A Parasite of Balantiopteryx Plicata (Chiroptera) in Mexico
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Parasite 2013, 20,47 Ó J.M. Caspeta-Mandujano et al., published by EDP Sciences, 2013 DOI: 10.1051/parasite/2013047 urn:lsid:zoobank.org:pub:E2016916-65BF-4F47-A68B-2F0E16B6710A Available online at: www.parasite-journal.org RESEARCH ARTICLE OPEN ACCESS Pterygodermatites (Pterygodermatites) mexicana n. sp. (Nematoda: Rictulariidae), a parasite of Balantiopteryx plicata (Chiroptera) in Mexico Juan Manuel Caspeta-Mandujano1,2,*, Francisco Agustı´n Jime´nez3, Jorge Luis Peralta-Rodrı´guez4, and Jose´ Antonio Guerrero5 1 Laboratorio de Parasitologı´a de Animales Silvestres, Facultad de Ciencias Biolo´gicas. Av. Universidad No. 1001, Col. Chamilpa, C.P. 62210, Cuernavaca, Morelos, Me´xico 2 Centro de Investigaciones Biolo´gicas, Universidad Auto´noma del Estado de Morelos, Av. Universidad No. 1001, Col. Chamilpa, C.P. 62210, Cuernavaca, Morelos, Me´xico 3 Department of Zoology, Southern Illinois University, Carbondale, Illinois 62901-6501, USA 4 Facultad de Ciencias Agropecuarias, Universidad Auto´noma del Estado de Morelos, Av. Universidad No. 1001, Col. Chamilpa, C.P. 62210, Cuernavaca, Morelos, Me´xico 5 Laboratorio de Sistema´tica y Morfologı´a, Facultad de Ciencias Biolo´gicas, Universidad Auto´noma del Estado de Morelos. Av. Universidad No. 1001, Col. Chamilpa, C.P. 62210, Cuernavaca, Morelos, Me´xico Received 18 July 2013, Accepted 10 November 2013, Published online 26 November 2013 Abstract – 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, Emballonuri- dae), 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 den- ticles 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 Pterygo- dermatites (Pterygodermatites) in the Mediterranean region and North Africa. Key words: Nematode, parasite, Pterygodermatites, Balantiopteryx plicata, chiroptera, Mexico. Re´sume´ – Pterygodermatites (Pterygodermatites) mexicana n. sp. (Nematoda: Rictulariidae), parasite de Balan- tiopteryx plicata (Chiroptera) au Mexique. Une nouvelle espe`ce de ne´matode, Pterygodermatites (Pterygodermatites) mexicana n. sp., est de´crite a` partir de spe´cimens collecte´s de l’intestin de la chauve-souris Balantiopteryx plicata (Chiroptera, Emballonuridae), de la Re´serve de la biosphe`re ‘‘Sierra de Huautla’’ dans l’E´ tat de Morelos, Mexique. C’est la deuxie`me espe`ce du genre de´crite de chauves-souris du Nouveau Monde, puisque la plupart des rictulaires mentionne´s dans ces hoˆtes appartiennent au genre proche Rictularia Froelich, 1802. Toutefois, les membres de Rictularia ne posse`dent qu’une seule dent œsophagienne a` la base de la capsule buccale, alors que dans les ne´matodes de´crits ici trois dents œsophagiennes sont pre´sentes et bien visibles. Ils sont donc inclus dans Pterygodermatites Wedl, 1861. La nouvelle espe`ce est caracte´rise´e par la pre´sence de 23 petits denticules sur la pe´riphe´rie de la capsule buccale et de 40 et 66 paires de processus cuticulaires respectivement chez les maˆles et les femelles. En outre, les maˆles posse`dent 3–4 processus pre´cloacaux ventraux en e´ventails, et les processus *Corresponding author: [email protected] Juan Manuel Caspeta-Mandujano – urn:lsid:zoobank.org:author:92E35B25-5C33-4C50-A0A4-3D46153F5CDA Francisco Agustı´n Jime´nez – urn:lsid:zoobank.org:author:C640E07E-20E8-419B-B50A-613013FD36EF Jorge Luis Peralta-Rodrı´guez – urn:lsid:zoobank.org:author:C33D4786-24A5-4056-B6E6-58A8E4B5FABE Jose´ Antonio Guerrero – urn:lsid:zoobank.org:author:74CB0969-01DC-485F-80FA-290FF59AAD97 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 2 J.M. Caspeta-Mandujano et al.: Parasite 2013, 20,47 cuticulaires des femelles sont divise´s en 40 paires de processus en peigne et 26 paires de processus en e´pine; la vulve s’ouvre approximativement au niveau de la paire 40. Le stoma dirige´ vers le dos et les 40 processus cuticulaires pre´vulvaires rendent difficile le placement de l’espe`ce dans l’un des sous-genres pre´sents dans le Nouveau Monde, mais les caracte`res correspondent au diagnostic de Pterygodermatites (Pterygodermatites) dans la re´gion me´diterrane´enne et l’Afrique du Nord. Introduction de Biologı´a, Universidad Nacional Auto´nomadeMe´xico and in the Coleccio´n Parasitolo´gica at the Universidad Auto´noma del Most species of rictulariid nematodes (Spirurida) occur in Estado de Morelos (UAEM), Mexico. Licencia de Colector rodents and carnivorous mammals, with relatively few species Cientı´ficoFAUT–0211fromSecretarı´a del Medio Ambiente infecting bats [9]. Characters used in the taxonomy of the group y Recursos Naturales (SEMARNAT). include the number of cuticular subventral processes on the worms, as well as the position of the vulva relative to these pro- cesses, the arrangement of caudal papillae and the orientation of Pterygodermatites (Pterygodermatites) the stoma [9]. Species traditionally included in Pterygoderma- mexicana n. sp. tites Wedl, 1861 are characterized by a dorsally displaced stoma, armed with three oesophageal teeth, and by possessing urn:lsid:zoobank.org:act:C45880BA-2373-4581-B304-201 between 29 and 60 pairs of prevulvar spines [5, 8, 9]. To date, C4C4C6354 only three species of Pterygodermatites and seven species of Figures 1–26 Rictularia Froelich, 1802 have been described from bats. Of Type host: Balantiopteryx plicata Peters, 1867 (Chiroptera: these, P. elegans (Travassos, 1928), R. lucifugus Douvres, Emballonuridae) Type locality: Mexico: Morelos State: municipality of Tla- 1956, R. macdonaldi (Dobson, 1880) and R. nana Caballero, 0 00 0 00 1943, have been recorded from bats in the New World [1, 3, quiltenango: Mina Ame´rica (18°27 46.47 N, 99°00 53.45 W). 4, 6, 7, 9, 11, 13]. Site of infection: Intestine. During an investigation of helminth parasites of bats in Prevalence and range of intensity: 20% (16 of 80 bats Mexico, carried out by the research team of the Laboratorio examined); 1–5 nematodes. de Parasitologı´a de Animales Silvestres, 26 nematodes of the Date of collection: From August 2008 to July 2009. Holo- genus Pterygodermatites were recovered from the intestines type; allotype and paratypes collected in October 2008. of the gray sac-winged bat, Balantiopteryx plicata Peters, Etymology: The species is named after its country of origin. 1867 (Chiroptera: Emballonuridae). A detailed morphological Deposition of type specimens: Holotype, allotype and para- analysis of this material revealed the presence of a new species, types, respectively, in the Institute of Biology, UNAM, in Mex- which is described below. ico, City (CNHE-8601, 8602, 8603); paratypes in the Faculty of Biology, Parasitological Collection of the Universidad Auto´n- oma del Estado de Morelos, Mexico (COPAUAEM N-450). Materials and methods Description Between August 2008 and July 2009, 80 specimens of B. plicata were collected by placing a mist net across the General: Small nematodes with annulated cuticle opening of the abandoned ‘‘Mina Ame´rica’’, located in the (Figure 11). Stoma semicircular, subterminal, opens dorsally Biosphere Reserve ‘‘Sierra de Huautla’’, municipality of (Figures 1, 11–14), with small irregularly spaced denticles on Tlaquiltenango, Morelos, Me´xico. Bats were killed by cervical margin, 23 in total, 10 dorsal and 13 ventral (Figures 12–14). dislocation and further subject to a helminthological Well developed sclerotized buccal capsule; three tooth-like pro- investigation. jections attached at base (Figures 2–3, 14). Lips not well The nematodes recovered from the intestine of the gray sac- defined, four lip-like protuberances present on anterior margin winged bats were washed in physiological saline, fixed in hot of stoma, each bearing one papilla. Four pairs of papillae 4% formaldehyde and cleared in glycerine for microscopic arranged in an outer circle, two dorsal and two ventral (Figures examination. Drawings were made with the aid of a Nikon 6, 11). Amphidial pores present on the lateral lip-like structures microscope drawing attachment (Nikon Corporation, Tokyo, (Figures 6, 12–13). Deirids present below the fifth pair of cutic- Japan). After examination, the specimens were stored in 70% ular comb-like processes (hereafter combs) at 275–464 from the ethanol. Four specimens were dehydrated progressively in a anterior end (Figure 16). Tail in both sexes conical (Figures 5, graded ethanol series, dried to a non-liquid state by critical point 8, 9, 21–25). drying using CO2, attached to a SEM stub and sputter coated Female (based on 10 specimens, holotype in parentheses): with gold palladium. Specimens imaged with SEM were Length of body, 11.49–20.64 (13.52), maximum width 250– exposed to a beam between 3 and 20 kV on a Hitachi 295 (295). Buccal capsule, 40–56 (56) long, measured from S2460 N scanning electron microscope (Hitachi, Ltd., Tokyo, ventral rim of capsule to basis, by 43–56 (56) wide.