Pterygodermatites (Pterygodermatites) mexicana n. sp. (Nematoda: Rictulariidae), a parasite of Balantiopteryx plicata (Chiroptera) in Mexico

A new species of nematode, Pterygodermatites (Pterygodermatites) mexicana n. sp., is described based on specimens recovered from the intestine of the gray sac-winged bat, Balantiopteryx plicata (Chiroptera, Emballonuridae), from the Biosphere Reserve “Sierra de Huautla” in the state of Morelos, Mexico. This is the second species in the genus described from bats in the New World, since most of the rictaluriids reported in these hosts belong to the closely related genus Rictularia Froelich, 1802. However, members of Rictularia possess only a single oesophageal tooth at the base of the buccal capsule, whereas in the current nematodes three conspicuous oesophageal teeth are present. They are therefore included in Pterygodermatites Wedl, 1861. The new species is characterized by the presence of 23 small denticles on the periphery of the buccal capsule and by the presence of 40 and 66 pairs of cuticular processes in males and females, respectively. Additionally, males possess 3–4 ventral precloacal fan-like processes, and the cuticular processes of females are divided into 40 pairs of comb-like and 26 pairs of spine-like processes; the vulva opens on the level of approximately pair 40. The dorsally directed stoma and the 40 prevulvar cuticular processes makes it difficult to place the species in any of the subgenera present in the New World, yet characters correspond with the diagnosis of Pterygodermatites (Pterygodermatites) in the Mediterranean region and North Africa.


Introduction
Most species of rictulariid nematodes (Spirurida) occur in rodents and carnivorous mammals, with relatively few species infecting bats [9]. Characters used in the taxonomy of the group include the number of cuticular subventral processes on the worms, as well as the position of the vulva relative to these processes, the arrangement of caudal papillae and the orientation of the stoma [9]. Species traditionally included in Pterygodermatites Wedl, 1861 are characterized by a dorsally displaced stoma, armed with three oesophageal teeth, and by possessing between 29 and 60 pairs of prevulvar spines [5,8,9]. To date, only three species of Pterygodermatites and seven species of Rictularia Froelich, 1802 have been described from bats. Of these, P. elegans (Travassos, 1928), R. lucifugus Douvres, 1956, R. macdonaldi (Dobson, 1880) and R. nana Caballero, 1943, have been recorded from bats in the New World [1,3,4,6,7,9,11,13].
During an investigation of helminth parasites of bats in Mexico, carried out by the research team of the Laboratorio de Parasitología de Animales Silvestres, 26 nematodes of the genus Pterygodermatites were recovered from the intestines of the gray sac-winged bat, Balantiopteryx plicata Peters, 1867 (Chiroptera: Emballonuridae). A detailed morphological analysis of this material revealed the presence of a new species, which is described below.

Materials and methods
Between August 2008 and July 2009, 80 specimens of B. plicata were collected by placing a mist net across the opening of the abandoned ''Mina América'', located in the Biosphere Reserve ''Sierra de Huautla'', municipality of Tlaquiltenango, Morelos, México. Bats were killed by cervical dislocation and further subject to a helminthological investigation.
The nematodes recovered from the intestine of the gray sacwinged bats were washed in physiological saline, fixed in hot 4% formaldehyde and cleared in glycerine for microscopic examination. Drawings were made with the aid of a Nikon microscope drawing attachment (Nikon Corporation, Tokyo, Japan). After examination, the specimens were stored in 70% ethanol. Four specimens were dehydrated progressively in a graded ethanol series, dried to a non-liquid state by critical point drying using CO 2 , attached to a SEM stub and sputter coated with gold palladium. Specimens imaged with SEM were exposed to a beam between 3 and 20 kV on a Hitachi S2460 N scanning electron microscope (Hitachi, Ltd., Tokyo, Japan). All measurements are given in micrometres unless otherwise stated. Type specimens and paratypes are deposited in the Colección Nacional de Helmintos (CNHE) at the Instituto

Remarks
Pterygodermatites (Pterygodermatites) mexicana can be discriminated from the other species occurring in the New World by the position of the stoma, the number of teeth on the edge of the buccal capsule, the number of cuticular processes in both males and females, and the position of the vulva relative to the cuticular processes. A unique feature of P. (P.) mexicana seems to be the position of the stoma, being almost entirely dorsal (Fig. 16). In addition, the cuticular outgrowth of the anal lips appears to be a unique feature (Figures 24,  25). The inclusion of the species in the subgenus is proposed based on four sets of characters: the dorsally oriented stoma; the presence of irregularly-spaced small denticles in the buccal cavity; the presence of 40 prevulvar cuticular processes, and the sublateral orientation of caudal papillae pairs 1, 4 and 8.
Pterygodermatites (P.) mexicana can be discriminated from P. (P.) spinosa by the number of cuticular elements. The new species features a total of 40 pairs plus an unpaired comb on the right in males; females feature a total of 66 pairs plus an unpaired comb on the right. In P. (P.) spinosa there are 43-44 and 77 in males and females, respectively [10]. Pterygodermatites (P.) spinosa has a Palearctic distribution and has been recorded in the whiskered bat Myotis mysticinus (Kuhl, 1817) (Chiroptera: Vespertilionidae) in Germany [9,10]. The third species, P. (N.) bovieri, infects vespertilionid bats and occurs in localities from Western Europe to Afghanistan [9,12]. Pterygodermatites (N.) bovieri and P. (P.) mexicana are similar in the number of cuticular processes in both males and females and the arrangement of caudal papillae [12]. However, differences between these two species include the number of teeth surrounding the buccal capsule, and the position of vulva relative to the cuticular processes. A maximum of 14 teeth surround the buccal capsule of P. Finally, irrespective of host and subgenera, P. (P.) mexicana can be discriminated from any other species in the genus occurring in North America by the position of the stoma, which opens dorsally, the number of denticles surrounding the buccal capsule (23), the markedly unequal spicules, the presence of 40 pairs of combs in males and the number of prevulvar processes. Several of the species in the genus showing peribuccal denticles recorded in North America infect rodents of the families Cricetidae, Heteromyidae and Sciuridae [8,9]. In these species, the stoma opens in an apical position, the spicules are more or less equal and the number of denticles and cuticular processes differs.
In particular, there are seven species that show a markedly different combination of characters and those include: P. (Paucipectines) coloradensis (Hall, 1916), parasite of the Colorado chipmunk Tamias quadrivittatus (Say, 1823) (Sciuridae) and the deer mouse Peromyscus maniculatus (Wagner, 1845) (Cricetidae), features 14-20 denticles, a total of 42 pairs of cuticular processes in males and less than 31 prevulvar pairs of cuticular processes in females. Pterygodermatites (Paucipectines) dipodomis (Tiner, 1948), parasite of kangaroo rats (Heteromyidae) in the American southwest, featuring 38-40 pairs of cuticular processes in males, and 40 prevulvar pairs of cuticular processes in females. Pterygodermatites (Paucipectines) microti (McPherson and Tiner, 1952), parasite of voles (Cricetidae) in Alaska, featuring no more than 26 peribuccal denticles, 45 pairs of cuticular processes in males and less than 33 pairs of prevulvar cuticular processes. Pterygodermatites (Paucipectines) ondatrae (Chandler, 1941), parasite of muskrats (Cricetidae) in southern United States, featuring no more than 52 pairs of cuticular processes in males, and no more than 32 prevulvar pairs of cuticular processes. Pterygodermatites (Paucipectines) onychomis (Cuckler, 1939), parasites of cricetids and sciurids, featuring no more than 26 denticles and less than 33 prevulvar pairs of cuticular processes. Pterygodermatites (Paucipectines) parkeri Lichtenfels, 1970, parasite of sciurid and cricetid rodents in the east of the United States, featuring a buccal capsule armed with 14-19 denticles, 42 pairs of cuticular processes in males and less than 32 prevulvar pairs of cuticular processes. Finally, P. (Paucipectines) peromysci Lichtenfels, 1970, parasite of sciurid and cricetid rodents in the eastern half of the United States, feature 16-19 denticles in the buccal capsule, a total of 41 pairs of cuticular processes in males and less than 32 prevulvar pairs of cuticular processes; males of this species and P. (Paucipectines) dipodomis, have unequal spicules of similar dimensions as those seen in P. (P.) mexicana, nevertheless, the gubernaculum in the latter has not been seen and the stoma opens dorsally.

Discussion
The gray sac-winged bat, Balantiopteryx plicata, is restricted to areas in the Pacific coast from Costa Rica to Mexico. In Mexico, the Central Neovolcanic Axis roughly acts as a northernmost boundary for this species. The gray sac-winged bat serves as host for both P. (P.) mexicana and Rictularia nana, and both species have been described based on material collected in localities in the Central Neovolcanic Axis separated by some 60 km. The two species belong to different genera, however, because there are three tooth-like projections emerging from the base of the buccal capsule of P. (P.) mexicana compared to a single tooth in R. nana. In addition, the number and arrangement of caudal papillae in males consists of seven pairs of subventral papillae in R. nana and nine pairs of subventral and subventral papillae in P. mexicana. The dorsal position of the stoma is a trait considered of valuable taxonomic relevance in the discrimination between both genera, however, Tkach and Swiderski [12], demonstrated that this feature is somewhat variable in bat-dwelling species of Pterygodermatites.
Individuals of P. (P.) mexicana and R. nana can be easily distinguished by the number of cuticular processes in males, which is 44 pairs in the latter and 40 pairs (plus the single process) in P. (P.) mexicana. In addition, both spicules are shorter in P. (P.) mexicana (30-50 and 83-111) compared to those in R. nana (57 and 122). Finally, and perhaps because of the lesser number of cuticular processes, the deirids are located at the level of the fifth pair of combs in P. mexicana, whereas these structures are located at the level of the eight pair in R. nana.