiculuris Schulz, 1924 and two news species of the genus. Pakistan Journal of Scientific Research 7:104–111.         [ Links ]

Carmona, A. 1994 Contribución al conocimiento de céstodos en roedores silvestres (Rodentia) del Estado de Hidalgo y Veracruz. Thesis, Escuela Nacional de Estudios Profesionales Iztacala, Universidad Nacional Autónoma de México. Mexico. 79 p.         [ Links ]

Erhadová–Kotrlá, B. and M. Daniel. 1970. Parasitic worms of small mammals from the mountain regions of the Eastern Hindu Kush. Folia Parasitologica 17:201–216.         [ Links ]

Erickson, A. B. 1938. Parasites of some Minnesota Cricetidae and Zapodidae and an host catalogue of helminth parasites of native American mice. American Midland Naturalist 20:575–589.         [ Links ]

Falcón–Ordaz, J. and M. de los Á. Sabrina–Espinosa. 1995. Especie nueva del genero Protospirura (Nemata: Spiruridae) de Peromyscus difficilis (Rodentia: Cricetidae) de Hidalgo, Mexico. Anales del Instituto de Biología, Universidad Autónoma de México, Serie Zoología 66:17–26.         [ Links ]

Falcón–Ordaz, J. and M. de los Á. Sabrina–Espinosa. 1996. Especie nueva del género Carolinensis (Nemata: Heligmosomidae) de Peromyscus difficilis de Hidalgo, Mexico. Anales del Instituto de Biología, Universidad Autónoma de México, Serie Zoología 67:67–75.         [ Links ]

Falcón–Ordaz, J. and M. de los Á. Sanabria–Espinoza. 1999. Dos nuevas especies de Stilestrongylus (Nematoda: Heligmonellidae) parásitos de Peromyscus (Rodentia: Cricetidae) de México. Revista de Biología Tropical 47:929–937.         [ Links ]

Falcón–Ordaz, J., J. A. Fernández and L. García–Prieto. 2010. Lamotheoxyuris ackerti (Krudenier and Mehra, 1959) n. gen. n. comb. (Nematoda: Heteroxynematidae) parasite of Neotoma spp. (Rodentia: Muridae). Revista Chilena de Historia Natural. 83: 259–266.         [ Links ]

García–Prieto, L., J. Falcón–Ordaz, G. Lira–Guerrero and B. Mendoza–Garfias. 2008. A new species of Heteromyoxyuris (Nematoda: Oxyuridae), parasite of Perognathus flavus (Rodentia: Heteromyidae) from Mexico. Journal of Parasitology 94:860–865.         [ Links ]

Hugot, J. P. 1980. Sur le genre Aspiculuris Schulz, 1924 (Nematoda, Heteroxynematidae), Oxyures parasites de Rongeurs Muroidea. Bulletin du Museum National d'Histoire Naturelle 2:723–735.         [ Links ]

Inglis, W. G., E. A. Harris and J. W. Lewis. 1990. A new species of the nematode genus Aspiculuris Schulz, 1924 from Aethomys namaquensis (Mammalia: Rodentia) in the Kruger National Park, South Africa. Systematic Parasitology 17:231–236.         [ Links ]

Miller, G. E. and G. D. Schmidt. 1982. Helminths of bushy–tailed wood rats, Neotoma cinerea subspp. from Colorado, Idaho, and Wyoming. Proceedings of the Helminthological Society of Washington 49:109–117.         [ Links ]

Pritchard, M. H. and G. O. W. Kruse. 1982. The collection and preservation of animal parasites. Technical Bulletin No. 1, The Harold W. Manter Laboratory. University of Nebraska Press, Lincoln. 141 p.         [ Links ]

Pulido–Flores, G., S. Moreno–Flores and S. Monks. 2005. Helminths of rodents (Rodentia: Muridae) from Metztitlán, San Cristóbal, and Rancho Santa Elena, Hidalgo, Mexico. Comparative Parasitology 72:186–192.         [ Links ]

Quentin, J. C. 1975. Essai de classification des Oxyures Heteroxynematidae. Memoires du Museum National d' Histoire Naturelle, Zoologie 94:51–96.         [ Links ]

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. Translated from Russian, Israel Program for Scientific Translation, Jerusalem. 526 p.         [ Links ]

Yamaguti, S. 1961. Systema Helminthum. The nematodes of vertebrates, Part I and II. Interscience, New York. 1261 p.         [ Links ]