Pseudangularia europaea sp. n. and other cestodes (Cyclophyllidea: Dilepididae and Paruterinidae) from the common swift, Apus apus

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1 Parasit, hung., 26:15-26, 1993 Hungarian Society of Parasitologists Pseudangularia europaea sp. n. and other cestodes (Cyclophyllidea: Dilepididae and Paruterinidae) from the common swift, Apus apus L. (Aves: Apodiformes) in Hungary Boyko B. GEORGIEV 1 and Éva M URAI 2 l Institute of Parasitology, Bulgarian Academy of Sciences. Acad. G Bonchev Street, Bl. 25, 1113 Sofia, Bulgaria 2 Zoological Department, Hungarian Natural History Museum, Baross u. 13, H-1088 Budapest, Hungary (Received June 20,1993) Abstract: Two species of the family Dilepididae, Pseudangularia europaea sp. n. and Neoliga sp., and one species of the family Paruterinidae, Notopentorchis iduncula (Spassky, 1946) (new geographical record), are reported fromapus apus collected in East Hungary in the Great Hungarian Plain. P. europaea differs from all the other members of the genus Pseudangularia Burt, 1938, by its considerably larger cirrus-sac. It is also distinguished from the morphologically closest species, P. triplacantha Burt, 1938, by its shorter vagina. The phenomenon of the breaking of the cirrus during the copulation was observed in P. europaea. Key words: Pseudangularia europaea sp.n., Neoliga sp., Notopentorchis iduncula, morphology, taxonomy, new geographical record, Apus apus, Hungary. INTRODUCTION The common swift (Apus apus Linnaeus, 1758) is the only member of the order Apodiformes occurring in Hungary (Keve 1960). Although it is abundant and nests in various places in Hungary, this bird is strongly protected (Haraszthy 1984). Consequently, parasitological investigations on swifts in Hungary have been based on a small number of samples. The only previous study (Sey 1973a,b) reported on the helminth parasites of 14 swifts collected during the summer months of from the Bakony Mountains (at Zirc and Pannonhalma); two digeneans, Brachydistomum salebrosum (Braun, 1901) and Lyperosomum clathratum (Deslongschamps, 1824) (Dicrocoeliidae), and one cestode, Neoliga depressa (Siebold, 1836) (Dilepididae) were recorded.

2 The late Dr Béla Edelényi (Zoological Department, University of Agricultural Sciences, Debrecen) made an extensive collection of avian parasites to the east of the River Tisza, mainly from the Hortobágy National Park, Biharugra and Szarvas (see Murai and Palotás 1989). After his death, this material was transferred to the Helminthological Collection of the Hungarian Natural History Museum, Budapest. The present paper reports the results of the examination of cestode specimens from common swifts collected by Dr Béla Edelényi. MATERIALS AND METHODS This investigation is based on specimens collected from the small intestines of three common swifts, Apus apus, captured in the forest in the flood-plain of the River Körös, near Szarvas, in the Great Hungarian Plain, on 6th October 1971 (migratory birds). The cestodes were fixed and stored in 70% ethanol, stained in alcoholic borax-carmine, dehydrated in an alcohol series, cleared in clove oil and mounted in Canada balsam. The slides arc deposited in Helminthological Collection of the Hungarian Natural History Museum, Budapest (HNHM) and the Institute of Parasitology, Bulgarian Academy of Sciences, Sofia (IPBAS). As comparative material, the type-specimens of Pseudangularia thompsoni Burt, 1938 (No ) and P. triplacantha Burt, 1938 (No ) from the Helminth Collection of The Natural History Museum, London, were examined. The drawings were made with the aid of a drawing tube. The measurements of internal organs were based on well-developed mature proglottides. Metrical and meristic characteristics are given as range with the mean (av.) and the number of measurements or counts taken (n) in parentheses. The dimensions are in micrometers except where otherwise stated. RESULTS AND DISCUSSION Family Dilepididae Fuhrmann, 1907 Genus Pseudangularia Burt, 1938 Pseudangularia europaea sp.n. Specimens studied: 5 complete specimens and 1 specimen without scolex as whole mounts; 1 of the scoleces in Berlese's fluid. Holotype HNHM No. E4282 (2 slides); paratypes: HNHM No. E4282 (4 slides); IPBAS No (1 slide). Description: Medium sized cestodes. Most developed specimens with length mm (av mm, n = 3), consisting of (av. 82, n = 3) proglottides: (av. 42) premature, (av. 17) mature 'male', (av. 18) mature 'hermaphroditic' and 2-6 (av. 4) pregravid. Gravid proglottides not available.

3 Maximum width of strobila at pregravid proglottides, mm (av mm, n = 3). Scolex (Figs 1A-B) trapezoidal, clearly distinguished from neck; (av. 299, n = 5) long, with maximum width (av. 291, n = 5) at level of suckers. Rostellum with large discoid anterior part, gradually tapering to posterior end, (av. 257, n = 5) long and (av. 175, n = 5) wide. Rostellar sheath with thick muscular wall, (av. 217, n = 5) long and (av. 169, n = 5) wide, reaching to posterior end of scolex. No fully-preserved rostellar crown present. Fig. 1. Pseudangularia europaea sp.n. A, B - scoleces; C - diagrammatic presentation of a rostellar hook demonstrating measurements taken; D - rostellar hooks. Scale-bars: A, B - 100/*; D - 50/z. Rostellar hooks arranged in three definite levels forming festoons with 5-6 hooks in each (Figs 4A-B); hook guard (Fig. ID) with irregular margins and considerably larger than blade; handle straight or slightly curved. Rostellar hooks measure (n = 4): a = (av. 46), b = (av. 51), c = 14 (av. 14), d = (av. 27) (a, b, c and d as shown in Fig. 1C); hooks in more posterior position appear to have shorter guard (e.g. 22) than those positioned more anteriorly (e.g. 31) and in between (e.g ) Suckers small, round, with diameter (av. 102, n = 18). Neck (av. 105, n = 5) long. Proglottides (Figs 2A-C) craspedote, wider than long even when

4 Fig. 2. Pseudangularia europaea sp.n., proglottides, dorsal view A - young mature ('male') proglottis; B - well-developed mature proglottis; C - pregravid proglottis. Scale-bar: A, B, C fi.

5 pregravid. Genital pores irregularly alternating in short series (e. g... 1, 2,1, 1, 4,1, 1, 2,1, 3,1, 2, 2,1,1, 4,1, 2; or... 2,1, 2, 2,2,1,1,1,1, 3,1, 2,1,1, 2, 1,1,2,1, 2,2,2, 2, 1); open in anterior 1/5-1/4 of lateral proglottis margin. Genital atrium (Fig. 3) consists of two parts: distal part with infundibular orifice and tubular lumen with diameter (av. 50, n = 10), surrounded by intensively stained cells and muscular fibres; genital papilla not observed, but probably this part protrudes prominently as papilla. Proximal part of atrium forms tube with pipette-like orifice and welldeveloped circular musculature, also surrounded by intensely stained cells; measurements of lumen x (av. 98 x 29, n = 8). Ventral osmoregulatory canals (av. 19, n = 10) wide, with transverse anastomoses. Dorsal osmoregulatory canals 5-11 (av. 9, n = 10) wide. Genital ducts dorsal to longitudinal osmoregulatory canals. Testes (av. 33, n = 24) in number, situated in median field posteriorly, laterally and dorsally to ovary and vitellarium; reaching anteriorly to level of cirrus-sac, may overlap osmoregulatory canals laterally (Fig. 2B). External vas deferens convoluted near anterior proglottis margin; very wide, resembling seminal vesicle; diameter (av. 31, n = 8); cellular covering on external vas deferens present as isolated single cells. Cirrus-sac (Figs 3A-C) with thick muscular wall; highly elongate, x (av. 582 x 82, n = 11); situated obliquely and very often reaching aporal osmoregulatory canals. Internal vas deferens in young mature ('male') proglottides enveloped with distinct cellular sleeve; internal vas deferens in well-developed mature proglottides very wide and similar to convoluted seminal vesicle; diameter (av. 33, n = 7). Ductus ejaculatorius with diameter 2-5 (av. 3.5, n = 8); its distal transformed into specialized structure, apparatus expulsor spermae (Figs 3 B-C). Evaginated cirrus consists of two parts: proximal part conical, at distance of (av. 25, n = 6) from base with spinose zone (av. 46, n = 6) long; diameter at base (av. 27, n = 6), diameter at terminal end of spinose zone (av. 15, n = 6), distal part of cirrus flagellum-like, usually convoluted, with diameter (av. 5.6, n = 8). Vitellarium median, lobed. Ovary rosette-shaped, two-winged, aporal wing larger than poral; each wing consists of several long digitiform lobes; in fully-developed ovary, lobes reach almost to longitudinal osmoregulatory canals. Mehlis' gland clearly visible, with diameter (av. 83, n = 10). Seminal receptacle elliptical, x (av. 396 x 166, n = 8), situated obliquely between centre of proglottis and cirrus-sac, in some cases overlapping cirrus-sac; sometimes seminal receptacle sigmoid. Vagina (Fig. 3) opens anteriorly to male pore, forms arch which passes dorsally to cirrus-sac; vaginal lumen x (av. 171 x 38, n = 10); vagina enveloped by intensely stained layer of glandular cells (av. 42, n = 8) wide. Vaginal sclerite (Figs 3B-C, 4C-D) situated between vagina and seminal receptacle, dumb-bell shaped; measuring (n = 15): length (av. 69), diameter of part directed towards vagina (av. 31), diameter of part directed towards seminal receptacle (av. 42), diameter of narrower median part (av. 13). Developing uterus (Fig. 2C) lobed, with many internal septae, occupies median field and parts of lateral fields.

6 In some postmature and pregravid proglottides cirrus-sac (Figs 3D, 4F) transformed into spherical body with thick muscular walls; then cirrus lost and only part of ductus ejaculatorius present (Fig. 3D). Narrow tubular structure, most probably terminal flagellum-like portion of cirrus, often observed in seminal receptacle. Evidently, the cirrus is normally broken during the course of the copulation. Fig. 3. Pseudangularia europaea sp.n., genital ducts, dorsal view A - in young mature ('male') proglottis; B, C - in mature proglottides; D - in postmature proglottis, male copulatory apparatus damaged as a result of the copulation. Scale-bar: A, B, C, D -100>.

7 Remarks: The genus Pseudangularia was described by Burt (1938) for two species, P. thompsoni Burt, 1938 (type-species) and P. triplacantha Burt, 1938, parasitizing Collocalia unicolor (Apodiformes, Apodidae) in Sri Lanka. Spasskaja and Spassky (1977) also placed Mehdiangularia swifti Shinde, 1969, from Apus affinis in India in Pseudangularia as they considered the monotypic genus Mehdiangularia to be a synonym of Pseudangularia. This synonymy was also accepted by Bona (in press). Galkin (1983) also placed P. brachycolpos (Dollfus, 1958) (=Anomotaenia brachycolpos Dollfus, 1958), in this genus; this species was described from Apus paliidus in Morocco (Dollfus 1958a, 1958b) and reported from,4. apus in Spain (Illescas Gomez and Lopez-Roman 1980). Galkin (1983) found one scolex of Pseudangularia sp. from A. apus in the Kurish Spit (Baltic coast). The genus Pseudangularia currently includes, therefore, four species parasitizing apodiform birds of the genera Collocalia and Apus; its geographical range includes Europe, Northern Africa and South Asia. In comparison with the species mentioned above, the present specimens have a larger cirrus-sac ( x ). They are easily distinguished by this character from P. thompsoni, P. brachycolpos and P. swifti, which have a relatively short, rounded cirrus-sac [240 x 115 (Burt 1938), x (Dollfus 1958a) and 170 x 50 (Shinde 1969), respectively]. The cirrus-sac does not cross the middle of the proglottis in these three species; but in the the Hungarian material, when fully developed, it reaches the aporal side of the median field. The cirrus-sac of P. triplacantha is similarly elongate to the Hungarian material and reaches to the aporal osmoregulatory canals, but it has smaller absolute dimensions [470 x 81, according to Burt (1938); x (av. 488 x 103, n=5), according to the present re-examination of the types]. Another morphological difference between the present material and P. triplacantha is associated with the dimensions of the vagina. The vagina of the present form is relatively short, extending from the genital atrium to the point where the female genital ducts cross the cirrus-sac; in contrast, the vagina of P. triplacantha is very large, 'extending from the opening into the ductus hermaphroditus at the base of the cirrus to the centre of the proglottis' (Burt 1938). The present re-examination of the type-specimens of P. triplacantha showed that its vaginal lumen is long and wide (av. 370 x 54, n=4), while the lumen of the vagina of the Hungarian specimens is little more than half this size. These comparisons indicate that the specimens from Apus apus from Hungary cannot be considered as conspecific with any of the known species of the genus Pseudangularia. On this basis, we regard them as a new species, which we name Pseudangularia europaea sp. n. The phenomenon of the breaking of the cirrus during the copulation is known for another dilepidid cestode with vaginal sclerites, i.e. Sureshia trychopea Kayton et Kritsky, However, in the latter species the cirrus lost by the partner is usually found in the vagina (Kayton and Kritsky 1984) while in P. europaea the terminal flagellum-like portion is situated in the seminal receptacle.

8 Genus Neoliga Singh, 1952 Neoliga sp. Specimen studied: one fragment without scolex, whole mount in Canada balsam, HNHM No. E4283. Description: Fragment with length 4.7 mm consisting of 20 proglottides (10 premature, 6 mature 'male' and 4 mature 'hermaphroditic'). Maximum width 0.79 mm at level of mature proglottides. Proglottides (Fig. 5A) craspedote, wider than long. Genital pores regularly alternating, situated at border of anterior 1/5-1/4 of lateral proglottis margin. Genital atrium (Fig. 5B) consists of two parts: terminal part with infundibular orifice and tubular lumen surrounded intensively stained cells and muscular fibres; inner part (ductus hermaphroditus) long, with well-developed circular musculature and lumen diameter of (av. 21, n = 3). Genital ducts dorsal to osmoregulatory canals. Testes (av. 23, n = 5) in number, situated in posterior half of median field, posteriorly, laterally and dorsally to female glands (Fig. 5A). Cirrus-sac elongate, oval, situated obliquely, reaching to aporal osmoregulatory canals (Fig. 5B); x (av. 465 x 88, n = 3). Evaginated cirrus present only in two proglottides, consisting (from base to distal end) of basal bulbus, smooth cylindrical zone, spinose zone, and flagellum-like terminal part; diameter of basal bulbus 20-22; diameter of cylindrical part 12-14; general length of smooth base (basal bulbus -I- cylindrical zone) 84-89; spinose zone in length and in diameter; flagellum-like terminal part coiled, with diameter 5-6. Vitellarium slightly lobed, median. Ovary two-winged, consists of digitiform lobes reaching laterally (when developed) almost to osmoregulatory canals. Mehlis' gland (as glandular structure) not observed. Seminal receptacle very large, flaskshaped, distal region folded, anterior to vitellarium. Vagina surrounded by thick sleeve of intensively stained cells; opens anteriorly or antero-dorsally to male pore, passies dorsally to cirrus-sac; separated from seminal receptacle by vaginal sclerite; diameter of vaginal lumen (av. 27, n = 3); diameter of vagina together with walls (av. 65, n = 3). Vaginal sclerite (av. 39, n = 3)long. Remarks: According to a recent revision of the family Dilepididae (see Bona, in press), there are three valid genera possessing vaginal sclerites and parasitizing swifts [some species are also recorded as accidental parasites of swallows (Passeriformes, Hirundinidae)]: Pseudangularia Burt, 1938, Neoliga Singh, 1952, and Echinotaenia Mokhehle, The present fragment corresponds well to the diagnosis of the genus Neoliga as defined by Bona (in press), in terms of its relatively short strobila, regularly alternating genital pores and long ductus hermaphroditus. The further identification of the specimen available is difficult due to the lack of a scolex and the lack of information on the morphology of proglottides ofneoliga spp. from Apus apus generally.this material neither correspond with Gallon's (1983) detailed descriptions of Ndepressa (Siebold,1836) and N. occidental Galkin, 1983, because its cirrus-sac is considerably larger ( in N. depressa, in N. occidentalis and in Neoliga sp. from

9 Fig. 4. A-F - Pseudangularia europaea sp.n. A, B - rostellar hooks; C, D, E - vaginal sclerite development (C - in premature proglottis, D - in mature 'male' proglottis, E - in mature 'hermaphroditic' proglottis); F - transformed cirrus-sac in pregravid proglottis; G-K- Notopentorchis iduncula (Spassky, 1946): G-H - rostellum; I - mature proglottides; J - postmature proglottides; K - pregravid proglottides. Scale-bars: A, B, F-H - 2ö>; C-E 35//; I-K 100>.

10 Hungary) nor with N. orientális Spasskaja et Spassky, 1971, because in the latter the vaginal sclerites are almost twice the size (Spasskaja and Spassky 1971). Fig. 5. Neoliga sp. A - mature proglottis, dorsal view; B - genital ducts, dorsal view. Scale-bars: A-25û>,B-100 /*.

11 Family Paruterinidae Fuhrmann, 1907 Genus Notopentorchis Burt, 1938 Notopentorchis iduncula (Spassky 1946) Spassky et Spasskaja, 1959 Specimens studied: One scolex and numerous fragments (of at least 3 specimens) in Canada balsam whole mounts (2 slides), HNHM No. E2479. Description: Fragments with maximum width 539 at level of pregravid proglottides. Scolex elongate, with maximum diameter of309 (n = 1) at the middle of suckers. Rostellum (Figs 4G-H) discoid, with diameter of 113 and with strong musculature. Rostellar hooks 44 (n = 1) in number, in two distinct rows (with two exceptions where single hooks occur in intermediate position); anterior hooks (av. 27.4, n = 3) in length, posterior hooks with length (n = 2). Suckers with weak musculature, slightly oval, with diameter of (av. 106, n = 4). Proglottides (Figs 4 I-K) craspedote, wider than long except when pregravid and gravid. Genital pores irregularly alternating in short series. Genital atrium simple, infundibular. Genital ducts ventral to osmoregulatory canals. Testes 4 (n = 2), 5 (n = 7) or 6 (n = 1) in number, encircling vitellarium, ovary and uterine primordium dorsally. Cirrus-sac thin-walled, lateral to or overlapping poral osmoregulatory canals, pyriform or flask-shaped, x (av. 70 x 33, n = 10). Vitellarium compact, median, near posterior margin of proglottis. Ovary transversely elongate, reniform or of irregular shape, compact. Seminal receptacle fusiform, elongate. Uterus spherical; paruterine organ wider than long, anterior to uterus. Proglottides with fully developed eggs not available. Remarks: N. iduncula was recently redescribed and discussed by Georgiev and Bray (1991). The aim of the present brief description is to document the first record of this species in Hungary rather than to provide taxonomic comments. The host range of N. iduncula includes four species of the genus Apus (A. apus, A.pacificus, A.paliidus and A. affinis). It is widespread throughout the Palaearctic region from Britain and Morocco to the Pacific coast of Asia (for a survey see Georgiev and Bray 1991). ACKNOWLEDGEMENTS We are grateful to Dr F.V. Bona for kindly permitting us to see a part of his unpublished manuscript, to the staff of the Parasitic Worms Division at the Natural History Museum (London) for the access to the types of Pseudangularia spp. during a visit funded by the European Economic Community, and Dr D.I.Gibson and Dr R. A Bray for reading the manuscript. Mr P. Peev provided valuable help with the preparation of the photographs. This investigation was completed with the financial support for one of the authors (B.G.) by the National Scientific Research Foundation of the Republic of Bulgaria, grant B - 44/1991.

12 Georgiev, B. B. és Murai, É.: Pseudangularia europaea sp. n. és egyéb galandférgek (Cyclophyllidea: Dilepididae és Paruterinidae) előfordulása sarlósfecskéből, Apus apus L. (Aves: Apodiformes) Magyarországon A szerzők Magyarországon gyűjtött sarlósfecskéből (Apus apus L.). származó két dilepidida fajt, a Pseudangularia europaea sp. n.-t ill. egy Neoliga sp.-t és egy, paruterinida galandféreget a Notopentorchis iduncula-t (Spassky 1946) írták le. A Pseudangularia europaea sp. n.-t a Pseudangularia nemzetség többi fajától a cirruszsák és a vagina nagysága alapján lehetett elkülöníteni. REFERENCES Bona F. V. (in press) The family Dilepididae Fuhrmann, In: Khalil L.F., Jones A and Bray R.A (eds) CAB International Institute of Parasitology. Keys to cestode parasites of vertebrates. - CAB International & British Museum (Natural History). Burt D. R. R. (1938): New avian cestodes of the family Dilepididae from Collocalia unicolor unicolor (Jerd.), the Indian edible-nest swiftlet, with descriptions of Pseudangularia thompsoni, P. triplacantha gen. et spp. nov. and Notopentorchis collocaliae gen. et sp. nov. - Ceylon Journal of Science, Section B, Zoology and Geology, 21: Dollfus R. Ph. (1958a): Miscellanea helminthologica maroccana XXV Sur quelques fragments de deux espèces de Dilepididae (Cestodes) à appareil oclusif chitinoid, parasites de l'intestin 6^Apus paliidus brehmorum Hartert. -Archives de l'institut Pasteur du Maroc, 5: Dollfus R. Ph. (1958b): Miscellanea helminthologica maroccana XXXI. Sur deux espèces de Dilepididae de l'intestin û'apus pallidas brehmorum Hartert, Archives de l'institut Pasteur du Maroc, 5: Galkin A K. (1983): Cestodes of Apus apus of the Kurish Spit.fln Russian]. - Trudy Zoologicheskogo Instituta Akademii Nauk SSSR, 121: Georgiev B. B. and Bray R. A (1991): Notopentorchis cyathiformis (Froelich, 1791) n. comb, and N. iduncula (Spassky, 1946) (Cestoda: Paruterinidae) from Palaearctic swifts (Aves: Apodiformes), with a review of the genus Notopentorchis Burt, Systematic Parasitology, 20: Haraszthy, L. (ed) (1984): Nesting birds of Hungary, [in Hungarian] - NATURA, Budapest, 247 pp. Illescas Gomez M. P. and Lopez-Roman R. (1980): Nuevos parasitos cestodes de Apus apus L. en Espana. -Revista Iberica de Parasitologia, 40: Kayton R. J. and Kritsky D. C. (1984): Sureshia trychopea sp. n. (Cestoda: Dilepididae) from white-throated swifts, Aeronautes s. saxatilis (Aves: Apodiformes) with notes on dilepidine cestodes having a vaginal sclerite. - Proceedings of the Helminthological Society of Washington, 51:

13 Keve, A. (1984): Nomenciator avium Hungáriáé. - Madártani Intézet, Budapest, 89 pp. Murai, É. & Palotás, G. (1989): In memóriám Dr Béla Edelényi ( ). - Miscnea zool. hung. 5: 3-7. Sey, O. (1973a): Contribution to the fauna of parasitic worms in the vertebrate animals of the Bakony Mts. II. Trematoda. [in Hungarian] - Mitt. Mus. Komit. Veszprém, 12: Sey, O. (1973b): Contribution to the fauna of parasitic worms in the vertebrate animals of the Bakony Mts. III. Cestoda. [in Hungarian] - Mitt. Mus. Komit. Veszrém, 12: Shinde G. B. (1969): Mehdiangularia swifti gen. et sp. nov. from the common house swift, Apus affînis in India. - Zoologischer Anzeiger, 182: Spasskaja L. P. and Spassky A. A (1971) Cestodes of birds in Tuva, [in Russian] - Kishinev, 'Shtiinza', 252 pp. Spasskaja L. P. and Spassky A A (1977) Cestodes of birds in the USSR. Dilepididae of terrestrial birds, [in Russian] - Moscow, Izdatel'stvo "Nauka", 300 pp.