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Helminthfauna of Bats in Spain. Iv. Parasites of Rhinolophus Ferrumequinum (Schreber, 1774) (Chiroptera: Rhinolophidae)

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Helminthfauna of Bats in Spain. Iv. Parasites of Rhinolophus Ferrumequinum (Schreber, 1774) (Chiroptera: Rhinolophidae) Research and Reviews in Parasitology. 59 (1·2): 57·68 (1999) Published by A.P.E. © 1999 Asociaci6n de Parasit61ogos Espaiiolcs (A.P.E.) Printed in Barcelona, Spain HELMINTHFAUNA OF BATS IN SPAIN. IV. PARASITES OF RHINOLOPHUS FERRUMEQUINUM (SCHREBER, 1774) (CHIROPTERA: RHINOLOPHIDAE) J.G. ESTEBA ,P. BOTELLA, R. TOLEDO & J.L. OLTRA-FERRERO Departamento de Parasitologia, Facultad de Farmacia, Universidad de Valencia. Av. Yicente Andres Estelles sin, 46100 Burjassot » Valencia, Spain Received 15 June \998; accepted 20 October \998 REFERENCE:ESTEBAN(J.G.), BOTELLA(P.), TOLEDO(R.) & OLTRA-FERRERO(J.L.), 1999.- Helminthfauna of bats in Spain. IV. Parasites of Rhino- lophus ferrumequinum (Schreber, 1774) (Chiroptera: Rhinolophidae). Research and Reviews in Parasitology, 59 (1-2): 57-68. ABSTRACTT:he helminthological analysis of 108 specimens of Rhinolophus ferrumequinum (Schreber, 1774) (Chiroptera: Rhinolophidae),coming from 17 different Spanish provinces, allowed us to find the following 13 parasitic species: Plagiorchis sp., Mesotretes peregrinus (Braun, 1900), l.ecithodendrium (Lecithodendrium) linstowi Dollfus, 1931, Pycnoporus heteroporus (Dujardin, 1845), Prosthodendrium (Prosthodendrium) par- vouterus (Bhalerao, 1926), P. (Prosthodendrium) corberensis Esteban, Oltra-Ferrero, Botella et Granel, 1991 and Lecithodendriidae gen. sp. (Tre- matoda: Digenea), Hymenolepis grisea (Beneden, 1873) and Hymenolepis sp. (Cestoda) and Strongylacantha glycirrhiza Beneden, 1873, Litomosa ottavianii Lagrange et Bettini, 1948, Physaloptera brevivaginata Seurat, 1917, and Ascarididae gen. sp. (larvae) (Nematoda).Larvae of Ascaridi- dae gen. sp. are found in bats of the Old Word for the first time. H. grisea and Hymenolepis sp. are new for the Spanish helminthfauna. L. (L.) lins- towi, P. heteroporus, P. (P.) parvouterus and L. ottavianii are found for the first time in R. ferrumequinum in Spain. R. ferrumequinum becomes a new host for P. brevivaginata. KEYWORDS:Helminths, Rhinolophus ferrumequinum, Rhinolophidae, Chiroptera, Spain. INTRODUCTION ding to CORDERO DELCAMPfLLO et al., 1980; DURETTE- DESSET, 1983; CORDERO DEL CAMPlLLO, CASTA -0 & As part of a research line conducted on the helminth REGUERA, 1994) in Huesca (SANCHEz-ACEDO, OTERO parasites of bats in Spain, the present paper studies the & ALBALA-PEREZ, 1974), and Molineidae gen. sp. (AL- helminthfauna of the Greater horseshoe bat, Rhinolo- VAREZ et al., 1991) (see reviews of ESTEBAN, OLTRA- phus ferrumequinum (Schreber, 1774) (Chiroptera: Rhi- FERRERO & MAS-COMA, 1991, 1992; CORDERO DEL nolophidae), a species widely distributed throughout the CAMP1LLO, CASTANON & REGUERA, 1994). world, and found in practically the entire meridional Pa- laearctic. This sedentary species is ubiquitous or relati- vely frequent in Spain, and occasionally displaces over MATERIAL A D METHODS distances of no more than 100 km. It can be found in A total of 108 specimens of R. ferrumequinum have been studied. very diverse refuges, but particularly in large spaces. It The material was obtained in 17 different geographic localities: I) spends the winter in caves, mines and tunnels, forming Province of Albacete: I specimen (Tobarra:I); 2) Province of As- monospecific groups. In the summer season it can also turias: 2 specimens (Peon: 2); 3) Province of Avila: 2 specimens be found in attic spaces or lofts, forming mixed colonies (Rarnacastafias: 2); 4) Province of Burgos: I specimen (Carazo: I); with different species of vespertilionids. In view of the 5) Province of Caceres: 4 specimens (Alia: 2; Serradilla: 2); 6) cosmopolitan nature of this bat, it is easily observed Province of Cantabria: 4 specimens (Guriezo:I; La Hermida: 2; Merilla: 1); 7) Province of Cuenca: 3 specimens (Tortola: I; Val- close to sea level or at higher elevations, though without decabras: 2); 8) Province of Gerona: 14 specimens (Capmany: 14); surpassing the tree line (BENZAL, PAZ & GISBERT, 9) Province of Guadalajara: 6 specimens (Abadanes: 2;Renales: I; 1991). Riofrfo del Llano: 2; Tamajon: I); 10) Province of Huesca: 4 spe- To date, the Spanish helminthfauna of the Greater hor- cimens (Villamia: 4); 11) Province of La Rioja: 1 specimen (Cala- seshoe bat comprised only six species: Plagiorchis (Pla- horra: I); 12) Province of Leon: 5 specimens (Matarrosa del Sil: 2; giorchis) vespertilionis (MUller, 1784) cited in C6rdoba Parade la de Muces: I; Vegacervera: 2); 13) Province of Madrid: 2 and/or Granada (LOPEZ-NEYRA, 1947), Huesca (SAN- specimens (Aranjuez: 2); 14) Province of Malaga: 2 specimens (Frigiliana: 2); 15) Province of Tarragona: I specimens (Altafulla: CHEZ-AcEDO, OTERO & ALBALA-PEREZ, 1974) and Gra- I); 16) Province of Toledo: 2 specimens (Campillo de la Jara: 2); nada (VAUCHER, 1975), Mesotretes peregrinus (Braun, 17) Province of Valencia: 54 specimens (Corbera de Alcira: 14; 1900) in Pontevedra and/or Lugo (ALVAREZ MASCATO Cortes de Pallas: 10; El Oro: 1; Onteniente: I; Torres Torres: 16; et al., 1985) and Pontevedra (ALVAREZ et al., 1991), Tous: 10; Serra: I; Sumacarcer: I). Strongylacantha pretoriensis Ortlepp, 1932 in C6rdoba (MARTINEZ GOMEZ et al., 1976 in CORDERO DEL CAM- PTLLO et al., 1980), S. glycirrhiza Beneden, 1873 (= S. RESULTS AND DISCUSSION pretoriensis sensu AL VAREZ MASCATO et al., 1985) (ALVAREZ et al., 1991), Parahistiostrongylus viguerasi The study of these 108 specimens has allowed us to Lopez-Neyra, 1946 (= Histiostrongylus viguerasi accor- detect 13 helminth species: 7 Trematodes, 2 Cestodes 58 J.G. ESTEBAN et at. and 4 Nematodes. The most outstanding systematic and La Hermida, Valdecabras, Capmany, Renales, Riofrio faunistic characteristics of the different helminth species del Llano, Villamia, Matarrosa del Sil, Paradela de Mu- found are described below. ces, Vegacervera, Corbera de AJcira, Cortes de Pallas, El Ora, Onteniente, Torres Torres and Tous), we detected a series of large-sized intestinal digeneans (Fig. l A), Trematoda which proved to be the most frequently found within the helminthfauna of the Greater horseshoe bat. The most relevant morphological characteristics are: body length Fam. Plagiorchiidae Ward, 1917 1690-4267 urn and maximum width 551-965 urn. Oral Plagiorchis sp.: In a great number of host specimens sucker subterminal, 172-276/161-264 urn, and ventral from different localities (Ramacastafias, Alia, Guriezo, sucker 138-230/92-218 urn. Sucker ratio (surface of the o o o e: Fig. 1.- Digenetic trematodes from Rhinolophus ferrumequinum: A) Plagiorchis sp. in dorsal view; B) Pycnoporus heteroporus ingravid specimen in ventral view; C) Lecithodendriidae gen. sp. in ventral view. Scale bars: A: LOOO urn; B: 200 urn; C: SOO urn (orig. J.G. Esteban). Helminths of Rhinolophus [errumequinum in Spain 59 oral sucker/surface of the ventral sucker) is 1.2-2.2. Dis- tes of this genus, classified as P. vespertilionis and P. ko- tance between suckers 287-689 urn. Prepharynx absent reanus, have already been found in different Spanish and pharynx 71-126/68-126 urn. Two testes, post-ova- bats, including R. ferrumequinum (see ESTEBAN, rian and obliquely situated: anterior 172-391/138-345 OLTRA-FERRERO& MAS-COMA, 1991, 1992; BOTELLA, urn and posterior 195-368/149-345 urn. Cirrus sac elon- SANCHEZ& ESTEBAN,1993; CORDERODEL CAMPILLO, gate, 391-827/69-115 urn.Cirrus thin (23 urn), long CASTANON& REGUERA,1994). The present paper broa- (368-460 urn when evaginated) and unarmed. Ovary dens the Spanish corology of these digeneans. 161-333/138-241 um. Vitellaria, in lateral fields over- lapping caeca, constituted by large vitelline follicles ex- Fam. Mesotretidae Poche, 1926 tending from the median level of ventral sucker or a little more anteriorly to a little anterior to the caudal end of Mesotretes peregrinus (Braun, 1900): Some large-sized body, near caecal ends. Eggs operculate, oval, brownish digenean individuals belonging to this species appeared yellow, 31-38/17-20 um. This material was easily classi- in the intestine of eleven host specimens from Peon, Gu- fied within the genus Plagiorchis Luhe, 1899, which is riezo, La Hermida, Riofrio del Llano and Villarnia. The known to include many species whose hosts belong to general morphology and the morphometry (see Table 1) most vertebrate classes.Nevertheless, attention is drawn agree with the description of the species by HURKOVA to the great systematic confusion presently resulting (1963), MTTUCH(1964) and ALVAREZet at. (1991). Be- from the marked morphological variability and the low fore the present paper, this mesotretid had already been host specificity of Plagiorchis species. Recently, RICCI detected in Spain in this host species and R. hipposideros (1995) emphasized the need for a general revision of the from Pontevedra, Plecotus auritus from Lugo, and Myo- genus Plagiorchis, in order to reach an agreement on the tis nattereri (ALVAREZet al., 1991), Miniopterus schrei- limits of the genus, to assess species validity and to esta- bersi (ESTEBAN,OLTRA-FERRERO& MAS-COMA, 1990) blish synonyms. This problem is even more apparent and Pipistrellus pipistrellus (BoTELLA, SANCHEZ& Bs- when considering the morphological differentiation and TEBAN, 1993). However, this is the first complete des- systematic status of Plagiorchis species occurring in cription of M. peregrinus from European R. ferrumequi- bats (OLSE, 1937; YAMAGUTI, 1958, 1971; SKVORT- num and broadens the Spanish corology of this species. ZOV, 1972; KIFUNE& SAWADA,1979; KRASOLOBOVA, 1987) and, more concretely, in morphologically very si- Fam. Lecithodendriidae Odhner, 1910 milar species, as
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