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

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) parvouterus (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.) linstowi, 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 relatively 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 is the case of those included in the «vespertilionis» group occurring in European bats: P. vesper- Lecithodendrium (Lecithodendrium) linstowi Dollfus, tilionis (MUlier, 1780), P. koreanus Ogata, 1938 and P. 1931: Based on the studies of different authors (DUBOIS, muelleri Tkach et Sharpilo, 1990 (OGATA, 1938; GROS- 1955, 1960; HURKOVA, 1963; MATSKASI, 1967; COM- CHAFf & TENORA, 1973, 1974; TKACH & SHARPILO, BES & CLERC, 1970; ESTEBA , OLTRA-FERRERO& 1990; SHARPILO& TKACH, 1992). The above-mentioned MAS-COMA, 1990) it was possible to classify some considerations advise against the temporary ascription of small-sized digeneans found in three host specimens the materials studied, looking for future morphological, from Capmany, Cortes de Pal las and Torres Torres. In biological and even molecular research to provide suffi- Spain, previous reports on this helminth concern the bat cient criteria for adequate species differentiation. Parasi- species Tadarida teniotis, Miniopterus schreibersi and

Source HURKOVA(1963) MITUCH(1964) ALvAREzetal. (1991) Presentestudy Host Various Rhinolophus spp. Various R. ferrumequinum Country Slovakia Slovakia Spain Spain

E. V. E. V. E. V. E. V.

Length 3060-5850 4300-6000 3825-5228 3180-4131 Maximumwidth 450-900 700-1000 663-1071 1007-1355 Oral sucker 150-300/150- 340 200-279/212-332 286-316/133-265 304-351/281-328 Ventralsucker 210-450/270-540 305-385/345-442 316-510/316-479 508-695/445-562 Suckerratio 0,3-0,5 0,3-0,4 Dist. betweensuckers 510-700 328-753 Pharynx 63-135/63-126 146/111 140-156/145-195 Cirrus pouch 412-665/53-70 663-755 265-562/211-234 Anteriortestis 630-990/150-210 625-870/146-212 745-1224 679-921/273-562 Posteriortestis 600-1050/150-210 715-851/ 176-226 1046-1402 562-757/242-414 Ovary 180-3301120-180 226-305/305-425 234-408/1 12-295 289-531/273-336 Eggs 54-63/30- 36 53-66/26-30 43-46121-24

Table 1.- Mesotretes peregrinus: comparativestudyof the measurementsin ~m of adults.E.V.=extremevalues. 60 J.G. ESTEBAN et at.

Pipistrellus pipistrellus (MARTlNEZ-GOMEZet al., 1974; and gives rise to two very short saccular intestinal caeca. ESTEBAN,OLTRA-FERRERO& MAS-COMA, 1990; BOTE- The genital pore is unarmed, ventral, median and it LLA,SANCHEZ& ESTEBAN,1993). The present study is, opens at the level of the ventral sucker. The testes are therefore, the first Spanish report of this digenean in R. subspherical to oval, and are located at acetabular-posta- ferrumequinum. cetabular level. The cirrus pouch is absent. The seminal vesicle is relatively large (141-443/27-101 urn), free in Pycnoporus heteroporus (Dujardin, 1845):Five non- the parenchyma, and situated at preacetabular level bet- gravid individuals (Fig. 1B) were found in the intestine ween the intestinal bifurcation and the ventral sucker. of two host specimens from Corbera de Alcira. The ge- The ovary is oval and located at acetabular-postacetabu- neral morphology, mainly referred to the ventral sucker, lar level. The vitelline follicles are thick and arranged in of this material agrees with the bibliographic descrip- two lateral dorsal fields at pharynx-caecal level. The ute- tions of this digenean species (DUBOIS, 1960; MATS- rus fills the post-testicular region. The eggs are opercu- KASI, 1967; ODENING,1968; COMBES& CLERC, 1970). late, oval, brownish yellow, and measure 21-26/10-15 Up to the present, in Spain only ESTEBAN,OLTRA-FE- urn.Among the different subfamilies included within the RRERO& MAS-COMA(1990) and BOTELLA,SANCHEZ& Lecithodendriidae (YAMAGUTI, 1971), only Allassogo- ESTEBAN(1993) have reported this helminth parasitizing noporinae Skarbilovich, 1943 and Castroiinae Yamaguti, Miniopterus schreibersi and Pipistrellus pipistrellus, 1958 resemble our materials, mainly in terms of the ab- respectively. The present study is therefore the first Spa- sence of a cirrus pouch. Nevertheless, the acetabular si- nish report of P. heteroporus in R. [errumequinum, tuation of the genital atrium in our specimens, which dif- though a part of this parasitological materials already fers in both subfamilies (marginal in Allassogonoporinae was the subject of an applied ecological work (ESTEBAN, and preacetabular in Castroiinae), constitutes a characte- OLTRA-FERRERO& MAS-COMA, 1991). ristic of sufficient relevance to not include our materials in any of these subfamilies.Consequently, the possibi- Prosthodendrium (Prosthodendrium) parvouterus lity of creating a new subfamily may be considered. Ho- (Bhalerao, 1926): One host specimen from Tous was wever, we prefer to look for additional materials to allow found infected by three intestinal individuals of Lecitho- a more complete morphological study, in order to esta- dendriinae, which have been classified within the spe- blish a definitive diagnosis of our specimens. cies P. (P.) parvouterus, according to several descrip- tions (DUBOIS, 1955, 1960; HURKOYA,1963; ODENING, 1968; COMBES & CLERC, 1970). This is the first time Cestoda that this species has been detected in R. ferrumequinum in Spain. Up to date it had only been found in Miniopte- Fam. Hymenolepididae Fuhrmann, 1907 rus schreibersi (ESTEBAN, OLTRA-FERRERO & MAS- COMA, 1990, 1991). Hymenolepis grisea (Beneden, 1873): Some bat specimens of the Greater horseshoe bat from La Hermida, Cap- Prosthodendrium (Prosthodendrium) corberensis Este- many, Villamia,Corbera de Alcira and Cortes de Pallas ban, OItra-Ferrero, Botella et Granel, 1991: Some were infected by intestinal parasites of the Hymenolepidi- elongated, rounded at both ends, and small intestinal tre- dae family. These materials (Fig. 2) presented: a scolex matodes were found in a host specimen from Tous. with an unarmed but patent rostellum; symmetrical pro- These helminths were classified as belonging to P.(P.) glottids, generally twice wider than long; genital pore al- corberensis, according to the original description in the ways unilateral in the first third part of the lateral margin same host species by ESTEBANet al. (1991) based on 35 of the proglottids; three oval testes with a triangular distri- mature specimens coming from two host individuals of bution and inside the excretory ducts; cirrus pouch up to Corbera de Alcira, a locality not far away from that of the midline of the proglottid with a smooth cirrus; ovary the present record. trilobated, ventral with respect to testes, and inside the excretory ducts; vitellarium slightly lobated, aporal and bet- Lecithodendriidae gen. sp.: In nine host specimens ween the excretory ducts; and uterus with saccular shape, from Cortes de Pallas, Torres Torres and Tous some di- occupying all the inner space of the proglottid but not sur- geneans were found whose general morphology (Fig. passing the excretory canals bilaterally. These morphoa- 1C) allowed us to classify them within the family Lecit- natomic characteristics and the compared morphometric hodendriidae (YAMAGUTl,1971). These intestinal trema- study in relation to 19 hymenolepidid species from Chi- todes are small, with a flattened oval body. The oral suc- roptera with unarmed rudimentary or patent rostellum ker is oval, subterminal-terminal, and the ventral sucker know to date (PARONA, 1893; JOYEUX& BAER, 1936; is circular, situated on the central body axis at pre-equa- SKARBILOYICH1, 946; JOHRI, 1960; SAWADA,1967a, b, torial level and is smaller than the oral sucker. The suc- 1968, 1970, 1971, 1972a, b, c, 1982, 1983, 1986, 1997a, ker ratio (surface of the oral sucker/surface of the aceta- b;ZDZITOWIECKI,1970; MURAl, 1976; SAWADA& HA- bulum) is 1,8-3,4. No prepharynx is present. The RADA,1988; SAWADA& MOHAMMAD,1989) allowed us pharynx is muscular and the oesophagus is very short to classify these parasites as belonging to H. grisea (see Helminths of Rhinolophusjerrumequinum in Spain 61

E :l. o o N

50 urn B I

E :l. o on N

...• o o G 'l:: 3

E :l. o o It>

H o

...• '"o 1: 3

<....

Fig. 2.- Hymenolepis grisea from Rhinolophus ferrumequinum: A) scolex; B) premature proglottid; C) mature proglottids; 0, E) postma- ture proglottids; F) pregravid proglottid; G) gravid proglottid; H) proglottid after the last gravid proglottid in young specimen; I) egg; J) oncospheral hooks.Scale bars: A: 90 urn; B: SO urn; C: 100 urn; 0: ISO urn; E: 200 urn; F: 250 urn; G: 300 urn; H: 400 urn; T: 30 urn; J: 10 urn (orig. J.G. Esteban). 62 J.G. ESTEBANet at.

Source JOYEUX& BAER(1936) ZDZITOWIEC(1970KI ) MURAl(1976) Presentestudy Host Various Various Various R. ferrumequinum Country France Poland Hungary Spain

E. V. E. V. E.V. E. V.

Length 10000 13000-27000 25000-40000 25000-34000 Maximumwidth 600 320-935 600 460-689 Scolexsize 250 136-235 190- 2301200 151-273 Rostellum 40-50 63-135/34-72 120-140/50-65 74-128129- 77 Suckers 70 53-103 70-80 66-114/66-103 Testes 23-69 50-70 51-71/37-62 Cirruspouch 150-160/40 77-157/13-18 40-100/30-45 97-105/26-31 Ext.sem.vesicle 16-85/16-52 35-40 48120 Ovary 74-157 40 71-143/54-97 Vitellarium 41-66120-56 60-100/51-77 Receptacumlumsem. 36-120122-72 90-140 17-43 Eggsize 47-57 32-35 43-51 Onosphere 30124 30-34125-31 22-32 37-43 Oncospheralhooks 18 13-16 15 11-14

Table2.- Hymenolepis grisea: comparativestudyof the measurementsin urn. E.V.=extremevalues.

Table 2). However, it should be mentioned that this spe- 18 hooks; 24 urn length) and V. schmidti Jensen et Ho- cies is an example of the lack of agreement between the well, 1983 (16; 16-21 urn) from Africa (BAER, 1933; different authors in the systematic classification of hyme- JENSEN& HOWELL,1983) and V. hipposideri (Prudhoe et nolepidids in general and, particularly, the different spe- Manger, 1969) (16-19; 20-24 urn) and V. macrostrobiloi- cies of Hymenolepis Weinland, 1958 sensu lato known in des Sawada, 1984 (18; 25 urn) from Asia (PRUDHOE& bats (SPASSKY,1954, 1959, 1963; RYBICKA, 1959; YA- MANGER, 1969; SAWADA, 1984, 1997b; SAWADA,HA- MAGUTI,1959; VAUCHER, 1971, 1992; RAUSCH, 1975; RADA & KOBAYASHI, 1984).However, none of them SCHMIDT,1986; SAWADA,1997b). Thus, H. (s. I.) grisea agrees with our specimens. The possibility of establis- has been indistinctly allocated within Milina Beneden, hing our material as a new species is under consideration. 1873 (STUNKARD,1961; ZDZITOWIECKI,1970), Vampiro- Nevertheless, we decided not to assign specifically these lepis Spassky, 1954 (SPASSKY, 1954; VAUCHER, 1992) specimens until new materials in good conditions for the and Myotolepis Spassky, 1954 (TENORA& BARUS, 1960; morphological study are obtained. MURAl, 1976; SCHMIDT, 1986; SAWADA, 1997b). This finding is the first reference of this species for the Spanish helminthfauna. Nematoda

Hymenolepis sp.: In the intestine of eight specimens of Fam. Strongylacanthidae R. ferrumequinum from the province of Valencia (Cor- (Yorke et Maplestone, 1926) bera de A1cira, Cortes de Pallas, Torres Torres, Tous and Sumacarcer) some hymenolepidids were found. Most of Strongylacantha glycirrhiza Beneden, 1873: The small them had a contracted strobila because of in situ fixation. intestine of some host specimens from Pe6n, Carazo, Se- The most relevant morphological characteristics of this rradilla, T6rtola, Valdecabras, Capmany, Abadanes, Rio- material are: scolex with an armed rostellum of 37-68/48- frio del L1ano, Tamaj6n, Matarrosa del Sil, Aranjuez, Fri- 81 urn bearing a crown of 14-19 hooks of 20-26 um long; giliana, Altafulla, Campillo de la Jara, Corbera de A1cira, testes in triangular arrangement and clearly separated in Cortes de Pallas, Onteniente, Torres Torres, Tous and Su- two groups by the female organs, one poral and two apo- macarcer presented nematodes with conspicuous intra- ral, and inside excretory ducts; cirrus pouch extending buccal hooks. This characteristic justifies their inclusion beyond the level of the excretory ducts; cirrus smooth; within Strongylacantha Beneden, 1873, the only genus of genital pore in median position; and uterus occupying the the family Strongylacantidae (DURETTE-DESSET,1983), whole proglottid between the excretory ducts. The com- which is considered to be a primitive group characteristic parison of this material with those species of Hymenole-. of the rhinolophids (DURETTE-DESSET& CHABAUD, pis s. I. parasitizing bats (SCHMlDT, 1986; SAWADA, 1975). To date, only four species of this genus have been 1997b) has lead us to the conclusion that our material dif- described: S. glycirrhiza, S pretoriensis Ortlepp, 1932, S. fers clearly from all of them. According to the number rhinolophi Yamaguti, 1935 and S. longicaudata Mesza- and size of the rostellar hooks, the most closely related ros, 1973. Some morphological characteristics of our ma- species are: Vampirolepis sandgroundi (Baer, 1933) (16- terials, i.e., the distance of the excretory pore from the an- Helminths of Rhinolophusferrumequinum in Spain 63

A c

E :::l o o 'ot

100 urn

D·

c.l F o o \:: 3 o o'" 't 3

Fig. 3.- Strongylacantha glycirrhiza from Rhinolophus ferrumequinum: A, B) anterior end and head end of the female in lateral and ventral views; C) genital tract (anatomy of the ovejector) of the female in lateral view; D) posterior end of the female in lateral view; E) caudal bursa of the male in lateral view; F) spicule; G) variability of the dorsal ray of male caudal bursa in ventral view. Scale bars: A: 700 urn; B: 100 urn; C: 400 urn; 0: 75 urn; E: 300 urn; F: 200 urn; G: 50 urn (orig. J.G. Esteban). 64 J.G. ESTEBA et at.

0:-0"'0 ~ nO 0 B q,d' ~ c n~ •..• ~ n 0 " ., ~ ~ n On 0 o I); ..:... . • 0" j "(I ~.,. 000 " no0 E f ::'l , I,.. I ~- 0 i 1 , 0 i , M , , 40~m

50~m

, t . , 0 ,I i 0 't: ,. 3

L . ~ ~.

\ E ~::;~:

Fig. 4.- Litomosa ottavianii from Rhinolophus [errumequinum: A. C) anterior end and buccal capsule of the female in ventral views; B) de- tail of the so-called «area rugosa» of the male; D. E) tail of the female in ventral and lateral views; F) posterior end of the male in lateral view. Scale bars:A: 50 urn; B: 40 urn; C: 300 urn; D. E: 30 urn;F: 100 urn (orig. J.G. Esteban). Helminths of Rhinolophus [errumequinum in Spain 65

terior extremity (68-100 urn) and the spicule length (276- men from Cortes de Pallas. Through exhaustive morpho- 437 urn) of the male, differentiate our specimens from S. logical study of the female reproductive system, this ne- rhinolophi (excretory pore-anterior extremity: 290-320 matode has been classified within the species P. breviva- urn; spicules: 143-165 urn) (YAMAGUTI, 1935; KAGE!, ginata, according to the recent redescription by SAWADA& HARADA,1985) and S. longicaudata (excre- ESTEBAN,BOTELLA& TOLEDO (1995) based on mate- tory pore-anterior extremity: 230 urn; spicules: 180 urn) rials from Myotis blythi (Tomes, 1857) from Cotes (Va- (MESZAROS,1973). S. pretoriensis was described on the lencia, Spain). This physalopterid produces an apparent basis of specimens found in R. zuluensis from South stomach lesion (see BOTELLA& ESTEBAN,1995) related Africa (ORTLEPP, 1932), after comparison with the re- to the burdens present. In the present finding, no sto- description of S. glycirrhiza by YORKE & MAPLESTONE mach lesion was observed. R. ferrumequinum shall be (1926) and neglecting the first exhaustive description of considered a new host for this helminth species from this species by SEURAT(1920, 1921). Accordingly, the now on. systematic validity of S. pretoriensis should be questio- ned. However, our materials (Fig. 3) were in perfect agre- Fam. Ascarididae Baird, 1853 ement with Seurat's description.This nematode has been found to be the most prevalent helminth species in the Ascarididae gen. sp. (larvae): In the abdominal cavity Greater horseshoe bat (almost 50%), with an abundance of one host specimen from Corbera de AIcira a nema- of 13 individuals in a single host. Moreover, this is an tode larval stage of 46200 urn of body length and 802 oioxenous parasite of this bat species that has been used urn of maximum width was found. The observation of as an indicator of the systematics and etho-ecology of the an intestinal caecum length of 172 urn and width sing ni- different Spanish rhinolophids (ESTEBAN, OLTRA-FE- ficantly smaller than that of the oesophagus, as well as RRERO& MAS-COMA, 1991). This nematode had only the absence of ventriculus, lead us to include it within been detected in R. ferrumequinum from Pontevedra (AL- Ascarididae (HARTWICH, 1974). The lack of sufficient VAREZet al., 1991) and, consequently, the present report material to make cuts of the cephalic extremity for apical markedly broadens its distribution in Spain. study did not allow a more accurate classification. This report in R. ferrumequinum is the first of an ascaridoi- dean nematode in bats of the Old Word, since among the Fam. Onchocercidae (Leiper, 1991) bibliography revised only the reports of Contracaecum Litomosa ottavianii Lagrange et Bettini, 1948: Some sp. larvae in Cuban bats are known (BARUS & VALLE, Onchocercinae nematodes appeared in the abdominal ca- 1976; RUTKOWSKA,1980). vity of different host specimens from Guriezo, Capmany, Corbera de AIcira and Torres Torres (Fig. 4). The seg- ments of the buccal capsule, the ventral cuticular orna- ACKNOWLEDGEMENTS mentation on the coiled part of the posterior extremity of the male (the so-called «area rugosa- by BAlN, 1966) and Study supported by Spanish DGICYT Projects PB92-0517 and PB96-0401-C02-02 of the Ministerio de Educacion y Ciencia, Ma- the tail of the female agree with the description of L. otta- drid, and by Project 26.08.PAI3D.227.07 of the Ministerio de San i- vianii (= L. beacournui Bain, 1966)(BAlN, 1966; SONIN, dad y Consumo, Madrid. The authors wish to thank Or. E. Balcells 1975; PETIT, 1980).However, the ornamentation of the (Jaca), Dr. J. Serra i Cobo (Barcelona), Lie.J. Benzal, Lie.O. de area rugosa of the male and the tail of the female of our Paz and Lie. J. Gisbert (Madrid), and Lie. F. Faus (Valencia), for individuals, different from those of Miniopterus schrei- supplying the majority of the host material studied in this paper. bersi (see ESTEBAN, OLTRA-FERRERO& MAS-COMA, The authors express their gratitude to the Direccion General de Po- 1990), should be mentioned. This typical Palaearctic spe- litica Forestal y Pesquera and to the Direccion General de Conser- vacion del Medio Natural de la Conselleria del Medio Ambiente de cies was reported for the first time in Spain in M. schrei- la Generalitat Valenciana (Valencia), as well as to the Seccion de bersi by MESZAROS& MAS-COMA (1980) as L. beau- Conservacion del Medio aturaJ de la Diputacion General de Ara- cournui (ESTEBA, OLTRA-FERRERO & MAS-COMA, gon (Aragon), for the official authorizations of bat captures. Thanks 1992) and later in the same host species (see ESTEBAN, are given to Or. J. Herrero, Dr. P. Granel and Lie, L. Sanchez (Va- OLTRA-FERRERO& MAS-COMA, 1990, 1991), as well as lencia) for their technical collaboration in the field work. in P. pipistrellus (BOTELLA, SA CHEZ & ESTEBAN, 1993). 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